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Review

Controlling Stored Products’ Pests with Plant Secondary Metabolites: A Review

by
Polyxeni Nikolaou
1,
Paweł Marciniak
1,
Zbigniew Adamski
1,2 and
Nikoletta Ntalli
3,*
1
Department of Animal Physiology and Development, Faculty of Biology, Adam Mickiewicz University, Uniwersytetu Poznańskiego 6., 61-614 Poznań, Poland
2
Laboratory of Electron and Confocal Microscopy, Faculty of Biology, Adam Mickiewicz University, Uniwersytetu Poznańskiego 6., 61-614 Poznań, Poland
3
Department of Pesticides Control and Phytopharmacy, Benaki Phytopathological Institute, 14561 Athens, Greece
*
Author to whom correspondence should be addressed.
Agriculture 2021, 11(9), 879; https://doi.org/10.3390/agriculture11090879
Submission received: 25 July 2021 / Revised: 8 September 2021 / Accepted: 9 September 2021 / Published: 14 September 2021
(This article belongs to the Special Issue Biopesticides: The Naturally Originating Plant Protection Products and Biocides)
Versions Notes

Abstract

:
To date, only a handful of pesticides have been authorized by the European Council for the protection of stored grains. Resistance issues and ecotoxicity concerns necessitate the development of ecofriendly tools in that direction. In this review, we refer to the recent findings on plant extracts and pure plant-derived substances with promising biological activity and the potential to be used as biopesticides for stored products. The main aim of biopesticides is to be effective against target pests, without harming humans and the environment. Many plant species, among those reported herein, are part of the human diet, and are thus not harmful to humans. Edible plant extracts produced with inorganic solvents represent safe candidates for use as repellants, fumigants or contact pesticides. Cinnamon, rosemary, parsley, garlic, oregano and basil are found in products destined for human consumption but also display significant biological activities. Interestingly, cinnamon is one of the most widely tested botanical matrixes, exhibiting the best lethal effects on almost all insect and mite taxa reported herein (Acaroidea, Coleoptera and Lepidoptera), followed by basil and garlic. Prunus persica, Azadirachta indica A. Juss and Carum sp. seem to be very promising too as miticides and/or insecticides, with A. indica already being represented commercially by a plant-derived acaricidal formulation.

1. Introduction

Over 800 million people worldwide suffer from malnutrition, and one-third of global food production is lost or wasted annually [1]. Pesticides are needed to control weeds, insect infestations and various pests and disease carriers (e.g., mosquitoes, ticks, rats and mice) in houses, offices, malls and streets [2]. Worldwide, approximately 2 million tons of pesticides are utilized annually [3]. However, the modes of action of pesticides are not always species-specific and exposure at even very low levels may have adverse health effects on humans. Additionally, concerns have been raised about environmental risks associated with exposure to these products through various routes (e.g., residues in food and drinking water) [2]. As a result, many pesticides have been withdrawn from the market. Interestingly, in an eight-year period (2001–2008), 26% of insecticides were banned from the European Union due to unintentional impacts [4], extending as far as unbalancing/damaging an entire ecosystem [5].
Due to the constant increase of the population, larger quantities of cereals are required to cover the needs of the growing human population, thus making it important to find ways to minimize the loss of stored grains. Cereal grains are in fact the most basic ingredients of the human diet. According to the FAO, ‘Cereals continue to be by far the most important source (in terms of calories) of total food consumption’. The food use of cereals has continued to increase, albeit at a decelerating rate. In developing countries, the per capita average is now 173 kg, providing 56 percent of total calories [6]. On the other hand, insects feeding on stored grains can cause losses of up to 420 million tons annually [1]. There are two classes of arthropods—arachnids (Arachnida) and insects (Insecta)—infesting grains and food products. Within the first class, the subclass mites (Acari) contains some species of great economic importance. Among insects, species belonging to the orders of beetles (Coleoptera), moths and butterflies (Lepidoptera) are significant pests. Stored products may be damaged either through contamination by primary pests or through secondary contamination due to previously damaged grains; either caused by other pests (primary pests) or by being poorly threshed, dried and handled. Flour and milled rice might exhibit a reduction in weight and a decrease in quality due to an infestation of pests. Insects can encourage mold germination, increase the fatty acid percentage in the grain and can cause grain rancidity due to the uric acid they release, as well as causing grain pollution through their exuviae or feces. This, in consequence, can cause price discounts and shipping restrictions [1]. Traditionally, stored product insects have been controlled with synthetic insecticides, most of which are now out of the market due to ecotoxicological concerns (EC 1107/2006), as well as resistance issues [7,8]. To date, only a few of their active ingredients are still registered in the EU for stored product pest control. In particular, these include the fumigants magnesium phosphide and aluminum phosphide; the synthetic pyrethroids cypermethrine and deltamerthine, the phosphorothioate pirimiphos methyl and piperonyl butoxide applied by dusting [7]. Natural molecules of botanical origin have attracted international research interest in recent years as ecofriendly alternatives to their synthetic pesticidal ancestors (in commercial terms) [9]. Recent reviews on the use of the secondary metabolites of plants against stored product insects are those of Rajendran and co-workers, reporting the fumigant toxicity results conducted with essential oils of plants (mainly belonging to Apiaceae, Lamiaceae, Lauraceae and Myrtaceae) and their components (cyanohydrins, monoterpenoids, sulphur compounds, thiocyanates and others) [10], as well as that of Stejskal and co-workers, reporting on gas, liquid, gel and solid formulations of natural pesticides for stored-product applications [11].
In the present review, we report on the most important arthropod pests affecting grains and food products, along with the plant-derived substances reported to exhibit significant activity in the last 10 years. We categorized pests based on their taxonomic class and order, exhibiting similar habits, life cycles and metabolism. We aim to pinpoint the natural plant-derived substances that could be developed to combat stored-product pest infestations.

2. Economically Important Groups of Stored-Product Pests and Plant-Derived Tools with Reported Activity

2.1. Mites (Acari)

There are several mite species that cause severe losses to grains and stored products, mostly because they reproduce in large numbers, tolerate lower temperatures than insects and are not readily seen, causing great impact on storage facilities. Among the mites that are regarded as the most important pests of stored grains and food products are the species Gohieria fusca and Lepidoglyphus destructor (Glycyphagidae); Blomia freeman (Echimypodiae) and Chortoglyphus arcuatus (Chortoglyphidae), as well as Aleuroglyphus ovatus, Tyrophagus longior, Tyrophagus putrescentiae, Tyroborus lini and Acarus farris and Acarus siro of the Acaridae [12,13,14,15].
Traditionally, mites have been eradicated using synthetic miticides such as organophosphates, pyrethroids, pyridazines, juvenile hormone analogs and chitin synthesis inhibitors [13,16,17]. In addition, elevated CO2 concentrations are applied [18]. However, benzyl-benzoate, a substance that is produced and used industrially but which is also naturally produced by a range of plants—cinnamon and cassia (Cinnamomum spp.), carnation (Dianthus caryophyllus L.), hyacinths (Hyacinthus spp.), tuberose (Agave amica Medik.), common jasmine (Jasminum officinale L.) and Santos mahogany (Myroxylon balsamum L. Harms)—is often used as a commercial acaricide or as a reference substance in acaricidal tests. However, this substance is regarded as an allergen [19].
Azadirachtin (neem), a commercially available plant-derived pesticide obtained from the plant species Azadirachta indica A. Juss, is one of the most commonly used natural substances that causes lethal and sublethal insecticidal and miticidal effects. As reviewed by Collins (2006), it limits the growth of populations and causes mortality of T. putrescentiae, A. siro and L. destructor [13] but it proved to be less effective against five species of stored product mite pests than synthetic commercial miticides [20].
The components of clove bud (Eugenia caryophyllata Thumb.) oil—methyleugenol (median lethal dose (LD50) = 1.18 μg/cm2, isoeugenol, ß-caryophyllene, eugenol and α-humulene (LD50 = 12.90 μg/cm2)—showed lethal toxicity against T. putrescentiae, with methyleugenol and isoeugenol being more toxic than benzyl benzoate [21]. Furthermore, Rosmarinus officinalis L. essential oil (EO) and its constituent compounds were active against this mite, both as a fumigant (LD50 = 8.24 μg/cm3) and in contact toxicity (LD50 = 5.49 μg/cm2). The constituent camphor appeared to be successful in combating the pest (fumigant toxicity LD50 = 2.25 μg/cm3, contact toxicity LD50 = 1.34 μg/cm2) more effectively than benzyl benzoate (LD50 = 12.56 μg/cm3, and 9.03 μg/cm2) [22]. Other constituent substances in rosemary oil are α-pinene, 1,8-cineole and camphene, all exhibiting miticidal activity [23]. Lee (2015) proved the fumigant and contact toxicity of the essential oil of Ligustrum japonicum leaves against T. putrescentiae and calculated the respective LD50 values to be 16.48 µg/cm3 and 8.02 µg/cm2, respectively. α-pinene is one of the compounds found in L. japonicum oil, showing the highest percentage [24]. These data indicate that camphor may be effective, as well as other compounds. However, camphor seems to be more toxic to mites than α-pinene [21]. Ottoboni et al. (1992) reported that caraway (Carum carvi L.) essential oil was a significant candidate to combat L. destructor, G. fusca, A. siro and T. putrescentiae [25,26]. Furthermore 3,4-methylenedioxybenzene and its derivatives were described as successful miticides against, among others, T. putrescentiae [27]. Interestingly, apiol, which naturally occurs in the seeds of parsley (Petroselinum sativum Hoffm), was not toxic against T. putrescentiae, although it has been proven to be active against Dermatophagoides species. Essential oils obtained from both the aerial parts and seeds of the forget-me-not plant (Myosotis arvensis (L.)) or ingredient compounds used individually, namely 2,4,5-trimethylbenzaldehyde, 2,4-methylbenzaldehyde, 2,5-dimethylbenzaldehyde, 2-methylbenzaldehyde, 2,3-dimethylbenzaldehyde, 3-methylbenzaldehyde, 4-methylbenzaldehyde, 3-octanone, butyl isothiocyanate and nonanal, showed significantly greater contact and vapor toxicity against T. putrescentiae than benzyl benzoate [28]. T. putrescentiae was proven to be susceptible to the essential oil of garlic (Allium sativum L.), basil (Ocimum basilicum L.) and fenugreek (Trigonella foenum-graecum L.), in descending order, when exposed for one to three days [29]. However, the sulfide-rich garlic essential oil was toxic to Cheyletus malaccensis, a predatory mite and natural enemy of A. siro, T. putrescentiae and L. destructor [30]. Nonetheless, garlic essential oil and its active compounds can be used as possible miticides against a range of mites [31]. Unfortunately, some botanical extracts have been proven to be lethal for beneficial insects, such as citronella, eucalyptus, garlic, pyrethrum and neem. Sometimes their effects may be non-lethal, such as inhibiting natural enemies from utilizing prey, reducing prey availability, decreasing reproduction, inhibiting the ability of natural enemies to recognize prey, influencing the sex ratio (females:males) and reducing mobility. Nonetheless, detailed knowledge of the lethal or non-lethal effects of botanical pesticides on beneficial insects is essential for the sustainable control of insect pests and pollination activities for improved and sustainable agricultural production [32].
De Assis and co-authors (2011) tested the fumigant toxicity of eugenol and essential oils from cinnamon (Cinnamomum zeylanicum Blume), Surinam cherry (Eugenia uniflora L.), uvalha (Eugenia uvalha Cambess.), weeping paperbark (Melaleuca leucadendra (L.)), cake bush (Piper marginatum Jacq.) and Brazilian peppertree (Schinus terebinthifolia G.Raddi) against T. putrescentiae. The lowest median lethal concentration (LC50) values were obtained for eugenol and C. zeylanicum essential oil. These data are in agreement, since eugenol is the major component of C. zeylanicum essential oil and its content may exceed ¾ of all the volatile ingredients of this oil [33]. The next most abundant component—linalool—is present in about nine times lower amounts [34]. Although it is not as important, linalool may increase toxic effects since it appeared to be toxic against T. longior in contact and fumigant toxicity studies. Similarly the toxicity of menthol, menthone, fenchone, linalyl acetate and eucalyptol, the most abundant substances in the essential oils of lavender (Lavandula angustifolia Mill, Lavandula stoechas L.), peppermint (Mentha x piperita L.) and eucalyptus (Eucaliptus globulus), should be assessed for their lethality [35].
The observation of the variable susceptibility of various species of mites to natural substances is also seen in the case of natural aldehydes used as miticides. This phenomenon was described for three natural aldehydes, namely, (2E)-hexenal, (2E, 6Z)-nonadienal and (2E)-nonenal, produced in plants from organic acids, when tested in feeding tests from 36 to 314 mg/g against A. siro, A. ovatus and T. putrescentiae. Specifically, the susceptibility of A. siro was similar for all three aldehydes, whereas T. putrescentiae was about eight times more susceptible to nonadienal than to hexenal, and was not significantly affected by nonenal [36]. In another study, benzaldehyde (LD50 = 4.23 µg/cm2) isolated from the peach Prunus persica, as well as salicylaldehyde (LD50 = 1.02 µg/cm2), cinnamaldehyde (LD50 = 1.66 µg/cm2) and phthaldialdehyde (LD50 = 5.16 µg/cm2), were tested against T. putrescentiae. All aldehydes exhibited better efficacies than benzyl benzoate (LD50 = 9.75 µg/cm2). However, the values calculated for P. persica essential oil (LD50 = 11.23 µg/cm2) were higher than those for benzyl benzoate [37]. This research shows that aldehydes and essential oils can be applied in grain and food protection. However, their application must be carefully adjusted to the tested species.
There are suggestions that jasmonic acid (JA) can be used as a miticide against mite-pests of grains and stored food. This compound may affect mite reproduction and limit losses. The tomato mutants that were unable to accumulate JA were characterized by a higher rate of egg-hatching of mite-pests compared to the wild type. Therefore, JA was suggested as a substance of ovicidal activity [38]. Most interestingly, JA additionally attracts predatory mites and therefore it may decrease the level of pests [39]. These data seem to open a field of interesting further research on the species of interest.
Angiosperms also deliver bioactive substances that may be useful in limiting losses caused by mites. For instance, essential oils obtained from gymnosperm plants such as Pinus pinea, Pinus halepensis, Pinus pinaster and Pinus nigra were described as toxic for T. putrescentiae [40], with P. pinea being the most effective. Moreover, 1,8-cineole and limonene showed miticidal activity when tested at 8 or 6 µL on 6 cm of filter paper. Likewise, Juniperus chinensis essential oil and its respective components were applied in impregnated disc biotests against T. putrescentiae, with the LD50 values calculated at 38.1, 15.33, and 42.85µg/cm2 for the essential oil, bornyl acetate and α-eudesmol, respectively [41]. Based on the effect and the content of the substances in the oil, the authors suggested that bornyl acetate is the major substance responsible for this acaricidal activity. The authors also reported that sabinene and α–thujene were not toxic to the mites.
The abovementioned results prove that plant-derived extracts and single compounds may become interesting alternatives to commercial miticides. In many cases, they are obtained from plants that are nontoxic to humans, since they are part of the human diet, for example, garlic or parsley (Table 1). Therefore, they can be used in food stores, being relatively safe to humans, of course depending on the concentration used.

2.2. Insects (Insecta)

Pests affecting grains can be found in various orders of insects. Some of these belong to the major pests affecting stored crops and food, whereas some are of minor importance. Among the most important ones are beetles (Coleoptera), true bugs (Hemiptera), butterflies and moths (Lepidoptera). Therefore, we will focus on these three orders.

2.2.1. Beetles (Coleoptera)

Coleopterans form the largest order within the animal kingdom, with more than 400,000 species and about 200 families. It is not surprising that within this order we may find pests affecting grains, which are of economic importance. One of the largest families of Coleoptera is Tenebrionidae, or as they are commonly known, darkling beetles. Within this family there are some very important grain pests. Firstly, there is the confused flour beetle Tribolium confusum Jacq. Du Val, a pest that feeds on all kinds of grains and flour. T. confusum can have as many as five generations per year and every female can lay as many as 600 eggs on the stored product. In the case of T. confusum, very few botanical insecticides have been tested. Firstly, Carum copticum and Cuminum cyminum were effective in their contact toxicity effects against T. confusum with LD50 values of 0.037 µg/mg and 0.039 µg/mg, respectively [65]. Secondly, Aster ageratoides [60], Juniperus polycarpos and Juniperus sabina [100] acted as fumigants in the form of EO, whereas Crithmum maritimum did not cause any mortality [83].
Tribolium castaneum Herbst, commonly known as the rust-red flour beetle, belongs to the same genus as T. confusum, with which it has physical similarities, life cycle and feeding habits, meaning it is also a secondary pest. T. castaneum, as a model beetle species, has been the most tested beetle in regard to the effects of botanical insecticides. The tested natural substances have been mainly evaluated for their fumigant toxicity, contact toxicity or repellant properties. Tagetes minuta [131], Tagetes patula [131], Platycladus orientalis (fruits) [128], A. sativum [49] and M. piperita [112] have been proven to be the most effective fumigants against the adults of this species. Eucalyptus procera [97], basil [79], orange [79] and Satureja hortensis oils were toxic after contact with T. confusum adults [129], whereas Citrus reticulata and Citrus sinensis essential oils were effective against larvae [76]. Finally, many plant extracts were proven to be effective as repellents; the repellency abilities of the botanical substances were assessed based on the area test, as described by McDonald et al. (1970) [220]—namely, Litsea salicifolia [108], Artemisia anethoides [55], Zanthoxylum planispinum [136] and Hyptis suaveolens exhibited repellency rates of more than 90% [98]. C. reticulata was also effective as a repellent in the form of powder of ethanol extract.
The yellow mealworm beetle, Tenebrio molitor L., is also a secondary pest, feeding on flour, grains and plant-based products. Garlic essential oil caused necrosis in larvae, pupae and adults of T. molitor L. after 20–40 h of exposure [48], whereas Bidens sulphurea and Adenocalymma nodosum were more effective against the pupae [44]. Cinnamon oil was most toxic to T. molitor L. larvae, whereas clove oil was most effective on adults. Cinnamon oil mainly yielded eugenol (10.19%), trans-3-caren-2-ol (9.92%) and benzyl benzoate (9.68%); whereas clove oil yielded eugenol (26.64%), caryophyllene (23.73%) and caryophyllene oxide (17.74%) [71]. Interestingly, some research on T. molitor L. has focused on the sublethal effects of glycoalkaloids, describing malformations of organelles, chromatin condensation and altered contractility of the heart and oviduct [130].
Another large family of Coleoptera is the Curculionidae, or as they are commonly known, “snout beetles”. In this family there are 83,000 species described worldwide. There are some important grain pests in this family. Sitophilus granarius L. is a frequent pest of wheat and barley, but also can attack other cereals, such as maize, sorghum and rice. Lower developmental stages (eggs, larvae and pupae) of S. granarius complete their development inside a seed kernel or products, which is common for all other primary insects. Every female of the species can produce as many as 400 eggs, which are placed separately inside the seeds. It is a primary pest which feeds on all Poaceae grains. Many plant extracts have been tested for acute toxicity against S. granarius with Calendula officinalis being amongst the most promising contact toxicant extracts [67], whereas Origanum acutidens [124], C. maritimum [83] and L. angustifolia were the best fumigants [106]. Furthermore, L. angustifolia [106], C. copticum and Cuminum cyminum were very powerful in terms of their contact toxicity [65]; L. angustifolia was also effective as a repellent [106].
The rice weevil (Sitophilus oryzae L.) is morphologically very similar to S. granarius, but it is more commonly found in stored rice. It feeds mainly on cereal seeds and is less likely to feed on grain products. It is also more resistant to lower temperatures than S. granarius. Among the natural substances trialed for their fumigant properties, the most effective were the essential oils obtained from Cymbopogon citratus and Zingiber officinale [85], O. basilicum [121], Origanum vulgare and Citrus lemon oils [57]. Essentials oils of fennel (Foeniculum vulgare), caraway (C. carvi), cinnamon (Cinnamomum verum), citronella (Cymbopogon winterianus), nutmeg (Myristica fragrans) and black cumin (Nigella sativa) were all proven to be highly competent as contact toxicity insecticides [64]. Additionally, Artemisia judaica, Callistemon viminals and O. vulgare caused high-contact toxicity to S. oryzae with LC50 values of 0.08, 0.09 and 0.11 mg/cm2, respectively [57]. Ocimum gratissimum (EO) and its constituents [123], as well as H. suaveolens (EO), seemed to be very effective as repellents [98]. Finally, some botanical extracts (Acorus calamus + Corchorus capsularis seed petroleum ether extract, A. calamus + Thevetia neriifolia seed petroleum ether extract and A. calamus + Zingiber cassumunar Roxb. rhizome petroleum ether extract) were assessed in terms of the synergism of their toxic effects [45] or repellent effects (Hyptis spicigera, Vepris heterophylla) [133].
The maize weevil (Sitophilus zeamais Motsch) is another important pest, of an appearance similar the previously mentioned beetles; it is mainly found in stored maize but can sometimes be found in wheat and barley. S. zeamais Motsch has the ability to fly; hence, the infestation can start in the ripening crop in the field and can carry on in storage. Chenopodium ambrosioides [221] has been a very effective toxic fumigant, as has Blumea balsamifera [222], as well as orange and basil oil [79]. Kadsura heteroclite stems (EO) were the most effective in terms of contact toxicity, followed by Cayratia japonica (EO) [101]. Furthermore, L. salicifolia [108] and Anethum graveolens (EO), Petroselinum crispum (EO), F. vulgare (EO) and C. cyminum (EO) were effective repellents against the maize weevil [53].
There are also some important pests of grains within other families. For example, Lasioderma serricorne (Fabricius) (Anobiidae), commonly known as the “cigarette beetle”, is a secondary pest, which feeds on a great variety of products, including grain-based products, herbs, and legumes. It can have up to four generations per year and it overwinters as larvae. Extracts of the botanical species O. acutidens seemed to be the most effective in terms of fumigant activities against this pest [124], followed by Artemisia mongolica [81], Alpinia blepharocalyx [50] and Perilla frutescens [127]. P. frutescens (L.) [127], Z. planispinum [127] and Artemisia stolonifera [59] extracts and ingredient components were also very promising as alternative and greener fumigants. Finally, M. piperita menthol extract showed very strong repellent properties, with 80% repellency after 4 h at the test concentration of 3.15 μL/cm2 [112], which was much greater than Z. planispinum essential oil, exhibiting 62% repellency after 4 h of exposure at 78.63 nL/cm2 [136], and Laurus nobilis, exhibiting 60% repellency at a concentration of 0.2 μL/cm2 after 24 h of exposure [103]. Cryptolestes ferrugineus (Stephens) and other Cryptolestes species (Cucujidae) are important secondary pests of food grains [223]. EO from C. reticulata peel achieved 100% fumigant mortality, contact toxicity that was fully effective (99.0% after 48 h of exposure at the dosage of 2.0 μL/cm2) and finally had a very good repellency rate (achieved >80.0% after 60 h of exposure at 0.4 μL/cm2) [77]. Unfortunately, according to other studies carried out with extracts of Melia azedarach, Linium usitatissium, Ferula narthex, Sasurrea costus, Viola odorata and Achyranthus aspera, they were not very effective, although M. azedarach was able to decrease larval and pupal emergence [122].
The saw-toothed grain beetle (Oryzaephilus surinamensis L. (Silvanidae)) feeds on grains, as well as bran and grain products. It is a secondary pest that lays eggs in flour and causes further qualitative and quantitative losses. Regarding the fumigant activity of O. gratissimum essential oil [123], which showed the best results at a concentration of 1 mL/L air, the oil caused a mortality rate of 99% 24 h after treatment, respectively, followed by C. maritimum [83], Eucalyptus globules and L. stoechas [95]. The essential oils of H. suaveolens leaves [98], C. maritimum [83] and Artemisia herba-alba and Artemisia absinthium caused necrosis to adults [56]. Powdered Salvia officinalis also caused a high mortality rate, reaching 80% (the powdered plant was added to culture containers at concentrations of 5.88%) [47]. Finally, Pongamia pinnata has the potential for use as a mediocre repellent [68]. Rhyzopertha dominica Fab. can be considered the main insect pest species in grains stored around the world [224,225]. It is a primary pest of stored products, feeding on all cereals and grain products. According to a study published in 2017 by Tawfeek et al., essential oils of fennel (F. vulgare), caraway (C. carvi), cinnamon (C. verum), citronella (C. winterianus), nutmeg (M. fragrans) and black cumin (N. sativa) seemed to be very active, with fennel being the most effective [64]. The essential oil of H. suaveolens is reported to have potential as a contact insecticide [98]. Lastly, L. nobilis and Eucalyptus floribundi are two essential oils with repellent and fumigant properties [94,189].
Khapra beetle (Trogoderma granarium Everts.) is the only genus from the family Dermestidae that feeds on plant-based products, especially stored grains. For many countries it is considered a quarantine concern because its spread occurs mainly through international trade. According to Derbalah and his team, in a research study in 2011, seven plant methanol extracts were tested for their insecticidal properties and the results were positive, with Cassia senna being the most effective (100 mg/L achieved 86.7% mortality after one week) [63]. Interestingly, the plant extracts of Bauhinia purpurea, C. senna, Caesalpinia gilliesii, Cassia fistula, Chrysanthemum frutescens, Euonymus japonicus and Thespesia populnea var. acutiloba were also effective towards the beetle and displayed no side effects to rats, indicating friendliness to mammals. Finally, the essential oil of O. basilicum was found to cause mortality at 54.33% after 72 h [122].
As one can see, there are not enough data concerning the sublethal action of plant-derived substances on beetles, such as the research on the sublethal effects of glycoalkaloids on T. molitor L. [130], as well as their mode of action (Table 1), compared to the research on other groups, especially moths and butterflies (see below). We think that basic research on these sublethal effects, including the analysis of both behavioral and physiological changes, may provide plenty of important data, which can be applied in studies leading to novel natural insecticides.

2.2.2. Butterflies and Moths (Lepidoptera)

The range of lepidopteran species representing pests of grains and the research on plant-derived substances tested against them is wide (Table 1). The most important pests affecting grains are found within the Pyralidae family, although Sitotroga cerealella Oliv., belonging to Gelechiidae, is also considered a serious pest affecting grains.
S. cerealella Oliv. burrows in grains and makes them unfit for human consumption. The families Asteraceae, Bignoniaceae, Fabaceae and Rubiaceae contain species with insecticidal and repellent properties with potential applications against S. cerealella in stored grains. The dried ground leaves and essential oil of Ocimum kilimandscharicum exhibited significant activity against this species in maize and sorghum grains in the laboratory. In particular, there was no adult survival or progeny production in grains treated with each of the two materials at doses of 25.0 g (dried ground leaves) and 0.3 g (essential oil) per 250 g of grain, respectively. In addition, ground leaves and the essential oil protected the grains against feeding, thus resulting in lower weight losses and numbers of damaged seeds compared with untreated grains [206]. When Ocimum suave as dry or ground leaves and essential oil was applied to S. cerealella in maize and sorghum, all treatments evoked higher mortalities in the moths, as well as significant reductions in the progeny produced by the insects [207]. Furthermore, individual plant secondary metabolites exhibit significant biological properties affecting S. cerealella. For instance, when two sesquiterpene lactones, isolated from the surface of leaves and flowers of Cyrtocymura cincta (Griseb.), were tested at 250 and 500 ppm in the diet of S. cerealella they lowered the percentage of adult emergence and produced malformations in adults, altered the oviposition capacity and viability of eggs laid and ceased the production of viable offspring [183]. In another study, the fumigant activity of A. sativum essential oil and its two major components, diallyl disulfide and diallyl trisulfide, expressed as a 50% lethal concentration for the adult moths, was calculated at 1.33, 0.99 and 1.02 µL/L air space, respectively. Additionally, behavioral deterrent activities were noticed, along with reduced adult longevity and inhibited oviposition by more than 70% at a concentration of 1.5 µL/25 g [143]. Considering the mode of action of diallyl trisulfide treatment, it was found to provoke a decrease in the cuticular chitin content of S. cerealella and to reduce the thermal stability and crystallinity of chitin [144]. Diallyl trisulfide was also found to accelerate the rate of metabolism in males at LC10, leading to the accumulation of greater levels of total soluble sugar to support life activities and to the increased synthesis of proteins to resist an adverse environment [145]. Furthermore, female circadian mating rhythms and calling periodicity changed significantly after diallyl trisulfide treatment, whereas mating frequency and mating duration declined [146]. A recent study proved the ovicidal effect of extracts of Tithonia diversifolia (Asteraceae) flowers and Psychotria prunifolia (Rubiaceae) leaves, as well as astilbin from Dimorphandra mollis (Fabaceae) flowers if applied at 1% (w/w or m/m) to eggs of S. cerealella, on grains of Triticum aestivum (Poaceae) and on the surfaces of Petri dishes [184]. When Adeyemo and co-authors applied the powders and extracts of Framomum melegueta on paddies at 0.1 to 0.8 g and 1% to 5%, respectively, they observed the significant reduction or prevention of S. cerealella adult emergence and an increase in the developmental period as well as the reduction or prevention of paddy seed weight loss [140]. In another study, the petroleum ether extract of A. calamus at the application rates of 1000, 500 and 250 μg/g and the acetone extract at 1000 and 500 μg/g completely inhibited the emergence of S. cerealella adults [139]. In a fumigant bioassay the essential oil of Coriandrum sativum was tested against S. cerealella and the LD50 was calculated at 18.76 μg/cm3. Camphor was considered the most active ingredient, with an LD50 of 19.31 μg/cm3 [177]. Furthermore, Nazeri and co-authors studied the fumigant toxicity and sublethal effects of essential oils from Artemisia khorassanica Podl. and Artemisia sieberi Besser on adults of S. cerealella. They found that A. khorassanica (LC50 = 7.38 µL/liter air) was a more active fumigant than A. sieberi (LC50 = 9.26 µL/liter air), and that the insecticidal effect of A. khorassanica (LT50: 9.01 h) was faster than that of A. sieberi (LT50 = 14.37 h). Lastly, the fecundity of S. cerealella was reduced by 25.29% and 35.78% following exposure to sublethal concentrations of A. sieberi and A. khorassanica, respectively [157]. The essential oil of Clausena anisata completely inhibited the viability of the larvae and the emergence of adult butterflies from the dose of 0.5 µL/mL, contrary to Polyalthia longifolia EO, which respectively recorded 10.0% and 50.0% at the dose of 3 µL/mL [174]. The leaf essential oils from Cupressus lusitanica and Eucalyptus saligna were proven to exhibit contact toxicity and air-in-space fumigation against S. cerealella, with LC50 values of 0.11% v/w and 7.02 µL/L, respectively [181]. In another study, Neroli bigarad oil (1.70 μg/cm3) was the most toxic against S. cerealella, followed by Citrus aurantium (1.80 μg/cm3) and Artemisia vulgaris (1.81 μg/cm3) [58,170].
The Indian meal moth (Plodia interpunctella Hubner Pyralidae) is an economically important pest affecting various food products, including cereals, grains and various dry food products. For the most part, the references on plant extracts used to combat P. interpunctella report on essential oils. In this context, when the fumigant toxicity of the C. copticum EO was assessed against growth stages of P. interpunctella, it was concluded that the adults were about 500 times (LC50 = 257.83 µL/m3 air and LC90 = 598.94 µL/m3 air) more susceptible than other growth stages. Furthermore, last-instar larvae (LC50 = 91.36 µL/L air and LC90 = 213.79 µL/L air) and pupae (LC50 = 105.69 µL/L air and LC90 = 203.24 µL/L air) were significantly more susceptible than eggs (LC50 = 184.61 µL/L air and LC90 = 435.32 µL/L air) [226]. In a choice test of P. interpunctella using an olfactometer, the strongest repellency was exhibited by the essential oil of A. graveolens (100%), Thymus vulgaris (100%) and R. officinalis L. (93.33%) and the weakest repellency by Hyossopus officinalis (7.69%) and P. sativum (9.48%) [152]. In another study, the essential oils of myrtle, laurel, marjoram and lemon provoked mortality at 41.66%, 50.83%, 57.50% and 26.66% for P. interpunctella eggs, respectively. At the moderate dose (50 µL/L air) the LT99 values of the most effective essential oil (savory) was 81.88 h for the eggs of the moth [205]. The eggs of P. interpunctella were the most tolerant to the essential oils of garlic, birch (Betula lenta), cinnamon (C. zeylanicum) and aniseed (Pimpinella anisum), with LC90 values ranging from 22.02 to 72.42 µL/L air [147]. The essential oils of oregano and savory were highly effective against P. interpunctella, with 100% mortality obtained after 24 h at 9 µL/L air [205]. The essential oil of Armoracia rusticana was assessed against P. interpunctella and adults were found to be much more susceptible than pupae; its relatively low fumigant effect on pupae might be due to the gas vapor being unable to permeate through the thick wall of the pupal case [54]. After 9 h of exposure, the LC50 values of the essential oil from S. hortensis and Z. officinale for P. interpunctella were 139.8 µL/L and 69.05 µL/L air, respectively [129,218]. In another study, insect-resistant films and anti-insect polymer strips containing cinnamon oil were developed to protect food products from the Indian meal moth [168,169]. When Thymus daenensis essential oil was tested for its fumigant toxicity against first- and third-instar larvae and adults the LC50 values were calculated at 25.32, 34.80 and 0.27 μL/L, respectively [217]. The fumigant activity of essential oil vapors distilled from sweet basil O. basilicum and spearmint Mentha spicata were tested against P. interpunctella at 0.5 to 1.500 µL/L air. Adult moths were the most sensitive, with a notable mortality (>80%) recorded after exposure to low doses such as 2.5 µL/L, but other than that, basil and spearmint oils did not show satisfactory overall insecticidal activity against the moth [202]. In another study, beads of encapsulated coriander and basil EO proved to be efficacious in funnel traps in stores of almonds and pet foods against P. interpunctella [178]. When two Indian spices, namely, Trachyspermum ammi and M. fragrans, were studied for the fumigant activity of their essential oil at 10 µL/L air against P. interpunctella, T. ammi was found to be comparatively more effective [204]. Similarly, the lethal and sublethal effects of essential oils of A. khorassanica and Vitex pseudo-negundo were studied on P. interpunctella. The fumigant toxicity of A. khorassanica (LC50 = 9.60 µL/L air) was higher than that of V. pseudo-negundo (LC50 = 23.05 µL/L air) and the exposure to sublethal concentrations of A. khorassanica negatively affected the protein, lipid and glycogen contents of the larvae coming from treated adults [158]. In another study, the toxicity of the essential oils isolated from parsley, P. crispum and coriander, C. sativum, was studied, and the LC50 values were calculated to be 55.197 and 50.956 μ/L air for P. interpunctella larvae, respectively. In another study, M. piperita and S. officinalis were incorporated into polylactic acid solution to test for contact toxicity on P. interpunctella. The product showed higher contact toxicity than the pure essential oil because the ploylactic acid nanofibers cause surface tension and longer efficiency times due to the slow release. Moreover, M. piperita showed higher toxicity than S. officinalis [165]. A multilayered insect-proof film preventing contamination with P. interpunctella was developed based on garlic and onion EOs and their compounds chosen as efficient anti-insect agents [142]. When lavender (L. angustifolia), peppermint (M. piperita), geranium (Geranium maculatum), palmarosa (Cymbopogon martini (Roxb.) Wats), eucalyptus (E. globulus) and bergamot (Citrus bergamia Risso) were used against adult moths, the contact toxicity assay showed that the EO from palmarosa was the most toxic, with an LD50 value of 22.8 μg/cm2, and the greatest fumigant toxicity was found with the EO from eucalyptus, with a KT50 value of 8.34 min [171]. In another study, low-density polyethylene-laminated polypropylene films printed with ink incorporating microencapsulated cinnamon oil using a large-scale film production system effectively repelled Indian meal moth larvae [167]. Eucalyptus dives oil and constituent 3-carvomenthenone, cyclohexanone (LD50 against, 2.45 and 3.63 μg/cm3), methylcyclohexanone (2.95 and 4.24 μg/cm3) and seudenone (3.02 and 4.44 μg/cm3) were proven to have fumigant activity against larvae and adults of Plodia interpunctella [190]. In a recent study, geranium EO (G. maculatum) was used to develop micro and nanoemulsions, adding Tween 80 as surfactant which was stable at 25 °C for 60 days. This formulation can increase the insecticidal efficacy of EO twofold [192]. The essential oil distilled from Lippia turbinata (“poleo”) was insecticidal on P. interpunctella larvae [198]. In a recent study, the essential oils (O. vulgare, P. anisum and Tanacetum cinerariifolium) and four plant extracts (Agastache rugosa, Capsicum annuum, C. reticulata and Ginkgo biloba) were proven to be repellent against P. interpunctella. Additionally, O. vulgare and T. cinerariifolium had greatest repellent efficacy against the moth larvae [46]. In another study, insect-resistant adhesives were developed for application to a cardboard packaging system for preventing P. interpunctella larvae infestation. Cinnamon EO was used as an , encapsulated with maltodextrin, β-cyclodextrin and polyvinyl alcohol, in corn starch paste that was able to control insect penetration in the distribution and storage steps [166].
There are fewer studies referring to other essential oil plant extracts and powders used for controlling P. interpunctella. In a study conducted by Akkineye and co-authors the root bark powder of Cleisthopholis patens at 1.0, 2.0 and 3.0 g/20 g of the maize evoked 100% adult moth mortality within 72 h of application, whereas the stem bark powder of C. patens at 1.0, 2.0 and 3.0 g/20 g of the maize produced 78%–100% moth mortality within 72 h of treatment. The leaf powder was moderately effective against the adult moth at 3.0 g/20 g of the maize grain, evoking 70%–80% adult mortality within 96 h of treatment [175]. The methanol extracts of Peganum harmala, Ajuga iva, R. officinalis L., L. stoechas, Lavandula dentata, Cistus ladanifer, Cistus salviaefolius, Cistus monspeliensis, Centaurium erythraea and Launaea arborescens were tested at 500 ppm on post-embryonic development parameters of P. interpunctella. Most plant extracts provoked a notable decrease in larval weight, causing significant alterations on pupation and adult emergence. When applied at 500, 750 and 1000 ppm, they also affected physiological parameters such as larval reserve substances and the midgut activities of hydrolytic and detoxification enzymes [141]. Plant protease inhibitors regulate proteolytic processes in insects and are thus considered to be a potential safe weapon against insect pests, either through their direct application or via their expression in transgenic plants. In this regard, medicinal legume plants, namely, senna (Cassia angustifolia) and fenugreek (T. foenum-graecum), could be used for their total proteolytic inhibitory activity against the Indian meal moth larval midgut [164]. Another study investigated a bioinspired cyanogenic grain coating with amygdalin as a cyanogenic precursor, mimicking the feeding-triggered release of hydrogen cyanide found, for example, in bitter almonds. Upon feeding of coated cyanogenic wheat grains to T. molitor L., R. dominica Steph. (lesser grain borer) and P. interpunctella, their reproduction, as well as consumption rate, were significantly reduced, whereas their germination ability increased compared to non-coated grains [216]. Diterpene resin acids are important components of oleoresin and greatly contribute to the defense strategies of conifers against herbivorous insects and also function as insect juvenile hormone antagonists that interfere with the juvenile hormone-mediated binding of the JH receptor methoprene-tolerant and steroid receptor coactivator protein [211]. Hexane extracts of the roots of Piper sarmentosum Roxb. and constituent asaricin 1, isoasarone 2 and trans-asarone 3 were toxic to P. interpunctella [212]. Plant juvenile hormone disruptor activity is concentrated in certain plant groups, families and their plant metabolites, which have insect group-specific activity. Reciprocal diversification has occurred between plants and insects through the evolution of secondary plant metabolism and juvenile hormone receptors, respectively, and that plant metabolites could be developed into insect group-specific pesticides with limited effects on non-target species [227].
The rice moth (Corcyra cephalonica Stainton, Pyralidae) feeds on both seeds and flour. Most of the literature on natural substances against C. cephalonica investigate essential oils, although constraints including a lack of data for single or multiple components of essential oils in terms of their sorption, tainting and residues in food commodities, and registration protocols are yet to be highlighted [10]. M. piperita and Piper nigrum EO LC50 values against the larvae were calculated at 343.9 and 530.5 µL/L of air 72 h after commencement [113]. In a fumigation assay, coriander and eucalyptus oils at 130μg/cm2, caused 100% toxicity to C. cephalonica within 24 h of treatment, whereas pine oil revealed 90% mortality at the same concentration after 72 h of treatment. In a contact assay, the test oils were effective against adults producing about 90% toxicity only after 72 h of treatment [82]. The fumigant toxicity of Origanum majorana essential oil against C. cephalonica adults and larvae was calculated, with LC50 values of 11.31 and 49.83 µL/L air, respectively. The contact toxicity against adult, pupa, larvae and eggs was observed, with LC50 values of 2.54, 0.95, 2.78 and 0.49 µL/L, respectively. The acetylesterase inhibition activity of O. majorana EO was observed against adults and larvae, with LC50 values of 35.89 and 118.54 µL/mL, respectively [208].
Plant extracts of Lawsonia inermis, petroleum ether (pet ether) extract, produced a complete inhibition of the moths, and were thus recorded as the best repellants (96.70%), whereas Parthenium hysterophorus, Dalbergia sissoo (acetone extracts) and Acacia nilotica (acetone and pet ether extracts) showed 70% repellency. However, a minimum of 30.81% repellency was exhibited by Eucalyptus rudis (pet ether extract) [138]. Larvicidal and pupicidal effects of Dryopteris filix-mas root and rhizome ethanolic extracts were studied against the third-instar larvae of C. cephalonica. D. filix-mas extract 0.20% (v/w) caused 100% larval mortality. The plant extracts reduced the pupation percentage, pupal death and adult emergence, indicating absolute toxicity to the pest [185]. Essential oils isolated from pine (Pinus longifolia), eucalyptus (Eucalyptus obliqua) and coriander (C. sativum) were screened for contact and fumigant activities. In a fumigation assay, coriander and eucalyptus oils at 130μg/cm2 caused 100% toxicity within 24 h of treatment, whereas pine oil revealed 90% mortality at the same concentration after 72 h of treatment. In a contact assay, the test oils were effective against adults, producing about 90% toxicity only after 72 h of treatment [82]. High larvicidal, adulticidal, antifeedant and oviposition deterrent activities were exhibited by hexane extracts of Glossocardia bosvallia 30 and 60 mg/mL in wheat grains [193]. Acetone extracts of young leaves, old leaves, flowers and stems of groundnut plant with Trichogramma chilonis (Ishii) and C. zastrowi sillemi (Esben-Petersen) revealed their kairomonal activities under in vitro conditions against C. cephalonica [154].
Fumigation with essential oils of Eucalyptus platyphylla and M. piperita, at different concentrations, on adults of the almond moth, Ephestia cautella Walker (Pyralidae), showed that those of M. piperita caused the highest mortality rates [191]. The almond moth, E. cautella Walker, comes from the family Pyralidae. In a filter paper contact toxicity bioassay, potent toxicity was produced from buchu leaf, niaouli and rosemary oils at 2.4 mg/cm and armoise, cypress, galbanum and mace oils at 4.7 mg/cm against E. cautella Walker. In vapor phase toxicity bioassays with larvae, cypress, galbanum, niaouli and rosemary oils were much more effective in closed containers than in open containers, indicating that the lethal effects of these oils were largely because of action in the vapor phase [159]. In another study, early eggs of E. cautella Walker showed a lower LC50 value of 48.56 µL/L, compared to 77.75 µL/L with late eggs, when the essential oil of Lantana camara was used to treat them with fumigation [194]. Finally, in a recent study it was found that extracts of Calotripis procera roots displayed the most potent activity, with 50% of E. cautella Walker eggs not hatching at 10.000 ppm (1%). The chemical composition analysis of the extracts demonstrated a high presence of cardenolides, including calactin, uscharidin, 15β-hydroxy-calactin, 16β-hydroxy-calactin and 12β-hydroxy-calactin [162]. When five Eucalyptus species, namely, E. camaldulensis, E. astringens, E. leucoxylon, E. lehmannii and E. rudis, were assessed for their fumigant activity on Ephestia spp., the E. camaldulensis essential oil was more toxic against E. cautella and Ephestia kuehniella Zeller and the LC50 values were 11.07 and 26.73 µL/L air, respectively. In all cases the fumigant activity was strongest for the summer season oils and E. cautella was the most sensitive species [189]. In a choice test, rosemary and eucalyptus revealed high percentages of repellency after 5 days, at 72% and 50%, respectively, in the case of E. kuehniella and 71% and 54%, respectively, in case of E. cautella.
The most effective oil in enhancing the potency of an entomopathogenic fungus, Metarhisium anisopliae, against insect species was rosemary and it decreased the LC50 for E. cautella and E. kuehniella, respectively [148]. When the oils of Capsicum frutescens, Anacardium occidentale, Monodora tenuifolia, Xylopia aethiopica and Ricinus communis were studied at 0.5 mL and 1.0 mL dosages against the egg, larvae and adults of E. cautella, A. occidentale was found to be the most effective [150]. E. angustifolia ethyl acetate and aqueous extracts caused mortality of E. cautella, observed after 24 and 48 h of treatment [186]. The ethanolic oil extract of M. tennuifolia achieved 100% E. cautella moth mortality and its effect was significantly (p < 0.05) different from that of all other extracts. However, petroleum ether increased the effect of the other extracts on the survival of the moth, as reflected by their LD50 values. Regardless of the solvent used, all the oils reduced the hatchability of the eggs of the insect, and the adult emergence of the insect was prevented by all the oil extracts [151]. Another study was conducted to evaluate the activity of the neem oil of Azadirachta indica and Bacillus thuringiensis alone and in combination in controlling E. cautella. The B. thuringiensis LC50 was at 0.1% concentration after one day of treatment, whereas the effect of the combination of B. thuringiensis and neem oil showed an increase in the mortality rate of larvae treated with the combination, as compared with the treatment with each separately [160].
The Mediterranean flour moth (also known as the mill moth, Ephestia kuehniella) is another species from the same family and genus as E. cautella, and is similarly an important pest affecting grains and flour. E. camaldulensis essential oil was toxic against E. cautella and the LC50 value was 11.07 µL/L air, whereas the median lethal time (LT50) value was 13.49h [189]. Exposure to vapors of essential oils from anise and cumin resulted in 100% mortality of E. kuehniella eggs. Oregano achieved mortality as high as 89%, whereas eucalyptus and rosemary achieved 45% and 65%, respectively [180]. In another study, the average mortality rates with a dose of 10 µL of essential oils of Origanum acutidens, Satureje hortensis, Hypericum scabrum, T. vulgaris, Micromere fruticosa, Salvia limbata C. A. Meyer, S. nemerosa and Hyssoppus officinalis were approximately 74%, 66%, 73%, 4%, 12%, 7%, 10% and 14% for S. granarius, and 79%, 62%, 72%, 24%, 24%, 6%, 0% and 14% for E. kuehniella, respectively [117]. Essential oil vapors of Micromeria fruticosa, Nepata racemosa and O. vulgare tested at 8 µL/L air provoked 100% mortality of the larvae (third instar) of E. kuehniella after 120 h of treatment [203]. Essential oil vapors from the plant species O. acutidens achieved 100% mortality with a dose of 2 µL/L air within 96 h in third-instar larvae of E. kuehniella [124]. Assessing the ovicidal activity of five essential oil vapors distilled from savory Satureja thymbra, laurel L. nobilis, myrtle Myrtus communis, lemon Citrus limon and marjoram O. majorana, the essential oil obtained from savory produced 100% mortality for the eggs of E. kuehniella and at the moderate dose (50 µL/L air) the LT99 values of the most effective essential oil, savory, were 158.50 and 81.88 h for the eggs of E. kuehniella [172]. The effects of vapors of essential oils from garlic, birch (B. lenta), cinnamon (C. zeylanicum) and aniseed (Pimpinella anisum) were studied on eggs of E. kuehniella. Generally, garlic and birch essential oils were more toxic to the eggs of the tested insect species than cinnamon and aniseed essential oils. Garlic and birch essential oils were found to be very promising since they also showed high fumigant toxicity on eggs of E. kuehniella [147]. When the essential oils from oregano, Origanum onites; savory, Satureja thymbra; and myrtle, Myrtus communis were tested on E. kuehniella adults, oregano and savory achieved 100% mortality, obtained after 24 h at 25 µL/L air [205]. Pistacia lentiscus oil was toxic to E. kuehniella with LC50 = 1.84 µL/L and LC95 = 5.14 µL/L, respectively. At 136 µL/L air, fecundities and hatching rates were 78 eggs/female and 29.49% [213]. The preventative properties of Cinnamomum camphora and Syzygium aromaticum to the E. kuehniella 5th-instar larvae penetration to packaged cereals were tested by Allahvaisi and co-workers. Four days after the initiation of the experiment, the results showed that S. aromaticum had more of a repellency effect than C. camphora [165]. In another study, the toxicity of S. hortensis essential oil was investigated against 12-to-14-day-old larvae of the Mediterranean flour moth. LC50 values were calculated as 80.9 µL/L after 9 h for E. kuhniella, and additional repellency was evident [129]. Origanum majorana and Citrus limon were the most effective essential oils against E. kuehniella and the LC50 and LC99 values were estimated to be 3.27 and 5.13 µL/L of air for marjoram and 4.05 and 5.57 μ/L of air for lemon essential oils at the longest exposure time [173]. O. basilicum and Z. officinale oils produced 100% mortality within 24 h with doses of 32 µL/L air for E. kuehniella adults, whereas A. graveolens oil was the most active against E. kuehniella larvae. The oils were selected as having a possible application as a 30% aqueous solution for the protection of wheat flour [153]. In another study, the insecticidal activity of the essential oil from cardamom, Elettaria cardamomum, on adults of E. kuehniella was investigated, and the highest mortality of these insects was seen after 12 h [187]. The fumigant toxicity varies with season, essential oil concentration and exposure time, as shown for five Eucalyptus species, as tested by Ben Jemâa and co-authors against E. kuehniella [189]. In another study, the LC50 value for E. kuehniella after 9 h was calculated as 258.95 µL/L air. In a contact toxicity assay, Z. officinale essential oil’s LC50 value for E. kuehniella was determined to be 0.61 µL/cm2 and its repellency was significant [218]. The toxicity of vapors of the essential oil of Ferula gummosa, Elettaria cardamomum and S. officinalis was tested on the adults and larvae of E. kuehniella and the results indicated that the effect of the essential oil of F. gummosa was the strongest [188]. The insecticidal effect of Cupressus sempervirens horizontalis resin essential oil exposure (48 h) on E. kuehniella eggs showed 20.83% mortality at a 100 µL/L air concentration [182]. In another study, the repellent effects of essential oils from L. nobilis and M. communis against adults of E. kuehniella were studied. Around 20.4% and 10.6% repellency rates were observed at the lowest concentration (0.50 µL/L) of L. nobilis and Myrtus commonis, respectively. Furthermore, at the highest-concentration (2.00 µL/L air) repellency rates reached 84.2%, obtained by L. nobilis, and 61.3%, obtained by M. commonis [195]. Hematological observations showed that in comparison to fumigation, the topical application of Callistemon viminalis and Ferula gummosa oils caused a drastic reduction in the total hemocyte counts of treated larvae in a dose-dependent manner at all time intervals [161]. When T. daenensis essential oil and its toxicity was investigated against the first- and third-instar larvae and adults of E. kuehniella in terms of fumigant toxicity, the adult stage was more sensitive, whereas the sensitivity of larvae decreased from the first to the third instar [217]. Essential oils of the resins of Pinus brutia and P. pinea were found to be insecticidal on E. kuehniella eggs [182]. When essential oils from sweet basil O. basilicum and spearmint Mentha spicata L. were tested against on E. kuehniella no significant differences were found in insecticidal action and both oils produced a notable level of mortality (>80%) after exposure to low doses, such as 2.5 µL/liter. Larvae and pupae were the most tolerant stages in all cases [202]. In another study, the fumigant toxicity potential of L. angustifolia oil (LC50 = 19 μL/L air) was greater than that of R. officinalis oil (LC50 = 28 μL/L air) as regards E. kuehniella larvae [196]. Εssential oils of Artemisia haussknechtii and Citrus vulgaris exhibited LC50 values of 479.13 and 110.98 µL/L air E. kuehniella [155]. The LC50 value of Ziziphora clinopodioides Lam. oil was estimated to be 54.61 µL/L air for E. kuehniella larvae and 1.39 µL/L air for adults [219]. Beads of encapsulated coriander and basil EO were tested in funnel traps in stores of almonds and pet foods for 2 months. The number of adult moth E. kuehniella dead captures was similar with either coriander or basil EO beads and with vapona tablets, although there were more insects alive in the control [178]. The LC50 values of C. sativum and P. crispum essential oils were 62.633 and 52.412 μL/L air against E. kuehniella [179]. Purslane oil (bulk) exhibited mortality against larvae of E. kuehniella, with 66.64%, 55.21%, 45.32% and 18.61% mortality rates gained at 3%, 1.5%, 0.5% and 0.2% concentrations, respectively. However, the mortality values amounted to 96.64%, 88.68%, 78.79% and 60.61% when the larvae were exposed to 0.1%, 0.5%, 0.05% and 0.005% concentrations of nano-purslane, respectively [215]. Concentrations of 5.42 and 6.81 µL/ml were obtained as LC50 values for C. copticum essential oils and thymol, and these significantly influenced the enzymatic activities of E. kuehniella [163]. As for E. cautella, as well as for E. kuehniella, the potential activities of four essential oils (anise, eucalyptus, garlic and rosemary) and the microbial agent M. anisopliae and their combinations were evaluated. The most effective oil in enhancing the potency of M. anisopliae was rosemary, against both insect species [149]. The LC50 value for M. longifolia essential oil in regard to E. kuehniella was 21,352 ppm, whereas this value for the nanoemulsion was 14,068 ppm. In addition, M. longifolia oil had lower durability and the 50% persistent time (PT50) was 2.39 days, compared to the nanoemulsion’s value of PT50 = 17.13 days, in the highest concentration of essential oil [199]. In another study, the effect of the essential oil of Origanum vulgaris was tested on the reproduction and mortality of the flour moth E. kuehniella. It was found to affect the pupal development. It also disrupted the reproduction of exuviated adults by extending the preoviposition period and reducing the period of egg-laying and fecundity because fecundated females could not live more than four days compared to the control group [209]. In a recent study, wormwood (A. herba-alba), O. vulgare and rue (Ruta montana) were evaluated for their repellent and fumigant toxic potential against larvae of the flour moth E. kuehniella. Origanum oil was the most repellent, with a 67% repellency rate, followed by Artemisia oil (46%) at 120 µL/mL after 2 h of exposure. The oil of R. montana showed attractant activity against the larvae and was the most toxic, with 56.7% of larval mortality in the first 24 h. The median lethal concentrations (LC50) recorded were 11.6, 175.4 and 1100.0 µL/L air for the plant oils R. montana, O. vulgare and A. herba-alba, respectively. R. montana and O. vulgare essential oils were shown to be efficient, with high toxic and repellent properties against E. kuehniella larvae [156]. The lethal concentration values of O. basilicum, Mentha pulegium and Ruta graveolens were, respectively, 0.96, 0.3 and 1.02 µL/L air on E. kuehniella [201]. In a recent study, highly synergistic effects, considering antifeedance, relative growth rate and relative consumption rate, were observed in 1.14 and 1.7 µL/L air of L. angustifolia in combination with 200 Gy of gamma radiation [197].

3. Practical Concerns

In recent years, environmental contamination, pesticide resistance and the destruction of nontarget organisms have led to increased support for environmentally safe pesticide alternatives to the use of synthetics. The research on botanical pesticides for pest management practices has intensified because they demonstrate a wide range of bioactivities and display contact and fumigant toxicity, as well as repellent activity, effects on oviposition and feeding deterrence. Additionally, many botanicals display low mammalian toxicity and rapid degradation. In this regard, EOs may prove to be reasonable alternatives to the more persistent synthetic pesticides as tools to control stored-product insects, even combined with gamma radiation or diatoms [228]. However, the number of commercial biopesticides based on EOs remains low and the key challenges include the stabilization processes (e.g., microencapsulation) and authorization requirements, as well as plant growing conditions and extraction processes [229]. Loading EOs in nanostructured systems represents a potential solution to their sensitivity to pH, oxygen, light and moderate temperatures. The use of biopolymers as nanocarriers provides the controlled release of the active ingredient, also ameliorating the issues of biodegradability, biocompatibility, environmental safety, low toxicity and competitive production costs [230]. Other than EO plant-based products (powders, extracts, essential oils, etc.) are also cost-effective alternatives to synthetic insecticides, and these are of great importance regarding insect pest control strategies for stored food commodities. To date, there have been serious bottlenecks in regard to their commercialization and standardization, including their low priority in agricultural policy, as well as biosafety and intellectual property rights issues [231]. The commercialization of new botanical insecticides and the market expansion of existing botanicals has lagged considerably, considering the academic interest demonstrated in the past 20 years. Some countries (such as Turkey, Uruguay, the United Arab Emirates and Australia) have relaxed regulatory requirements for specific plant extracts and oils, whereas in North America and the European Union, stricter requirements have slowed progress toward the commercialization of new products. Thus, botanicals are likely to remain niche products for some countries, while having the greatest impact in places where the source plants are readily available and where conventional products are both expensive and dangerous to users [9].

4. Conclusions

Plant extracts have been tested mainly in the form of essential oils against stored grain pests and, in some cases, the research has extended as far as including the main components of these oils.
Regarding mites, studies have addressed the effects on pests, as well as predatory species. There are three substances that have shown the best results when tested in the lowest of concentrations, even lower than benzyl-benzoate (an already industrially available product). These substances are components of the clove bud (E. caryophyllata) essential oil, methyleugenol, forget-me-not (M. arvensis) essential oil and benzaldehyde of P. persica. Furthermore, cinnamon (naturally containing benzyl-benzoate) has been proven to be effective against T. putrescentiae, T. molitor, S. oryzae, R. dominica, P. interpunctella and E. kuhniella as a contact toxicant to larvae or adults, as a repellant or as a fumigant. However, detailed knowledge of the lethal or non-lethal effects of botanical pesticides on beneficial insects is important for integrated pest management (IPM).
Regarding the impact of pesticides on Coleoptera and Lepidoptera, many plant species have been studied for their pesticidal properties. C. copticum was found to be active against T. confusum, S. granarius, P. interpunctella and E. kuehniella, whereas basil was effective as a fumigant for S. zeamais, O. surinamensis and E. kuehniella. Most interestingly various Citrus species were effective as fumigants, contact toxicants and as repellants, for both Coleopterans (T. castaneum, S. oryzae and C. ferrugineus) and Lepidoptera (P. interpunctella, S. cerealella and E. kuehniella). In addition, in regard to Lepidoptera, many substances have been evaluated for sublethal effects (C. cincta lowered the percentage of adult emergence, and A. sativum reduced adult longevity and inhibited oviposition), whereas for Coleoptera only a few studies of sublethal effects are available.
T. minuta and T. patula extracts were very effective fumigants against T. castaneum Herbst, whereas Eucalyptus spp. extracts were very effective fumigants against the adults of R. dominica, T. castaneum and O. surinamensis, but were also very effective against Lepidoptera (E. kuehniella, E. cautella, C. cephalonica and P. interpunctella) as fumigants or repellents. C. reticulata and C. sinensis essential oils were among the few substances found to be effective against Coleoptera (T. castaneum) larvae, as was the garlic essential oil, causing necrosis to the larvae, pupae and adults of T. molitor L. The fumigant properties of C. citratus and Z. officinale were the most effective fumigants against the rice weevil. Furthermore, A. judaica and C. viminals had two of the lowest LC50 values observed in this entire review. L. salicifolia, L. nobilis and E. floribundi were significantly effective repellents, whereas O. acutidens and C. reticulata were effective fumigants against L. serricorne and C. ferrugineus.
Finally, regarding Lepidoptera, the essential oil of C. anisata was found to be completely toxic to the larval stages, and also inhibited the emergence of adults. M. piperita and S. officinalis incorporated into polylactic acid solution showed significant contact toxicity on P. interpunctella, whereas M. piperita showed higher toxicity than S. officinalis. The essential oils exhibiting contact toxicity showed higher toxic effects when they were loaded on polymeric nanoparticles, as in the case of palmarosa (C. martinii), geranium (G. maculatum), and peppermint (M. piperita) against P. interpunctella. Eucalyptus spp. was the most tested substance in Lepidoptera, achieving 100% mortality, and it was effective as a fumigant and exhibited contact toxicity. Additionally, purslane essential oil was very effective against E. cautella in terms of fumigant toxicity, oviposition deterrence and persistence against larvae and adults. M. tennuifolia achieved 100% E. cautella moth mortality and reduced the hatchability of the eggs, whereas adult emergence was prevented, making it a very useful tool against E. cautella; as was birch essential oil, which displayed high fumigant toxicity on the eggs of E. kuehniella. Furthermore, A. graveolens oil was found to be the most active against E. kuehniella larvae, the life stage of the Lepidoptera species that causes the most damage. Finally, the essential oil of O. vulgaris was found to affect pupal development and disrupt the reproduction of exuviated adults by extending the preoviposition period and reducing the period of egg-laying and fecundity.
In general, there is a shortage of tools for combatting stored-product pests, as an alternative to the use of synthetics. With this review, we refer to the botanical substances reported in the literature of recent years to exhibit pesticidal properties of potential utility in the management of stored products.

Author Contributions

Conceptualization, P.N., P.M., Z.A. and N.N.; writing—original draft preparation, P.N., P.M., Z.A. and N.N.; writing—review and editing, P.N., P.M., Z.A. and N.N. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. Plant species reported to exhibit significant activity against stored-product pests in recent years.
Table 1. Plant species reported to exhibit significant activity against stored-product pests in recent years.
Mites
Plant SpeciesFormulation Pest SpeciesReference
Allium sativumessential oil Tyrophagus putrescentiae [29,31]
essential oilCheyletus malaccensis[30]
Azadirachta indicaCommercial product of neem Tyrophagus putrescentiae [13,20]
(Fortune AZA) Acarus siro
Lepidoglyphus destructor
Carum carviessential oil Gohieria fusca [25]
Lepidoglyphus destructor
Acarus siro
Tyrophagus putrescentiae
Cinnamomum zeylanicumessential oil Tyrophagus putrescentiae [33]
Eucaliptus globulusessential oil Tyrophagus longior [35]
Eugenia caryophyllataessential oil Tyrophagus putrescentiae [21]
Eugenia unifloraessential oil Tyrophagus putrescentiae [33]
Eugenia uvalhaessential oil Tyrophagus putrescentiae [33]
Juniperus chinensisessential oil Tyrophagus putrescentiae [41]
Lavandula angustifoliaessential oil Tyrophagus longior [35]
Lavandula stoechasessential oil Tyrophagus longior [35]
Ligustrum japonicumessential oil Tyrophagus putrescentiae [24]
Melaleuca leucadendraessential oil Tyrophagus putrescentiae [33]
Mentha piperitaessential oil Tyrophagus longior [35]
Myosotis arvensisessential oil Tyrophagus putrescentiae [28]
Ocimum basilicumessential oil Tyrophagus putrescentiae [29]
Petroselinum sativumactive constituents Tyrophagus putrescentiae [27]
Pinus pineaessential oil Tyrophagus putrescentiae [40]
Pinus halepensisessential oil Tyrophagus putrescentiae [40]
Pinus pinasteressential oil Tyrophagus putrescentiae [40]
Pinus nigraessential oil Tyrophagus putrescentiae [40]
Piper marginatumessential oil Tyrophagus putrescentiae [33]
Prunus persicaessential oil Tyrophagus putrescentiae [37]
Rosmarinus officinalisessential oil Tyrophagus putrescentiae [22]
Schinus terebinthifoliusessential oil Tyrophagus putrescentiae [33]
Trigonella foenum-graecumessential oil Tyrophagus putrescentiae [29]
Coleoptera
Plant SpeciesFormulationPest SpeciesReference
Achillea wilhelmsiiessential oilTribolium castaneum[42]
Achyranthus asperaessential oilCryptolestes ferrugineus[43]
Acisanthera.ethanolic extractTenebrio molitor[44]
Acorus calamusessential oilSitophilus oryzae[45]
Tribolium castaneum
Adenocalymma nodosumethanolic extractTenebrio molitor[44]
Agastache rugosaplant extractTribolium castaneum[46]
Allium sativumpowderOryzaephilus surinamensis[47]
essential oilTenebrio molitor[48]
essential oilSitophilus oryzae[49]
Tribolium castaneum
Alpinia blepharocalyxessential oilLasioderma serricorne[50]
Amomum maximumessential oilTribolium castaneum[51]
Amomum tsaokoessential oilLasioderma serricorne[52]
Tribolium castaneum
Anethum graveolensessential oilSitophilus zeamais[53]
Armoracia rusticanaessential oilSitophilus zeamais[54]
Artemisia absinthiumpowderOryzaephilus surinamensis[47]
Artemisia anethoidesessential oilLasioderma serricorne[55]
Tribolium castaneum
Artemisia herba-albaessential oilOryzaephilus surinamensis[56]
Tribolium castaneum
Artemisia judaicaessential oilSitophilus oryzae[57]
Artemisia monosperma
Artemisia vulgarisessential oilSitophilus zeamais[58]
Artemisia stoloniferaessential oilLasioderma serricorne[59]
Tribolium castaneum
Aster ageratoidesessential oilSitophilus zeamais[60]
Tribolium confusum
Astoma seselifoliumessential oilSitophilus oryzae[57]
Atalantia guillauminiiessential oilLasioderma serricorne[61]
Tribolium castaneum
Azadirachta indicaessential oilTribolium castaneum [62]
seed oil
Bauhinia purpureamethanol extractTrogoderma granarium[63]
Bidens sulphureaethanolic extractTenebrio molitor[44]
Caesalpinia gilliesiimethanol extractTrogoderma granarium[63]
Carum carviessential oilTribolium castaneum[64]
Sitophilus oryzae
Rhizopertha dominica
Carum copticumessential oilSitophilus granarius[65]
Tribolium confusum
Caryopteris incanaessential oilSitophilus zeamais[66]
Calendula officinalisessential oilSitophilus granarius[67]
Callistemon viminalsessential oilSitophilus oryzae[57]
Capsicum annuumplant extractTribolium castaneum [46]
Cassia fistulamethanol extractTrogoderma granarium[63]
Cassia occidentaliswater extractOryzaephilus surinamensis[68]
ethanol extract
acetone extract
Cassia sennamethanol extractTrogoderma granarium[63]
Cayratia japonicaessential oilSitophilus zeamais[69]
Tribolium castaneum
Chenopodium albumether extractOryzaephilus surinamensis[70]
Chrysanthemum frutescensmethanol extractTrogoderma granarium[63]
Cinnamomum verumessential oilTenebrio molitor[71]
Tribolium castaneum[64]
Sitophilus oryzae
Rhizopertha dominica
Citrus aurantifoliaessential oilSitophilus oryzae[57]
Citrus lemonessential oilSitophilus oryzae[57]
Citrus medicaessential oilTribolium castaneum[72]
Citrus paradisiessential oilRhizopertha dominica[73]
Citrus reticulataessential oilTribolium confusum[74]
powderTribolium castaneum[46,75]
ethanol extract
essential oil[76]
essential oilCryptolestes ferrugineus[77]
essential oilRhyzopertha dominica[73]
Citrus sinensisessential oilTribolium castaneum[76]
essential oilRhizopertha dominica[78]
essential oilSitophilus oryzae[57]
essential oilSitophilus zeamais[79]
Calamintha glandulosaessential oilTribolium castaneum[80]
Clausena anisum-olensessential oilLasioderma serricorne[81]
Cleome viscosawater extractOryzaephilus surinamensis[68]
ethanol extract
acetone extract
Coriandrum sativumessential oilSitophilus oryzae[82]
Crithmum maritimumessential oilOryzaephilus surinamensis[83]
Sitophilus granarius
Sitophilus oryzae
Tribolium castaneum
Tribolium confusum
Cuminum cyminumessential oilSitophilus zeamais[53]
Cupressus lusitanicaessential oilSitophilus zeamais[84]
Tribolium castaneum
Cupressus macrocarpaessential oilSitophilus oryzae[57]
Cupressus sempervirensessential oilSitophilus oryzae[57]
Cymbopogon citratusessential oilSitophilus oryzae[85]
essential oilTribolium castaneum[86]
Cymbopogon giganteusessential oilTribolium castaneum[86]
Cymbopogon schoenanthusessential oilTribolium castaneum[86]
Cymbopogon winterianusessential oilTribolium castaneum[64]
Sitophilus oryzae
Rhizopertha dominica
Dahlia pinnataessential oilSitophilus oryzae[50]
Sitophilus zeamais
Dennettia tripetalaessential oilSitophilus oryzae[87]
Dimorphandra mollisethanolic extractTenebrio molitor[44]
Dracocephalum moldavicaessential oilSitophilus zeamais[88]
Tribolium confusum
Drimys winteriessential oilTribolium castaneum[89]
Dictamnus dasycarpusessential oilLasioderma serricorne[90]
Eruca sativaessential oilTribolium confusum[74]
Etlingera yunnanensisessential oilTribolium castaneum[91]
Eucalyptus camaldulensisessential oilSitophilus oryzae[92,93]
Tribolium castaneum
Eucalyptus citriodoraessential oilTribolium castaneum[86]
Eucalyptus floribundiessential oilOryzaephilus surinamensis[94]
Rhizopertha dominica
Eucalyptus globulusessential oilTribolium confusum[74]
essential oilLasioderma serricorne[95]
Rhizopertha dominica
Eucalyptus intertextaessential oilSitophilus oryzae[93]
Tribolium castaneum
Eucalyptus leucoxylonessential oilSitophilus oryzae[96]
Tribolium castaneum
Eucalyptus obliquaessential oilSitophilus oryzae[82]
Eucalyptus proceraessential oilTribolium castaneum[97]
Eucalyptus salignaessential oilSitophilus zeamais[84]
Tribolium castaneum
Eucalyptus sargentiiessential oilSitophilus oryzae[93]
Tribolium castaneum
Euonymus japonicusmethanol extractTrogoderma granarium[63]
Ferula narthexessential oilCryptolestes ferrugineus[43]
Foeniculum vulgareessential oilSitophilus zeamais[53]
essential oilTribolium castaneum[64]
Sitophilus oryzae
Rhizopertha dominica
Ginkgo bilobaplant extractTribolium castaneum[46]
Hyptis suaveolensessential oilRhizopertha dominica[98]
Sitophilus oryzae
Tribolium castaneum
Juniperus formosanaessential oilTribolium castaneum[99]
Juniperus polycarpusessential oilTribolium confusum[100]
Juniperus sabinaessential oilTribolium confusum
Kadsura heteroclitaessential oilSitophilus zeamais[101]
Laurelia sempervirensessential oilSitophilus zeamais[102]
essential oilTribolium castaneum [89]
Laurus nobilisessential oilLasioderma serricorne[103]
Rhizopertha dominica [104]
Tribolium castaneum
Laggera pterodontaessential oilLasioderma serricorne[105]
Lavandula angustifoliaessential oilSitophilus granarius[106]
Lavandula officinalisessential oilSitophilus oryzae [92]
Tribolium castaneum
Lavandula stoechasessential oilLasioderma serricorne[95]
Rhizopertha dominica
Tribolium castaneum
Lepidoploa aureaethanolic extractTenebrio molitor [44]
Litsea cubebaessential oilLasioderma serricorne[107]
Litsea salicifoliaessential oilSitophilus zeamais[108]
Tribolium castaneum
Linium usitatissiumessential oilCryptolestes ferrugineus[43]
Lippia javanicaessential oilSitophilus zeamais[109]
Lippia sidoidesessential oilTenebrio molitor[110]
Liriope muscariessential oilLasioderma serricorne[111]
Tribolium castaneum
Maytenus emarginataether extractOryzaephilus surinamensis[70]
Melia azedarachessential oilCryptolestes ferrugineus[43]
Mentha piperitapowderOryzaephilus surinamensis[47]
essential oilTribolium castaneum [112]
Lasioderma serricorne
essential oilSitophilus oryzae[113]
Mentha longifoliaessential oilTribolium castaneum[42]
essential oilSitophilus zeamais[114]
Mentha pulegiumessential oilSitophilus granarius[115]
essential oilTribolium castaneum [116]
Lasioderma serricorne
Mentha .essential oilSitophilus oryzae [85]
Mesua ferreawater extractOryzaephilus surinamensis[68]
ethanol extract
acetone extract
Micromeria fruticosaessential oilSitophilus granarius[117]
Minthostachys verticillataessential oilSitophilus zeamais[118]
Mosla soochowensisessential oilSitophilus zeamais[119]
Tribolium confusum
Myristica fragransessential oilTribolium castaneum[64]
Sitophilus oryzae
Rhizopertha dominica
Myrtus communisessential oilSitophilus oryzae [57]
Nardostachys chinensisessential oilTribolium castaneum Lasioderma serricorne[120]
supercritical CO2 fluid extract
Nigella sativaessential oilTribolium castaneum [64]
Sitophilus oryzae
Rhizopertha dominica
Ocimum basilicumessential oilSitophilus oryzae [121]
essential oilSitophilus zeamais[79]
Tribolium castaneum[122]
Tribolium confusum
Trogoderma granarium
Ocimum gratissimumessential oilOryzaephilus surinamensis [123]
Rhizopertha dominica
Sitophilus oryzae
Tribolium castaneum
Origanum acutidensessential oilLasioderma serricorne [124]
Sitophilus granarius
Origanum majoranaessential oilTribolium confusum[125]
Origanum minutiflorumessential oilTribolium confusum
Origanum onitesessential oilTribolium confusum
Origanum syriacumessential oilTribolium confusum
Origanum vulgareessential oilSitophilus oryzae[57]
essential oilTribolium castaneum[46,125]
Ostericum viridiflorumessential oilTribolium castaneum[126]
Petroselinum crispumessential oilSitophilus zeamais[53]
Perilla frutescensessential oilLasioderma serricorne[127]
Pimenta dioicapowderOryzaephilus surinamensis[47]
Pimpinella anisumessential oilTribolium castaneum[46]
Pinus longifoliaessential oilSitophilus oryzae[82]
Pituranthos tortuosusessential oilSitophilus oryzae[57]
Platycladus orientalisessential oilSitophilus oryzae[128]
Tribolium castaneum
Pongamia pinnatawater extractOryzaephilus surinamensis[68]
ethanol extract
acetone extract
Psidium guajavapowderTribolium castaneum[75]
ethanol extract
Pulicaria gnaphalodesessential oilTribolium castaneum[42]
Punica gronatumether extractOryzaephilus surinamensis [70]
Ricinus communisessential oilTribolium castaneum [116]
Lasioderma serricorne
essential oilTribolium confusum[74]
Rosmarinus officinalisessential oilTribolium confusum[74]
Salvia officinalispowderOryzaephilus surinamensis [47]
Salvertia convallariaeodoraether extractOryzaephilus surinamensis [70]
Sasurrea costusessential oilCryptolestes ferrugineus[43]
Satureja hortensisessential oilTribolium castaneum[129]
Schinus molleessential oilSitophilus oryzae [57]
Schinus terebinthifolius
Solanum nigrumglycoalkaloid extractTenebrio molitor[130]
Syzygium aromaticumessential oilTenebrio molitor [71]
Sitophilus oryzae[92]
Tribolium castaneum
Syzygium cuminiessential oilTribolium confusum[74]
essential oilSitophilus oryzae[57]
Tanacetum cinerariifoliumessential oilTribolium castaneum[46]
Tagetes erectaessential oilSitophilus oryzae[131]
Tribolium castaneum
Tagetes minutaessential oilSitophilus oryzae[131]
Tribolium castaneum
Tagetes patulaessential oilSitophilus oryzae[131]
Tribolium castaneum
Teucrium poliumessential oilTribolium castaneum [132]
Thespesia populnea var. acutilobamethanol extractTrogoderma granarium [63]
Thuja occidentalisessential oilSitophilus oryzae[57]
Trewia nudiflorawater extractOryzaephilus surinamensis[68]
ethanol extract
acetone extract
Typhonium trilobatumwater extractOryzaephilus surinamensis [68]
ethanol extract
acetone extract
Valeriana jatamansiessential oilTribolium castaneum[120]
supercritical CO2 fluid extractLasioderma serricorne
Valeriana officinalisessential oilTribolium castaneum Lasioderma serricorne[120]
supercritical CO2 fluid extract
Vepris heterophyllaessential oilSitophilus oryzae[133]
Verbascum cheiranthifoliumethanol extractSitophilus oryzae [134]
Verbascum speciosumethanol extractSitophilus oryzae[134]
Viola odorataessential oilCryptolestes ferrugineus[43]
Vitex negundoether extractOryzaephilus surinamensis [70]
Xylopia aethiopicaessential oilSitophilus oryzae [87]
Zanthoxylum armatumessential oilLasioderma serricorne[135]
Tribolium castaneum
Zanthoxylum dissitumessential oilLasioderma serricorne[135]
Tribolium castaneum
Zanthoxylum planispinum var. dintanensisessential oilTribolium castaneum Lasioderma serricorne[136]
Zingiber officinaleessential oilSitophilus oryzae[85]
Zingiber purpureumessential oilLasioderma serricorne[137]
essential oilTribolium castaneum
Lepidoptera
Plant SpeciesFormulationPest SpeciesReference
Acacia niloticaacetone and pet ether extractsCorcyra cephalonica [138]
Acorus calamuspetroleum ether extractSitotroga cerealella[139]
acetone extract
Aframomum meleguetapowderSitotroga cerealella[140]
extract
Agastache rugosaplant extractPlodia interpunctella [46]
Ajuga ivamethanol extractPlodia interpunctella[141]
Allium cepaessential oilPlodia interpunctella [142]
Allium sativumessential oilSitotroga cerealella [143]
major component: diallyl disulfide and diallyl trisulfideSitotroga cerealella [143]
major component: diallyl trisulfideSitotroga cerealella [144,145,146]
essential oilEphestia kuehniella[147,148,149]
essential oilEphestia cautella[149]
essential oilPlodia interpunctella [147]
Anacardium occidentaleessential oilEphestia cautella[150]
ethanolic oil extract and petroleum ether extractEphestia cautella[151]
Anethum graveolensessential oilPlodia interpunctella[152]
oils applied as a 30% aqueous solutionEphestia kuehniella [153]
Arachis hypogaeaacetone extractCorcyra cephalonica [154]
Armoracia rusticanaessential oilPlodia interpunctella [54]
Artemisia haussknechtiiessential oilEphestia kuehniella[155]
Artemisia herba albaessential oilEphestia kuehniella [156]
Artemisia khorassanicaessential oilSitotroga cerealella[157]
essential oilPlodia interpunctella [158]
Artemisia sieberi Bessessential oilSitotroga cerealella[157]
Artemisia vulgarisessential oilCadra cautella [159]
essential oilSitotroga cerealella [58]
Azadirachta indicaessential oilEphestia cautella [160]
Azadirachta indica + Bacilus thuringiensis Ephestia cautella[160]
Betula lentaessential oilPlodia interpunctella[147]
Ephestia kuehniella
Brassica albaessential oilEphestia cautella[148]
Callistemon viminalisessential oilEphestia kuehniella [161]
Calotripis procera rootsextractCadra cautella [162]
Capsicum annuumplant extractPlodia interpunctella [46]
Capsicum frutescensessential oilEphestia cautella [150]
ethanolic oil extract and petroleum ether extractEphestia cautella[151]
Carum copticumessential oilEphestia kuehniella[163]
Plodia interpunctella
Cassia angustifoliaprotease inhibitorPlodia interpunctella[164]
Centaurium erythraeamethanol extractPlodia interpunctella[141]
Cinnamomum camphoraessential oilEphestia kuehniella[165]
Cinnamomum.oil encapsulated with different types of alcoholPlodia interpunctella[166]
polyethylene-laminated polypropylene filmsPlodia interpunctella[167]
Cinnamomum zeylanicumessential oilPlodia interpunctella [168,169]
essential oilPlodia interpunctella[147]
essential oilEphestia kuehniella
Cistus ladanifermethanol extractPlodia interpunctella[141]
Cistus monspeliensismethanol extractPlodia interpunctella
Cistus salviaefoliusmethanol extractPlodia interpunctella
Citrus aurantiumessential oilSitotroga cerealella [170]
Citrus bergamiaessential oilPlodia interpunctella[171]
Citrus limonessential oilPlodia interpunctella[172]
Ephestia kuehniella
essential oilEphestia kuehniella[173]
Citrus reticulataplant extractPlodia interpunctella [46]
Citrus vulgarisessential oilEphestia kuehniella[155]
Clausena anisataessential oilSitotroga cerealella [174]
Cleisthopholis patensroot bark powderPlodia interpunctella[175]
stem bark powderPlodia interpunctella
leaf powderPlodia interpunctella
Conocarpus lancifolius (leaves)aqueous and ethanolic extractEphestia cautella[176]
Coriandrum sativumessential oilSitotroga cerealella [177]
essential oilEphestia kuehniella[178,179]
essential oilPlodia interpunctella[178]
essential oilCorcyra cephalonica[82]
Cuminum cyminumessential oilEphestia kuehniella [180]
Cupressus lusitanicaleaf essential oilsSitotroga cerealella[181]
Cupressus sempervirensessential oilCadra cautella [159]
Cupressus sempervirens L. horizontalisresin essential oilEphestia kuehniella[182]
Cymbopogon martiniiessential oilPlodia interpunctella [171]
Cyrtocymura cinctasesquiterpene lactones isolated from leaves and flowersSitotroga cerealella [183]
Dalbergia sissooacetone extractCorcyra cephalonica[138]
Dimorphandra mollisflowersSitotroga cerealella [184]
Dryopteris filix (mas root and rhizome)ethanolic extractCorcyra cephalonica[185]
Elaeagnus angustifoliaethyl acetate Ephestia cautella[186]
aqueous Ephestia cautella
Elettaria cardamomumessential oilEphestia kuehniella [187,188]
Eucalyptus astringensessential oilEphestia cautella[189]
Ephestia kuehniella
Eucalyptus camaldulensisessential oilEphestia kuehniella [180]
essential oilEphestia cautella[189]
Ephestia kuehniella
Cadra cautella
Eucalyptus divesoil and constituentsPlodia interpunctella [190]
Eucalyptus globulusessential oilEphestia cautella[149]
Ephestia kuehniella
essential oilPlodia interpunctella [171]
Eucalyptus lehmanniiessential oilEphestia cautella [189]
Ephestia kuehniella
Eucalyptus leucoxylonessential oilEphestia cautella[189]
Ephestia kuehniella
Eucalyptus obliquaessential oilCorcyra cephalonica[82]
Eucalyptus platyphyllaessential oilEphestia cautella [191]
Eucalyptus rudisessential oilEphestia cautella [189]
Ephestia kuehniella
Eucalyptus salignaleaf essential oilsSitotroga cerealella[181]
Ferula galbanifluaessential oilCadra cautella[159]
Ferula gummosaessential oilEphestia kuehniella[161,188]
Geranium maculatumessential oilPlodia interpunctella[171,192]
Ginkgo bilobaplant extractPlodia interpunctella[46]
Glossocardia bosvalliahexane extractsCorcyra cephalonica [193]
Hyossopus officinalisessential oilPlodia interpunctella[152]
Hypericum scabrumessential oilEphestia kuehniella[117]
Hyssoppus officinalisessential oilEphestia kuehniella[117]
Lantana camaraessential oilCadra cautella[194]
Launaea arborescensmethanol extractPlodia interpunctella[141]
Laurus nobilisessential oilEphestia kuehniella[195]
essential oilPlodia interpunctella[172]
Ephestia kuehniella
Lavandula angustifoliaessential oilEphestia kuehniella[196]
Lavandula angustifoliaextractEphestia kuehniella[197]
Lavandula angustifoliaessential oilPlodia interpunctella[171]
Lavandula dentatamethanol extractPlodia interpunctella[141]
Lawsonia inermispet ether extractCorcyra cephalonica[138]
Lippia turbinataessential oilPlodia interpunctella[198]
Maxillaria tenuifoliaethanolic oil extract and petroleum ether extractEphestia cautella[151]
Melaleuca viridifloraessential oilCadra cautella[159]
Mentha longifoliaessential oilEphestia kuehniella[199]
Mentha piperitaessential oilCorcyra cephalonica[113]
polylactic acid solutionPlodia interpunctella[200]
essential oilPlodia interpunctella[171,192]
essential oilEphestia cautella[191]
Mentha pulegiumessential oilEphestia kuehniella[201]
Mentha spicataessential oilPlodia interpunctella[202]
Ephestia kuehniella
Micromere fruticosaessential oilEphestia kuehniella[117,203]
Monodora tenuifoliaessential oilEphestia cautella[150]
Myristica fragransessential oilCadra cautella[159]
essential oilPlodia interpunctella[204]
Myrtus commonisessential oilEphestia kuehniella[195,205]
essential oilPlodia interpunctella[172]
Ephestia kuehniella
Nepata racemosaessential oilEphestia kuehniella[203]
Neroli birgardessential oilSitotroga cerealella[170]
Ocimum basilicumoils applied as a 30% aqueous solutionEphestia kuehniella[153]
essential oilEphestia kuehniella[178,201,202]
essential oilPlodia interpunctella[178,202]
Ocimum kilimandscharicumground leavesSitotroga cerealella[206]
essential oilSitotroga cerealella
Ocimum suaveessential oilSitotroga cerealella[207]
dry or ground leavesSitotroga cerealella
Origanum acutidensessential oilEphestia kuehniella[117,124]
Origanum majoranaessential oilCorcyra cephalonica[208]
essential oilPlodia interpunctella[172]
Ephestia kuehniella
essential oilEphestia kuehniella[173]
Origanum onitesessential oilPlodia interpunctella[205]
Ephestia kuehniella
Origanum syriacum var. bevaniiessential oilEphestia kuehniella[180]
Origanum vulgareessential oilPlodia interpunctella[46]
essential oilEphestia kuehniella[156,203]
Origanum vulgarisessential oilEphestia kuehniella[209]
Parthenium hysterophorusacetone extractCorcyra cephalonica[138]
Peganum harmalamethanol extractPlodia interpunctella[141]
Petroselinum crispumessential oilEphestia kuehniella[179]
Petroselinum sativumessential oilPlodia interpunctella[152]
Pimpinella anisumessential oilEphestia cautella[149]
essential oilEphestia kuehniella[147,149,180]
essential oilPlodia interpunctella[46,147]
Pinus brutiaessential oilEphestia kuehniella[210]
Pinus densifloraditerpene resin acids (DRAs)Plodia interpunctella[211]
Pinus longifoliaessential oilCorcyra cephalonica[82]
Pinus pineaessential oilEphestia kuehniella[210]
Piper nigrumessential oilCorcyra cephalonica[113]
Piper sarmentosumhexane extractsPlodia interpunctella[212]
Pistacia lentiscusessential oilEphestia kuehniella[213]
Polyalthia longifoliaessential oilSitotroga cerealella[174]
Portulaca oleraceaessential oilEphestia cautella[214]
essential oilEphestia kuehniella[215]
Prunusgrain coating with amygdalinPlodia interpunctella[216]
Psychotria prunifolialeavesSitotroga cerealella[184]
Ricinus communisessential oilEphestia cautella[150,214]
ethanolic oil extract and petroleum ether extractEphestia cautella[151]
Rosemarinus officinalisessential oilEphestia kuehniella[149,180,196]
essential oilEphestia cautella[149]
essential oilCadra cautella[159]
essential oilPlodia interpunctella[152]
methanol extractPlodia interpunctella[141]
Ruta graveolensessential oilEphestia kuehniella[201]
Ruta montanaessential oilEphestia kuehniella[156]
Salvia limbataessential oilEphestia kuehniella[117]
Salvia nemorosaessential oilEphestia kuehniella[117]
Salvia officinalisessential oilEphestia kuehniella[188]
polylactic acid solutionPlodia interpunctella[200]
Satureja hortensisessential oilPlodia interpunctella[129]
Ephestia kuehniella[129]
essential oilCadra cautella[159]
Satureja thymbraessential oilPlodia interpunctella[205]
Ephestia kuehniella[172,205]
Satureje hortensisessential oilEphestia kuehniella[117]
Syzygium aromaticumessential oilEphestia kuehniella[165]
Tanacetum cinerariifoliumessential oilPlodia interpunctella[46]
Thymus daenensisessential oilPlodia interpunctella[217]
Ephestia kuehniella
Thymus vulgarisessential oilPlodia interpunctella[152]
essential oilEphestia kuehniella[117]
Tithonia diversifolialeavesSitotroga cerealella[184]
Trachyspermum ammiessential oilPlodia interpunctella[204]
Trigonella foenum-graecumprotease inhibitorPlodia interpunctella[164]
Vitex pseudo-negundoessential oilPlodia interpunctella[158]
Xylopia aethiopicaessential oilEphestia cautella[150]
ethanolic oil extract and petroleum ether extractEphestia cautella[151]
Zingiber officinaleessential oilEphestia kuehniella[153]
essential oilEphestia kuehniella[218]
essential oilPlodia interpunctella[218]
Ziziphora clinopodioides Lam.essential oilEphestia kuehniella[219]
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MDPI and ACS Style

Nikolaou, P.; Marciniak, P.; Adamski, Z.; Ntalli, N. Controlling Stored Products’ Pests with Plant Secondary Metabolites: A Review. Agriculture 2021, 11, 879. https://doi.org/10.3390/agriculture11090879

AMA Style

Nikolaou P, Marciniak P, Adamski Z, Ntalli N. Controlling Stored Products’ Pests with Plant Secondary Metabolites: A Review. Agriculture. 2021; 11(9):879. https://doi.org/10.3390/agriculture11090879

Chicago/Turabian Style

Nikolaou, Polyxeni, Paweł Marciniak, Zbigniew Adamski, and Nikoletta Ntalli. 2021. "Controlling Stored Products’ Pests with Plant Secondary Metabolites: A Review" Agriculture 11, no. 9: 879. https://doi.org/10.3390/agriculture11090879

APA Style

Nikolaou, P., Marciniak, P., Adamski, Z., & Ntalli, N. (2021). Controlling Stored Products’ Pests with Plant Secondary Metabolites: A Review. Agriculture, 11(9), 879. https://doi.org/10.3390/agriculture11090879

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