Next Article in Journal
The Influence of the Policy of Replacing Environmental Protection Fees with Taxes on Enterprise Green Innovation—Evidence from China’s Heavily Polluting Industries
Previous Article in Journal
Research on Construction Suggestions of China’s Endowment Service Supply Model from the Perspective of Welfare Pluralism
Previous Article in Special Issue
Characteristics of Selected Silphium Species as Alternative Plants for Cultivation and Industry with Particular Emphasis on Research Conducted in Poland: A Review
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 14
Issue 11
10.3390/su14116847
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

When Scent Becomes a Weapon—Plant Essential Oils as Potent Bioinsecticides

by
Nina Devrnja
*,
Milica Milutinović
and
Jelena Savić
Institute for Biological Research “Siniša Stanković”—National Institute of Republic of Serbia, University of Belgrade, Bulevar Despota Stefana 142, 11060 Belgrade, Serbia
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(11), 6847; https://doi.org/10.3390/su14116847
Submission received: 1 May 2022 / Revised: 31 May 2022 / Accepted: 31 May 2022 / Published: 3 June 2022
(This article belongs to the Special Issue Plant-Based Resources as a Green Alternative for a Sustainable Future)
Browse Figures
Versions Notes

Abstract

:
Crop protection still mostly relies on synthetic pesticides for crop pest control. However, the rationale for their continued use is shaded by the revealed adverse effects, such as relatively long environmental persistence that leads to water and soil contamination and retention of residues in food that brings high risks to human and animal health. As part of integrated pest management, biopesticides may provide crop protection, being eco-friendly and safe for humans and non-target organisms. Essential oils, complex mixtures of low-molecular-weight, highly volatile compounds, have been highlighted as major candidates for plant-derived bioinsecticides that are up to the sustainable biological standard. In this review, we screened the insecticidal activity of essential oils or their purified compounds, with focus given to their modes of action, along with the analyzed advantages and problems associated with their wider usage as plant-derived insecticides in agriculture.

1. Introduction

“Finding enough to eat today so that you stay alive tomorrow is the mark of individual success. Finding so much today that you can afford to devote tomorrow to thinking is the start of civilization” [1].
From the collection of wild grain at least 105,000 years ago [2], through the domestication of crops starting from the Neolithic period around 9500 BC [3], to the implementation of intensively developed irrigation and crop rotation in the past 200 years, ending in the replacement of human labor by mechanization assisted by synthetic fertilizers, pesticides, and selective breeding, food production has been a challenge facing mankind. Despite huge efforts and great investments made, the inexorable growth of the human population, together with actual demands on food safety and quality, are still not enough to feed mankind. According to the United Nations (UN) Food and Agriculture Organization (FAO) for 2020 [4], about 800 million people do not have a safe food supply every day. Due to a shaken economy caused by COVID-19, around 118 million more people suffered from hunger in 2020 than in 2019, and a scenario will be further complicated by the enduring effects of the pandemic.
However, modern intensive agricultural food production, developed from highly selective breeding over the centuries, relies on monocultures that are extremely vulnerable to different challenges and frequently subjected to great losses due to different climate and/or biotic factors. The most adopted protective agricultural practices rely on the application of different chemicals, i.e., fertilizers and pesticides (including herbicides, fungicides, and insecticides), frequently in huge quantities. However, this is one of the most striking issues that seriously jeopardizes a sustainable approach to modern agriculture due to contamination of the produced food with synthetic chemicals used for the crop treatments. The over-used chemicals bring high risk to human and animal well-being, but also cause dramatic environmental footprints that lead to water and soil contamination. For instance, 4.17 million tons of different classes of pesticides were produced in 2019 (FAOSTAT, accessed on 10 April 2022), and about 385 million cases of unintentional acute pesticide poisoning (UAPP) occur annually worldwide, with around 11,000 fatalities [5]. Moreover, just 0.1% of the total pesticides used affect the target pests, and the remaining quantity contaminates water, air, and soil ecosystems [6]. Due to the phenomena of biomagnification, an enhanced amount of toxic pesticide residues increases at higher trophic levels [7,8]. Thus, there is an increasing demand to consider alternatives to widely used chemicals in agricultural food production systems and implement more diverse ecologically based practices. Although the prevalence of chemicals over natural pesticides (biopesticides) is continuing, legitimated by an increase in the agricultural output, there is an increasing call for food quality and safety.
As an effect of that call, the research and development of biopesticides in general (insecticides, nematicides, rodenticides, fungicides, bactericides, and others) are expanding, governments are offering supportive policies for biological control of pests, and global markets are aiming to increase the popularity of biopesticides. The concept of “green pesticides” refers to all types of nature-oriented and beneficial pest control materials that can contribute to reducing the pest population and increasing food production [9]. The current support of sustainable pest control strategies will be continued by encouraging farmers to implement biological pest control methods. For example, the EU Commission will act to reduce the use and risk of chemical pesticides by 50% by 2030.
This review aims to present the state of the art in bioinsecticide research and application and nominate the most promising trajectories (approaches, solutions, directions) for modern and efficient EO-based insecticide production. It points out all the advantages of plant-derived insecticides over chemical ones, along with an overview of their modes of action and new techniques for their efficient application, as well as the problems yet to be solved. Neurotoxic modes of action are highlighted as a promising mechanism of EO-based insecticides that do not cause high selective pressure on pest populations but act toward several target sites so it can be hard to develop resistance.

2. Insects as the Super-Pests of Modern Agriculture

The threat during all stages of agricultural production of food comes from insect pests that are continuously adapting to crop hosts [10]. Insect pests reduce agricultural yields by up to 30% before and after harvest, in similar proportions [11]. Interestingly, only about 20–30 insect species (from a total of about 6 million identified species) are considered important pests for major crops, making significant agricultural and economic impacts [12]. According to the Kew Royal Botanic Garden [13], some of the most harmful are the cotton bollworm (Helicoverpa armigera Hubner), tobacco whitefly (Bemisia tabaci Gennadius), Colorado potato beetle (Leptinotarsa decemlineata Say), diamondback moth (Plutella xylostella L.), and fall armyworm (Spodoptera frugiperda Smith). The populations of these pests are dominant in agricultural ecosystems. They can develop resistance to chemicals [14] and consequently have several generations annually, with the high fecundity of females increasing the probability of random mutation and rapid aggregation of resistant mutants [15].
The extent of detrimental pest insects’ impacts is even greater in the modern world, with intensive human movements, international trade, and goods transportation. Populations of pests are unintentionally dispersed beyond their native ranges, and these so-called invasive species, introduced to an area where they are not known to occur, spread explosively, causing disturbance of co-evolutionary, antagonistic interactions with predators, parasitoids, and pathogens present in invaded areas [16]. It is estimated that USD 76.9 billion are required annually to manage and mitigate the impacts of biological invasions worldwide [17]. It is more frightening that future costs are likely to increase as invasive insects expand their ranges in response to global warming [18], and both insects’ population growth and metabolic rates will also increase [19].
Insect pests are frequently attributed as super-pests with continuously developing eco-physiological mechanisms and behavioral activities that allow them to overcome all obstacles to their successful spread [10]. As an example of the “indestructible” pest, the Colorado potato beetle is exhibiting a plethora of “responses” to agrotechnical control measures, but also co-evolutionary developed plants’ “traps” [10,20]. This insect continually increases the number of new hosts (avoiding co-evolved plant defensive strategies) [21], expands the territory it inhabits (due to climatic change and human activity) [22], manages developmental dynamics in response to climatic conditions (by shortening larval stages in unfavorable conditions and digging deeper into the soil when it is cold) [23], and develops resistance to insecticidal agents (by detoxifying them, or by adapting its digestive process) [24]. In general, all major insect pests are exhibiting a similar “arsenal” of adopting strategies, giving them super-pest characteristics.
This extraordinary ability of insect pests to overcome agricultural practices employed to eliminate their populations (crop rotation, physical barricades, thermal or electromagnetic control, insect removal by machinery, etc.) constantly pushes the development of new strategies and new insecticide products, but with the imperative to be in line with Integrated Pest Management (IPM).

3. The Chemical Teeter: Plant-Based Alternatives for Insecticidal Chemicals

The overview of the current global insecticide market still shows the undoubted dominance of chemicals over bioinsecticidal products. In the period of 2017–2019, approximately 0.7 Mt of total insecticides were produced annually, and the value of the global market was about USD 14.5 billion [25]. Just about one fifth of the share in production value is devoted to the bioinsecticide market, but with an indication of growing from USD 2.2 billion in 2020 to USD 4.6 billion by 2025 [26]. This growing trend is expected to be even more intensive since chemical insecticides start to lose popularity mainly because of their extremely negative impact on the environment and non-target organisms, i.e., beneficial insects (pollinators, predators), domestic animals, or humans [27]. Bioinsecticides could derive from diverse natural sources, including animals, plants, microbes, and minerals [28].
One of the desirable biological means of insect pest regulation that is fast gaining popularity is the application of natural compounds isolated from plants. Due to their sessile way of life, plants have developed a full range of different strategies, including the synthesis of compounds that enable them to survive in the battle against pests and pathogens. Although only a small portion of known higher plant species has been screened for pesticide activity so far [29], an increase in the research of plant-derived compounds with pesticide potential during the last few decades has been noticed, judging by scientific publications.
Insecticidal plant-derived chemicals are considered to be safe in general, exposing low toxicity to non-target organisms (Figure 1).
In contrast to conventional insecticides as broad-spectrum products affecting different organisms, plant-based or botanical insecticides are more selective due to the high compatibility between active ingredients and targeted pest metabolic pathways [30]. On the other hand, they may directly kill pests [31,32], but the modes of action imply indirectly interfere with pest physiology and/or reproduction [33] or may simply repel pests by compounds they avoid [34]. This way, populations of pests are suppressed and can be managed over time. In addition, pest resistance is hard to achieve due to multiple component mixtures that cause toxicity by interfering with many aspects of insect physiology and biochemistry [35]. Botanical insecticides also tend to decompose quickly and leave fewer residues on food and the environment [36]. The renewable nature of plant material, together with all the above-mentioned advantages, as well as intensified attempts to reduce production costs, will drag market tendencies toward the plant-based insecticide industry.

4. Scent That Can Hurt—Essential Oils as Insecticides

Recently, plant essential oils (EOs) have been brought into focus as major candidates for plant-derived bioinsecticides that are up to the sustainable biological standard of IPM. These complex mixtures are part of the plant’s defensive arsenal against different enemies, with repellent, fumigant, feeding deterrent, and larvicidal activity [37,38,39]. Essential oil constituents are highly volatile organic compounds (VOCs) with low molecular weight, commonly with terpenoids as the dominant group [40]. They are mixtures of two to more than 100 active substances and are determined by up to three components present at relatively high concentrations compared to other EO compounds. The major components usually shape the biological properties of EO and can be divided into two main groups: (1) terpene hydro-carbons (monoterpenes and sesquiterpenes) and (2) oxygenated compounds (alcohols, phenols, aldehydes, and esters). Terpenes are dominant constituents of EOs related to aromatic and oxygenated compounds [41].
A plethora of published studies has confirmed that mixtures of EOs have insecticidal activity against diverse insects, mostly under in vitro conditions, and bioactivity is frequently related to their synergistic interactions. A literature survey of the potential use of EOs as bioinsecticides indicated that EOs obtained from several plant families, including Meliaceae, Asteraceae, Myrtaceae, Apiaceae, Lamiaceae, and Rutaceae, have very potent insecticidal activity. They act as a repellent or fumigant, expressing contact or digestive toxicity in larvae or adults of the Lepidoptera, Diptera, Coleopteran, Hemiptera, and Isopteran orders (Table 1).
The first promoted EO-based bioinsecticides were those obtained from the neem tree (Azadirachta indica A.Juss) and Dalmatian chrysanthemum (Tanacetum cinerariaefolium Sch.Bip.). The cores of both insecticides are terpenoid compounds, azadirachtin and pyrethrin. Azadirachtin is found in the seeds of the neem tree, and chemically it belongs to the group of triterpenes with a very complex molecular structure known as limonoids. It is a highly oxidized tetranortriterpenoid with a plethora of oxygen-bearing functional groups that ensure its biological functions. The first experiments showed it to be active as a feeding inhibitor towards the desert locust (Schistocerca gregaria Forsskal) [49], but subsequent formulations with neem oil have shown it to be antifeedant and a growth disruptor contact insecticide against about 200 insect species [50,51,52]. It is considered non-toxic to pollinators and fishes, having low mammalian toxicity (LD50 of >5000 mg/kg) [53]. Neem oil is also one of the least toxic bioinsecticides to humans. Thus, azadirachtin is still the active ingredient in many pesticides, including TreeAzin (BioForest Technologies, Inc., Sault Ste. Marie, ON, Canada), AzaMax (Hawthorne Gardening Co., Vancouver, WA, USA), BioNEEM (GroSafe Chemicals, Ltd., Mount Maunganui, New Zealand), AzaGuard (BioSafe Systems, LLC., East Hartford, CT, USA), AzaSol (Arbojet, Inc., Woburn, MA, USA), and Terramera (Terramera, Inc., Vancouver, BC, Canada). Due to its sensitivity to light and temperature and its low stability under field conditions, neem oil has a high rate of photodegradation [54]. Employment of modern technologies enables “trapping” of volatile azadirachtin, maintaining it as one of the most prominent biopesticides and tagging it as the most successful botanical pesticide in agricultural usage worldwide [55]. Similarly, pyrethrin as a natural insecticidal constituent of EO extracted from the dried flower buds of Dalmatian chrysanthemum also exhibits high photosensitivity, but exceptional insecticidal potential. The fact that pyrethrins degrade rapidly after application promotes the development of pyrethroids, synthetic pyrethrins. Therefore, through comprehensive chemical modifications, a total of 42 substances were placed in the fourth class of insecticides by the World Health Organization classification [56]. These so-called pyrethroids, characterized by decreased light-induced degradation in the field, are potent biopesticides that are about 2.250 times more toxic to insects than to higher animals [57]. Based on the toxicological and physical properties, pyrethroids are grouped into two classes, Type I and Type II, based on the presence of the cyano group in the molecule. However, all pyrethroids as synthetic chemical compounds are less degradable in the environment, but exhibit higher toxicity [58,59] than natural pyrethrin.
Besides bioinsecticidal formulations containing the two most popular, azadirachtin and pyrethrin, only one tenth of other EOs have passed comprehensive and strict regulations and commercialization procedures and can be found on global markets. Most of these insect repellents and pesticides contain mixtures of EOs from garlic, rosemary, clove, thyme, peppermint, and lemongrass, and/or purified essential oil compounds like carvacrol, thymol, geraniol, and eugenol (EcoSMART Technologies, Alpharetta, GA, USA).

5. Mechanisms of Neurotoxic Insecticidal Activity of the Essential Oils—How EOs Conquer the Battlefield in the Targeted Insect Pests

Essential oils exert their insecticidal effects through multiple modes of action such as reduced growth, affected molting and prolonged development, induced sterility, altered behavior, midgut membrane disruption, metabolic disorders, neuromuscular toxicity, and non-specific multi-site inhibitions [60,61,62].
It has been reported that common EOs with insecticidal activities can be inhaled, ingested or skin absorbed by insects. Once components of EOs have entered the insect body, due to their lipophilic chemical structure and good penetrance, they switch on different signaling pathways and insecticidal mechanisms, causing biochemical, physiological, developmental dysfunction, and eventually mortality [63]. They can also increase the bioavailability of co-administered products, which makes them good synergists [64]. The toxicity of EOs depends both on the chemical compounds that act as toxins, and many other factors affecting total toxicity. The key factors inducing EO toxicity are the point of toxin entry, molecular weights, and mechanisms of action.
Generally, mortality has been considered a desirable toxicological endpoint of conventional insecticides. However, not only are pests targeted and killed but also numerous non-target insect species that come into contact with lethal doses in the treated areas and surrounding environment [65]. Moreover, recent studies showed the tendency to fast resistance development in populations of insect pests treated with insecticides with high mortality effects [66]. The alternatives to these mechanisms that put high selective pressure on pest populations are neuroactive insecticides with several action sites defined so far in the most prevalent insect pests [67]. The advantages of neuroactive insecticides are (1) rapid activity that stops crop damage immediately, (2) the presence of many sites of action that are highly sensitive when even a small disruption may be lethal, (3) the lipophilic nature of insecticides that allows for easy penetrance through the lipoidal sheath, and (4) the lack of a detoxification mechanism in nerves, thus prolonging insecticidal activity. These advantages significantly shaped the modern insecticide industry, with the majority of synthetic insecticides today having a neurotoxic activity, most often by inhibiting acetylcholine esterases (carbamates) or disrupting the function of ion channels in the nerve cell membranes (pyrethroids) [67]. Being highly lipophilic, volatile constituents of EOs are therefore promising candidates for bioinsecticides with neuroactivity, and in vitro proofs have been numerous already. The complex nature of EO mixtures could potentially be an advantage in targeting even more sites of action at once.

5.1. Inhibitors of Acetylcholinesterase

Acetylcholinesterase (AChE), the enzyme found primarily in the synaptic cleft of insects, is responsible for the deactivation of the principal neurotransmitter acetylcholine (ACh) that transmits nerve impulses from one nerve cell to another or to involuntary muscles. This enzyme is the target site for most neurotoxic insecticides [68,69,70,71,72]. AChE of insects differs from that in the mammalian system, thus making AChE an insect selective marker for newly developing insecticides, which will be safer for non-target vertebrates, including humans. Approximately 70% of the world’s insecticide market is based on synthetic AChE inhibitors (organophosphates, carbamates, and neonicotinoids). Gathered data suggest that the insecticidal action of EOs could be neurotoxic, leading to symptoms similar to those produced by organophosphates and carbamates [73]. Among various constituents of EOs, the evidence of anti-AChE activity was reported for 1,8 cineol, carvacrol, thymol, geraniol, α-pinene, and eugenol [74,75,76,77]. Fenchone, S-carvone, and linalool, followed by estragole, were also shown to efficiently inhibit the AChE of stored-product pests under in vitro conditions [70]. It should be noted that the activity of EO complex compounds and their mode of action may differ from the activity of their single component [78,79]. Some EO constituents function as competitive inhibitors, whereas others possess the opposite role (Figure 2).
As competitive inhibitors, EO or its constituents prevents the binding of AChE by attaching to its binding sites, thus maintaining the enzymes’ activity unchanged. However, uncompetitive inhibitors prefer binding to the enzyme–substrate complex than to the enzyme alone, consequently altering the enzyme activity and formation of the product. Tea tree (Melaleuca alternifolia (Maiden & Betche) Cheel) EO acts as an uncompetitive inhibitor, whereas its single components may act as competitive inhibitors. As was shown in the study by Taylor and Radić [80], the AChE enzyme has two target sites. Accordingly, some EO components can act as dual binding site inhibitors and perform competitive and uncompetitive inhibition. Action toward AChE also depends on the interaction between different EO terpenoid constituents that can be synergistic or antagonistic [81]. Savalev et al. [82] proposed synergism between 1,8-cineole and α-pinene, whereas oppositely, an interaction between 1,8-cineole and camphor was antagonistic. Interestingly, Miyazawa and Yamafuji [74] revealed that EO exhibited less activity due to the oxygenated functional groups in the bicyclic terpene structure.
The inhibition of AChE is one of the most investigated mechanisms of action in EOs. However, the study on EOs as AChE inhibitors showed that EOs are rather weak inhibitors of AChE. The majority of EO constituents displayed anti-AChE activity in mM concentration. So far, only carvacrol has inhibited AChE in a µM concentration [83]. Thus, scientific literature suggests that AChE inhibition is most likely not the primary neurotoxic mechanism of EOs [84].

5.2. Alternant of GABA Receptors

Gamma-aminobutyric acid (GABA) is an inhibitory neurotransmitter in insects’ nervous system and the muscles that binds to specific receptors (GABArs) associated with chloride (Cl−) channels located on the post-synaptic plasma membrane of neurons and disrupts the functioning of the GABA synapse. The binding sites for the EO components in mammalian GABArs have been defined in numerous studies. Some of the EO components (e.g., menthol, borneol, and geraniol) show structural similarity to a known ligand of the GABArs anaesthetic site. The binding of GABA to GABArs causes the opening of Cl- channels to allow the flow of chloride ions into the neurons and cause inhibition of the nervous system [85,86]. Pharmacologically, insect and mammalian ionotropic GABArs have different sensitivities to various chemicals; thus, GABArs can be used as a specific target for the development of new insecticides. Insect GABArs have three different subunits: RDL (resistant to dieldrin), GRD (GABA and glycine-like receptor of Drosophila), and LCCH3 (ligand-gated chloride channel homologue 3) [87]. However, the data regarding the effects of EOs on insect GABArs are still very limited. It was shown that monoterpenoid EO components are positive allosteric modulators of insect GABArs and increase the GABA-induced Cl− uptake [88]. The research on RDL receptors has shown that thymol caused strong potentiation of the Cl− current evoked by GABA. In addition, thymol, carvacrol, and pulegone intensified the binding of [3H]-TBOB to insects’ neuron membranes. For example, some monoterpenes, such as thujone, can induce neurotoxic effects by acting GABA receptors in insects [89]. As a target for insecticidal activity, ion channels that include GABA-gated chloride channels and acetylcholine-gated cation channels contribute to the fast knock-down effects due to their presence in the peripheral nervous system of insects, especially in the neuromuscular junction. However, further research is necessary to elucidate the exact mechanism of EOs and their bioactive compounds on insect GABArs.

5.3. Ligands of Octopamine Receptors

Several papers have demonstrated that EO constituents replicate the activity of octopamine. This molecule is a neuromodulator involved in the regulation of different forms of insect activity [90]. The octopamine receptor was not found in vertebrates. Therefore, EOs as bioinsecticides have selective toxicity to mammals. Octopamine exerts its effects through interaction with at least two classes of receptors that pharmacologically have been designated as octopamine-1 and octopamine-2 [91]. Roeder [92] demonstrated am existence of octopamine receptor class 3 in the locust nervous system. Many of the effects of octopamines binding to G-protein-coupled membrane octopamine-2 receptors might be mediated by cAMP [93] and linked to octopamine-sensitive adenylate cyclase, and agonists were shown to increase cAMP levels in the target tissue [93,94,95]. In addition, G protein induces the activation of phospholipase C, which elevates the calcium intracellular level and the activity of calcium-dependent protein kinase C. This results in the phosphorylation of many proteins, ultimately changing cell function. Studies have shown that α-terpineol, geraniol, citral, eugenol, cinnamyl alcohol, two natural terpenes (ZP-51 and SEM-76), and trans-anethole increased Ca2+ concentrations and cAMP levels in a similar way to octopamine [84,96,97,98,99]. Tripathi and Upadhyay [100] suggested insecticidal activity of Hyptis suaveolens EO against Callosobruchus maculatus Fabricius, Rhyzopertha dominica Fabricius, Sitophilus oryzae L., and Tribolium castaneum Herbst by octopamine receptor alteration. All these results provide strong arguments that the EO components interplay with octopamine, mainly as agonists of these receptors. The effects of EO components on octopamine receptors specific to insects lead to the conclusion that essential oils represent an insufficiently studied but promising pool of molecules with insecticidal activity.

6. The Future Is Here—New Technologies for EO-Based Insecticide Application

Based on reported investigations and available data in the literature, the usage of EOs has significant potential in IPM, but numerous limitations and constraints threaten to jeopardize this approach. Besides the arduous biopesticide registration process, which needs to be accelerated and adjusted to better accommodate these products, there are some “technical” issues concerning the safe and effective application of EO-based bioinsecticides.
Insecticides based on EOs or their constituents are commonly applied as fumigants, direct liquid sprays (in water or organic solvents), or granular formulations, mixed with various solid ingredients (talc, kaolin, clays, calcium carbonate, etc.), enabling the uniform spread of active compounds. The most-discussed constraint regards restraining the usage of these natural insecticides in common agricultural practices and is related to the volatility and limited persistence of EO under field conditions. This problem is enhanced by the lipophilic nature of most EO components and their inability to be fully dissolved in water to obtain a safe application. Due to high volatility, the efficacy of these substances falls short after EO application and pests reinvade the treated crop soon after the treatment, requiring frequent reapplication when used out of doors. This increases the plant material needed, which, together with high application rates (as high as 1% active ingredient), adds an additional challenge and elevates the production costs of this concept. Special attention should be given to the use of formulation ingredients that improve the stability and effectiveness of the biopesticide product, since it could be affected by air, light, and elevated temperatures [101]. These volatile substances are known to be susceptible to oxidative and polymerization reactions that can affect their properties and result in loss of activity. Therefore, nowadays, efforts are focused on the possibility of using innovative formulations for EO encapsulation that provide a controlled EO release, increasing the solubility, durability, bioavailability, and efficiency of EO, thus providing an optimal anti-insecticidal effect. In addition, reducing the dosage of pesticides and human exposure to them also represents a goal to be achieved. These innovative formulations include emulsions (nano- and microemulsion); nanoencapsulation technology, including inorganic nanomaterial (metal, metal oxide, nanoclays), lipid-based nanoformulations (liposomes, solid lipid nanoparticles); and polymer-based nanoformulations (nanocapsules, nanospheres, micelles, and nanogels).
Microemulsions (droplet size 100 to 400 nm) and nanoemulsions (<100 nm) are isotropic dispersions of two immiscible liquids, oil and water [102]. These two systems are different in terms of thermodynamic stability. Microemulsions are thermodynamically stable system dispersions formed spontaneously, but a lot depends on thermodynamic variables such as temperature and composition. Each one of the phases can exhibit very different geometries, such as liquid crystalline, bicontinuous structures, hexagonal, or spherical micelles [103,104]. Nanoemulsions are formulated using specific devices (like ultrasound generators or high-pressure homogenizers) able to supply enough energy to increase the water/oil interfacial area for generating submicronic droplets or by spontaneous emulsification without requiring any device, just mixing a lipophilic phase, into which a hydrophilic surfactant is solubilized to form a homogeneous liquid, and an aqueous phase, which can be pure water [103]. For nanoemulsion formulation, the crucial point is to first mix surfactants with the oily phase. There are four types of surfactants: cationic, anionic, amphoteric, and nonionic, bur for the formation of nanoemulsions for pesticide applications, nonionic surfactants are usually used. The kinetics of the destabilization of nanoemulsions is so slow (∼months) that they are considered kinetically stable. Micro- and nanoemulsions result in a larger surface area for release, and compared to their counterparts, they exhibited more effective accumulation and uptake of the active ingredients with additional greater protection against photodegradation. Nanoemulsion against Aedes aegypti L. using copaiba (Copaifera duckei Dwyer) oleoresin has been developed and classified as a promising insecticidal agent against Aedes aegypti L. larvae [105]. Duarte et al. [106] presented the larvicidal effect of nanoemulsion prepared with Rosmarinus officinalis L. essential oil on also against Aedes aegypti L. larvae. Essential oil of Eucalyptus globulus was used for nanoemulsion formation that exhibited insecticidal activity against Tribolium castaneum Herbst and Sitophilus oryzae L. [107,108]. Nanoemulsions of eight commercial essential oils (anise Pimpinella anisum L., artemisia Artemisia vulgaris L., fennel Foeniculum vulgare Mill., garlic Allium sativum L., lavender Lavandula angustifolia Mill., mint Mentha x piperita, rosemary Rosmarinus officinalis L., and sage Salvia officinalis L.) was formulated and showed pesticidal activity against Tribolium confusum Jacquelin du Val, a key stored product pest [109]. Citrus x sinensis essential oil-based nanoemulsion was developed and applied as an aerosol, which was efficient at controlling and repelling T. confusum Jacquelin du Val and Cryptolestes ferrugineus Stephens [110].
By combining EOs with nonorganic materials such as hydroxyapatite (Hap), titanium dioxide, and zinc oxide, the highly stable inorganic nanoparticles can be designed with a wide variety of sizes, structures, and geometries [111,112]. However, some nonorganic nanoparticles, like titanium dioxide, showed strong negative impacts on soil microbial function [113]. Gold and silver in the form of oxide or salt in the presence of EO are employed for metal nanoparticle formation [114,115]. Fennel EO was encapsulated in silica nanoparticles and assayed against the crop pest Spodoptera litura Fabricius and the dengue vector Aedes aegypti L. [116]. Nanoparticles of cinnamon oil encapsulated with silica tested against the sixth instar larvae of the rice moth (Corcyra cephalonica Stainton) decreased the pupation percentage and prevented pupae from emerging [117].
Lipid-based formulations are most specifically spherical particles consisting of a lipid bilayer surrounding an inner aqueous compartment. The most-used lipids for the formulations include glyceryl monostearate, precirol, stearic acid, and acetyl palmitate [118]. Lipid nanoparticles have beneficial properties such as good physiochemical storage stability, a non-toxic nature, a high loading capacity, feasibility, and a target-oriented release profile [119,120,121].
Different polymers have been suggested for the encapsulation of EOs to polymeric nanoparticles consisting of solid colloidal particles that conserve and protect EOs from outside aggression by physical or chemical interaction with a matrix, but also allow their sustained or delayed release at an optimal threshold in the environment [122,123]. In order to maximize the utilization efficiency of pesticides, controlled-release formulations are highly desirable. Biodegradable polymeric nanoparticles are environmentally friendly and do not result in the production of any harmful by-products [124,125].
Before application, the minimum and the maximum release rate must be determined concerning the efficiency and phytotoxicity report of the EO or its active agent. The polymers serve to encapsulate EO or its active ingredient through the formation of different morphological nano-range forms [126]. Starch and its derivates (dextrins, maltodextrins, cyclodextrins), chitin, alginates, and polyesters (e.g., polyethylene glycol) are usually used for the synthesis of polymeric nanoparticles containing EO [123,127,128,129,130]. Thus, the essential oil of Achillea millefolium L. encapsulated with chitosan showed long-term acaricidal effects against adult Tetranychus urticae Koch due to the slow and persistent release of the essential oil used [131]. Piper nigrum L. essential oil has been encapsulated in chitosan nanoparticles, enhancing the fumigant toxicity and altering the neurotransmitter acetylcholine in T. castaneum and S. oryzae [132].

7. Conclusions

Increasing bioinsecticide adoption has arisen partially due to increasing global food demand, but also increased awareness of food quality, biodiversity, and environmental safety. Although a plethora of reported insecticidal properties have promoted many plant-derived essential oils as potent bioinsecticides, only a handful of them have been registered and are available on regional or global markets. According to a comprehensive research literature survey and analysis of current market offers, production pathways that will likely be considered in the future include the use of EO complexes with potent neurotoxic activity encapsulated to provide a controlled release, increased solubility, durability, bioavailability, and efficiency. The intensive investigation of the insecticidal potential of plant scents should be transferred from the laboratory to real field conditions, new plant species must be taken into consideration and extensive farming practices have to be developed, standard techniques for EO blend isolation have to be upgraded, and all of these steps have to be accomplished with adopted clear registration policies and market regulations.

Author Contributions

All authors (N.D.; M.M.; J.S.) contributed equally to the conceptualization, writing, and visualization. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Ministry of Education, Science and Technological Development of the Republic of Serbia, grant number 451-03-68/2022-14/200007.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Moore, D. Blights, Rusts, Bunts, and Mycoses. In Slayers, Saviors, Servants and Sex; Springer: New York, NY, USA, 2001; pp. 19–37. [Google Scholar]
  2. Mercader, J. Mozambican grass seed consumption during the Middle Stone Age. Science 2009, 326, 1680–1683. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Zeder, A.M. The Origins of Agriculture in the Near East. Curr. Anthropol. 2011, 52, 221–235. [Google Scholar] [CrossRef] [Green Version]
  4. Food and Agriculture Organization of the United Nations; International Fund for Agricultural Development; World Food Programme; World Health Organization; The United Nations Children’s Fund. The State of Food Security and Nutrition in the World 2020. Transforming Food Systems for Affordable Healthy Diets; FAO: Rome, Italy, 2020. [Google Scholar]
  5. Boedeker, W.; Watts, M.; Clausing, P.; Marquez, E. The global distribution of acute unintentional pesticide poisoning: Estimations based on a systematic review. BMC Public Health 2020, 20, 1–9. [Google Scholar] [CrossRef] [PubMed]
  6. Carriger, J.F.; Rand, G.M.; Gardinali, P.R.; Perry, W.B.; Tompkins, M.S.; Fernandez, A.M. Pesticides of potential ecological concern in sediment from South Florida canals: An ecological risk prioritization for aquatic arthropods. Soil Sediment Contam. 2006, 15, 21–45. [Google Scholar] [CrossRef]
  7. Katagi, T.; Tanaka, H. Metabolism, bioaccumulation, and toxicity of pesticides in aquatic insect larvae. J. Pestic. Sci. 2016, 41, 25–37. [Google Scholar] [CrossRef] [Green Version]
  8. Tongo, I.; Onokpasa, A.; Emerure, F.; Balogun, P.T.; Enuneku, A.A.; Erhunmwunse, N.; Asemota, O.; Ogbomida, E.; Ogbeide, O.; Ezemonye, L. Levels, bioaccumulation and biomagnification of pesticide residues in a tropical freshwater food web. Int. J. Environ. Sci. Technol. 2022, 19, 1467–1482. [Google Scholar] [CrossRef]
  9. Koul, O.; Walia, S.; Dhaliwal, G.S. Essential oils as green pesticides: Potential and constraints. Biopestic. Int. 2008, 4, 63–84. [Google Scholar]
  10. Cingel, A.; Savić, J.; Lazarević, J.; Ćosić, T.; Raspor, M.; Smigocki, A.; Ninković, S. Extraordinary adaptive plasticity of Colorado potato beetle: “Ten-Striped Spearman” in the era of biotechnological warfare. Int. J. Mol. Sci. 2016, 17, 1538. [Google Scholar] [CrossRef]
  11. Bebber, D.P.; Ramotowski, M.A.T.; Gurr, S.J. Crop pests and pathogens move polewards in a warming world. Nat. Clim. Change 2013, 3, 985–988. [Google Scholar] [CrossRef]
  12. García-Lara, S.; Serna Saldivar, S.O. Insect Pests. In Encyclopedia of Food and Health; Caballero, B., Finglas, P.M., Toldrá, F., Eds.; Academic Press: London, UK, 2016; pp. 432–436. [Google Scholar]
  13. Willis, K.J. State of the World’s Plants 2017; Report; Royal Botanic Gardens: Kew, UK, 2017. [Google Scholar]
  14. Whalon, M.E.; Mota-Sanchez, D.; Hollingworth, R.M. Analysis of global pesticide resistance in arthropods. Glob. Pestic. Resist. Arthropods 2008, 5, 31. [Google Scholar]
  15. Bishop, B.A.; Grafius, E.J. Insecticide resistance in the Colorado potato beetle. Chrysomelidae Biol. 1996, 1, 355–377. [Google Scholar]
  16. Venette, R.C.; Hutchison, W.D. Invasive insect species: Global challenges, strategies & opportunities. Front. Insect Sci. 2021, 1, 650520. [Google Scholar]
  17. Bradshaw, C.J.; Leroy, B.; Bellard, C.; Roiz, D.; Albert, C.; Fournier, A.; Barbet-Massin, M.; Salles, J.M.; Simard, F.; Courchamp, F. Massive yet grossly underestimated global costs of invasive insects. Nat. Commun. 2016, 7, 1–8. [Google Scholar] [CrossRef]
  18. Lehmann, P.; Ammunét, T.; Barton, M.; Battisti, A.; Eigenbrode, S.D.; Jepsen, J.U.; Kalinkat, G.; Neuvonen, S.; Niemelä, P.; Terblanche, J.S.; et al. Complex responses of global insect pests to climate warming. Front. Ecol. Environ. 2020, 18, 141–150. [Google Scholar] [CrossRef] [Green Version]
  19. Deutsch, C.A.; Tewksbury, J.J.; Tigchelaar, M.; Battisti, D.S.; Merrill, S.C.; Huey, R.B.; Naylor, R.L. Increase in crop losses to insect pests in a warming climate. Science 2018, 361, 916–919. [Google Scholar] [CrossRef] [Green Version]
  20. Alyokhin, A.; Baker, M.; Mota-Sanchez, D.; Dively, G.; Grafius, E. Colorado Potato Beetle Resistance to Insecticides. Am. J. Potato Res. 2008, 85, 395–413. [Google Scholar] [CrossRef]
  21. Agosta, S.J. On ecological fitting, plant–insect associations, herbivore host shifts, and host plant selection. Oikos 2006, 114, 556–565. [Google Scholar] [CrossRef]
  22. Grapputo, A.; Boman, S.; Lindstroem, L.; Lyytinen, A.; Mappes, J. The voyage of an invasive species across continents: Genetic diversity of North American and European Colorado potato beetle populations. Mol. Ecol. 2005, 14, 4207–4219. [Google Scholar] [CrossRef]
  23. Weber, D. Colorado beetle: Pest on the move. Pestic. Outlook 2003, 14, 256–259. [Google Scholar] [CrossRef]
  24. Cingel, A.; Savić, J.; Vinterhalter, B.; Vinterhalter, D.; Kostić, M.; Šešlija Jovanović, D.; Smigocki, A.; Ninković, S. Growth and development of Colorado potato beetle larvae, Leptinotarsa decemlineata, on potato plants expressing the oryzacystatin II proteinase inhibitor. Transgenic Res. 2015, 24, 729–740. [Google Scholar] [CrossRef]
  25. Insecticides Market by Type (Pyrethroids, Organophosphorus, Carbamates, Organochlorine, Botanicals), Crop Type, Mode of Application, Formulation (WP, EC, SC, EW, ME, GR), and Region-Global Forecast to 2022. Available online: https://www.marketsandmarkets.com/Market-Reports/insecticide-market-142427569.html (accessed on 26 April 2020).
  26. Market Value of Bioinsecticides Worldwide in 2016 and 2020 with a Forecast for 2025. Available online: https://www.statista.com/statistics/1024754/market-value-bioinsecticides-globally/ (accessed on 26 April 2022).
  27. Johansen, C.A. Pesticides and pollinators. Annu. Rev. Entomol. 1977, 22, 177–192. [Google Scholar] [CrossRef] [Green Version]
  28. Copping, L.G.; Menn, J.J. Biopesticides: A review of their action, applications and efficacy. Pest Manag. Sci. 2000, 56, 651–676. [Google Scholar] [CrossRef]
  29. Pino, O.; Sánchez, Y.; Rojas, M.M. Plant secondary metabolites as an alternative in pest management. I: Background, research approaches and trends. Rev. Prot. Veg. 2013, 28, 81–89. [Google Scholar]
  30. Lima, P.S.A.; Santana, D.R.E.; Santos, C.C.A.; Silva, E.J.; Ribeiro, T.G.; Pinheiro, A.M.Í.; Santos, T.B.F.; Blank, F.A.; Araújo, A.P.A.; Bacci, L. Insecticide activity of botanical compounds against Spodoptera frugiperda and selectivity to the predatory bug Podisus nigrispinus. Crop Prot. 2020, 136, 105230. [Google Scholar] [CrossRef]
  31. Ma, S.; Jia, R.; Guo, M.; Qin, K.; Zhang, L. Insecticidal activity of essential oil from Cephalotaxus sinensis and its main components against various agricultural pests. Ind. Crops Prod. 2020, 150, 112403. [Google Scholar] [CrossRef]
  32. Ríos, N.; Stashenko, E.E.; Duque, J.E. Evaluation of the insecticidal activity of essential oils and their mixtures against Aedes aegypti (Diptera: Culicidae). Rev. Bras. Entomol. 2017, 61, 307–311. [Google Scholar] [CrossRef]
  33. Farag, M.A.; Ezzat, S.M.; Salama, M.M.; Tadros, M.G.; Serya, R.A. Anti-acetylcholinesterase activity of essential oils and their major constituents from four Ocimum species. Z Nat. C J. Biosci. 2016, 71, 393–402. [Google Scholar] [CrossRef]
  34. Mishra, B.B.; Tripathi, S.P.; Tripathi, C.P.M. Repellent effect of leaves essential oils from Eucalyptus globulus (Mirtaceae) and Ocimum basilicum (Lamiaceae) against two major stored grain insect pests of Coleopterons. Nat. Sci. 2012, 10, 50–54. [Google Scholar]
  35. Kiran, S.; Anupam, K.; Laluram, P.; Ramalakshmi, K.; Bhanu, P. Assessment of toxicity and biochemical mechanisms underlying the insecticidal activity of chemically characterized Boswellia carterii essential oil against insect pest of legume seeds. Pestic. Biochem. Phys. 2017, 139, 17–23. [Google Scholar]
  36. Ahmed, N.; Alam, M.; Saeed, M.; Ullah, H.; Iqbal, T.; Al-Mutairi, K.A.; Shahjeer, K.; Ullah, R.; Ahmed, S.; Ahmed, N.A.A.H.; et al. Botanical Insecticides Are a Non-Toxic Alternative to Conventional Pesticides in the Control of Insects and Pests. In Global Decline of Insects; El-Shafie, H., Ed.; IntechOpen: London, UK, 2021. [Google Scholar]
  37. Hummelbrunner, L.; Isman, M.B. Acute, Sublethal, Antifeedant, and Synergistic Effects of Monoterpenoid Essential Oil Compounds on the Tobacco Cutworm, Spodopteralitura (Lep., Noctuidae). J. Agric. Food Chem. 2001, 49, 715–720. [Google Scholar] [CrossRef]
  38. Hierro, I.; Valero, A.; Perez, P.; Gonzalez, P.; Cabo, M.; Montilla, P.; Navarro, C. Action of different monoterpenic compounds against Anisakis simplex L3 larvae. Phytomedicine 2004, 11, 77–82. [Google Scholar] [CrossRef] [PubMed]
  39. Ajayi, E.; Appel, G.; Fadamiro, Y. Fumigation toxicity of essential oil monoterpenes to Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae). J. Insects 2014, 2014, 917212. [Google Scholar] [CrossRef] [Green Version]
  40. Sadgrove, N.J.; Padilla-González, G.F.; Phumthum, M. Fundamental Chemistry of Essential Oils and Volatile Organic Compounds, Methods of Analysis and Authentication. Plants 2022, 11, 789. [Google Scholar] [CrossRef] [PubMed]
  41. Zhi-Jing, N.; Xin, W.; Yi, S.; Kiran, T.; Jinzhi, H.; Jian-Guo, Z.; Fei, H.; Zhao-Jun, W. Recent updates on the chemistry, bioactivities, mode of action, and industrial applications of plant essential oils. Trends Food Sci. Technol. 2021, 110, 78–89. [Google Scholar]
  42. Paes, J.L.; LRD’A, F.; Dhingra, O.D.; Cecon, P.R.; Silva, T.A. Insecticidal fumigant action of mustard essential oil against Sitophilus zeamais in maize grains. Crop Prot. 2012, 34, 56–58. [Google Scholar] [CrossRef]
  43. Koul, O.; Singh, R.; Kaur, B.; Kanda, D. Comparative study on the behavioral response and acute toxicity of some essential oil compounds and their binary mixtures to larvae of Helicoverpa armigera, Spodoptera litura and Chilo partellus. Ind. Crops Prod. 2013, 49, 428–436. [Google Scholar] [CrossRef]
  44. Shahriari, M.; Zibaee, A.; Sahebzadeh, N.; Shamakhi, L. Effects of α-pinene, trans-anethole, and thymol as the essential oil constituents on antioxidant system and acetylcholine esterase of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Pestic. Biochem. Phys. 2018, 150, 40–47. [Google Scholar] [CrossRef]
  45. Oliveira, A.P.; Santos, A.A.; Santana, A.S.; Lima, A.P.S.; Melo, C.R.; Santana, E.D.; Sampaio, T.S.; Blank, A.F.; Araújo, A.P.A.; Cristaldo, P.F.; et al. Essential oil of Lippia sidoides and its major compound thymol: Toxicity and walking response of populations of Sitophilus zeamais (Coleoptera: Curculionidae). Crop Prot. 2018, 112, 33–38. [Google Scholar] [CrossRef]
  46. Pavela, R.; Benelli, G.; Canale, A.; Maggi, F.; Mártonfi, P. Exploring essential oils of Slovak medicinal plants for insecticidal activity: The case of Thymus alternans and Teucrium montanum subsp. jailae. Food Chem.Toxicol. 2020, 138, 111203. [Google Scholar] [CrossRef]
  47. Demeter, S.; Lebbe, O.; Hecq, F.; Nicolis, S.C.; Kenne Kemene, T.; Martin, H.; Fauconnier, M.L.; Hance, T. Insecticidal Activity of 25 Essential Oils on the Stored Product Pest, Sitophilus granarius. Foods 2021, 10, 200. [Google Scholar] [CrossRef]
  48. Pavela, R.; Maggi, F.; Petrelli, R.; Cappellacci, L.; Buccioni, M.; Palmieri, A.; Canale, A.; Benelli, G. Outstanding insecticidal activity and sublethal effects of Carlina acaulis root essential oil on the housefly, Musca domestica, with insights on its toxicity on human cells. Food Chem. Toxicol. 2020, 136, 111037. [Google Scholar] [CrossRef]
  49. Butterworth, J.; Morgan, E. Isolation of a Substance that suppresses Feeding in Locusts. Chem. Comm. 1968, 1, 23. [Google Scholar] [CrossRef]
  50. Abdel-Shafy, S.; Zayed, A.A. In vitro acaricidal effect of plant extract of neem seed oil (Azadirachta indica) on egg, immature, and adult stages of Hyalomma anatolicum excavatum (Ixodoidea: Ixodidae). Vet. Parasitol. 2002, 106, 89–96. [Google Scholar] [CrossRef]
  51. Tavares, W.S.; Costa, M.A.; Cruz, I.; Silveira, R.D.; Serrão, J.E.; Zanuncio, J.C. Selective effects of natural and synthetic insecticides on mortality of Spodoptera frugiperda (Lepidoptera: Noctuidae) and its predator Eriopis connexa (Coleoptera: Coccinellidae). J. Environ. Sci. Health B. 2010, 45, 557–561. [Google Scholar] [CrossRef]
  52. Scudeler, E.L.; dos Santos, D.C. Effects of neem oil (Azadirachta indica A. Juss) on midgut cells of predatory larvae Ceraeochrysa claveri (Navás, 1911) (Neuroptera: Chrysopidae). Micron 2013, 44, 125–132. [Google Scholar] [CrossRef]
  53. Dubey, N.K.; Shukla, R.A.V.I.N.D.R.A.; Kumar, A.S.H.O.K.; Singh, P.; Prakash, B. Global scenario on the application of natural products in integrated pest management programmes. Nat. Prod. Plant Pest Manag. 2011, 1, 1–20. [Google Scholar]
  54. Wei-Hong, T.; Zhan-qian, S. Research on effect of four natural ultraviolet light absorbers on photostabilization of azadirachtin-A. Agric. Sci. China 2006, 5, 855–858. [Google Scholar]
  55. Chaudhary, S.; Kanwar, R.K.; Sehgal, A.; Cahill, D.M.; Barrow, C.J.; Sehgal, R.; Kanwar, J.R. Progress on Azadirachta indica based biopesticides in replacing synthetic toxic pesticides. Front. Plant Sci. 2017, 8, 610. [Google Scholar] [CrossRef]
  56. World Health Organization (WHO). Pesticide Evaluation Scheme, Vector Ecology and Management; World Health Organization: Geneva, Switzerland, 2016. [Google Scholar]
  57. Bradberry, S.M.; Cage, S.A.; Proudfoot, A.T.; Vale, J.A. Poisoning due to pyrethroids. Toxicol. Rev. 2005, 24, 93–106. [Google Scholar] [CrossRef]
  58. Ramchandra, A.M.; Chacko, B.; Victor, P.J. Pyrethroid Poisoning. Indian J. Crit. Care Med. 2019, 23, 267–271. [Google Scholar] [CrossRef]
  59. Ray, D.E.; Forshaw, P.J. Pyrethroid insecticides: Poisoning syndromes, synergies, and therapy. J. Toxicol. Clin. Toxicol. 2000, 38, 95–101. [Google Scholar] [CrossRef]
  60. Isman, M.B. Commercial development of plant essential oils and their constituents as active ingredients in bioinsecticides. Phytochem. Rev. 2020, 19, 235–241. [Google Scholar] [CrossRef]
  61. Sparks, T.C.; Nauen, R. IRAC: Mode of action classification and insecticide resistance management. Pestic. Biochem. Physiol. 2015, 121, 122–128. [Google Scholar] [CrossRef] [Green Version]
  62. Regnault-Roger, C.; Vincent, C.; Arnason, J.T. Essential oils in insect control: Low-risk products in a high-stakes world. Annu. Rev. Entomol. 2012, 57, 405–424. [Google Scholar] [CrossRef]
  63. War, A.R.; Paulraj, M.G.; Ahmad, T.; Buhroo, A.A.; Hussain, B.; Ignacimuthu, S.; Sharma, H.C. Mechanisms of plant defense against insect herbivores. Plant Signal. Behav. 2012, 7, 1306–1320. [Google Scholar] [CrossRef] [Green Version]
  64. Jensen, H.R.; Scott, I.M.; Sims, S.R.; Trudeau, V.L.; Arnason, J.T. The effect of a synergistic concentration of a Piper nigrum extract used in conjunction with pyrethrum upon gene expression in Drosophila melanogaster. Insect. Mol. Biol. 2006, 15, 329–339. [Google Scholar] [CrossRef]
  65. Guedes, R.N.C.; Smagghe, G.; Stark, J.D.; Desneux, N. Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu. Rev. Entomol. 2016, 61, 43–62. [Google Scholar] [CrossRef] [Green Version]
  66. Van Toor, R.F.; Foster, S.P.; Anstead, J.A.; Mitchinson, S.; Fenton, B.; Kasprowicz, L. Insecticide resistance and genetic composition of Myzus persicae (Hemiptera: Aphididae) on field potatoes in New Zealand. Crop Prot. 2008, 27, 236–247. [Google Scholar] [CrossRef]
  67. Casida, J.E.; Durkin, K.A. Neuroactive insecticides: Targets, selectivity, resistance, and secondary effects. Annu. Rev. Entomol. 2013, 58, 99–117. [Google Scholar] [CrossRef]
  68. Owokotomo, I.A.; Ekundayo, O.; Abayomi, T.G.; Chukwuka, A.V. In-vitro anti-cholinesterase activity of essential oil from four tropical medicinal plants. Toxicol. Rep. 2015, 2, 850–857. [Google Scholar] [CrossRef] [Green Version]
  69. Park, C.G.; Jang, M.; Yoon, K.A.; Kim, J. Insecticidal and acetylcholinesterase inhibitory activities of Lamiaceae plant essential oils and their major components against Drosophila suzukii (Diptera: Drosophilidae). Ind. Crop. Prod. 2016, 89, 507–513. [Google Scholar] [CrossRef]
  70. López, V.; Cascella, M.; Benelli, G.; Maggi, F.; Gómez-Rincón, C. Green drugs in the fight against Anisakis simplex—larvicidal activity and acetylcholinesterase inhibition of Origanum compactum essential oil. Parasitol. Res. 2018, 117, 861–867. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  71. da Silva Barbosa, D.C.; Holanda, V.N.; de Assis, C.R.D.; de Oliveira Farias, J.C.R.; Henrique doNascimento, P.; da Silva, W.V.; Navarro, D.M.D.A.F.; da Silva, M.V.; de Menezes Lima, V.L.; dos Santos Correia, M.T. Chemical composition and acetylcholinesterase inhibitory potential, in silico, of Myrciaria floribunda (H. West ex Willd.) O. Berg fruit peel essential oil. Ind. Crops Prod. 2020, 151, 112372. [Google Scholar] [CrossRef]
  72. Bhavya, M.L.; Obulaxmi, S.; Devi, S.S. Efficacy of Ocimum tenuiflorum essential oil as grain protectant against coleopteran beetle, infesting stored pulses. J. Food Sci. Technol. 2021, 58, 1611–1616. [Google Scholar] [CrossRef]
  73. Isman, M.B. Plant essential oils for pest and disease management. Crop Prot. 2000, 19, 603–608. [Google Scholar] [CrossRef]
  74. Miyazawa, M.; Yamafuji, C. Inhibition of acetylcholinesterase activity by bicyclic monoterpenoids. J. Agric. Food Chem. 2005, 53, 1765–1768. [Google Scholar] [CrossRef]
  75. Tong, F.; Gross, A.D.; Dolan, M.C.; Coats, J.R. The phenolic monoterpenoid carvacrol inhibits the binding of nicotine to the housefly nicotinic acetylcholine receptor. Pest Manag. Sci. 2013, 69, 775–780. [Google Scholar] [CrossRef] [Green Version]
  76. Bhavya, M.L.; Chandu, A.G.S.; Devi, S.S. Ocimum tenuiflorum oil, a potential insecticide against rice weevil with anti-acetylcholinesterase activity. Ind. Crops Prod. 2018, 126, 434–439. [Google Scholar] [CrossRef]
  77. Yeom, H.J.; Kang, J.S.; Kim, G.H.; Park, I.K. Insecticidal and acetylcholine esterase inhibition activity of Apiaceae plant essential oils and their constituents against adults of German cockroach (Blattella germanica). J. Agric. Food Chem. 2012, 60, 7194–7203. [Google Scholar] [CrossRef]
  78. Mills, C.; Cleary, B.V.; Walsh, J.J.; Gilmer, J.F. Inhibition of acetylcholinesterase by tea tree oil. J. Pharm. Pharmacol. 2004, 56, 375–379. [Google Scholar] [CrossRef]
  79. Patel, M.B.; Amin, D. Sphaeranthus indicus flower derived constituents exhibits synergistic effect against acetylcholinesterase and possess potential antiamnestic activity. J. Complement. Integr. Med. 2012, 9, 1. [Google Scholar] [CrossRef]
  80. Taylor, P.; Radić, Z. The cholinesterases: From genes to proteins. Annu. Rev. Pharmacol. Toxicol. 1994, 34, 281–320. [Google Scholar] [CrossRef]
  81. Yu, Z.; Wang, B.; Yang, F.; Sun, Q.; Yang, Z.; Zhu, L. Chemical compositionand anti-acetyl cholinesterase activity of flower essential oils of artemisiaannuaat different flowering stage. Iran. J. Pharm. Res. 2011, 10, 265. [Google Scholar]
  82. Savelev, S.; Okello, E.; Perry, N.S.L.; Wilkins, R.M.; Perry, E.K. Synergistic and antagonistic interactions of anticholinesterase terpenoids in Salvia lavandulaefolia essential oil. Pharmacol. Biochem. Behav. 2003, 75, 661–668. [Google Scholar] [CrossRef]
  83. Anderson, J.A.; Coats, J.R. Acetylcholinesterase inhibition by nootkatone and carvacrol in arthropods. Pestic. Biochem. Physiol. 2012, 102, 124–128. [Google Scholar] [CrossRef] [Green Version]
  84. Jankowska, M.; Rogalska, J.; Wyszkowska, J.; Stankiewicz, M. Molecular targets for components of essential oils in the insect nervous system—A review. Molecules 2017, 23, 34. [Google Scholar] [CrossRef] [Green Version]
  85. Raymond-Delpech, V.; Matsuda, K.; Sattelle, B.M.; Rauh, J.J.; Sattelle, D.B. Ion channels: Molecular targets of neuroactive insecticides. Invertebr. Neurosci. 2005, 5, 119–133. [Google Scholar] [CrossRef]
  86. Ashby, J.A.; McGonigle, I.V.; Price, K.L.; Cohen, N.; Comitani, F.; Dougherty, D.A.; Molteni, C.; Lummis, S.C. GABA binding to an insect GABA receptor: A molecular dynamics and mutagenesis study. Biophys. J. 2012, 103, 2071–2081. [Google Scholar] [CrossRef] [Green Version]
  87. Henderson, J.E.; Soderlund, D.M.; Knipple, D.C. Characterization of a putative γ-aminobutyric-acid (GABA) receptor β-subunit gene from Drosophila melanogaster. Biochem. Biophys. Res. Commun. 1993, 193, 474–482. [Google Scholar] [CrossRef]
  88. Tong, F.; Coats, J.R. Effects of monoterpenoid insecticides on [3H]-TBOB binding in house fly GABA receptor and 36Cl − uptakein American cockroach ventral nerve cord. Pestic. Biochem. Phys. 2010, 98, 317–324. [Google Scholar] [CrossRef]
  89. Höld, K.M.; Sirisoma, N.S.; Ikeda, T.; Narahashi, T.; Casida, J.E. α-Thujone (the active component of absinthe): γ-aminobutyric acid type A receptor modulation and metabolic detoxification. Proc. Natl. Acad. Sci. USA 2000, 97, 3826–3831. [Google Scholar] [CrossRef] [Green Version]
  90. Zhou, C.; Rao, Y.; Rao, Y. A subset of octopaminergic neurons are important for Drosophila aggression. Nat. Neurosci. 2008, 11, 1059–1067. [Google Scholar] [CrossRef]
  91. Evans, P.D. Multiple receptor types for octopamine in the locust. J. Physiol. Lond. 1981, 318, 99–122. [Google Scholar] [CrossRef] [Green Version]
  92. Roeder, T. A new octopamine receptor class in locust nervous tissue, the octopamine 3 (OA3) receptor. Life Sci. 1992, 50, 21–28. [Google Scholar] [CrossRef]
  93. Evans, P.D. A modulatory octopaminergic neurone increases cyclic nucleotide levels in locust skeletal muscle. J. Physiol. 1984, 348, 307–324. [Google Scholar] [CrossRef] [Green Version]
  94. Nathanson, J.A. Octopamine receptors, adenosine 3′, 5′-monophosphate, and neural control of firefly flashing. Science 1979, 203, 65–68. [Google Scholar] [CrossRef]
  95. Bodnarky, R.P. Cyclic nucleotides. In Endocrinology of Insects; Downer, R.G., Laufer, H., Eds.; Alan R. Liss. Inc.: New York, NY, USA, 1983; pp. 567–614. [Google Scholar]
  96. Enan, E. Insecticidal activity of essential oils: Octopaminergic sites of action. Comp. Biochem. Physiol. Part-C Toxicol. Pharmacol. 2001, 130, 325–337. [Google Scholar] [CrossRef]
  97. Enan, E.E. Molecular and pharmacological analysis of an octopamine receptor from American cockroach and fruit fly in response to plant essential oils. Arch. Insect Biochem. Physiol. 2005, 59, 161–171. [Google Scholar] [CrossRef]
  98. Kostyukovsky, M.; Rafaeli, A.; Gileadi, C.; Demchenko, N.; Shaaya, E. Activation of octopaminergic receptors by essential oil constituents isolated from aromatic plants: Possible mode of action against insect pests. Pest Manag. Sci. 2002, 58, 1101–1106. [Google Scholar] [CrossRef]
  99. Price, D.N.; Berry, M.S. Comparison of effects of octopamine and insecticidal essential oils on activity in the nerve cord, foregut, and dorsal unpaired median neurons of cockroaches. J. Insect Physiol. 2006, 52, 309–319. [Google Scholar] [CrossRef]
  100. Tripathi, A.K.; Upadhyay, S. Repellent and insecticidal activities of Hyptis suaveolens (Lamiaceae) leaf essential oil against four stored-grain coleopteran pests. Int. J. Trop. Insect. Sci. 2009, 29, 219–228. [Google Scholar] [CrossRef]
  101. Turek, C.; Stintzing, F.C. Stability of essential oils: A review. Compr. Rev. Food Sci. Food Saf. 2013, 12, 40–53. [Google Scholar] [CrossRef]
  102. Seng, K.K.; Loong, W.V. Introductory Chapter: From Microemulsions to Nanoemulsions. In Nanoemulsions-Properties, Fabrications and Applications; Koh, K.S., Wong, V.L., Eds.; IntechOpen: London, UK, 2019. [Google Scholar]
  103. Anton, N.; Vandamme, T.F. Nano-emulsions and micro-emulsions: Clarifications of the critical differences. Pharm. Res. 2011, 28, 978–985. [Google Scholar] [CrossRef] [PubMed]
  104. Cimino, C.; Maurel, O.M.; Musumeci, T.; Bonaccorso, A.; Drago, F.; Souto, E.M.B.; Pignatello, R.; Carbone, C. Essential Oils: Pharmaceutical Applications and Encapsulation Strategies into Lipid-Based Delivery Systems. Pharmaceutics 2021, 13, 327. [Google Scholar] [CrossRef]
  105. Rodrigues, C.R.; Ferreira, A.M.; Vilhena, J.C.E.; Almeida, F.B.; Cruz, R.A.S.; Florentino, A.C.; Souto, R.N.P. Development of a larvicidal nanoemulsion with Copaiba (Copaifera duckei) oleoresin. Rev. Bras. Farmacogn. 2014, 24, 699–705. [Google Scholar] [CrossRef] [Green Version]
  106. Duarte, J.L.; Amado, J.R.; Oliveira, A.E.; Cruz, R.A.; Ferreira, A.M.; Souto, R.N.; Falcão, D.Q.; Carvalho, J.C.; Fernandes, C.P. Evaluation of larvicidal activity of a nanoemulsion of Rosmarinus officinalis essential oil. Rev. Bras. Farmacogn. 2015, 25, 189–192. [Google Scholar] [CrossRef] [Green Version]
  107. Pant, M.; Dubey, S.; Patanjali, P.K.; Naik, S.N.; Sharma, S. Insecticidal activity of eucalyptus oil nanoemulsion with karanja and jatropha aqueous filtrates. Int. Biodeterior. Biodegrad. 2014, 91, 119–127. [Google Scholar] [CrossRef]
  108. Adak, T.; Barik, N.; Patil, N.B.; Govindharaj, G.P.P.; Gadratagi, B.G.; Annamalai, M.; Mukherjee, A.K.; Rath, P.C. Nanoemulsion of eucalyptus oil: An alternative to synthetic pesticides against two major storage insects Sitophilus oryzae (L.) and Tribolium castaneum (Herbst)) of rice. Ind. Crops Prod. 2020, 143, 111849. [Google Scholar] [CrossRef]
  109. Yasur, J.; Rani, P.U. Lepidopteran insect susceptibility to silver nanoparticles and measurement of changes in their growth, development and physiology. Chemosphere 2015, 124, 92–102. [Google Scholar] [CrossRef]
  110. Giunti, G.; Palermo, D.; Laudani, F.; Algeri, G.M.; Campolo, O.; Palmeri, V. Repellence and acute toxicity of a nano-emulsion of sweet orange essential oil toward two major stored grain insect pests. Ind. Crops Prod. 2019, 142, 111869. [Google Scholar] [CrossRef]
  111. Alizadeh-Sani, M.; Mohammadian, E.; McClements, D.J. Eco-friendly active packaging consisting of nanostructured biopolymer matrix reinforced with TiO2 and essential oil: Application for preservation of refrigerated meat. Food Chem. 2020, 322, 126782. [Google Scholar] [CrossRef]
  112. Mizielinska, M.; Nawrotek, P.; Stachurska, X.; Ordon, M.; Bartkowiak, A. Packaging covered with antiviral and antibacterial coatings based on ZnO nanoparticles supplemented with geraniol and carvacrol. Int. J. Mol. Sci. 2021, 22, 1717. [Google Scholar] [CrossRef]
  113. Simonin, M.; Richaume, A.; Guyonnet, J.P.; Dubost, A.; Martins, J.M.F.; Pommier, T. Titanium dioxide nanoparticles strongly impact soil microbial function by affecting archaeal nitrifiers. Sci. Rep. 2016, 6, 33643. [Google Scholar] [CrossRef]
  114. Jabir, M.S.; Taha, A.A.; Sahib, U.I. Linalool loaded on glutathione-modified gold nanoparticles: A drug delivery system for a successful antimicrobial therapy. Artif. Cells Nanomed. Biotechnol. 2018, 46, 345–355. [Google Scholar] [CrossRef]
  115. Aldosary, S.K.; El-Rahman, S.N.A.; Al-Jameel, S.S.; Alromihi, N.M. Antioxidant and antimicrobial activities of Thymus vulgaris essential oil contained and synthesis thymus (Vulgaris) silver nanoparticles. Braz. J. Biol. 2021, 83, e244675. [Google Scholar] [CrossRef]
  116. Suresh, U.; Murugan, K.; Panneerselvam, C.; Cianfaglione, K.; Wang, L.; Maggi, F. Encapsulation of sea fennel (Crithmum maritimum) essential oil in nanoemulsion and SiO2 nanoparticles for treatment of the crop pest Spodoptera litura and the dengue vector Aedes aegypti. Ind. Crops Prod. 2020, 158, 113033. [Google Scholar] [CrossRef]
  117. Attia, R.G.; Rizk, S.A.; Hussein, M.A.; Fattah, H.M.A.; Khalil, M.; Ma’Moun, S.A. Effect of cinnamon oil encapsulated with silica nanoparticles on some biological and biochemical aspects of the rice moth, Corcyra cephalonica (Staint.) (Lepidoptera: Pyralidae). Ann. Agric. Sci. 2020, 65, 1–5. [Google Scholar] [CrossRef]
  118. Mitchell, M.J.; Billingsley, M.M.; Haley, R.M.; Wechsler, M.E.; Peppas, N.A.; Langer, R. Engineering precision nanoparticles for drug delivery. Nat. Rev. Drug Discov. 2021, 20, 101–124. [Google Scholar] [CrossRef]
  119. Nguyen, H.M.; Hwang, I.-C.; Park, J.-W.; Park, H.-J. Photoprotection for deltamethrin using chitosan-coated beeswax solid lipid nanoparticles. Pest. Manag. Sci. 2012, 68, 1062–1068. [Google Scholar] [CrossRef]
  120. Lin, L.; Cui, H.; Zhou, H.; Zhang, X.; Bortolini, C.; Chen, M.; Liu, L.; Dong, M. Nanoliposomes containing Eucalyptus citriodora as antibiotic with specific antimicrobial activity. Chem. Comm. 2015, 51, 2653–2655. [Google Scholar] [CrossRef]
  121. Pan, Y.; Tikekar, R.V.; Nitin, N. Distribution of a model bioactive within solid lipid nanoparticles and nanostructured lipid carriers influences its loading efficiency and oxidative stability. Int. J. Pharm. 2016, 511, 322–330. [Google Scholar] [CrossRef] [Green Version]
  122. Nair, R.; Varghese, S.H.; Nair, B.G.; Maekawa, T.; Yoshida, Y.; Kumar, D.S. Nanoparticulate material delivery to plants. Plant Sci. 2010, 179, 154–163. [Google Scholar] [CrossRef]
  123. Lopez, M.D.; Maudhuit, A.; Pascual-Villalobos, M.J.; Poncelet, D. Development of formulations to improve the controlled-release of linalool to be applied as an insecticide. J. Agric. Food Chem. 2012, 60, 1187–1192. [Google Scholar] [CrossRef]
  124. Kumar, S.; Bhanjana, G.; Sharma, A.; Dilbaghi, N.; Sidhu, M.C.; Kim, K.H. Development of nanoformulation approaches for the control of weeds. Sci. Total Environ. 2017, 586, 1272–1278. [Google Scholar] [CrossRef]
  125. Ramasamy, T.; Ruttala, H.B.; Gupta, B.; Poudel, B.K.; Choi, H.G.; Yong, C.S.; Kim, J.O. Smart chemistry-based nanosized drug delivery systems for systemic applications: A comprehensive review. J. Control. Release 2017, 258, 226–253. [Google Scholar] [CrossRef]
  126. Perlatti, B.; Bergo, P.L.d.S.; Silva, M.F.d.G.F.d.; Fernandes, J.B.; Forim, M.R. Polymeric nanoparticle-based insecticides: A controlled release purpose for agrochemicals. In Insecticides−Development of Safer and More Effective Technologies; Trdan, S., Ed.; Intech Open Access Publisher: London, UK, 2013; pp. 523–550. [Google Scholar]
  127. Kulkarni, A.R.; Soppimath, K.S.; Aminabhavi, T.M.; Dave, A.M.; Mehta, M.H. Glutaraldehyde crosslinked sodium alginate beads containing liquid pesticide for soil application. J. Control. Release 2000, 63, 97–105. [Google Scholar] [CrossRef]
  128. Ye, Z.; Guo, J.; Wu, D.; Tan, M.; Xiong, X.; Yin, Y.; He, G. Photo-responsive shell cross-linked micelles based on carboxymethyl chitosan and their application in controlled release of pesticide. Carbohydr. Polym. 2015, 132, 520–528. [Google Scholar] [CrossRef]
  129. Vishwakarma, G.S.; Gautam, N.; Babu, J.N.; Mittal, S.; Jaitak, V. Polymeric encapsulates of essential oils and their constituents: A review of preparation techniques, characterization, and sustainable release mechanisms. Polym. Rev. 2016, 56, 668–701. [Google Scholar] [CrossRef]
  130. Campos, E.V.R.; Proença, P.L.F.; Oliveira, J.L.; Melville, C.C.; Vechia, J.F.D.; de Andrade, D.J.; Fraceto, L.F. Chitosan nanoparticles functionalized with β-cyclodextrin: A promising carrier for botanical pesticides. Sci. Rep. 2018, 8, 2067. [Google Scholar] [CrossRef]
  131. Ahmadi, Z.; Saber, M.; Bagheri, M.; Mahdavinia, G.R. Achillea millefolium essential oil and chitosan nanocapsules with enhanced activity against Tetranychus urticae. J. Pest Sci. 2018, 91, 837–848. [Google Scholar] [CrossRef]
  132. Rajkumar, V.; Gunasekaran, C.; Dharmaraj, J.; Chinnaraj, P.; Paul, C.A.; Kanithachristy, I. Structural characterization of chitosan nanoparticle loaded with Piper nigrum essential oil for biological efficacy against the stored grain pest control. Pestic. Biochem. Physiol. 2020, 166, 104566. [Google Scholar] [CrossRef] [PubMed]
Sustainability 14 06847 g001 550
Figure 1. Advantages of plant-derived insecticides over chemical insecticides.
Figure 1. Advantages of plant-derived insecticides over chemical insecticides.
Sustainability 14 06847 g001
Sustainability 14 06847 g002 550
Figure 2. Neurotoxic mechanism of essential oil EO-based bioinsecticide by inhibiting the acetylcholinesterase (AChE) activity and preventing the hydrolysis of acetylcholine (Ach) molecules that bind to nicotinic acetylcholine receptors (nAChr).
Figure 2. Neurotoxic mechanism of essential oil EO-based bioinsecticide by inhibiting the acetylcholinesterase (AChE) activity and preventing the hydrolysis of acetylcholine (Ach) molecules that bind to nicotinic acetylcholine receptors (nAChr).
Sustainability 14 06847 g002
Table
Table 1. Essential oils and their major constituents with insecticidal activity.
Table 1. Essential oils and their major constituents with insecticidal activity.
Plant SpeciesInsectsMajor EO
Constituents		Lethal (LC50) and Inhibition * (IC50 *) ConcentrationsRef. No
Cephalotaxus sinensisMegoura japonicaα-Pinene8.82 mg/L
6.74 mg/L
7.35 mg/L
3.57 mg/L		[31]
Plutella xylostellaβ-Caryophyllene
Sitophilus zeamaisGermacrene D
Brassica nigraSitophilus zeamaisAllyl isothiocyanate6.19 µL/L (larvae)
7.01 µL/L (adults)		[42]
/ Thymol189.7; 28.5; 290.8 µg/larva
462.4; 85.5; 431.5 µg/larva
412.1; 126.6; 406.8 µg/larva
409.7; 64.3; 378.6 µg/larva
550.3; 55.7; 414.7 µg/larva		 [43]
Chilo partellusLinalool
Spodoptera litura1,8-Cineole
Helicoverpa armigeratrans-Anethole
Carvacrol
/Ephestia kuehniellaα-Pinene0.864 μL/mL *
0.490 μL/mL *
0.137 μL/mL *		[44]
trans-Anethole
Thymol
Lippia sidoidesSitophilus zeamaisEO mix35.48 to 118.29 μL/L air[45]
Thymol65.00 to 91.23 μL/L air
p-Cymene801.24 to 2188.83 μL/L air
Thymus vulgarisAedes aegyptiThymol,
p-Cymene		45.73 mg/mL[32]
Salvia officinalis1,8-Cineol,
α-Thujone		76.43 mg/mL
Lippia origanoidesLimonene,
p-Cymene,
α-Phellandrene		53.79 mg/mL
Eucalyptus globulusThymol,
p-Cymene		92.55 mg/mL
Cymbopogon nardus1,8-Cineol75.85 mg/mL
Cymbopogon martiniiCitronellal, Citronellol,
Geraniol		114.65 mg/mL
Lippia albaGeraniol72.34 mg/mL
Pelargonium graveolensCarrvone,
Limonene,
Citronellol		108.96 mg/mL
Thymus
alternans		 (E)-Nerolidol,
Linalool,
Germacrene D		156.3 mg/L
103.7 mg/L
221.1 mg/L		[46]
Spodoptera littoralis,
Musca domestica,
Culex quinquefasciatus
Teucrium
montanum
subsp. jailae		 Germacrene D,
(E)-Caryophyllene		56.7 mg/L
154.9 mg/L
180.5 mg/L
Allium sativum Diallyl disulfide,
Diallyl trisulfide		0.64%
Cumimum cyminum Cuminaldehyde
γ-Terpinene,
p-Cymene		3.05%
Eucalyptus citriodora β-Pinene2.98%
Eucalyptus dives Citronellal2.03%
Gaultheria procumbens Piperitone,
α-Phellandrene
Methyl salicylate		1.59%
Illicum verum trans-Anethole3.02%
Lavandulla hybrida super Linalool,
Linalyl acetate		3.41%
Melaleuca alternifolia Terpinene-4-ol,
γ-Terpinene		2.86%
Mentha arvensis Menthol2.27%
Myristica fragransSitophilus granariesα-Pinene,
α-Thujene,
Sabinene,
β-Pinene		3.40%[47]
Ocimum bassilicum spp. basilicum Estragol,
Linalool		3.14%
Ocimum sanctum Eugenol,
β-Caryophyllene,
Methyl eugenol		1.77%
Origanum majorana α-Pinene,
1,8-Cineole, Camphor,
Camphene		3.04%
Rosmarinus officinalis CT camphor α-Pinene,
1,8-Cineole, Camphor,
Camphene		3.72%
Thymus vulgaris CT geraniol Geraniol,
Geranyl acetate		2.90%
Carlina
acaulis root		Musca domesticaCarlina oxide2.74 µL (male)
5.96 µL (female)		[48]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Devrnja, N.; Milutinović, M.; Savić, J. When Scent Becomes a Weapon—Plant Essential Oils as Potent Bioinsecticides. Sustainability 2022, 14, 6847. https://doi.org/10.3390/su14116847

AMA Style

Devrnja N, Milutinović M, Savić J. When Scent Becomes a Weapon—Plant Essential Oils as Potent Bioinsecticides. Sustainability. 2022; 14(11):6847. https://doi.org/10.3390/su14116847

Chicago/Turabian Style

Devrnja, Nina, Milica Milutinović, and Jelena Savić. 2022. "When Scent Becomes a Weapon—Plant Essential Oils as Potent Bioinsecticides" Sustainability 14, no. 11: 6847. https://doi.org/10.3390/su14116847

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop