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Article

Essential Oil Coating: Mediterranean Culinary Plants as Grain Protectants against Larvae and Adults of Tribolium castaneum and Trogoderma granarium

by
Nikos E. Papanikolaou
1,†,
Nickolas G. Kavallieratos
1,*,
Vassilios Iliopoulos
2,
Epameinondas Evergetis
2,
Anna Skourti
1,
Erifili P. Nika
1 and
Serkos A. Haroutounian
2
1
Laboratory of Agricultural Zoology and Entomology, Department of Crop Science, Agricultural University of Athens, 75 Iera Odos Str., 11855 Athens, Greece
2
Laboratory of Nutritional Feeding, Department of Animal Science, School of Animal Biosciences, Agricultural University of Athens, 75 Iera Odos Str., 11855 Athens, Greece
*
Author to whom correspondence should be addressed.
†
Nikos E. Papanikolaou: Deceased.
Insects 2022, 13(2), 165; https://doi.org/10.3390/insects13020165
Submission received: 18 January 2022 / Revised: 25 January 2022 / Accepted: 31 January 2022 / Published: 3 February 2022
(This article belongs to the Special Issue Selected Papers from the 1st International Electronic Conference on Entomology)
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Abstract

:

Simple Summary

The protection of stored agricultural products has been established as a global priority serving both food safety and security. Toxicity and residual issues of synthetic insecticides shifted the research focus towards natural pest control agents. In this context, six edible plants were selected for the conduction of a novel bioprospecting effort aiming to identify potential control agents against the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) and the khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae). The proposed bioprospecting effort aims to identify the chemodiversity of essential oils (EOs) and exploit the potential of EO-based microemulsion (ME) coating as alternative tools for the management of the tested stored-product insects and the concomitant postharvest losses. Elevated toxicity was recorded against T. castaneum larvae and T. granarium adults. The fact that these EO-based MEs originate from culinary plants renders them safe for human consumption. The present study pioneers the utilization of EO-based MEs as grain protectants in the form of grain coating.

Abstract

Postharvest agricultural losses constitute a major food security risk. In contrast, postharvest protection is strongly linked with food safety. The present study aims to develop novel postharvest protection tools through a bioprospecting protocol utilizing edible essential oils (EOs) as grain coatings. For this purpose, six Mediterranean culinary plants were selected for evaluation. The EOs of juniper, Juniperus phoenicea L. (Pinales: Cupressaceae), marjoram, Origanum majorana L. (Lamiales: Lamiaceae), oregano, Origanum vulgare ssp. hirtum (Link) A.Terracc. (Lamiales: Lamiaceae), bay laurel, Laurus nobilis L. (Laurales: Lauraceae) and tarhan, Echinophora tenuifolia ssp. sibthorpiana (Guss.) Tutin (Apiales: Apiaceae) were retrieved through steam distillation, while lemon, Citrus limon (L.) Osbeck (Sapindales: Rutaceae) EO was retrieved through cold press extraction. All EOs were formulated to microemulsions (MEs) and applied uniformly as a coating on wheat against larvae and adults of Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) and Trogoderma granarium Everts (Coleoptera: Dermestidae). All EO-based MEs have been evaluated for the first time as grain coatings. They caused moderate to high mortality to T. castaneum larvae (67.8–93.3% 14 days post-exposure) and T. granarium adults (70.0–87.8% after 7 days of exposure). Citrus limon, O. majorana and E. tenuifolia ssp. sibthorpiana EO-based MEs were the most efficient against T. castaneum larvae, by exhibiting 93.3%, 91.1% and 90.0% mortality 14 days post-exposure, respectively. Origanum majorana, L. nobilis and J. phoenicea EO-based MEs were the most efficient against T. granarium adults, exhibiting 87.8%, 84.4% and 83.3% mortality after 7 days of exposure, respectively. These results indicate that EO-based ME coating is a potent tool against the tested postharvest pests.

1. Introduction

Food security, under the perspectives of global population increase and shifting consumer habits, is one of the main future challenges for the agricultural sector [1,2,3]. In the European Union, the main instrument of agricultural development, i.e., the Common Agricultural Policy (CAP), has set as a target, in order to address this challenge, the increase of agricultural production by 20% in 2030 [4]. The Food and Agricultural Organization (FAO) provides an alternative perspective of food security by focusing on the postharvest losses of agricultural production which is estimated to be 10% in developed countries and exceed 20% in developing countries [5,6].
The interconnectivity of these two approaches is well established and has been highlighted as a challenge since the Bronze Age [7,8,9]. While postharvest pest infection is horizontal across the sum of agricultural products [10], it is elevated as a significant risk for global food security in the case of staple food infections, with cereals and legumes being prominent among them [11]. Numerous efforts towards the eradication of fungal infestations have been summarized by Schmidt et al. [12], concluding the necessity of a combinatorial approach against the microbe contamination of stored grains such as cold atmospheric pressure plasma and electrolyzed water treatments. Similar advances may also be traced for insect and mite postharvest pests, focusing on their judicious management [13]. A prominent position among orders of insects that are related to stored products is reserved for Coleoptera. More than 600 coleopteran species have been identified as pests of food commodities with a cosmopolitan anthropochore distribution and have been established as major factors of stored-grain degradation [14]. Adults and larvae of these holometabolous insects cause serious direct and indirect damages in stored products by biting and chewing with their mandibles. Although some adults of these species do not feed or rarely feed upon stored commodities, they are also important since they are the vehicles of reproduction. Furthermore, due to the fact that several coleopterans are strong fliers, they can be easily distributed within/among storage facilities and between field and storage facilities [5,14].
Despite the fact that chemical insecticides are effective against a wide spectrum of insects, they may negatively affect the environment and health of consumers [15,16]. It is well documented that stored-product insects have developed resistance to major classes of insecticides, such as pyrethroids and organophosphates, due to their continuous exposure to synthetic insecticides [17,18,19,20]. Therefore, recent advances in policies but also on the regulation of active substances emphasize the use of non-synthetic plant protection products [21,22]. While novel approaches such as cold plasma [23] and ozone [24] treatments have been proven efficient, they have also presented significant side effects, mostly in relation to the nutritional value and physical and chemical properties of grains. On the other hand, natural products have been demonstrated as a promising source of plant protection tools [22,25,26,27].
Among natural products, essential oils (EOs) constitute a distinct class, representing complex clusters of plant secondary metabolites, with decreased mammalian toxicity and ecosystem penetrability and a selective mode of action circumnavigating the risk of resistance development [28,29]. Essential oils have been studied in relation to their fumigant toxicity [30,31,32] and their contact toxicity [33,34,35], but only recently has there been a focus on novel application methods of EOs [36,37]. This research interest became fruitful by providing a solid methodological approach for the application of volatile compounds as stored grain coatings in the form of nanoemulsions (NE) [38,39,40,41]. Microemulsions (ME), on the other hand, are kinetically stable, oily droplets in water, with a Surfactant-to-Oil Ratio (SOR) usually higher than 2 [42]. Previous reports have indicated that MEs are effective against different species of insects [43,44].
The present study builds upon the advances of MEs and aims at ameliorating the knowledge on EOs toxicity against stored-product pests through the introduction of a novel bioprospecting protocol. For this purpose, EO-based MEs have been implemented for first time as grain coating agents. The subjects of investigation were retrieved from the Greek biodiversity pool with a distinct focus on edible and/or culinary plants [45,46,47,48,49,50]. This way, the EO-based ME grain coating will be compatible with human consumption. The ME preparation utilized food grade emulsifiers and solvents. As target pests, the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), a highly destructive stored-product insect pest of Indo-Australian origin [51,52], and the khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae), a highly destructive pest affecting a wide variety of commodities worldwide of animal and plant origin [52,53,54,55,56,57] and included in the 100 most important invasive species worldwide [58], were selected.

2. Materials and Methods

2.1. Plant Material

Plant material from six Greek indigenous culinary species was examined in the present study. These species are lemon, Citrus limon (L.) Osbeck (Sapindales: Rutaceae), juniper, Juniperus phoenicea L. (Pinales: Cupressaceae), bay laurel, Laurus nobilis L. (Laurales: Lauraceae), tarhan, Echinophora tenuifolia ssp. sibthorpiana (Guss.) Tutin (Apiales: Apiaceae), marjoram, Origanum majorana L. (Lamiales: Lamiaceae) and oregano, Origanum vulgare ssp. hirtum (Link) A.Terracc. (Lamiales: Lamiaceae) (Table 1). All authentic samples utilized for the identification of EO compounds were obtained from Sigma-Aldrich (Steinheim, Germany), except for germacrene D and α-thujene, which had been isolated in the context of previous studies. The food grade emulsifier, TWEEN® 20 (97%) (Sigma-Aldrich, Steinheim, Germany), was utilized for the preparation of formulations.

2.2. Commodity

Hard wheat, Triticum durum Desf. (var. Claudio), commercially acquired, that was free from pest infestations and pesticides was used in the bioassays. Wheat was sieved to remove the impurities and stored at subzero temperatures for several months. Prior to experimentation, the wheat was warmed under room temperature. The moisture content was 12.2% as determined by a calibrated moisture meter (mini GAC plus, Dickey-John Europe S.A.S., Colombes, France).

2.3. Insect Species

The insect species used in the bioassays were obtained from cultures that are kept at the Laboratory of Agricultural Zoology and Entomology, Agricultural University of Athens. The founding individuals of T. castaneum and T. granarium have been collected from Greek storage facilities since 2003 and 2014, respectively. The selected insect individuals of both species and developmental stages, as well as the conditions they were cultured in, were adapted from previous studies [40,59].

2.4. Essential Oil Isolation and Analysis

All EOs were obtained by hydro-distillation using a modified Clevenger apparatus, according to previously described procedure [60]. The isolation yields of all EOs are included in Table 1. The chemical composition of EOs was determined on a gas chromatographer (GC) coupled to a mass spectrometer (MS) and Flame Ionization Detector (FID) in accordance with a previously described method [60]. Mass spectra were compared with NIST 11 and Willey 275 databases and authentic samples where available.

2.5. Bioassays

A stock solution of EO and TWEEN® 20 (Sigma-Aldrich Chemie GmbH, Taufkirchen, Germany) (1:1) was prepared from each plant according to the specifications presented in Table 1. The analogy of the EO and the emulsifier was decided according to previously a described protocol [61] in order to produce an ME upon dilution with water. The EO-based ME stock solutions were tested at the concentration of 1000 ppm, where water (0.05% TWEEN® 20) served as control. The selection of this concentration was based on preliminary tests. The experiments were conducted according to Kavallieratos et al. [62], while the application protocol of the MEs followed the guidelines provided by Golden et al. [38]. In this task, treatments were performed on plates, each one representing a treatment replicate. Quantities of 0.20 kg of wheat were each sprayed with 1 mL of the test solution by using an AG-4 airbrush (Mecafer S.A., Valence, France). Different plates were used per spraying. Between treatments, the airbrush was cleaned with alcohol to avoid cross contamination. The sprayed whole wheat was inserted separately in 1 kg plastic canisters and was shaken for 10 min to achieve the balanced distribution of the EO-based MEs on the whole quantity of grains. Three subsamples of 10 g were obtained and placed in Petri dishes (9 cm diameter, 1.5 cm height) using a different scoop that was inside each canister. The covers of the dishes bore a circular opening (1.5 cm diameter) on their centers that was covered by muslin cloth. Thus, the content of the dishes would be adequately aerated. The upper internal vertical sides of each dish were covered by polytetrafluoroethylen (60 wt % dispersion in water) (Sigma-Aldrich Chemie GmbH, Taufkirchen, Germany) to prevent the escape of insects from the treated wheat. The samples of 10 g of wheat were weighed with a Precisa XB3200D electronic balance (Alpha Analytical Instruments, Gerakas, Greece) on filter paper. Paper was changed each time weighing was conducted. After this, 10 adults or larvae of each species were transferred. The mortality of larvae of both species and T. castaneum adults was determined after 1, 3, 7 and 14 days of exposure, while the mortality of T. granarium adults was determined after 1, 3 and 7 days due to the shorter adult longevity of this species [63].

2.6. Data Analysis

Mortality in the control treatments was low (<5%) for both species, therefore no correction was considered necessary for the mortality values (correction is conducted when control mortality ranges between 5% and 20% [64]). In order to normalize the variance, mortality data were log (x + 1) transformed prior to being submitted to ANOVA separately for each tested species and life stage [62,65]. The pairwise comparisons were conducted by using the Fischer LSD test (α = 0.05). All the analyses were performed with SigmaPlot 14.0 [66].

3. Results

3.1. Phytochemical Analysis

The results of the EO analysis revealed the presence of 48 phytochemical compounds, which are explicitly presented in Table 2. The main compounds in each plant’s EO are presented in Figure 1, while the presence of principal and secondary molecular structures in each EO are included in Table 1. From the EOs included in the present study, O. vulgare ssp. hirtum and O. majorana presented phenol carvacrol as the main compound, while in O. majorana, isomer thymol was also present in comparable quantity. Citrus limon and J. phoenicea EOs contain limonene and α-pinene as major compounds, respectively. Laurus nobilis EO was found to contain eucalyptol as a major compound, and E. tenuifolia ssp. sibthorpiana almost equal amounts of methyl eugenol and α-phellandrene.

3.2. Insecticidal Activity against T. castaneum

The mean mortality rate of T. castaneum larvae was significantly increased 1, 3 and 7 days after application of the EO-based MEs (Table 3). Thereafter, a significant increase in larval mortality was detected only for the application of the C. limon EO-based ME. Mean mortality rates of T. castaneum larvae 14 days after the application of C. limon, J. phoenicea, L. nobilis, E. tenuifolia ssp. sibthorpiana, O. majorana and O. vulgare ssp. hirtum EO-based MEs were 93.3%, 67.8%, 77.8%, 90.0%, 91.1% and 87.8%, respectively. However, all the tested EO-based MEs showed low mortality on T. castaneum adults. Thus, the observed mean mortality rates were 16.7%, 26.7%, 34.4%, 17.8%, 24.4% and 25.6% on wheat treated with C. limon, J. phoenicea, L. nobilis, E. tenuifolia ssp. sibthorpiana, O. majorana and O. vulgare ssp. hirtum EO-based MEs, respectively, 14 days post-exposure.

3.3. Insecticidal Activity against T. granarium

Concerning the efficacy on T. granarium, the tested EO-based MEs showed low mortality on insects’ larvae (Table 4). Depending on plant species, the efficacy of EO-based MEs ranged from 8.9% (L. nobilis) to 30.0% (O. majorana) 14 days after the exposure. However, T. granarium adults showed an increasing mortality rate after 1, 3 and 7 days exposure. Thus, mean mortality rates of insects’ adults 7 days after the application of C. limon, J. phoenicea, L. nobilis, E. tenuifolia ssp. sibthorpiana, O. majorana and O. vulgare ssp. hirtum EO-based MEs on wheat were 72.2%, 83.3%, 84.4%, 70.0%, 87.8% and 82.2 %, respectively.

4. Discussion

The composition of O. majorana EO is compatible with previous reports that indicate both thymol [67] and carvacrol [68] as main compounds and its significant chemical diversity is recognized. It must be noted that previous analyses of O. majorana EO from Greece [69] have also revealed the molecule of cymene as a major compound but not γ-terpinene. The L. nobilis EO composition is also consistent with previous reports identifying eucalyptol as the main compound [70], while the major compound α-terpinenyl acetate has also been reported [71]. The composition of E. tenuifolia ssp. sibthorpiana, O. vulgare, C. limon and J. phoenicea EOs has been presented and extensively discussed in previous studies [60,72,73].
EOs exhibit a significant range of pesticidal activities [32,72,74,75,76]. They can be produced easily, in a green and low-cost way, i.e., not including organic solvents or complicated methods of extraction [22]. In addition, EOs provide secondary metabolites that can act as modifying agents to resistant organisms, by inhibiting their proteins [77]. Citrus limon EO has been previously studied as a fumigant against T. castaneum adults with elevated efficacy [78,79]. By testing the contact toxicity and repellency of O. majorana EO against T. castaneum adults, Teke et al. [80] found potent repellency (97.2%) but not insecticidal activity after 3 days of exposure. Likewise, O. vulgare EO exhibited high fumigant and repellent properties against T. castaneum adults [81,82]. The evaluation of L. nobilis EO against T. castaneum in semolina suggested significant insecticidal potentials with simultaneous retention of crucial semolina quality characteristics [83].
Our study clearly shows the effectiveness of the EO-based MEs of the Mediterranean plants C. limon, J. phoenicea, L nobilis, E. tenuifolia ssp. sibthorpiana, O. majorana and O. vulgare ssp. hirtum against the two tested stored-product insect pests. Citrus limon, O. majorana and E. tenuifolia ssp. sibthorpiana EO-based MEs were the most effective for the management of T. castaneum larvae, by killing 93.3%, 91.1% and 90.0% of the exposed individuals after 14 days of exposure, respectively. Origanum majorana, L. nobilis and J. phoenicea EO-based MEs killed 87.8%, 84.4% and 83.3% of T. granarium adults after 7 days of exposure, respectively. The findings indicate that the evaluated EO-based MEs are effective grain protectants for the management of T. granarium adults and T. castaneum larvae. So far, limited research has been conducted on EOs as grain protectants. For example, Demirel et al. [84] suggested that the EOs extracted from rosemary, Rosmarinus officinalis L. (Lamiales: Lamiaceae), O. majorana and thyme, Thymus vulgaris L. (Lamiales: Lamiaceae), can be used as a potential source of environment-friendly wheat protectants for the control of the confused flour beetle, Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae). Recently, Kavallieratos et al. [85] showed that EOs obtained from horse mint, Mentha longifolia (L.) Huds. (Lamiales: Lamiaceae), wormseed, Dysphania ambrosioides (L.) Mosyakin & Clemants (Caryophyllales: Chenopodioideae), stemless carline thistle, Carlina acaulis L. (Asterales: Compositae), and anise, Pimpinella anisum L. (Apiales: Apiaceae) are stored maize and wheat protectants against two stored-product insects pest, the larger grain borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrychidae) and T. granarium. In addition, Pavela et al. [76] revealed that the essential oils of Ferula assa-foetida L. (Apiales: Apiaceae) and Ferula gummosa Boiss. (Apiales: Apiaceae) were highly effective against adults of T. granarium when applied on stored wheat.
The insect developmental stage is a critical aspect of the efficacy of the EO as grain protectants [62,76]. Tribolium castaneum larvae were more susceptible to the EO-based MEs than adults. On the basis of our results, C. limon, J. phoenicea, L. nobilis, E. tenuifolia ssp. sibthorpiana, O. majorana and O. vulgare ssp. hirtum EO-based MEs provided low adult mortality levels, ranging from 16.7% to 34.4% 14 days post-exposure. In contrast, in the case of larvae, the same EO-based MEs provided moderate to high mortality levels, ranging from 67.8% to 93.3% after 14 days of exposure. Similarly, a 6% (w/w) Hazomalania voyronii (Jum.) Capuron (Laurales: Hernandiaceae) EO-based NE caused low mortality to T. castaneum adults (i.e., 18.7%) vs. high mortality to larvae (i.e., 97.4%) 7 days post-exposure [40]. However, in the case of T. granarium, adults were more vulnerable than larvae. The tested EO-based MEs caused the death of a low percentage of the exposed T. granarium larvae (8.9–30.0%) after 14 days of exposure, while they caused elevated mortality (72.2–87.7%) to T. granarium adults, 7 days post-exposure. It is well documented that T. granarium larvae are more tolerant than adults to EOs [85] and compounds of botanical origin [22,40,62] when applied on wheat. This could be attributed to the long and dense hairs that cover the body of larvae, protecting them from coming in contact with the treated wheat [86]. In contrast, larvae of Tribolium spp. are covered by few hairs [87], an issue that increases the likelihood of their contact with the toxicant. The increased tolerance of T. castaneum adults in comparison to larvae could be attributed to the different structure of their cuticles [88]. Another hypothesis is that the expression of the TcCYP6BQ7 gene, which is responsible for the detoxification of plant toxicants, is higher in adults than larvae of T. castaneum [89].
In general, pesticide treatment with synthetic insecticides is a common practice against stored-product insect pests [36,62]. However, food safety is generally associated with integrated pest management, aiming to use alternative protectants and/or low-risk pesticides [22,90,91,92]. Botanicals are low-risk alternative products, linked with reduced regulatory registration procedures [93]. Our results lean towards this direction, as we showed that the EO-based MEs of several plants have the potential to serve as efficient tools against major stored-product insect pests. Developing grain protectants from plants will bring benefits to the food supply chain with simple and cost-effective products of insecticidal activity [94].

5. Conclusions

All EO-based MEs included in the current bioprospecting study exhibit the prevailing phytochemical EO profile for the respective plant taxa. This fact enhances the replicability and upscale of the findings, since the exploited raw materials are widely available in nature [34,45,46,47,48,49,50,95,96]. In addition, we expect our results to have bearing on the control and the integrated pest management of stored-product insect pests. Further research on the insecticidal activity of several Mediterranean plants as grain protectants will gather together more information towards efficient, more sustainable management strategies in storage facilities.

Author Contributions

Conceptualization, N.E.P., N.G.K., E.E. and S.A.H.; Methodology, N.E.P., N.G.K., E.E. and S.A.H.; Validation, N.E.P., N.G.K., V.I., E.E. and S.A.H.; Formal Analysis, N.E.P., V.I. and E.E.; Investigation, N.E.P., V.I., E.E., A.S. and E.P.N.; Resources, N.E.P., N.G.K. and S.A.H.; Data Curation, N.E.P. and E.E.; Writing—Original Draft Preparation, N.E.P., N.G.K., E.E. and S.A.H.; Writing—Review and Editing, N.E.P., N.G.K., E.E., A.S., E.P.N. and S.A.H.; Visualization, N.G.K., E.E. and S.A.H.; Supervision, N.G.K. and S.A.H.; Project Administration, N.E.P. and S.A.H.; Funding Acquisition, N.E.P. and N.G.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research is co-financed by Greece and the European Union (European Social Fund-ESF) through the Operational Program “Human Resources Development, Education and Lifelong Learning” in the context of the project “Reinforcement of Postdoctoral Researchers-2nd Cycle” (MIS-5033021), implemented by the State Scholarships Foundation (ΙΚΥ).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflict of interest.

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Insects 13 00165 g001 550
Figure 1. Main compounds of the EOs (>10%).
Figure 1. Main compounds of the EOs (>10%).
Insects 13 00165 g001
Table
Table 1. Essentials oils, plant origin and stock solution composition.
Table 1. Essentials oils, plant origin and stock solution composition.
TaxonSourceStock Solution
EOTWEEN® 20Water
Citrus limonIndustrial byproduct20%20%60%
Juniperus phoeniceaWild gathered20%20%60%
Laurus nobilisCultivated20%20%60%
Echinophora tenuifolia ssp. sibthorpianaWild gathered20%20%60%
Origanum majoranaCultivated20%20%60%
Origanum vulgare ssp. hirtumCultivated20%20%60%
Table
Table 2. EOs qualitative and quantitative composition. RI = Retention Index; Identification Method: a = MS, b = RI, c = comparison with authentic standards.
Table 2. EOs qualitative and quantitative composition. RI = Retention Index; Identification Method: a = MS, b = RI, c = comparison with authentic standards.
CompoundsRIC. limonJ. phoeniceaL. nobilisE. tenuifolia ssp. sibthorpianaO. majoranaO. vulgare ssp. hirtumIdentification
α-thujene9300.6 0.21.50.1a, b, c
α-pinene9392.373.93.90.60.9 a, b, c
camphene954 0.5 0.3 a, b, c
sabinene975 0.310.20.1 a, b, c
β-pinene98010.51.93.60.10.3 a, b
1-octen-3-ol981 0.3 a, b
myrcene9912.03.30.90.21.50.2a, b, c
α-phellandrene1003 3.10.532.50.2 a, b
α-terpinene1017 0.70.92.00.2a, b
para-cymene1025 10.30.11.0a, b
ortho-Cymene1027 0.8 8.1 a, b
limonene102937.2 a, b, c
β-phellandrene1031 6.5 a, b
eucalyptol1032 45.7 t a, b
trans-β-ocimene10510.2 a, b
γ-terpinene106010.40.20.70.614.10.9a, b, c
α-terpinolene10890.70.7 0.5 0.4a, b
linalool1098 1.7 0.2 a, b
nonanal11010.2 a, b
camphor1145 0.5 a, b
citronelal11530.3 a, b
borneol1168 0.50.2a, b
4-terpineol1178 0.22.4 0.50.1a, b
α-terpineol11890.30.43.0 a, b
neral12381.2 a, b
carvacrol methyl ether1245 0.7 a, b
piperitone1253 0.1 a, b
bornyl acetate1287 0.9 a, b
lavandulyl acetate12900.9 a, b
thymol1293 0.118.30.6a, b
carvacrol1299 0.543.795.3a, b, c
citral13202.0 a, b
δ-eIemene1338 0.1 a, b
a-terpinelyl acetate1351 1.114.0 a, b
eugenol1359 2.5 a, b
neryl acetate13621.2 a, b
β-elemene1391 0.2 a, b
methyl eugenol1406 1.243.8 a, b
β-caryophyllene14190.61.3 1.90.4a, b, c
α-bergamotene1435 1.0 a, b
γ-elemene1437 0.2 a, b
α-humulene1455 0.6 a, b
germacrene D1485 4.2 a, b, c
valencene14960.2 a, b
bicyclogermacrene15000.1 a, b
β-bisabolene15061.5 0.30.2a, b
δ-cadinene1523 0.2 a, b
germacrene B1561 1.2 a, b
Total 72.495.392.796.895.499.8
Table
Table 3. Mean mortality rate (% ± SE) of T. castaneum (larvae and adults) 1, 3, 7 and 14 days after application with EO-based MEs. Means in the same row followed by different uppercase letters are significantly different; means in a column followed by different lowercase letters are significantly different (Fisher LSD test, α = 0.05).
Table 3. Mean mortality rate (% ± SE) of T. castaneum (larvae and adults) 1, 3, 7 and 14 days after application with EO-based MEs. Means in the same row followed by different uppercase letters are significantly different; means in a column followed by different lowercase letters are significantly different (Fisher LSD test, α = 0.05).
Plant SpeciesDevelopmental
Stage		Days after the TreatmentDFFp
1 Day3 Days7 Days14 Days
C. limonLarvae8.9 ± 2.0 Aa40.0 ± 7.1 Bab72.2 ± 6.0 Cad93.3 ± 2.4 Da359.772<0.001
Adults0.0 ± 0.0 Aa0.0 ± 0.0 Aa3.3 ± 2.4 Aa16.7 ± 6.9 Ba35.0950.005
J. phoeniceaLarvae13.3 ± 5.3 Aa32.2 ± 6.8 Bab54.4 ± 8.2 Cbc67.8 ± 8.5 Cb311.801<0.001
Adults2.2 ± 1.5 Aa7.78 ± 4.0 Aa13.3 ± 5.3 ABa26.7 ± 6.5 Ba34.9600.006
L. nobilisLarvae14.4 ± 4.1 Aa33.3 ± 5.3 Bab57.8 ± 5.7 Ccd77.8 ± 8.0 Cbcd322.470<0.001
Adults5.6 ± 4.4 Aa8.9 ± 5.6 Aa15.6 ± 5.8 Aa34.4 ± 6.0 Ba35.5550.003
E. tenuifolia ssp. sibthorpianaLarvae13.3 ± 4.4 Aa40.0 ± 4.1 Bbc77.8 ± 2.2 Ca90.0 ± 2.9 Cad383.773<0.001
Adults0.0 ± 0.0 Aa2.2 ± 1.5 Aa5.6 ± 1.8 Aa17.8 ± 3.6 Ba313.814<0.001
O. majoranaLarvae15.6 ± 1.8 Aa57.8 ± 5.5 Bc80.0 ± 4.7 Ca91.1 ± 3.5 Cac380.600<0.001
Adults7.8 ± 4.7 Aa14.4 ± 5.3 Aa17.8 ± 7.2 Aa24.4 ± 6.5 Aa31.3860.265
O. vulgare ssp. hirtumLarvae11.1 ± 4.2 Aa44.4 ± 6.5 Bbc72.2 ± 4.9 Cad87.8 ± 3.2 Cad350.233<0.001
Adults0.0 ± 0.0 Aa2.2 ± 1.5 Aa4.4 ± 1.8 Aa25.6 ± 4.8 Ba322.016<0.001
DFLarvae5555
Adults5555
FLarvae0.4112.4093.7963.431
Adults1.6052.2961.8441.232
pLarvae0.8390.0500.0050.010
Adults0.1770.0600.1220.309
Table
Table 4. Mean mortality rate (% ± SE) of T. granarium (larvae and adults) 1, 3, 7 and 14 days after application with EO-based MEs. Means in the same row followed by different uppercase letters are significantly different; means in a column followed by different lowercase letters are significantly different (Fisher LSD test, α = 0.05).
Table 4. Mean mortality rate (% ± SE) of T. granarium (larvae and adults) 1, 3, 7 and 14 days after application with EO-based MEs. Means in the same row followed by different uppercase letters are significantly different; means in a column followed by different lowercase letters are significantly different (Fisher LSD test, α = 0.05).
Plant SpeciesDevelopmental
Stage		Days after the TreatmentDFFp
1 Day3 Days7 Days14 Days
C. limonLarvae3.3 ± 1.7 Aa4.4 ± 2.4 Aab10.0 ± 4.1 Aac13.3 ± 3.7 Aab32.2820.098
Adults8.9 ± 2.6 Aa26.7 ± 2.4 Ba72.2 ± 4.0 CaN/A2111.285<0.001
J. phoeniceaLarvae3.3 ± 1.7 Aa16.7 ± 2.3 Bc26.7 ± 4.4 BCb34.4 ± 4.4 Cc316.049<0.001
Adults14.4 ± 2.9 Aa27.8 ± 2.8 Ba83.3 ± 5.3 CaN/A290.937<0.001
L. nobilisLarvae3.3 ± 1.7 Aa4.4 ± 1.8 Aab8.9 ± 2.6 Aac8.9 ± 2.6 Aa31.7190.183
Adults11.1 ± 2.0 Aa25.6 ± 2.4 Ba84.4 ± 2.9 CaN/A2214.397<0.001
E. tenuifolia ssp. sibthorpianaLarvae1.1 ± 1.1 Aa8.9 ± 2.6 Bbc16.7 ± 3.7 BCbc20.0 ± 3.3 Cbd39.122<0.001
Adults8.9 ± 2.6 Aa17.8 ± 2.8 Aa70.0 ± 7.5 BaN/A252.800<0.001
O. majoranaLarvae2.2 ± 1.5 Aa16.7 ± 4.4 Bc23.3 ± 6.0 BCbc30.0 ± 6.0 Ccd36.2320.002
Adults6.7 ± 3.3 Aa21.1 ± 3.5 Ba87.8 ± 5.7 CaN/A290.808<0.001
O. vulgare ssp. hirtumLarvae2.2 ± 1.5 Aa5.6 ± 2.4 Aab12.2 ± 1.5 BCac14.4 ± 1.8 Cab310.171<0.001
Adults12.2 ± 2.2 Aa23.3 ± 1.7 Ba82.2 ± 1.5 CaN/A2310.817<0.001
DFLarvae5555
Adults555N/A
FLarvae0.3564.1433.3107
Adults1.1422.0402.157N/A
pLarvae0.8760.0030.012<0.001
Adults0.3510.0900.075N/A
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Papanikolaou, N.E.; Kavallieratos, N.G.; Iliopoulos, V.; Evergetis, E.; Skourti, A.; Nika, E.P.; Haroutounian, S.A. Essential Oil Coating: Mediterranean Culinary Plants as Grain Protectants against Larvae and Adults of Tribolium castaneum and Trogoderma granarium. Insects 2022, 13, 165. https://doi.org/10.3390/insects13020165

AMA Style

Papanikolaou NE, Kavallieratos NG, Iliopoulos V, Evergetis E, Skourti A, Nika EP, Haroutounian SA. Essential Oil Coating: Mediterranean Culinary Plants as Grain Protectants against Larvae and Adults of Tribolium castaneum and Trogoderma granarium. Insects. 2022; 13(2):165. https://doi.org/10.3390/insects13020165

Chicago/Turabian Style

Papanikolaou, Nikos E., Nickolas G. Kavallieratos, Vassilios Iliopoulos, Epameinondas Evergetis, Anna Skourti, Erifili P. Nika, and Serkos A. Haroutounian. 2022. "Essential Oil Coating: Mediterranean Culinary Plants as Grain Protectants against Larvae and Adults of Tribolium castaneum and Trogoderma granarium" Insects 13, no. 2: 165. https://doi.org/10.3390/insects13020165

APA Style

Papanikolaou, N. E., Kavallieratos, N. G., Iliopoulos, V., Evergetis, E., Skourti, A., Nika, E. P., & Haroutounian, S. A. (2022). Essential Oil Coating: Mediterranean Culinary Plants as Grain Protectants against Larvae and Adults of Tribolium castaneum and Trogoderma granarium. Insects, 13(2), 165. https://doi.org/10.3390/insects13020165

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