Abstract
Pesticides are widely used in producing food to control pests. However, it has been determined that synthetic pesticides present severe toxicity (residual), while they also result in environmental contamination and development of high-level resistance in some insect species. Due to this, some of these susbtances have been banned or restricted in many countries, which has reduced the number of agrochemicals that can be used for pest control, particularly in the case of crops exported to green markets such as Europe and Asia. Under this scenario, essential oils (EOs) are being increasingly studied as bioinsecticides because they are renewable, natural, biodegradable, non-persistent in the environment and safe to non-target organism and humans. It has been determined that EOs have repellent, ovicidal, larvicidal, and insecticidal effects against different types of pests, but they also have some drawbacks due to their high volatility and low aqueous solubility. This mini-review focusses on EOs used as bioinsecticides for the control of Curculionidae and on current stabilization techniques, such as nanoencapsulation, to prolog the biocidal effect of EOs against these pests.
Introduction
Curculionids (Curculionidae), known as weevils, are a family of herbivorous phytophagous coleopterans. Some species of weevil are harmful to agriculture, affecting plantations and stored products (Tewari et al., 2014). The life cycle of this pest passes through the stages of egg, larva, pupa, and adult (Fiaboe et al., 2012). When they are in the larval stage, they attack plantations, causing damage to the neck and crown of the plants (Espinoza et al., 2018). Adults have a mouthpart with powerful jaws that allow them to consume the laminae of leaves, shoots, twigs, and fruits, causing deep gouges in lignified tissues of trees and woody shrubs (Espinoza et al., 2016). Some subspecies of this group are classified as quarantine pests requiring phytosanitary treatments to ensure that exported products are free of these pests.
Insect damage on Brassica (Brassica napus L, Brassica oleracea var. botrytis, Brassica olearaceae var. capitata) crops ranges from 10 to 90%, with an average of 35 to 45% (Pavela, 2016), varying significantly depending on the type of pest and crop, climatic conditions, and incidence of natural enemies (Grzywacz et al., 2014). Even though traditional methods used to control pests with synthetic insecticides have successfully counteracted such damage, their use and excessive application have harmed human health and the environment (Nicolopoulou-Stamati et al., 2016). Because of this, some synthetic insecticides have been banned or their use has been restricted and regulated, with maximum residue limits (MRLs) being lowered in some countries. As a result, producers have higher costs, while their products may not have access to some international markets (Rodriguez-Saona et al., 2019; Wahab et al., 2022). Under this scenario, the need to reduce or replace the use of synthetic insecticides with natural products has led to the search for eco-friendly methods of pest control. In recent years, essential oils (EOs) have gained popularity because they are readily available in different plants, and they also present low toxicity for mammals and high degradation patterns.
EOs have been tested as botanical insecticides against a wide range of pests that attack crops such as lettuce, coffee, soybean, cereal grains, legumes, and maize. (Boulogne et al., 2012; Menossi et al., 2021). Carvacrol, linalool, alpha-pinene, menthol, cinnamaldehyde, eugenol, 1-8 cineole, geraniol, and limonene are some of the components of EOs that have shown insecticidal activity against different pests (Regnault-Roger et al., 2012; de Oliveira et al., 2014; Singh et al., 2021). However, the main disadvantage of EOs is that they are highly volatile and susceptible to degradation by factors such as moisture, light, or air (Menossi et al., 2021). In this sense, nanoencapsulation can improve the effectiveness and stability of EOs, preventing fast volatilization and degradation.
This mini-review focusses on EOs used as bioinsecticides for the control of Curculionidae and on current encapsulation techniques to prolong the biocidal effect of EOs against these pests.
Pests
Globally, the Curculionidae is the largest family of insects, with about 60,000 species (Anderson, 2002), but not all of them are considered pests. In terms of natural pest control, only a limited number of these species has been managed using EOs.
The most important Curculionidae pests are described in Table 1. Sitophilus zeamais, commonly known as corn weevil or rice weevil, is one of the most important pests that attack grains and stored seeds, resulting in both quantitative and qualitative losses (Romani et al., 2019). Larvae and adults cause the most significant damage, affecting nutritional levels, weight loss, taste, odor, and decrease in the germination capacity of the grains such as wheat, rice, sorghum, maize, and others (Patiño-Bayona et al., 2021b). Sitophilus zeamais and Sitophilus oryzae are very closely related species that are difficult to differentiate, and thus morphological or DNA tests are required (Moon, 2015). Sitophilus oryzae is also one of the most destructive pests of grains, causing weight loss and affecting the nutritional value of grains, and finally resulting in significant economic losses (Maazoun et al., 2017).
Table 1
| Species | Common name | Affected crops | References |
|---|---|---|---|
| Rhynchophorus ferrugineus | Red palm weevil | Palm trees | (Mazza et al., 2014) |
| Rhynchophorus palmarum | Black palm weevil | Coconut palm | (Hoddle et al., 2020) |
| Sitophilus oryzae | Rice weevil | Seeds | (Wu and Yan, 2018) |
| Sitophilus zeamais | Maize weevil | Maize | |
| Sitophilus granarius | Rice weevil | Rice | (Lemic et al., 2020) |
| Aegorhinus superciliosus | Raspberry weevil | Berries | (Zavala et al., 2011) |
| Aegorhinus nodipennis | Fruit weevil | Hazelnut | |
| Diocalandra frumenti | Coconut weevil | Coconut | (Vacas et al., 2017) |
| Cosmopolites sordidus Germar | Banana corm weevil | Banana | (Alpizar et al., 2012) |
| Diaprepes abbreviates | Root weevil | Citrus fruits | (Lapointe et al., 2012) |
| Sitona lineatus | Pea leaf weevil | Leguminous | (Vankosky et al., 2011) |
| Sternechus subsignatus | Soybean stalk weevil | Soybean | (Socías et al., 2014) |
| Heilipus lauri | Avocado seed weevil | Avocado | (Romero-Frías et al., 2019) |
| Rhabdoscelus obscurus | Sugarcane weevil | Sugar Cane | (Reddy et al., 2011) |
| Scyphophorus acupunctatus | Agave weevil | Agaves | (Cuervo-Parra et al., 2019) |
| Hypothenemus hampei | Coffe berry borer | Coffe | (Ruiz-Diaz and Rodrigues, 2021) |
| Sternochetus Mangiferae | Mango seed weevil | Mango | (Abdulla et al., 2016) |
| Euscepes postfasciatus | West Indian sweet potato weevil | Potato | (Okada et al., 2014) |
| Cylas formicarius Elegantulus | Sweet potato weevil | Potato | |
| Anthonomus grandis grandis Boheman | Boll weevil | Cotton | (Burbano-Figueroa et al., 2021) |
| Anthonomus eugenii Cano | Pepper weevil | Pepper | (Rossini et al., 2020) |
| Anthonomus musculus Say | Cranberry weevil | Blueberry, Cranberry | (Szendrei et al., 2011) |
| Anthonomus rubi Herbst | Strawberry blossom weevil | Strawberry | (Tonina et al., 2021) |
Important Cuculionidae pests (Tewari et al., 2014; Barkai-Golan and Follett, 2017; Bandeira et al., 2021).
Sitophilus granarius or wheat weevil attacks stored grains, also causing significant damage. Unfortunately, this insect is difficult to detect, and once it has infested a facility, all stored products must be destroyed (Plata-Rueda et al., 2018). The most effective control method for this type of pest, which specifically attacks stored products, is fumigation (Abdelgaleil et al., 2016).
Rhynchophorus ferrugineus, known as the red palm weevil, attacks coconut, date, and oil palm crops, resulting in significant damage (Antony et al., 2016). The larva is the most damaging stage of the pest, specifically attacking the heart of the palm, where it can live between 25 and 105 days before turning into a pupa. When the damage caused by the pest is visible, it means that the palm tree is already critically infested with high population levels, resulting in palm trees being felled and transported to a safe place to prevent further propagation (Al Dawsari Mona, 2020). Adults do not cause the highest level of damage, but they can fly 900 m in a single flight and travel up to 7 km, infesting quickly (Fiaboe et al., 2012).
Other important curculinoid pests are Aegorhinus superciliosus and Aegorhinus nodipennis, which mainly attack hazelnut, blueberry, and raspberry plantations. These pests are found mainly in Chile and Argentina (Espinoza et al., 2016). The larval stage of both Aegorhinus species causes damage to the collar or crown of plants, causing premature reddening, yellowing, reduction of new twigs, and even death of plants when the attack is severe. Adults have mouthparts with powerful mandibles that allow them to consume leaf laminae, shoots, twigs, and fruits, causing deep gouges in lignified tissues of trees and woody shrubs (Tampe et al., 2015; Tampe et al., 2016; Tampe et al., 2020).
There is litte information on the use of EOs for the control of Hylastinus obscurus, Hypothenemus hampei, Listronotus oregonesis, and Xylosandrus germanus, known as ambrosia beetles. The most common exotic ambrosia beetle is Xylosandrus germanus, attacking ornamental nursery plants. Unlike other pests, X. germanus bores holes to cultivate the fungus Ambrosiella grosmanniae, which serves as food for larvae and adults (Ranger et al., 2011; Ranger et al., 2012; Galko et al., 2018). On the other hand, Hylastinus obscurus, significantly affects red clover yields (Parra et al., 2013; Quiroz et al., 2017; Espinoza et al., 2018). Hypothenemus hampei reduces coffee production and compromises the quality of stored coffee beans (Reyes et al., 2019). In fact, H.hampei attacks coffee plantations, ovipositing inside coffee berries or stored green coffee so that larvae feed on them. Finally, Listronotus oregonesis, or carrot weevil, causes damage to Apiaceae (parsley, carrot, celery, and dill) plantations since larvae feed on their roots, reducing crop yield by up to 50% (Gagnon et al., 2021).
Essential Oils for Curculionidae Pest Control
EOs are aromatic and volatile substances with an oily consistency. They are extracted from different plant parts (leaf, stem, flower, bark and fruit) using conventional methods such as hydrodistillation, steam distillation, dry distillation, or environmentally friendly methods like supercritical fluid extraction, microwave-assisted extraction, ultrasound-assisted extraction, and others (Regnault-Roger et al., 2012; Boukroufa et al., 2015). EOs are mainly composed of terpenoids and phenylpropanoids, which provide them with unique properties (antioxidant, antibacterial, and insecticidal), and can therefore be applied in areas such as pharmaceuticals, food and agriculture (Pavela, 2015; Plata-Rueda et al., 2018).
Research on the use of EOs as insecticides has increased considerably because sustainable agriculture has gained great acceptance, while preference to organic or ecological crops is increasingly becoming popular worldwide. On the other hand, the FDA (Food and Drug Administration) of the United States has recognized that EOs are safer than synthetic insecticides (Hikal et al., 2017). Given the interest in EOs, several research studies have shown that EOs have repellent, insecticidal, ovicidal, and growth inhibitory effects (Hikal et al., 2017; Ikbal and Pavela, 2019; Isman, 2020; Chaudhari et al., 2021). Insecticidal activity can be evaluated by methods such as: a) fumigation, in which EOs can be absorbed, ingested, or inhaled; b) contact, in which EOs should penetrate the cuticle of the insects; and c) ingestion (Nenaah, 2014; de Lira et al., 2015).
One of the essential oils that excels in controlling a wide range of insects of the Curculionidae family is eugenol, which is extracted from cloves, nutmeg, and cinnamon. Contact toxicity tests against different curculionids, such as S. zeamais (Gonzales Correa et al., 2015) and S. granarius (Plata-Rueda et al., 2018), have reported lethal concentrations to eliminate 50% (LC50) of insects of 0.69 (µL/cm²) for cinnamon against S. zeamais, and 2.765 (µL/mL) for eugenol against S. granarius. Furthermore, its contact and fumigant toxicity has also been studied against S. oryzae (rice weevil), where two LC50 were reported; 0.376 (µL/cm²) and 963.3 (µL/L) of Ocimum tenuiflorum oil (eugenol is the major component of this oil) (Bhavya et al., 2018). On the other hand, a study conducted by Al Dawsari Mona (2020) determined that the application of 0.7 mL of clove essential oil extract (high concentration of eugenol) and 7 mg of clove powder caused 100% of mortality in the R. ferrugineus pest, on the first and third day of exposure, respectively.
The presence of α-pinene in the composition of different essential oils allows for insecticidal effects. The α-pinene is found in more significant quantities in plants such as: Azilia eryngioides (Apiaceae, endemic to Iran), accounting for 63.8% (Ebadollahi and Mahboubi, 2011); Hypericum myricariifolium (found in high mountain regions of the Andes in Central and South America), accounting for 45.52% (Patiño-Bayona et al., 2021b); Cupressus sempervirens (Mediterranean cypress), accounting for 37.88% (Abdelgaleil et al., 2016); and Rosmarinus officinalis, accounting 23.52% of the total composition. Ebadollahi and Mahboubi (2011) determined that the essential oil of A. eryngioides presented a toxic fumigant activity against S. granarius in the adult stage, with an LC50 of 20.05 (µL/L) (Ebadollahi and Mahboubi, 2011). Patiño-Bayona et al. (2021b) found that H. myricariifolium essential oil showed fumigant toxicity against adult Sitophilus zeamais with an LC50 of 463.1 (µL/L) The essential oil of C. lusitanica showed contact toxicity against Sitophilus zeamais in the adult stage, reaching a mortality rate of 59.2% at a concentration of 2% v/w (Bett et al., 2016).
Limonene is an essential oil that has also been studied for pest control. It comes from citrus species such as Citrus sinensis, Citrus lemon, Citrus aurantifolia, and Citrus reticulata, as well as other plants such as Aegle marmelos (originally from Asia) and Lippia alba (Mishra et al., 2013; Abdelgaleil et al., 2016; Fouad and da Camara, 2017; Patiño-Bayona et al., 2021a). A study on its insecticidal activity against adults of S. zeamais (Fouad and da Camara, 2017) showed that the oil of C. reticulata had a lower mean lethal concentration than that of C. aurantifolia, which recorded values of 51.29 µL/mL, 1.52 µL/g and 41.92 µL/L in the air when tested for toxicity by contact, ingestion, and fumigant effects, respectively. Table 2 shows the most recent studies related to the effectiveness of EOs against Curculionidae pests.
Table 2
| Essential Oils | Major constituents | Mode of toxicity | LC50 | Target Curculionidae | State | References |
|---|---|---|---|---|---|---|
| Illicium pachyphyllum | trans-ρ-mentha-1(7),8-dien-2-ol | Fumigant | 11.49 mg/L | Sitophilus zeamais | Adult | (Liu et al., 2012) |
| Contact | 17.33 µg/adult | Adult | ||||
| Lippia alba | Limonene | Fumigant | 254.1 (µL/L) | Sitophilus zeamais | Adult | (Patiño-Bayona et al., 2021a) |
| R. officinalis | 1,8-Cineole, α-Pinene | 243.7 (µL/L) | ||||
| H. mexicanum | nonane | 223.5 (µL/L) | ||||
| Eucalyptus sp | 1,8-cineole | 184.3 (µL/L) | ||||
| Laurelia sempervirens | undetermined | Contact | 2.3 (mL/kg) | Sitophilus zeamais | Adult | (Torres et al., 2014) |
| Fumigant | 177 (µL/L air) | |||||
| Alpinia purpurata | β-pinene, α-Pinene | Fumigant | 41.4 (µL/L air) | Sitophilus zeamais | Adult | (de Lira et al., 2015) |
| Lippia alba | Carvone | Contact | 15.2 (µL/mL) | Sitophilus zeamais | Adult | (Peixoto et al., 2015) |
| Citral | 16.7 (µL/mL) | |||||
| Clove | Eugenol | Contact | 0.45 (µL/cm²) | Sitophilus zeamais | Adult | (Gonzales Correa et al., 2015) |
| Cinnamon | Eugenol | 0.69 (µL/cm²) | ||||
| Pimenta pseudocaryophyllus | Chavibetol | Contact | 1522 (mg/kg) | Sitophilus zeamais | Adult | (Ribeiro et al., 2015) |
| Cupressus lusitanica | Umbellulone, α-pinene, sabinene, limonene | Contact | 0.21 (%v/w) | Sitophilus zeamais | Adult | (Bett et al., 2016) |
| Fumigant | 29.11 (µL/L air) | |||||
| Eucalyptus saligna | 1,8-Cineole, α-Pinene | Contact | 17.0 (%v/w) | |||
| Fumigant | 26.85 (µL/L air) | |||||
| Ocimum basilicum | Linalool, Methylchavicol | Fumigant | 26.59 (µL/L air) | Sitophilus zeamais | Adult | (de Araújo et al., 2017) |
| Piper hispidinervum | Safrole | 7.42 (µL/L air) | ||||
| Citrus aurantifolia | (S)-Limonene | Contact | 71.18 (µL/mL) | Sitophilus zeamais | Adult | (Fouad and da Camara, 2017) |
| Fumigant | 58.51 (µL/L air) | |||||
| Ingestion | 2.75 (µL/g) | |||||
| Citrus reticulata | (R)-Limonene | Contact | 51.29 (µL/mL) | |||
| Fumigant | 41.92 (µL/L air) | |||||
| Ingestion | 1.52 (µL/g) | |||||
| Lippia sidoides (NFs) | Thymol | Contact | 26,44 (μg/mg) | Sitophilus zeamais | Adult | (Oliveira et al., 2017) |
| Lippia sidoides | Thymol | Contact | 7.10 (μg/mg) | Sitophilus zeamais | Adult | |
| Mustard | Allyl isothiocyanate (AITC) | Fumigant | 4.03 (µL/L) | Sitophilus zeamais | Adult | (de Souza et al., 2018) |
| Lippia sidoides | thymol and ρ-cymene | Fumigant | 86.55 (μL/L air) | Sitophilus zeamais | Adult | (Oliveira et al., 2018) |
| Cupressus sempervirens | α-pinene | Contact | 13.394 ppm | Sitophilus zeamais | Adult | (Langsi et al., 2020) |
| Fumigant | 1.402 ppm | |||||
| 3-carene | Contact | 6.348 ppm | ||||
| Fumigant | 0.610 ppm | |||||
| Hypericum mexicanum | n-nonane | Fumigant | 223.5 (µL/L) | Sitophilus zeamais | Adult | (Patiño-Bayona et al., 2021b) |
| Hypericum myricariifolium | α-pinene | 463.1 (µL/L) | ||||
| Ocimum basilicum | Linalool and estragole | Fumigant | 25.4 (µL/L air) | Sitophilus zeamais | Adult | (Moura et al., 2021) |
| Lavandula dentata | eucalyptol | Fumigant | 26.9 (µL/L air) | Sitophilus zeamais | Adult | (Wagner et al., 2021) |
| Syzygium aromaticum | Eugenol | Fumigant | 17.326 (µL/2 cm²) | Sitophilus oryzae | Adult | (Mishra et al., 2013) |
| Aegle marmelos | Limonene | 18.488 (µL/2 cm²) | ||||
| Origanum vulgare | Pulegone | Fumigant | 1.64 (mg/L air) | Sitophilus oryzae | Adult | (Abdelgaleil et al., 2016) |
| Contact | 0.11 (mg/cm²) | |||||
| Citrus lemon | Limonene | Fumigant | 9.89 (mg/L air) | |||
| Contact | 0.20 (mg/cm²) | |||||
| Callistemon viminals | 1,8-Cineole | Fumigant | 16.17 (mg/L air) | |||
| Contact | 0.09 (mg/cm²) | |||||
| Cupressus sempervirens | α-Pinene | Fumigant | 17.16 (mg/L air) | |||
| Contact | 0.6 (mg/cm²) | |||||
| Citrus sinensis | Limonene | Fumigant | 19.65 (mg/L air) | |||
| Contact | 0.27 (mg/cm²) | |||||
| Mentha piperita | Menthol | Fumigant | 299.51 (µL/L air) | Sitophilus oryzae | Adult | (Khani et al., 2017) |
| Rosmarinus officinalis | α-pinene | 115.63 (µL/L air) | ||||
| Hyssopus officinalis | cis-pinocamphone | 78.16 (µL/L air) | ||||
| Ocimum tenuiflorum | Eugenol | Fumigant | 963.3 (µL/L) | Sitophilus oryzae | Adult | (Bhavya et al., 2018) |
| Contact | 0.376 (µL/cm²) | |||||
| Agave americana | undetermined | Contact | 8.99 (μg/cm²) | Sitophilus oryzae | Adult | (Maazoun et al., 2019) |
| Mentha piperita | menthone | Fumigant | 3.79 (µL/L) | Sitophilus oryzae | Adult | (Mackled et al., 2019) |
| Contact | 0.036 (mg/cm²) | |||||
| Pinus roxburghii | longifolene | Fumigant | 21.31 (µL/L) | |||
| Contact | 0.076 (mg/cm²) | |||||
| Rosa | methyl eugenol | Fumigant | >100 (µL/L) | |||
| Contact | 0.52 (mg/cm²) | |||||
| Melaleuca bracteata | methyl eugenol | Contact | 20.4 (μg/adult) | Sitophilus oryzae | Adult | (Zhang et al., 2021) |
| Cinnamon | eugenol, trans-3-caren-2-ol and benzyl benzoate | Contact | 13.80 (w/v) | Sitophilus granarius | Adult | (Plata-Rueda et al., 2018) |
| Clove | eugenol and caryophyllene | 11.95 (w/v) | ||||
| Comercial | Eugenol | 2.765 (µL/mL) | ||||
| Caryophyllene oxide | 2.784 (µL/mL) | |||||
| α-pineno | 4.235 (µL/mL) | |||||
| Humulus lupulus | undetermined | Contact | 16.17 (µg/adult) | Sitophilus granarius | Adult | (Paventi et al., 2021) |
| Piper nigrum | piperine | Ingestion | 342.62 (mg/l) | Rhynchophorus ferrugineus | Larval | (Hussain et al., 2017) |
| Thymus vulgaris | p- cimeno | Contac | 11.4 (µg/mL) | Rhynchophorus ferrugineus | Larval | (Darrag et al., 2021) |
| 1032 (µL/mL) | Adult | |||||
| Ocimum basilicum | thymol | 14.6 (µg/mL) | Larval | |||
| 1246 (µL/mL) | Adult | |||||
| Eucalyptus resinifera | 1.8-cineole | Fumigant | 64.72 (μL/L) | Hypothenemus hampei | Adult | (Reyes et al., 2019) |
Current research on the effectiveness of EOs against Curculionidae pests.
Modes of Action: Insecticidal Essential Oils
The modes of action (insecticidal effects) of EOs against curculionidae have not been fully described. In general terms, it has been described that EOs inhibit some physiological functions of gamma-aminobutyric acid (GABA) receptors, which is the primary inhibitory neurotransmitter of the central nervous system of insects (Tampe et al., 2015). It has also been determined that plant metabolites can inhibit the actions of acetylcholinesterase (AChE), which hydrolyzes acetylcholine, a neurotransmitter responsible for signal transmission in the central nervous system (López and Pascual-Villalobos, 2010). Bhavya et al. (2018) analyzed the effect of eugenol and Ocimum tenuiflorum essential oil on AChE activity in S. oryzae (in vivo), and reported that eugenol reaches a higher percentage of AChE inhibition after two hours, while both EOs inhibit approximately 40% of AChE only after 4 h of contact. These values are related to the high insecticidal activity of eugenol and O. tenuiflorum since inhibiting AChE produces neurotoxic effects against S. oryzae, which finally results in the death of the pest (Bhavya et al., 2018).
Another neurotransmitter affected by EOs is octopamine. This substance acts as a neurohormone and neuromodulator, which means that it is involved in several biological processes (Pavela and Benelli, 2016; Upadhyay et al., 2018; Chaudhari et al., 2021). This effect was analyzed by Plata-Rueda et al. (2018), who determined that eugenol, α-pinene, α-humulene, and α-phellandrene produce muscle contractions in the legs and abdomen of the insect, along with an impairment in locomotor behavior associated with the fact that these EOs would cause blockage of octopamine receptor binding sites, which would be related to a modulatory influence on the nervous-muscular system (Plata-Rueda et al., 2018). Furthermore, this neurotoxic effect is responsible for the rapid death of S. granarius when in contact with EOs above mentioned.
Hussain et al. (2017) analyzed the insecticidal activity of Piper nigrum extract against R. ferrugineus, and determined that piperine, which is the main component of the extract, increased the expression of the cytochrome P450 gene, being responsible for the metabolism leading to the release of toxins in insects. Furthermore, when piperine was used in the diet of R. ferrugineus larvae, cytochrome P450 expression increased 35-fold, resulting in larval death within six days when using a concentration of 500 mg/L of piperine (Hussain et al., 2017).
Encapsulation for Prolonged Effect
Essential oil-based insecticides have several advantages and have proven effective against some Curculionidae species, but they are highly volatile under certain environmental conditions of temperature and pressure conditions. Nanoencapsulation is one of the techniques that can help solve this problem. Nanoencapsulation is based on encapsulating EOs in materials that have some of their dimensions in the nanometer range (between 1-100 nm), including nanoemulsions, lipid nanomaterials, polymeric nanoparticles, and clay nanomaterials (Kumar et al., 2019; Chaudhari et al., 2021; Esmaili et al., 2021).
Nanoemulsions
A nanoemulsion is produced when two phases are mixed, water in oil (W/O) or oil in water (O/W). To properly stabilize these mixtures, surfactants are used to reduce the surface tension between water and oil. It should be noted that O/W nanoemulsions are used to encapsulate EOs (Singh et al., 2017; Heydari et al., 2020; Mohd Narawi et al., 2020). The nanometric size of the droplets produced allows them to have physical stability over time, as it protects EOs from environmental factors.
Nanoemulsions are obtained by two types of techniques: a) high-energy methods and b) low-energy methods. Both techniques are expected to obtain a monomodal droplet size distribution (Espitia et al., 2019). High-energy methods use mechanical devices, which use disruptive forces to obtain smaller droplets; their disadvantages are the high acquisition values of each device and the temperature increases associated with the friction generated by the emulsions. Some of the equipment used include ultrasonic, high-pressure valve homogenization (HPVH), and microfluidization (Sneha and Kumar, 2021). Low-energy methods include phase inversion composition (PIC), phase inversion temperature (PIT), solvent displacement, emulsion inversion point (EIP), bubble bursting, and spontaneous nanoemulsion, which is the most commonly used method to encapsulate EOs (Kupikowska-Stobba and Kasprzak, 2021).
The use of EOs-based nanoemulsions for Curculionidae control has been analyzed in two studies in the literature. Adak et al. (2020) reported 100% and 80% mortality rates for eucalyptus nanoemulsion and eucalyptus oil against Sitophilus oryzae (adult) at a concentration of 1.5 µL/cm2 (Adak et al., 2020). Oliveira et al. (2017) analyzed the lethal time (LT50) of thymol nanoemulsion and thymol oil against Sitophilus zeamais populations from Maracaju. They found an LT50 of 47.5 hours for thymol nanoemulsion versus an LT50 of 26.3 hours for thymol oil (Oliveira et al., 2017). Both studies reported that EO-based nanoemulsions resulted in higher insecticidal activity compared to oils, while mortality rates were maintained over time.
Polymeric Nanoparticles
Polymeric nanoparticles can be obtained using biodegradable polymers (obtained from renewable resources) or synthetic polymers, also working with a blend of polymers. Some of the most used polymers are chitosan, pectin, cellulose, alginate, cyclodextrin, starch, polycaprolactone, and polyethylene glycol (Esmaili et al., 2021; Ramachandraiah and Hong, 2021). Biodegradable polymers from renewable resources are inexpensive and readily available in nature (Campos et al., 2015).
EOs can be encapsulated in different forms in the polymer (Figure 1). For example, they can be adsorbed on the nanoparticle’s surface, coupled to the nanoparticle via linkers, encapsulated by a hydrophilic or hydrophobic polymer shell, or trapped in a polymer matrix (Kumar et al., 2019). In addition, polymeric nanoparticles can be obtained by electrospray, supercritical fluid, solvent evaporation, ionotropic gelation, nanoprecipitation, and salinization (Sagiri et al., 2016; George et al., 2019).
Figure 1
Unfortunately, there are no reports of essential oils encapsulated in polymeric nanoparticles evaluated against Curculionidae. However, the efficiency of polymeric nanoparticles-EOs against other pests has been demonstrated. For instance, Werdin González et al. (2014) determined that polyethylene glycol (PEG) 6000 nanoparticles can stabilize geranium or bergamot EOs, as their volatility and degradation were significantly decreased. The obtained results demonstrated that only 25% of the encapsulated EOs were volatilized in a 6-month-period. Furthermore, PEG-EOs nanoparticles may control and effectively release the oil against Tribolium castaneum and Rhizopertha dominica, since their toxicity by contact increased from 4 weeks to 24 weeks (Werdin González et al., 2014). de Oliveira et al. (2019) evaluated the effect of nanoparticles of zein containing blends of the EOs–geraniol, -eugenol, and -cinnamaldehyde against Chrysodeixis includes and Tetranychus urticae. Nanoencapsulation prevented a decrease in acute toxicity and the rapid degradation of EOs, while it also increased the effectiveness against the target pest over 120 days (de Oliveira et al., 2019). These results demonstrate the potentiality of the polymeric nanoparticles to improve the effectiveness of EOs, highlighting the need for further research on Curculionidae pests.
Clay Nanomaterials
Nanoclays are nanoparticles with a high specific surface area and ion exchange capacity, which enables them to change their nature from hydrophobic to hydrophilic or vice versa, while they are also economically viable and biocompatible (de Oliveira et al., 2022). Furthermore, most clays are lamellar aggregates, with the presence of interlamellar cations (Na+), which allow ion exchange to make clays more compatible with EOs, facilitating their adsorption and then controlling their release through the “tortuous path” produced by the clay lamellae and by the interactions that occur (Garrido-Miranda et al., 2018). Furthermore, surfactants such as ammonium salts are used to alter the hydrophobicity of clays, which change the net charge of the solid, facilitating the interaction between molecular species such as EOs, and increasing the interlaminar space (Brito et al., 2018). Finally, montmorillonite and kaolinite are the most commonly used clays for encapsulating EOs as insecticides (Goletti et al., 2015). An example of this is the encapsulation of Ocimum gratissimum in montmorillonite. This formulation resulted in S. zeamais moratality rates of 100% in the first days and 75% after 30 days, proving the effectiveness of clays in the gradual release of EOs (Nguemtchouin et al., 2013).
Conclusion
Essential oils have a great potential as natural insecticides against curculionids or other species. In fact, they can play an important role in pest management and organic farming because they do not generate toxic residues and are environmentally friendly. The disadvantages they present, which are related to their high volatibility and degradation, can be minimized by using current encapsulation methods. Therefore, future research should focus on determining how encapsulation of EOs or mixtures of EOs can increase the effectiveness in controlling different life stages of pests under changing environmental conditions.
Funding
Projects ANID/FONDECYT/POSTDOCTORAL 3220459, 3210599, FONDEF ID21I10050, and a postdoctoral scholarship from the Universidad de La Frontera.
Publisher’s Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Statements
Author contributions
KG-M: Writing - original draft - review & editing. JG: Writing - review & editing. MS: Writing - review & editing. All authors contributed to the article and approved the submitted version.
Conflict of interest
The authors declare that the mini-review was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.
References
1
AbdelgaleilS. A. M.MohamedM. I. E.ShawirM. S.Abou-TalebH. K. (2016). Chemical Composition, Insecticidal and Biochemical Effects of Essential Oils of Different Plant Species From Northern Egypt on the Rice Weevil, Sitophilus Oryzae L. J. Pest Sci.89, 219–229. doi: 10.1007/s10340-015-0665-z
2
AbdullaN. R.RwegasiraG. M.JensenK. M. V.MwatawalaM. W.OffenbergJ. (2016). Control of Mango Seed Weevils (Sternochetus Mangiferae) Using the African Weaver Ant (Oecophylla Longinoda Latreille) (Hymenoptera: Formicidae). J. Appl. Entomol.140, 500–506. doi: 10.1111/jen.12260
3
AdakT.BarikN.PatilN. B.GovindharajG. P. P.GadratagiB. G.AnnamalaiM.et al. (2020). 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.143, 111849. doi: 10.1016/j.indcrop.2019.111849
4
Al Dawsari MonaM. (2020). Insecticidal Potential of Cardamom and Clove Extracts on Adult Red Palm Weevil Rhynchophorus Ferrugineus. Saudi. J. Biol. Sci.27, 195–201. doi: 10.1016/j.sjbs.2019.07.009
5
AlpizarD.FallasM.OehlschlagerA. C.GonzalezL. M. (2012). Management of Cosmopolites Sordidus and Metamasius Hemipterus in Banana by Pheromone-Based Mass Trapping. J. Chem. Ecol.38, 245–252. doi: 10.1007/S10886-012-0091-0/FIGURES/6
6
AndersonR. S. (2002). “Family 131 Curculionidae Latreille 1802,” in American Beetles, Volume II Polyphaga: Scarabaeoidea Through Curculionoidea. Eds. ArnettR. J.ThomasM. C.SkelleyP. E.FrankJ. H. (Boca Raton: CRC Press), 722–815.
7
AntonyB.SoffanA.JakšeJ.AbdelazimM. M.AldosariS. A.AldawoodA. S.et al. (2016). Identification of the Genes Involved in Odorant Reception and Detection in the Palm Weevil Rhynchophorus Ferrugineus, an Important Quarantine Pest, by Antennal Transcriptome Analysis. BMC Genomics17, 69. doi: 10.1186/s12864-016-2362-6
8
BandeiraP. T.FávaroC. F.FranckeW.BergmannJ.ZarbinP. H. G. (2021). Aggregation Pheromones of Weevils (Coleoptera: Curculionidae): Advances in the Identification and Potential Uses in Semiochemical-Based Pest Management Strategies. J. Chem. Ecol.47, 968–986. doi: 10.1007/s10886-021-01319-1
9
Barkai-GolanR.FollettP. A. (2017). “Phytosanitary Irradiation: Generic Treatments,” in Irradiation for Quality Improvement, Microbial Safety and Phytosanitation of Fresh Produce, 191–206. doi: 10.1016/b978-0-12-811025-6.00011-2
10
BettP. K.DengA. L.OgendoJ. O.KariukiS. T.Kamatenesi-MugishaM.MihaleJ. M.et al. (2016). Chemical Composition of Cupressus Lusitanica and Eucalyptus Saligna Leaf Essential Oils and Bioactivity Against Major Insect Pests of Stored Food Grains. Ind. Crops Prod.82, 51–62. doi: 10.1016/j.indcrop.2015.12.009
11
BhavyaM. L.ChanduA. G. S.DeviS. S. (2018). Ocimum Tenuiflorum Oil, a Potential Insecticide Against Rice Weevil With Anti-Acetylcholinesterase Activity. Ind. Crops Prod.126, 434–439. doi: 10.1016/j.indcrop.2018.10.043
12
BoukroufaM.BoutekedjiretC.PetignyL.RakotomanomanaN.ChematF. (2015). Bio-Refinery of Orange Peels Waste: A New Concept Based on Integrated Green and Solvent Free Extraction Processes Using Ultrasound and Microwave Techniques to Obtain Essential Oil, Polyphenols and Pectin. Ultrason. Sonochem.24, 72–79. doi: 10.1016/j.ultsonch.2014.11.015
13
BoulogneI.PetitP.Ozier-LafontaineH.DesfontainesL.Loranger-MercirisG. (2012). Insecticidal and Antifungal Chemicals Produced by Plants: A Review. Environ. Chem. Lett.10, 325–347. doi: 10.1007/s10311-012-0359-1
14
BritoD. F.Da Silva FilhoE. C.FonsecaM. G.JaberM. (2018). Organophilic Bentonites Obtained by Microwave Heating as Adsorbents for Anionic Dyes. J. Environ. Chem. Eng.6, 7080–7090. doi: 10.1016/j.jece.2018.11.006
15
Burbano-FigueroaO.Sierra-MonroyA.Grandett MartinezL.BorgemeisterC.LuedelingE. (2021). Management of the Boll Weevil (Coleoptera: Curculionidae) in the Colombian Caribbean: A Conceptual Model. J. Integr. Pest Manage.12, 1–14. doi: 10.1093/jipm/pmab009
16
CamposE. V. R.de OliveiraJ. L.FracetoL. F.SinghB. (2015). Polysaccharides as Safer Release Systems for Agrochemicals. Agron. Sustain. Dev.35, 47–66. doi: 10.1007/s13593-014-0263-0
17
ChaudhariA. K.SinghV. K.KediaA.DasS.DubeyN. K. (2021). Essential Oils and Their Bioactive Compounds as Eco-Friendly Novel Green Pesticides for Management of Storage Insect Pests: Prospects and Retrospects. Environ. Sci. Pollut. Res.28, 18918–18940. doi: 10.1007/S11356-021-12841-W
18
Cuervo-ParraJ. A.Pérez-EspañaV. H.PérezP. A. L.Morales-OvandoM. A.Arce-CervantesO.Aparicio-BurgosJ. E.et al. (2019). Scyphophorus Acupunctatus (Coleoptera: Dryophthoridae): A Weevil Threatening the Production of Agave in Mexico. Florida Entomol.102, 1–9. doi: 10.1653/024.102.0101
19
DarragH. M.AlhajhojM. R.KhalilH. E. (2021). Bio-Insecticide of Thymus Vulgaris and Ocimum Basilicum Extract From Cell Suspensions and Their Inhibitory Effect Against Serine, Cysteine, and Metalloproteinases of the Red Palm Weevil (Rhynchophorus Ferrugineus). Insects12, 405. doi: 10.3390/insects12050405
20
de AraújoA. M. N.FaroniL. R. D.de OliveiraJ. V.do Amaral Ferraz NavarroD. M.E Silva BarbosaD. R.BredaM. O.et al. (2017). Lethal and Sublethal Responses of Sitophilus Zeamais Populations to Essential Oils. J. Pest Sci. (2004).90, 589–600. doi: 10.1007/s10340-016-0822-z
21
de LiraC. S.PontualE. V.de AlbuquerqueL. P.PaivaL. M.PaivaP. M. G.de OliveiraJ. V.et al. (2015). Evaluation of the Toxicity of Essential Oil From Alpinia Purpurata Inflorescences to Sitophilus Zeamais (Maize Weevil). Crop Prot.71, 95–100. doi: 10.1016/j.cropro.2015.02.004
22
de OliveiraJ. L.CamposE. V. R.BakshiM.AbhilashP. C.FracetoL. F. (2014). Application of Nanotechnology for the Encapsulation of Botanical Insecticides for Sustainable Agriculture: Prospects and Promises. Biotechnol. Adv.32, 1550–1561. doi: 10.1016/j.biotechadv.2014.10.010
23
de OliveiraJ. L.CamposE. V. R.Germano-CostaT.LimaR.VechiaJ. F.Della, SoaresS. T.et al. (2019). Association of Zein Nanoparticles With Botanical Compounds for Effective Pest Control Systems. Pest Manage. Sci.75, 1855–1865. doi: 10.1002/ps.5338
24
de OliveiraL. H.TrigueiroP.SouzaJ. S. N.de CarvalhoM. S.OsajimaJ. A.da Silva-FilhoE. C.et al. (2022). Montmorillonite With Essential Oils as Antimicrobial Agents, Packaging, Repellents, and Insecticides: An Overview. Colloids. Surfaces. B. Biointerfaces.209, 112186. doi: 10.1016/j.colsurfb.2021.112186
25
de SouzaL. P.FaroniL. R. D.LopesL. M.de SousaA. H.PratesL. H. F. (2018). Toxicity and Sublethal Effects of Allyl Isothiocyanate to Sitophilus Zeamais on Population Development and Walking Behavior. J. Pest Sci. (2004).91, 761–770. doi: 10.1007/s10340-017-0950-0
26
EbadollahiA.MahboubiM. (2011). Insecticidal Activity of the Essential Oil Isolated From Azilia Eryngioides (PAU) Hedge Et Lamond Against Two Beetle Pests. Chil. J. Agric. Res.71, 406–411. doi: 10.4067/s0718-58392011000300010
27
EsmailiF.Sanei-DehkordiA.AmoozegarF.OsanlooM. (2021). A Review on the Use of Essential Oil-Based Nanoformulations in Control of Mosquitoes. Bioointerface. Res. Appl. Chem.11, 12516–12529. doi: 10.33263/BRIAC115.1251612529
28
EspinozaJ.UrzúaA.BardehleL.QuirozA.EcheverríaJ.González-TeuberM. (2018). Antifeedant Effects of Essential Oil, Extracts, and Isolated Sesquiterpenes From Pilgerodendron Uviferum (D. Don) Florin Heartwood on Red Clover Borer Hylastinus Obscurus (Coleoptera: Curculionidae). Molecules23, 1282. doi: 10.3390/molecules23061282
29
EspinozaJ.UrzúaA.TampeJ.ParraL.QuirozA. (2016). Repellent Activity of the Essential Oil From the Heartwood of Pilgerodendron Uviferum (D. Don) Florin Against Aegorhinus Superciliosus (Coleoptera: Curculionidae). Molecules21, 1–7. doi: 10.3390/molecules21040533
30
EspitiaP. J. P.FuenmayorC. A.OtoniC. G. (2019). Nanoemulsions: Synthesis, Characterization, and Application in Bio-Based Active Food Packaging. Compr. Rev. Food Sci. Food Saf.18, 264–285. doi: 10.1111/1541-4337.12405
31
FiaboeK. K. M.PetersonA. T.KairoM. T. K.RodaA. L. (2012). Predicting the Potential Worldwide Distribution of the Red Palm Weevil Rhynchophorus Ferrugineus (Olivier) (Coleoptera: Curculionidae) Using Ecological Niche Modeling. Florida Entomol.95, 659–673. doi: 10.1653/024.095.0317
32
FouadH. A.da CamaraC. A. G. (2017). Chemical Composition and Bioactivity of Peel Oils From Citrus Aurantiifolia and Citrus Reticulata and Enantiomers of Their Major Constituent Against Sitophilus Zeamais (Coleoptera: Curculionidae). J. Stored. Prod. Res.73, 30–36. doi: 10.1016/j.jspr.2017.06.001
33
GagnonA.È.BoivinG.BlattS. (2021). Response of Carrot Weevil (Listronotus Oregonensis) to Different Host-Plant Essential Oils. Crop Prot.149, 105763. doi: 10.1016/j.cropro.2021.105763
34
GalkoJ.DzurenkoM.RangerC. M.KulfanJ.KulaE.NikolovC.et al. (2018). Distribution, Habitat Preference, and Management of the Invasive Ambrosia Beetle Xylosandrus Germanus (Coleoptera: Curculionidae, Scolytinae) in European Forests With an Emphasis on the West Carpathians. Forests10, 10. doi: 10.3390/f10010010
35
Garrido-MirandaK. A.RivasB. L.Pérez -RiveraM. A.SanfuentesE. A.Peña-FarfalC. (2018). Antioxidant and Antifungal Effects of Eugenol Incorporated in Bionanocomposites of Poly(3-Hydroxybutyrate)-Thermoplastic Starch. LWT. - Food Sci. Technol.98, 260–267. doi: 10.1016/j.lwt.2018.08.046
36
GeorgeJ.AzadL. B.PouloseA. M.AnY.SarmahA. K. (2019). Nano-Mechanical Behaviour of Biochar-Starch Polymer Composite: Investigation Through Advanced Dynamic Atomic Force Microscopy. Compos. Part A. Appl. Sci. Manuf.124, 105486. doi: 10.1016/j.compositesa.2019.105486
37
GolettiM.NguemtchouinM.NgassoumM. B.KamgaR.DeabateS.LagergeS.et al. (2015). Characterization of Inorganic and Organic Clay Modified Materials: An Approach for Adsorption of an Insecticidal Terpenic Compound. Appl. Clay. Sci. J.104, 110–118. doi: 10.1016/j.clay.2014.11.016
38
Gonzales CorreaY. D. C.FaroniL. R. A.HaddiK.OliveiraE. E.PereiraE. J. G. (2015). Locomotory and Physiological Responses Induced by Clove and Cinnamon Essential Oils in the Maize Weevil Sitophilus Zeamais. Pestic. Biochem. Physiol.125, 31–37. doi: 10.1016/j.pestbp.2015.06.005
39
GrzywaczD.StevensonP. C.MushoboziW. L.BelmainS.WilsonK. (2014). The Use of Indigenous Ecological Resources for Pest Control in Africa. Food Secur.6, 71–86. doi: 10.1007/S12571-013-0313-5
40
HeydariM.AmirjaniA.BagheriM.SharifianI.SabahiQ. (2020). Eco-Friendly Pesticide Based on Peppermint Oil Nanoemulsion: Preparation, Physicochemical Properties, and its Aphicidal Activity Against Cotton Aphid. Environ. Sci. Pollut. Res.27, 6667–6679. doi: 10.1007/S11356-019-07332-y
41
HikalW. M.BaeshenR. S.AhlH. A. H. S.-A. (2017). Botanical Insecticide as Simple Extractives for Pest Control. Cogent. Biol.3, 1404274. doi: 10.1080/23312025.2017.1404274
42
HoddleM. S.HoddleC. D.MilosavljevićI. (2020). How Far Can Rhynchophorus Palmarum (Coleoptera: Curculionidae) Fly? J. Econ. Entomol.113, 1786–1795. doi: 10.1093/jee/toaa115
43
HussainA.Rizwan-ul-HaqM.Al-AyedhH.AljabrA. M. (2017). Toxicity and Detoxification Mechanism of Black Pepper and Its Major Constituent in Controlling Rhynchophorus Ferrugineus Olivier (Curculionidae: Coleoptera). Neotrop. Entomol.46, 685–693. doi: 10.1007/s13744-017-0501-7
44
IkbalC.PavelaR. (2019). Essential Oils as Active Ingredients of Botanical Insecticides Against Aphids. J. Pest Sci. (2004).92, 971–986. doi: 10.1007/s10340-019-01089-6
45
IsmanM. B. (2020). Botanical Insecticides in the Twenty-First Century-Fulfilling Their Promise? Annu. Rev. Entomol.65, 233–249. doi: 10.1146/annurev-ento-011019-025010
46
KhaniM.MaroufA.AminiS.YazdaniD.FarashianiM. E.AhvaziM.et al. (2017). Efficacy of Three Herbal Essential Oils Against Rice Weevil, Sitophilus Oryzae (Coleoptera: Curculionidae). J. Essent. Oil-Bearing. Plants20, 937–950. doi: 10.1080/0972060X.2017.1355748
47
KumarS.NehraM.DilbaghiN.MarrazzaG.HassanA. A.KimK. H. (2019). Nano-Based Smart Pesticide Formulations: Emerging Opportunities for Agriculture. J. Control. Release.294, 131–153. doi: 10.1016/j.jconrel.2018.12.012
48
Kupikowska-StobbaB.KasprzakM. (2021). Fabrication of Nanoparticles for Bone Regeneration: New Insight Into Applications of Nanoemulsion Technology. J. Mater. Chem. B.9, 5221–5244. doi: 10.1039/d1tb00559f
49
LangsiJ. D.NukenineE. N.OumarouK. M.MoktarH.FokunangC. N.MbataG. N. (2020). Evaluation of the Insecticidal Activities of α-Pinene and 3-Carene on Sitophilus Zeamais Motschulsky (Coleoptera: Curculionidae). Insects11, 1–11. doi: 10.3390/insects11080540
50
LapointeS. L.AlessandroR. T.RobbinsP. S.KhrimianA.SvatosA.DickensJ. C.et al. (2012). Identification and Synthesis of a Male-Produced Pheromone for the Neotropical Root Weevil Diaprepes Abbreviates. J. Chem. Ecol.38, 408–417. doi: 10.1007/s10886-012-0096-8
51
LemicD.MikacK. M.GendaM.JukićŽ.ŽivkovićI. P. (2020). Durum Wheat Cultivars Express Different Level of Resistance to Granary Weevil, Sitophilus Granarius (Coleoptera; Curculionidae) Infestation. Insects11, 343. doi: 10.3390/insects11060343
52
LiuP.LiuX. C.DongH. W.LiuZ. L.DuS. S.DengZ. W. (2012). Chemical Composition and Insecticidal Activity of the Essential Oil of Illicium Pachyphyllum Fruits Against Two Grain Storage Insects. Molecules17, 14870–14881. doi: 10.3390/molecules171214870
53
LópezM. D.Pascual-VillalobosM. J. (2010). Mode of Inhibition of Acetylcholinesterase by Monoterpenoids and Implications for Pest Control. Ind. Crops Prod.31, 284–288. doi: 10.1016/j.indcrop.2009.11.005
54
MaazounA. M.HamdiS. H.BelhadjF.JemâaJ.M.B.MessaoudC.MarzoukiM. N. (2019). Phytochemical Profile and Insecticidal Activity of Agave Americana Leaf Extract Towards Sitophilus Oryzae (L.) (Coleoptera: Curculionidae). Environ. Sci. Pollut. Res.26, 19468–19480. doi: 10.1007/S11356-019-05316-6
55
MaazounA. M.HlelT.B.HamdiS. H.BelhadjF.JemâaJ.M.B.MarzoukiM. N. (2017). Screening for Insecticidal Potential and Acetylcholinesterase Activity Inhibition of Urginea Maritima Bulbs Extract for the Control of Sitophilus Oryzae (L.). J. Asia. Pac. Entomol.20, 752–760. doi: 10.1016/j.aspen.2017.04.004
56
MackledM. I.El-HefnyM.Bin-JumahM.WahbaT. F.AllamA. A. (2019). Assessment of the Toxicity of Natural Oils From Mentha Piperita, Pinus Roxburghii, and Rosa Spp. Against Three Stored Product Insects. Process7, 861. doi: 10.3390/pr7110861
57
MazzaG.FrancardiV.SimoniS.BenvenutiC.CervoR.FaleiroJ. R.et al. (2014). An Overview on the Natural Enemies of Rhynchophorus Palm Weevils, With Focus on R. Ferrugineus. Biol. Control.77, 83–92. doi: 10.1016/j.biocontrol.2014.06.010
58
MenossiM.OllierR. P.CasalonguéC. A.AlvarezV. A. (2021). Essential Oil-Loaded Bio-Nanomaterials for Sustainable Agricultural Applications. J. Chem. Technol. Biotechnol.96, 2109–2122. doi: 10.1002/jctb.6705
59
MishraB. B.TripathiS. P.TripathiC. P. M. (2013). Bioactivity of Two Plant Derived Essential Oils Against the Rice Weevils Sitophilus Oryzae (L.) (Coleoptera: Curculionidae). Proc. Natl. Acad. Sci. India. Sect. B. - Biol. Sci.83, 171–175. doi: 10.1007/S40011-012-0123-0
60
Mohd NarawiM.ChiuH. I.YongY. K.Mohamad ZainN. N.RamachandranM. R.ThamC. L.et al. (2020). Biocompatible Nutmeg Oil-Loaded Nanoemulsion as Phyto-Repellent. Front. Pharmacol.11. doi: 10.3389/fphar.2020.00214
61
MoonM. J. (2015). Microstructure of Mandibulate Mouthparts in the Greater Rice Weevil, Sitophilus Zeamais (Coleoptera: Curculionidae). Entomol. Res.45, 9–15. doi: 10.1111/1748-5967.12086
62
MouraE.daS.FaroniL. R. D.HelenoF. F.RodriguesA. A. Z. (2021). Toxicological Stability of Ocimum Basilicum Essential Oil and its Major Components in the Control of Sitophilus Zeamais. Molecules26, 6483. doi: 10.3390/molecules26216483
63
NenaahG. E. (2014). Chemical Composition, Toxicity and Growth Inhibitory Activities of Essential Oils of Three Achillea Species and Their Nano-Emulsions Against Tribolium Castaneum (Herbst). Ind. Crops Prod.53, 252–260. doi: 10.1016/j.indcrop.2013.12.042
64
NguemtchouinM. G. M.NgassoumM. B.ChalierP.KamgaR.NgamoL. S. T.CretinM. (2013). Ocimum Gratissimum Essential Oil and Modified Montmorillonite Clay, a Means of Controlling Insect Pests in Stored Products. J. Stored. Prod. Res.52, 57–62. doi: 10.1016/j.jspr.2012.09.006
65
Nicolopoulou-StamatiP.MaipasS.KotampasiC.StamatisP.HensL. (2016). Chemical Pesticides and Human Health: The Urgent Need for a New Concept in Agriculture. Front. Public Heal.4. doi: 10.3389/fpubh.2016.00148
66
OkadaY.YasudaK.SakaiT.IchinoseK. (2014). Sweet Potato Resistance to Euscepes Post-Fasciatus (Coleoptera: Curculionidae): Larval Performance Adversely Effected by Adult’s Preference to Tuber for Food and Oviposition. J. Econ. Entomol.107, 1662–1673. doi: 10.1603/EC13377
67
OliveiraA. P.SantanaA. S.SantanaE. D. R.LimaA. P. S.FaroR. R. N.NunesR. S.et al. (2017). Nanoformulation Prototype of the Essential Oil of Lippia Sidoides and Thymol to Population Management of Sitophilus Zeamais (Coleoptera: Curculionidae). Ind. Crops Prod.107, 198–205. doi: 10.1016/j.indcrop.2017.05.046
68
OliveiraA. P.SantosA. A.SantanaA. S.Paula LimaA. S.MeloC. R.SantanaE. D.et al. (2018). Essential Oil of Lippia Sidoides and its Major Compound Thymol: Toxicity and Walking Response of Populations of Sitophilus Zeamais (Coleoptera: Curculionidae). Crop Prot.112, 33–38. doi: 10.1016/j.cropro.2018.05.011
69
ParraL.MutisA.OrtegaF.QuirozA. (2013). Field Response of Hylastinus Obscurus Marsham (Coleoptera: Curculionidae) to E-2-Hexenal and Limonene, Two Host-Derived Semiochemicals. Cienc. e Investig. Agrar.40, 637–642. doi: 10.4067/S0718-16202013000300016
70
Patiño-BayonaW. R.Nagles GaleanoL. J.Bustos CortesJ. J.Delgado ÁvilaW. A.Herrera DazaE.SuárezL. E. C.et al. (2021a). Effects of Essential Oils From 24 Plant Species on Sitophilus Zeamais Motsch (Coleoptera, Curculionidae). Insects12. doi: 10.3390/insects12060532
71
Patiño-BayonaW. R.PlazasE.Bustos-CortesJ. J.Prieto-RodríguezJ. A.Patiño-LadinoO. J. (2021b). Essential Oils of Three Hypericum Species From Colombia: Chemical Composition, Insecticidal and Repellent Activity Against Sitophilus Zeamais Motsch. (Coleoptera: Curculionidae). Rec. Nat. Prod.15, 111–121. doi: 10.25135/rnp.192.20.05.1665
72
PavelaR. (2015). Essential Oils for the Development of Eco-Friendly Mosquito Larvicides: A Review. Ind. Crops Prod.76, 174–187. doi: 10.1016/j.indcrop.2015.06.050
73
PavelaR. (2016). History, Presence and Perspective of Using Plant Extracts as Commercial Botanical Insecticides and Farm Products for Protection Against Insects-A Review. Plant Prot. Sci.52, 229–241. doi: 10.17221/31/2016-PPS
74
PavelaR.BenelliG. (2016). Essential Oils as Ecofriendly Biopesticides? Challenges and Constraints. Trends Plant Sci.21, 1000–1007. doi: 10.1016/j.tplants.2016.10.005
75
PaventiG.RotundoG.PistilloM.D’isitaI.GerminaraG. S. (2021). Bioactivity of Wild Hop Extracts Against the Granary Weevil, Sitophilus Granarius (L.). Insects12, 564. doi: 10.3390/insects12060564
76
PeixotoM. G.BacciL.Fitzgerald BlankA.AraújoA. P. A.AlvesP. B.SilvaJ. H. S.et al. (2015). Toxicity and Repellency of Essential Oils of Lippia Alba Chemotypes and Their Major Monoterpenes Against Stored Grain Insects. Ind. Crops Prod.71, 31–36. doi: 10.1016/j.indcrop.2015.03.084
77
Plata-RuedaA.CamposJ. M.da Silva RolimG.MartínezL. C.Dos SantosM. H.FernandesF. L.et al. (2018). Terpenoid Constituents of Cinnamon and Clove Essential Oils Cause Toxic Effects and Behavior Repellency Response on Granary Weevil, Sitophilus Granarius. Ecotoxicol. Environ. Saf.156, 263–270. doi: 10.1016/j.ecoenv.2018.03.033
78
QuirozA.MendezL.MutisA.HormazabalE.OrtegaF.BirkettM. A.et al. (2017). Antifeedant Activity of Red Clover Root Isoflavonoids on Hylastinus Obscurus. J. Soil Sci. Plant Nutr.17, 231–239. doi: 10.4067/S0718-95162017005000018
79
RamachandraiahK.HongG. P. (2021). Polymeric Nanomaterials for the Development of Sustainable Plant Food Value Chains. Food Biosci.41, 2212–4292. doi: 10.1016/j.fbio.2021.100978
80
RangerC. M.RedingM. E.OliverJ. B.SchultzP. B.MoyseenkoJ. J.YoussefN. (2011). Comparative Efficacy of Plant-Derived Essential Oils for Managing Ambrosia Beetles (Coleoptera: Curculionidae: Scolytinae) and Their Corresponding Mass Spectral Characterization. J. Econ. Entomol.104, 1665–1674. doi: 10.1603/EC11106
81
RangerC. M.RedingM. E.SchultzP. B.OliverJ. B. (2012). Ambrosia Beetle (Coleoptera: Curculionidae) Responses to Volatile Emissions Associated With Ethanol-Injected Magnolia Virginiana. Environ. Entomol.41, 636–647. doi: 10.1603/EN11299
82
ReddyG. V. P.BalakrishnanS.RemolonaJ. E.KikuchiR.BambaJ. P. (2011). Influence of Trap Type, Size, Color, and Trapping Location on Capture of Rhabdoscelus Obscurus (Coleoptera: Curculionidae). Ann. Entomol. Soc Am.104, 594–603. doi: 10.1603/AN10200
83
Regnault-RogerC.VincentC.ArnasonJ. T. (2012). Essential Oils in Insect Control: Low-Risk Products in a High-Stakes World. Annu. Rev. Entomol.57, 405–424. doi: 10.1146/annurev-ento-120710-100554
84
ReyesE. I. M.FariasE. S.SilvaE. M. P.FilomenoC. A.PlataM. A. B.PicançoM. C.et al. (2019). Eucalyptus Resinifera Essential Oils Have Fumigant and Repellent Action Against Hypothenemus Hampei. Crop Prot.116, 49–55. doi: 10.1016/j.cropro.2018.09.018
85
RibeiroL. P.AnsanteT. F.NiculauE. S.PavariniR.SilvaM. F. G. F.SeffrinR. C.et al. (2015). Pimenta Pseudocaryophyllus Derivatives: Extraction Methods and Bioactivity Against Sitophilus Zeamais Motschulsky (Coleoptera: Curculionidae). Neotrop. Entomol.44, 634–642. doi: 10.1007/S13744-015-0321-6
86
Rodriguez-SaonaC.VincentC.IsaacsR. (2019). Blueberry IPM: Past Successes and Future Challenges. Annu. Rev. Entomol.64, 95–114. doi: 10.1146/annurev-ento-011118-112147
87
RomaniR.BediniS.SalernoG.AscrizziR.FlaminiG.EcheverriaM. C.et al. (2019). Andean Flora as a Source of New Repellents Against Insect Pests: Behavioral, Morphological and Electrophysiological Studies on Sitophilus Zeamais (Coleoptera: Curculionidae). Insects10, 171. doi: 10.3390/insects10060171
88
Romero-FríasA. A.SinucoD. C.BentoJ. M. S. (2019). Male-Specific Volatiles Released by the Big Avocado Seed Weevil Heilipus Lauri Boheman (Coleoptera: Curculionidae). J. Braz. Chem. Soc30, 158–163. doi: 10.21577/0103-5053.20180166
89
RossiniL.ContariniM.SeveriniM.TalanoD.SperanzaS. (2020). A Modelling Approach to Describe the Anthonomus Eugenii (Coleoptera: Curculionidae) Life Cycle in Plant Protection: A Priori and a Posteriori Analysis. Florida Entomol.103, 259–263. doi: 10.1653/024.103.0217
90
Ruiz-DiazC. P.RodriguesJ. C. V. (2021). Vertical Trapping of the Coffee Berry Borer, Hypothenemus Hampei (Coleoptera: Scolytinae), in Coffee. Insects12, 607. doi: 10.3390/insects12070607
91
SagiriS. S.AnisA.PalK. (2016). Review on Encapsulation of Vegetable Oils: Strategies, Preparation Methods, and Applications Review on Encapsulation of Vegetable Oils: Strategies, Preparation Methods, and Applications. Polym. Plast. Technol. Eng.55, 291–311. doi: 10.1080/03602559.2015.1050521
92
SinghY.MeherJ. G.RavalK.KhanF. A.ChaurasiaM.JainN. K.et al. (2017). Nanoemulsion: Concepts, Development and Applications in Drug Delivery. J. Control. Release.252, 28–49. doi: 10.1016/j.jconrel.2017.03.008
93
SinghK. D.MoboladeA. J.BharaliR.SahooD.RajashekarY. (2021). Main Plant Volatiles as Stored Grain Pest Management Approach: A Review. J. Agric. Food Res.4, 100127. doi: 10.1016/j.jafr.2021.100127
94
SnehaK.KumarA. (2021). Nanoemulsions: Techniques for the Preparation and the Recent Advances in Their Food Applications. Innov. Food Sci. Emerg. Technol.76, 102914. doi: 10.1016/j.ifset.2021.102914
95
SocíasM. G.LiljesthrömG. G.CasmuzA. S.MurúaM. G.GastaminzaG. (2014). Density and Spatial Distribution of Different Development Stages of Sternechus Subsignatus Boheman (Coleoptera: Curculionidae) in Soybean Crops. Crop Prot.65, 15–20. doi: 10.1016/j.cropro.2014.06.020
96
SzendreiZ.AverillA.AlbornH.Rodriguez-SaonaC. (2011). Identification and Field Evaluation of Attractants for the Cranberry Weevil, Anthonomus Musculus Say. J. Chem. Ecol.37, 387–397. doi: 10.1007/S10886-011-9938-z
97
TampeJ.EspinozaJ.Chacón-FuentesM.QuirozA.RubilarM. (2020). Evaluation of Drimys Winteri (Canelo) Essential Oil as Insecticide Against Acanthoscelides Obtectus (Coleoptera: Bruchidae) and Aegorhinus Superciliosus (Coleoptera: Curculionidae). Insects11, 1–15. doi: 10.3390/insects11060335
98
TampeJ.ParraL.HuaiquilK.MutisA.QuirozA. (2015). Repellent Effect and Metabolite Volatile Profile of the Essential Oil of Achillea Millefolium Against Aegorhinus Nodipennis (Hope) (Coleoptera: Curculionidae). Neotrop. Entomol.44, 279–285. doi: 10.1007/s13744-015-0278-5
99
TampeJ.ParraL.HuaiquilK.QuirozA. (2016). Potential Repellent Activity of the Essential Oil of Ruta Chalepensis (Linnaeus) From Chile Against Aegorhinus Superciliosus (Guérin) (Coleoptera: Curculionidae). J. Soil Sci. Plant Nutr.16, 48–59. doi: 10.4067/S0718-95162016005000004
100
TewariS.LeskeyT. C.NielsenA. L.PiñeroJ. C.Rodriguez-SaonaC. R. (2014). “Use of Pheromones in Insect Pest Management, With Special Attention to Weevil Pheromones,” in Integrated Pest Management: Current Concepts and Ecological Perspective (Elsevier Inc), 141–168. doi: 10.1016/B978-0-12-398529-3.00010-5
101
ToninaL.ZanettinG.MiorelliP.PuppatoS.CuthbertsonA. G. S.GrassiA. (2021). Anthonomus Rubi on Strawberry Fruit: Its Biology, Ecology, Damage, and Control From an Ipm Perspective. Insects12, 701. doi: 10.3390/insects12080701
102
TorresC.SilvaG.TapiaM.RodríguezJ. C.FigueroaI.LagunesA.et al. (2014). Insecticidal Activity of Laurelia Sempervirens (Ruiz & Pav.) Tul. Essential Oil Against Sitophilus Zeamais Motschulsky. Chil. J. Agric. Res.74, 421–426. doi: 10.4067/S0718-58392014000400007
103
UpadhyayN.DwivedyA. K.KumarM.PrakashB.DubeyN. K. (2018). Essential Oils as Eco-Friendly Alternatives to Synthetic Pesticides for the Control of Tribolium Castaneum (Herbst) (Coleoptera: Tenebrionidae). J. Essent. Oil-Bearing. Plants21, 282–297. doi: 10.1080/0972060X.2018.1459875
104
VacasS.NavarroI.SerisE.RamosC.HernándezE.Navarro-LlopisV.et al. (2017). Identification of the Male-Produced Aggregation Pheromone of the Four-Spotted Coconut Weevil, Diocalandra Frumenti. J. Agric. Food Chem.65, 270–275. doi: 10.1021/acs.jafc.6b04829
105
VankoskyM. A.CrcamoH. A.DosdallL. M. (2011). Response of Pisum Sativum (Fabales: Fabaceae) to Sitona Lineatus (Coleoptera: Curculionidae) Infestation: Effect of Adult Weevil Density on Damage, Larval Population, and Yield Loss. J. Econ. Entomol.104, 1550–1560. doi: 10.1603/EC10392
106
WagnerL. S.SequinC. J.FotiN.Campos-SoldiniM. P. (2021). Insecticidal, Fungicidal, Phytotoxic Activity and Chemical Composition of Lavandula Dentata Essential Oil. Biocatal. Agric. Biotechnol.35, 102092. doi: 10.1016/j.bcab.2021.102092
107
WahabS.MuzammilK.NasirN.KhanM. S.AhmadM. F.KhalidM.et al. (2022). Advancement and New Trends in Analysis of Pesticide Residues in Food: A Comprehensive Review. Plants11, 1106. doi: 10.3390/PLANTS11091106
108
Werdin GonzálezJ. O.GutiérrezM. M.FerreroA. A.Fernández BandB. (2014). Essential Oils Nanoformulations for Stored-Product Pest Control – Characterization and Biological Properties. Chemosphere100, 130–138. doi: 10.1016/j.chemosphere.2013.11.056
109
WuF.YanX. P. (2018). Distribution of the Related Weevil Species Sitophilus Oryzae and S. Zeamais (Coleoptera: Curculionidae) in Farmer Stored Grains of China. J. Econ. Entomol.111, 1461–1468. doi: 10.1093/jee/toy061
110
ZavalaA.ElguetaM.AbarzúaJ.AguileraA.QuirozA.RebolledoR. (2011). Diversity and Distribution of the Aegorhinus Genus in the La Araucanía Region of Chile, With Special Reference to A. Superciliosus and A.Nodipennis. Cienc. e Investig. Agrar.38, 367–377. doi: 10.4067/s0718-16202011000300006
111
ZhangJ.WangY.FengY.DuS.JiaL. (2021). Contact Toxicity and Repellent Efficacy of Essential Oil From Aerial Parts of Melaleuca Bracteata and its Major Compositions Against Three Kinds of Insects. J. Essent. Oil-Bearing. Plants24, 349–359. doi: 10.1080/0972060X.2021.1886995
Summary
Keywords
essential oils, curculionidae, bioinsecticide, nanoencapsulation, pest
Citation
Garrido-Miranda KA, Giraldo JD and Schoebitz M (2022) Essential Oils and Their Formulations for the Control of Curculionidae Pests. Front. Agron. 4:876687. doi: 10.3389/fagro.2022.876687
Received
15 February 2022
Accepted
17 May 2022
Published
15 June 2022
Volume
4 - 2022
Edited by
Salvatore Arpaia, Energy and Sustainable Economic Development (ENEA), Italy
Reviewed by
Javaid Iqbal, King Saud University, Saudi Arabia
Updates
Copyright
© 2022 Garrido-Miranda, Giraldo and Schoebitz.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Karla A. Garrido-Miranda, karla.garrido@ufrontera.cl
This article was submitted to Pest Management, a section of the journal Frontiers in Agronomy
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