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Article

Exploring the Efficacy of Four Essential Oils as Potential Insecticides against Thrips flavus

by
Yulong Niu
1,†,
Tianhao Pei
1,†,
Yijin Zhao
1,2,†,
Changjun Zhou
3,
Bing Liu
3,
Shusen Shi
1,
Meng-Lei Xu
4,* and
Yu Gao
1,*
1
Key Laboratory of Soybean Disease and Pest Control (Ministry of Agriculture and Rural Affairs), College of Plant Protection, Jilin Agricultural University, Changchun 130118, China
2
Dalian City Investment Asset Management Co., Ltd., Dalian 116021, China
3
Daqing Branch, Heilongjiang Academy of Agricultrual Science, Daqing 163316, China
4
State Key Laboratory of Supramolecular Structure and Materials, College of Food Science and Engineering, Jilin University, Changchun 130062, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2024, 14(6), 1212; https://doi.org/10.3390/agronomy14061212
Submission received: 3 May 2024 / Revised: 21 May 2024 / Accepted: 31 May 2024 / Published: 4 June 2024
(This article belongs to the Special Issue Recent Advances in Legume Crop Protection)
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Abstract

:
Plant essential oils are important alternatives in green integrated pest management. This study examined the chemical composition, bioactivity, and control efficacy of four Lamiaceae essential oils (EOs) against Thrips flavus Schrank in laboratory conditions with the goal of exploiting plant-derived insecticides to control Thrips flavus. The four EOs tested were marjoram oil (Origanum majorana L.), clary sage oil (Salvia sclarea L.), perilla leaf oil (Perilla frutescens (L.) Britt.), and spearmint oil (Mentha spicata L.). All these EOs exhibited a certain degree of insecticidal activity against Thrips flavus. The median lethal concentration (LC50) was determined after treatment by the leaf-dipping method in laboratory bioassays, and its values were 0.41 mg/mL for marjoram oil, 0.42 mg/mL for clary sage oil, 0.43 mg/mL for perilla leaf oil, and 0.54 mg/mL for spearmint oil. In the pot experiment, the number of dead insects was recorded at 1, 3, and 7 days post-application, and the control efficacy of EOs against Thrips flavus was calculated. The concentration of 900.00 g a.i.·hm−2 of spearmint oil was 100% lethal against Thrips flavus after treating potted plants for seven days. The Y-tube olfactometer method was used to test for the attraction or repellent response of EOs against Thrips flavus. The spearmint oil significantly attracted female adults in the olfactory test. Furthermore, gas chromatography–mass spectrometry (GC–MS) was used to examine the chemical composition of the EOs. Linalool (24.52%), isopropyl myristate (28.74%), (+)-limonene (32.44%), and (+)-carvone (70.3%) were their primary ingredients. The findings suggest that all four EOs are highly effective against Thrips flavus and may be a possible alternative in the management of Thrips flavus, especially when considering reducing the use of synthetic pesticides.

1. Introduction

Thrips flavus Schrank (Thysanoptera, Thripidae) is an important pest affecting cash crops, a member of the Thripidae (Thysanoptera), which is found worldwide and can seriously damage crops at various stages of growth [1]. Thrips flavus is regarded as a major pest of flowering plants of the Asteraceae (Compositae) and Fabaceae (Leguminosae) families, among others, in Northern China. This pest typically causes premature senescence or deformation of flowers and curling, distortion, and wilting of leaves [2,3]. Various ecological factors have been shown to affect Thrips flavus survival and development. Recent research indicates that Cucumis sativus L. and Glycine max (L.) Merr. were two potentially suitable host plants for Thrips flavus [1]. The ambient CO2 concentrations can accelerate the development of thrips but reduce their survival rate [4]. The survival of thrips gradually decreased with increasing temperature from 19 °C to 31 °C [5]. Currently, chemical insecticides are predominantly used to control Thrips flavus, which shows greater sensitivity to imidacloprid, avermectin, and lambda-cyhalothrin emulsifiable concentrate compared to Frankliniella occidentalis (Pergande) (Thripidae) in the Yunnan region [6]. However, concerns over the increasing resistance of Thripidae to chemical insecticides and their environmental and ecological impacts have led to a search for safer, environmentally friendly alternatives [7,8]. Essential oils (EOs), secondary plant metabolites, offer such an alternative. These substances possess a range of bioactivities, including oviposition inhibition, avoidance, egg hatching inhibition, larval development suppression, antifeedant and repellent effects, as well as the capacity to knock down, poison, and fumigate phytophagous pests [9,10]. EOs also exhibit attractive behavior to certain pests [11]. They are characterized by their diverse bioactivities, safety for non-target organisms, availability from various sources, environmental friendliness, natural degradation, the ability to delay the development of pest resistance, and the potential to replace chemical insecticides [12,13,14]. The target pests, thrips, are unlikely to become resistant to these EOs, as products containing EOs are more complex chemically than traditional insecticide products with a single active ingredient [15]. Thrips flavus can potentially be controlled using EOs and products derived from EOs.
Lamiaceae, the sixth largest angiosperm family, comprises more than 7000 species across approximately 230 genera [16]. Many of these species are well-known as ornamental and medicinal plants; examples include lavender (Lavandula angustifolia Mill.), basil (Ocimum basilicum L.), peppermint (Mentha × piperita), rosemary (Rosmarinus officinalis L.), thyme (Thymus mongolicus (Ronniger) Ronniger), etc. The EOs are synthesized and accumulated in the leaves, stems, and epidermal glands of the reproductive structures [17]. Numerous EOs have been widely utilized in the food, cosmetic, pharmaceutical, and crop protection industries [18,19,20]. Lamiaceae EOs consist of a diverse array of chemical components, including aliphatic and aromatic molecules, with general compounds such as β-caryophyllene, linalool, limonene, β-pinene, 1,8-cineol, α-pinene and thymol [21,22,23]. For instance, terpenoids and isoprenoids are a class of organic substances found in peppermint oil that are among the most diverse naturally occurring compounds derived from plants [24]. The chemical composition of Lamiaceae EOs determines their mechanism of action and their target applications, and their active ingredients with insecticidal properties show promise for developing plant-derived insecticides [25,26]. Numerous studies have demonstrated the versatile effects of EOs derived from plants of the Lamiaceae family against various agricultural pests. Marjoram oil showed significant antifeedant activity against Hylobius abietis (L.) (Curculionidae) and significant toxicity as a fumigant against Tribolium castaneum (Herbst) (Tenebrionidae) [27,28]. Rosemary oil contains 1,8-eudesmol, which demonstrated attractant activity against Frankliniella occidentalis (Pergande), and lavandula oil exhibited attractant activity against Drosophila suzukii (Matsumura) (Drosophilidae) [29,30]. Conversely, thyme oil showed remarkable repellent activity against Sitophilus zeamais Motsch (Curculionidae) [31]. Culex pipiens L. (Culicidae) oviposition is strongly inhibited by the EOs of mint and basil [32]. However, no studies have yet explored the use of Lamiaceae EOs to control soybean (Glycine max (L.) Merr.) pest thrips. This study aimed to assess the insecticidal potential of EOs against Thrips flavus, providing insights for the development of botanical insecticides and offering practical guidelines to protect crops from Thrips flavus infestations.

2. Materials and Methods

2.1. Insects

The thrips were collected from a soybean field of the Ministry of Agriculture and Rural Development (Jilin) (located at 125°24′19″ E, 43°48′17″ N, approximately 225 m above sea level). No pesticides are applied to this experimental field during the experimental period. The region is characterized by a temperate continental semi-humid monsoon climate. Thrips were brought back to the laboratory and placed in a rearing cage using the sweeping method. Thrips were identified using the key of Y.F. Han (1997) [33] and Mound et al. (2018) [34] and continuously reared three generations. The insect cage was then kept in an incubator with soybean plants for two to three days at 25 ± 1 °C, 70 ± 5% relative humidity, and a 16:8 h light: dark photoperiod. The soybean plants were cultivated for two to three days under a 16:8 h light–dark photoperiod and were watered three to five times weekly [35].

2.2. Essential Oils

The four EOs assessed were perilla leaf oil (Perilla frutescens (L.) Britt.), marjoram oil (Origanum majorana L.), clary sage oil (Salvia sclarea L.), and spearmint oil (Mentha spicata L.), which were obtained from Lamiaceae species by Ji’an Zhongxiang Natural Plants Co. Ltd. (Ji’an City, Jiangxi Province, China) The EOs were extracted by steam distillation, and their purity was >98%.

2.3. Chemical Composition Analysis

Gas chromatography–mass spectrometry (GC–MS) (QP2010 plus, Shimadzu, Japan) was utilized to analyze the chemical composition of the four EOs [36,37,38]. The heating procedure was according to the methodology adopted by Pei et al. [36]. GC–MS software (version 2.53) tools (NIST 147 and NIST 27) were used for compound identification.

2.4. Laboratory Bioassay

The leaf-dipping method was used to determine the toxicity of the four EOs [36]. Fresh soybean leaves of the same size that were undamaged and free of pests and diseases were selected, washed in water, and allowed to dry naturally. Serial dilutions of the four EOs (0.2, 0.4, 0.6, 0.8, 1.0 mg/mL) were prepared in acetone to be tested. The leaves were then immersed in the different EOs, removed after ten seconds, and dried again naturally. One leaf (4 cm × 2 cm) was then placed in a centrifuge tube (50 mL) with moistened filter paper inside. Thirty female thrips (3-day-old) were introduced into the tubes. Subsequently, the tube opening was promptly sealed with Parafilm sealing film. Approximately 70 micro-holes were punched into the film using a 2# insect pin, ensuring an even distribution of the micro-holes. Leaves from the control group were treated without EOs. The 30% thiamethoxam SC was purchased from Hebei Zhongbaolvnong Science & Technology Co., Ltd. (Langfang City, Hebei Province, China) and used as a control group of commonly used insecticides, with serial dilutions of 0.005, 0.008, 0.012, 0.015, 0.018 mg/mL. This procedure was repeated for each EO. Each group was replicated three times. After 24 h of treatment at room temperature, thrips mortality was assessed. After counting the number of dead and surviving insects, the mortality and adjusted mortality rates were calculated [39]. The mortality rate was calculated by Equation (1):
M 0 = M 1 M 2 × 100
where M0 is the mortality rate (%); M1 is the number of dead thrips; M2 is the total number of thrips in each treatment.
The adjusted mortality rate was calculated by Equation (2):
A M = N 1 − N 2 1 − N 2 × 100
where AM is the adjusted mortality rate (%); N1 is the mortality rate of the treatment group (%); N2 is the mortality rate of the control group (%).

2.5. Olfactory Test

The ability of each EO to attract or repel adult Thrips flavus was assessed by an olfactory test. A Y-tube olfactometer was used to test the attraction or repellent rate [40]. Prior to the olfactory tests, both female and male adults were removed and cultivated separately. Lights were positioned in parallel to avoid light interference, and humidified air was used as a control. The EO was diluted to 1.0 mg/mL with acetone and tested with a 1 μL volume dropped on filter paper in the odor chamber. Clean, humid air was passed through each arm of the odor chamber and Y-tube at a flow rate of 300 mL/min. An adult Thrips flavus was placed in the front end inside the olfactometer. Its position in the tube was recorded after five minutes. Female and male adults were tested separately, with at least thirty individuals of each sex being treated with each EO. The response criteria were as follows: the adult was considered to have selected that odor source if it crawled more than half-length into either of the tubes and remained there for at least one minute; if the adult did not select or remained motionless after five minutes, it was considered not to have selected the odor source (no response) [36]. The selection rate was used as an informative indicator to evaluate the level of activity.

2.6. Pot Experiment

A pot experiment was conducted to assess the control efficacy of four EOs against Thrips flavus. The pot experiment procedure was performed as described by Pei et al. [36]. The schematic diagram of the pot experiment is shown in Figure S1. Soybean plants were planted in pots in batches, and when the 2nd compound leaf was grown, plants with uniform growth were selected, and one soybean seedling free of pests and diseases was kept in each pot. Five concentrations of four EOs were set at 180.00, 360.00, 540.00, 720.00, and 900.00 g a.i.·hm−2. The control treatment was acetone without the EOs. Each concentration and control treatment was replicated three times. After spraying 5 mL evenly per pot with a spray bottle, the potted plants dried naturally in a windless area, and then thirty adult thrips were introduced per pot. The treated pots were arranged in randomized blocks one meter apart. At one, three, and seven days after treatment, the number of insects that died was counted, and the control efficacy was calculated. The control efficacy was calculated using Equation (3):
C E = ( 1 − P 1 × P 2 P 3 × P 4 ) × 100
where CE is the control efficacy (%); P1 is the number of thrips in the treatment group after treatment with EOs; P2 is the number of thrips in the control group before treatment with EOs; P3 is the number of thrips in the treatment group before treatment with EOs, and P4 is the number of thrips in the control group after treatment with EOs [36].

2.7. Statistical Analysis

The laboratory bioassay results were used to calculate the 95% confidence intervals, the median lethal concentration (LC50), and the bioactivity regression equation using DPS 9.50 (Hangzhou Ruifeng Information Technology Co., Ltd.) [41]. One-way analysis of variance (ANOVA) was performed using IBM SPSS 20.0, and Tukey’s test was used to compare significant differences between treatments [42]. The olfactory behavior response test results were processed using IBM SPSS 20.0, and the chi-square test was used to determine the main differences between treatments. The results were plotted using Origin 2021.

3. Results

3.1. Laboratory Bioassay

In the toxicity test, although the LC50 value of marjoram oil was slightly lower than those of the other three EOs (perilla leaf oil, spearmint oil, and clary sage oil), the 95% confidence intervals overlapped, and, therefore, there was no difference in the toxicity of these four essential oils (Table 1). The four EOs exhibited similar bioactivity for Thrips flavus. The LC50 of thiamethoxam used in this experiment was only 0.0077 mg/mL, significantly lower than those of the four EOs above. This indicates that the toxicity of these EOs is significantly lower than 30% thiamethoxam.

3.2. Pot Experiment

After one day of treatment, there were no significant differences in the control efficacy against Thrips flavus between the 180.00 g a.i.·hm−2 (F = 2.818, p = 0.107), 360.00 g a.i.·hm−2 (F = 1.699, p = 0.244), and 540.00 g a.i.·hm−2 (F = 3.792, p = 0.058) application rates. At 720.00 g a.i.·hm−2 (F = 5.684, p = 0.022), the control efficacy of spearmint oil was not significantly different from that of the other two EOs and was significantly higher than that of clary sage oil. In addition to this, marjoram oil at 900.00 g a.i.·hm−2 (F = 4.605, p = 0.037) concentration was significantly more effective than clary sage oil against thrips, and there was no significant difference between the former and the other two EOs (Figure 1).
The control efficacy of perilla leaf oil at 900.00 g a.i.·hm−2 did not differ significantly from the other two EOs three days after application, although it was significantly more effective against thrips than clary sage oil (F = 6.624, p = 0.015). The control efficacy of the four EOs against thrips did not differ significantly at concentrations of 180.00 g a.i.·hm−2 (F = 3.841, p = 0.057), 360.00 g a.i.·hm−2 (F = 0.406, p = 0.753), 540.00 g a.i.·hm−2 (F = 0.649, p = 0.605), and 720.00 g a.i.·hm−2 (F = 1.230, p = 0.361) (Figure 2).
After seven days of treatment at 180.00 g a.i.·hm−2 (F = 3.054, p = 0.092), 720.00 g a.i.·hm−2 (F = 1.203, p = 0.369), and 900.00 g a.i.·hm−2 (F = 1.562, p = 0.273), there was no significant difference in the control efficacy against Thrips flavus. In contrast, both marjoram oil and spearmint oil had significantly higher control efficacy compared to perilla leaf oil at 360.00 g a.i.·hm−2 (F = 5.870, p = 0.020). Moreover, spearmint oil and clary sage oil were significantly higher than perilla leaf oil at 540.00 g a.i.·hm−2 (F = 5.428, p = 0.025), and marjoram oil was not significantly different from the first two EOs (Figure 3).
The control of thrips by the four EOs, marjoram oil, clary sage oil, perilla leaf oil, and spearmint oil, was significantly improved with longer application times and higher concentrations. Spearmint and marjoram oil had a higher efficacy at all concentrations, one day, three days, and seven days after application. Perilla leaf oil had a better control efficacy at one day and three days after application. However, seven days after application, perilla leaf oil was inferior to the other EOs at low concentrations. One day and three days after application, perilla leaf oil applied at a low concentration had a significantly lower control efficacy than the other oils, but at seven days, at the higher concentrations, it was not significantly different compared to the other oils. Clary sage oil showed better efficacy seven days after application and was not significantly different from spearmint and marjoram oil. Clary sage oil applied at a high concentration was significantly less effective than the other EOs after one day of application and three days after application. In contrast, the low concentration of clary sage oil did not differ in efficacy from the other EOs. The four EOs reached the highest efficacy seven days after application, with no significant differences observed between the different concentrations.

3.3. Olfactory Test

Female adults of Thrips flavus showed different olfactory behavioral responses to the EOs of different Lamiaceae species. Female adult thrips were significantly attracted to spearmint oil (χ2 = 4.948, p = 0.026) with an attraction rate of 71.05%. There were no significant differences in attraction between clary sage oil (χ2 = 0.178, p = 0.673), marjoram oil (χ2 = 0.530, p = 0.467), and perilla leaf oil (χ2 = 0.166, p = 0.684). Thrips flavus showed 67.86%, 84.09%, 56.45%, and 81.25% selectivity for the four EOs (Figure 4). Among the four EOs tested, spearmint oil had a significant attractant effect on adult females.
Male adults of Thrips flavus show no significant attraction response to spearmint oil (χ2 = 0.000, p = 1.000), clary sage oil (χ2 = 2.381, p = 0.123), marjoram oil (χ2 = 0.617, p = 0.432), and perilla leaf oil (χ2 = 0.617, p = 0.432). Thrips flavus exhibited a selectivity of 65.22%, 80.00%, 65.96%, and 63.27% for the four EOs (Figure 5).

3.4. Chemical Analysis of Essential Oils

Marjoram oil consisted of seventeen major compounds, ranging in concentration from 24.52% to 0.26%, the most abundant being linalool (24.52%), followed by benzyl acetate (16.42%) and α-hexylcinnamaldehyde (14.28%), and the least abundant leaf alcohol (0.26%). Of these, five belong to esters, representing 29.27% of the constituents. They were followed by three types of terpene alcohols, accounting for 25.35% of the constituents. There were also aldehydes (14.28%), alcohols (8.87%), phenols (3.99%), amides (2.95%), and ketones (0.96%) (Table 2).
Clary sage oil consisted of nineteen major chemical constituents, ranging in concentration from 28.74% to 0.34%. The most abundant component of clary sage oil was isopropyl myristate (28.74%), followed by linalyl acetate (20.07%), and the least abundant was linalyl anthranilate (0.34%). Of these, six belong to the ester compound group, representing 62.14% of the content. They were followed by two types of terpene alcohols, accounting for 22.49% of the total constituents. There were also alcohols (4.74%), ketones (4.13%), terpenes (3.07%), phenols (2.23%), and aldehydes (1.2%) (Table 3).
Perilla leaf oil consisted of nine major chemical constituents ranging in concentration from 32.44% to 0.59%. The most abundant was (+)-limonene (32.44%), followed by γ-terpinene (23.92%), and the least abundant was cis-linalool oxide (0.59%). Of these, three belong to the terpene group, representing 56.97% of the total constituents. Aldehydes followed with 15.61% of the total. There are also phenols (13.25%), terpene alcohols (10.53%), olefins (2.34%), ketones (0.70%), and alcohols (0.59%) (Table 4).
Spearmint oil consists of five major chemical constituents ranging in concentration from 70.34% to 1.05%. The most abundant is (+)-carvone (70.34%), followed by (+)-limonene (26.22%), and the least abundant is α-pinene (1.05%). Of these, three belong to the terpene group, representing 28.64% of the total constituents. There are also ketones (70.34%) and alcohols (1.20%) (Table 5).

4. Discussion

EOs have several advantages when used as biocontrol agents for pest control. Firstly, they are made from natural plant components and can be broken down in the environment, making them environmentally friendly. Secondly, the extraction of EOs can effectively use excess peelings, twigs, and leaves from agricultural production, thus minimizing the waste of resources. Thirdly, EOs have specific insecticidal activity against certain pests and are safer against non-target species [43,44]. This study investigated the toxicity against Thrips flavus of four EOs: marjoram oil (LC50 = 0.41 mg/mL); clary sage oil (LC50 = 0.42 mg/mL); perilla leaf oil (LC50 = 0.43 mg/mL); and spearmint oil (LC50 = 0.54 mg/mL) under laboratory conditions. All four EOs exhibited some degree of toxicity. The use of Lamiaceae EOs for pest control has been studied extensively. Spearmint oil was shown to be toxic as a fumigant to Reticulitermes dabieshanensis Wang and Li (Rhinotermitidae) with an LC50 of 0.194 μL/L [45]. At a concentration of 5 mg, spearmint oil and basil oil could control 100% of male Blattella germanica L. (Blattidae) [46]. Similar results in the Lamiaceae reported that pennyroyal oil (Mentha pulegium L.) and Thymus mastichina L. essential oil exhibited fumigant effect against Frankliniella occidentalis with LC50 of 3.1 mg/L and 3.6 mg/L [47]. Mentha pulegium essential oil treatment also showed a significant fumigant effect on Thrips tabaci Lindeman [48] and was the most toxic fumigant to Thrips palmi Karny (Thripidae) [49]. The EOs of Syzygium aromaticum Merr. and L.M. Perry, Cinnamomum bejolghota (Buch.–Ham.) Sweet and Cymbopogon citratus (Dc.ex.Nees) showed high fumigant toxicity against Frankliniella schultzei (Trybom) (Thripidae) [50]. Whether the four EOs in this study have fumigant activity against Thrips flavus will be further investigated by fumigation toxicology assays. To further confirm the insecticidal activity of the four EOs, the pot experiment was conducted using live soybean potted plants. Spearmint oil showed 100% lethality against Thrips flavus at a concentration of 900.00 g a.i.·hm−2 after seven days of treatment. At the same time, after seven days of treatment, the other EOs showed more than 90% lethality against Thrips flavus at a concentration of 900.00 g a.i.·hm−2. These results suggest that the exploitation and development of Lamiaceae EOs into plant-derived insecticides holds great potential. Because the insecticidal mechanism of these EOs is not yet clear, further research will be conducted exploratively.
EOs can be found in large quantities and with various chemical compositions. Several factors influence the biological activity, content, and composition of EOs. These include the plant growth stage [51], the extraction site and technique [52,53,54], and the geographical environment [55]. The use of innovative technologies to increase extraction efficiency can also improve the quality of EOs [56,57]. The chemical composition of the four EOs used in this study varied significantly based on GC–MS analysis. The highest concentration of (+)-carvone was found in spearmint oil, while isopropyl myristate was most abundant in clary sage oil, limonene in perilla leaf oil, and linalool in marjoram oil. Previous studies have shown that the main constituents of perilla leaf oil are 2-furyl methyl ketone (71.83%), decahydro-1-methyl-2-methylene-naphthalene (10.47%), limonene (5.16%) and caryophyllene (1.66%) [58]. On the other hand, β-terpineol and γ-terpinene were shown to be the main constituents of marjoram oil [27]. Similarly, limonene (+1,8-cineole; 14.3%) and carvone (67.1%) were identified as the major constituents of spearmint oil by GC–MS analysis [59]. When EOs are used as insecticides for pest control, one of the problems to be solved is that the production and quality properties of plant material cannot be standardized, and the control efficacy varies widely. Therefore, further research is needed to study the efficacy of individual chemical constituents in controlling pests and to refine the component with the best control efficacy to be used in the development of plant-derived insecticides.
This study found that of the four EOs tested, spearmint oil was a particularly strong attractant for mature female Thrips flavus. Recent studies have shown that some Lamiaceae EOs have a significant attractant effect on certain pests [60]. Rosmarinus officinialis L. was attractive to Frankliniella occidentalis, which is attracted by the major component 1,8-cineole [30]. Rosemary oil with a certain concentration of β-caryophyllene and limonene was found to be an attractant for Bemisia tabaci (Gennadius) [61]. The EO of Tetradenia riparia (Hochst.) Codd, of which the primary compounds are fenchone, δ-cadinene, 14-hydroxy-β-caryophyllene, and tau-cadinol, is an attractant for Ceratitis capitata (Wiedemann) (Tephritidae) [62]. In addition, some pests can be repelled by Lamiaceae EOs. For example, patchouli oil has significantly repelled Tribolium castaneum [63]. EO of Origanum majorana L. captured 87% fewer Thrips tabaci (Thripidae) than that in the control treatment, and this EO is a promising onion thrips repellent [64]. Cinnamomum verum Presl showed repellent activity against Hercinothrips femoralis (Reuter) (Thripidae) [65]. Rosmarinus. officinalis EO showed repellent activity against female adults of Thrips tabaci [66]. Rosmarinus officinialis EO can also inhibit the oviposition of Frankliniella occidentalis (Thripidae), Frankliniella intonsa (Thripidae), and Thrips palmi. α-Pinene was repellent to Frankliniella occidentalis and Frankliniella intonsa. Eucalyptol showed significant repellent activity in these three thrips species [67]. Moreover, carvacrol, cinnamaldehyde, and thymol, common constituents of Lamiaceae EOs, can be combined with nanogel technology to repel mosquitoes [68]. The EOs can be utilized as attractants or repellents for pest management by exploiting their ability to attract or repel pests [69]. In the olfactory test, spearmint oil had a different effect on the male and female Thrips flavus. This may be due to the chemical composition of the spearmint oil affecting adult male and female thrips differently. This phenomenon was reported in some thrips species [66,67]. The volatile dihydrotagetone alone attracted females Megalurothrips sjostedti (Trybom) (Thripidae) but had neither repellent nor attractive activity to males [70]. Tagetes minuta (L.) flower oil resulted in different olfactory responses to different sexes of Ceratitis capitata, causing attraction to males and avoidance to females. This suggests that the composition of EOs influences their olfactory properties [71]. In addition, their different effects on males and females may be due to other environmental factors. At a 0.01% concentration, the EO derived from celery seeds attracted both male and female adult Tribolium castaneum. However, at a 0.1% concentration, the EO had the opposite effect, repelling male adults but attracting female adults. In addition, basil oil at 0.01% repelled adult males but did not affect adult females [72]. This suggests that the olfactory effects of EOs are concentration-dependent and can have different effects on different sexes of insects of the same species. The behavioral responses of Thrips flavus to single compounds and different compound blends will be investigated.
It has been shown that changing the application method could effectively improve the control efficacy of EOs against pests [73,74,75]. The utilization of nanomaterials is an important part of the implementation of novel application methods. When rosemary essential oil was incorporated into biodegradable poly (epsilon-caprolactone) nanoparticles and administered topically to Drosophila suzukii, it effectively prolonged and enhanced the plant’s resistance to the insect. The results of this study will provide useful inspiration for our subsequent research [76,77]. In addition, nanoemulsion technologies are also being investigated; research is underway to use the EOs of Ayapana triplinervis (Vahl) R.M. King and H. Robinson to create more stable and long-lasting nanoemulsions to inhibit the reproduction of Aedes aegypti L. (Culicidae) larvae [78]. In addition, the stability of EOs has been improved through the use of microencapsulation technologies. An advantage of this method is that bioactive components’ release, solubilization, and protection can be controlled [79]. The application method used in the pot experiment in this study was spraying, which is proven to be almost safe for soybean potted plants (Table S1). The appropriate application method requires further testing and screening. In this study, the main aim is to screen the EOs for their potential insecticidal activities against Thrips flavus under laboratory conditions. Further studies will encompass greenhouse or field trials aimed at further assessing the effectiveness of the efficacy of different EOs for thrips control. The proven potential for control of Thysanoptera pests should be fully exploited in management strategies that include combined approaches [80].

5. Conclusions

Four Lamiaceae EOs showed significant control efficacy against thrips. The EOs caused more than 90% mortality at the concentration of 900.00 g a.i.·hm−2 and higher after 7 days. Spearmint oil caused a significant attraction response in adult females. The other EOs showed no significant attraction or repellent effects toward adult Thrips flavus of either sex. Linalool (24.52%), isopropyl myristate (28.74%), (+)-limonene (32.44%), and (+)-carvone (70.3%) were the primary chemical constituents of the EOs. The results of this preliminary study demonstrate that the four Lamiaceae EOs have the potential to develop plant-based insecticides and may be a possible alternative in the management of Thrips flavus, especially when considering reducing the use of synthetic pesticides.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/agronomy14061212/s1, Figure S1: Schematic diagram of the structure of a Y–tube olfactometer. Table S1 The phytotoxicity grades of four essential oils to soybean potted plants.

Author Contributions

Conceptualization, Y.G.; methodology, S.S. and Y.G.; investigation, T.P., Y.N., M.-L.X. and Y.Z.; data curation, T.P. and Y.N.; writing—original draft preparation, Y.N., T.P., C.Z., B.L., S.S., Y.G., M.-L.X. and Y.Z.; writing—review and editing, Y.G., Y.N., M.-L.X. and T.P.; funding acquisition, Y.G. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the National Key Research and Development Program of China (Grant No. 2023YFD1401000), the Science and Technology Projects of the Education Department of Jilin Province of China (Grant No. JJKH20230408KJ), and the Earmarked Fund for China Agriculture Research System of MOF and MARA (Grant No. CARS–04).

Data Availability Statement

Data are contained within this article or Supplementary Materials.

Acknowledgments

We would like to express our gratitude to our students, Hui Wang, Long Wang, and He-Xin Gao, for the plant management and insect collection.

Conflicts of Interest

Author Yijin Zhao was employed by the company Dalian City Investment Asset Management Co., Ltd. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Gao, Y.; Zhao, Y.J.; Wang, D.; Yang, J.; Ding, N.; Shi, S.S. Effect of different plants on the growth and reproduction of Thrips flavus (Thysanoptera: Thripidae). Insects 2021, 12, 502. [Google Scholar] [CrossRef] [PubMed]
  2. Dillon, F.M.; Panagos, C.; Gouveia, G.; Tayyari, F.; Chludil, H.D.; Edison, A.S.; Zavala, J.A. Changes in primary metabolite content may affect thrips feeding preference in soybean crops. Phytochemistry 2024, 220, 114014. [Google Scholar] [CrossRef] [PubMed]
  3. Adhikari, R.; Seal, D.R.; Schaffer, B.; Liburd, O.E.; Khan, R.A. Within-plant and within-field distribution patterns of asian bean thrips and melon thrips in snap bean. Insects 2023, 14, 175. [Google Scholar] [CrossRef] [PubMed]
  4. Gu, Z.Y.; Zhang, T.; Long, S.C.; Li, S.; Wang, C.; Chen, Q.C.; Chen, J.; Feng, Z.Y.; Cao, Y. Responses of Thrips hawaiiensis and Thrips flavus populations to elevated CO2 concentrations. J. Econ. Entomol. 2023, 116, 416–425. [Google Scholar] [CrossRef] [PubMed]
  5. Gao, Y.; Ding, N.; Wang, D.; Zhao, Y.J.; Cui, J.; Li, W.B.; Pei, T.H.; Shi, S.S. Effect of temperature on the development and reproduction of Thrips flavus (Thysanoptera: Thripidae). Agric. For. Entomol. 2022, 24, 279–288. [Google Scholar] [CrossRef]
  6. Sun, Y.; Hu, C.X.; Chen, G.H.; Li, X.X.; Liu, J.H.; Xu, Z.W.; Zhou, Y.; Wu, D.H.; Zhang, X.M. Insecticide-mediated changes in the population and toxicity of the thrips species, Frankliniella occidentalis (Pergande) and Thrips flavus (Schrank) (Thysanoptera: Thripidae). J. Econ. Entomol. 2024, 117, 293–301. [Google Scholar] [CrossRef] [PubMed]
  7. Shen, X.J.; Chen, J.C.; Cao, L.J.; Ma, Z.Z.; Sun, L.N.; Gao, Y.F.; Ma, L.J.; Wang, J.X.; Ren, Y.J.; Cao, H.Q.; et al. Interspecific and intraspecific variation in susceptibility of two co-occurring pest thrips, Frankliniella occidentalis and Thrips palmi, to nine insecticides. Pest Manag. Sci. 2023, 79, 3218–3226. [Google Scholar] [CrossRef] [PubMed]
  8. Reitz, S.R.; Gao, Y.L.; Kirk, W.D.J.; Hoddle, M.S.; Leiss, K.A.; Funderburk, J.E. Invasion biology, ecology and management of western flower thrips. Annu. Rev. Entomol. 2020, 65, 17–37. [Google Scholar] [CrossRef] [PubMed]
  9. Kilaso, M. Toxicity for control of Frankliniella schultzei and Selenothrips rubrocinctus (Thysanoptera: Thripidae) of several common synthetic insecticides. Fla. Entomol. 2022, 105, 155–159. [Google Scholar] [CrossRef]
  10. Monzote, L.; Scull, R.; Cos, P.; Setzer, W.N. Essential oil from piper aduncum: Chemical analysis, antimicrobial assessment, and literature review. Medicines 2017, 4, 49. [Google Scholar] [CrossRef]
  11. Kheloul, L.; Kellouche, A.; Bréard, D.; Gay, M.; Gadenne, C.; Anton, S. Trade-off between attraction to aggregation pheromones and repellent effects of spike lavender essential oil and its main constituent linalool in the flour beetle Tribolium confusum. Entomol. Exp. Appl. 2019, 167, 826–834. [Google Scholar] [CrossRef]
  12. Li, Y.; Yu, S.; Huang, J.; Wang, Z.Y.; Zeng, Y.F.; Wu, X.M.; Han, K.Z.; Zhou, H.J.; Wang, G.H.; Yu, Z.W. Study of behavioral, electrophysiological response, and the active compounds of the essential oils from six kinds of flowers against Solenopsis invicta Buren (Hymenoptera: Formicidae). Ind. Crop. Prod. 2022, 188, 115603. [Google Scholar] [CrossRef]
  13. Hu, Z.J.; Yang, J.W.; Chen, Z.H.; Chang, C.; Ma, Y.P.; Li, N.; Deng, M.; Mao, G.L.; Bao, Q.; Deng, S.Z.; et al. Exploration of clove bud (Syzygium aromaticum) essential oil as a novel attractant against Bactrocera dorsalis (Hendel) and its safety evaluation. Insects 2022, 13, 918. [Google Scholar] [CrossRef]
  14. Ikbal, C.; Pavela, R. Essential oils as active ingredients of botanical insecticides against aphids. J. Pest Sci. 2019, 92, 971–986. [Google Scholar] [CrossRef]
  15. Nenaah, G.E.; Alasmari, S.; Almadiy, A.A.; Albogami, B.Z.; Shawer, D.M.; Fadl, A.E. Bio-efficacy of Salvia officinalis essential oil, nanoemulsion and monoterpene components as eco-friendly green insecticides for controlling the granary weevil. Ind. Crop. Prod. 2023, 204, 117298. [Google Scholar] [CrossRef]
  16. Zhao, F.; Chen, Y.P.; Salmaki, Y.; Drew, B.T.; Wilson, T.C.; Scheen, A.C.; Celep, F.; Bräuchler, C.; Bendiksby, M.; Wang, Q.; et al. An updated tribal classification of Lamiaceae based on plastome phylogenomics. BMC Biol. 2021, 19, 2. [Google Scholar] [CrossRef]
  17. Singh, P.; Pandey, A.K. Prospective of essential oils of the Genus Mentha as biopesticides: A review. Front. Plant Sci. 2018, 9, 1295. [Google Scholar] [CrossRef]
  18. Patrignani, F.; Prasad, S.; Novakovic, M.; Marin, P.D.; Bukvicki, D. Lamiaceae in the treatment of cardiovascular diseases. Front. Biosci. 2021, 26, 612–643. [Google Scholar] [CrossRef]
  19. Ahmed, A.M.A.; Elsayed, A.A.A.; El-Gohary, A.E.; Khalid, K.A. Exogenous l-tyrosine motivates diversities in horsemint essential oil. J. Essent. Oil Bear. Plants. 2022, 25, 601–610. [Google Scholar] [CrossRef]
  20. Chrysargyris, A.; Tomou, E.M.; Goula, K.; Dimakopoulou, K.; Tzortzakis, N.; Skaltsa, H. Sideritis L. essential oils: A systematic review. Phytochemistry 2023, 209, 113607. [Google Scholar] [CrossRef]
  21. Chen, Y.J.; Luo, J.X.; Zhang, N.; Yu, W.J.; Jiang, J.X.; Dai, G.H. Insecticidal activities of Salvia hispanica L. essential oil and combinations of their main compounds against the beet armyworm Spodoptera exigua. Ind. Crop. Prod. 2021, 162, 113271. [Google Scholar] [CrossRef]
  22. Karpinski, T.M. Essential oils of lamiaceae family plants as antifungals. Biomolecules 2020, 10, 103. [Google Scholar] [CrossRef]
  23. Bedini, S.; Djebbi, T.; Ascrizzi, R.; Farina, P.; Pieracci, Y.; Echeverría, M.C.; Flamini, G.; Trusendi, F.; Ortega, S.; Chiliquinga, A.; et al. Repellence and attractiveness: The hormetic effect of aromatic plant essential oils on insect behavior. Ind. Crop. Prod. 2024, 210, 118122. [Google Scholar] [CrossRef]
  24. Fuchs, L.K.; Holland, A.H.; Ludlow, R.A.; Coates, R.J.; Armstrong, H.; Pickett, J.A.; Harwood, J.L.; Scofield, S. Genetic manipulation of biosynthetic pathways in mint. Front. Plant Sci. 2022, 13, 928178. [Google Scholar] [CrossRef]
  25. Ebadollahi, A.; Ziaee, M.; Palla, F. Essential oils extracted from different species of the Lamiaceae plant family as prospective bioagents against several detrimental pests. Molecules 2020, 25, 1556. [Google Scholar] [CrossRef]
  26. Peschiutta, M.L.; Achimon, F.; Brito, V.D.; Pizzolitto, R.P.; Zygadlo, J.A.; Zunino, M.P. Fumigant toxicity of essential oils against Sitophilus zeamais (Motschulsky) (Coleoptera: Curculionidae): A systematic review and meta-analysis. J. Pest Sci. 2022, 95, 1037–1056. [Google Scholar] [CrossRef]
  27. Teke, M.A.; Mutlu, Ç. Insecticidal and behavioral effects of some plant essential oils against Sitophilus granarius L. and Tribolium castaneum (Herbst). J. Plant Dis. Prot. 2021, 128, 109–119. [Google Scholar] [CrossRef]
  28. Azeem, M.; Iqbal, Z.; Emami, S.N.; Nordlander, G.; Nordenhem, H.; Mozuraitis, R.; El-Seedi, H.R.; Borg-Karlson, A.K. Chemical composition and antifeedant activity of some aromatic plants against pine weevil (Hylobius abietis). Ann. Appl. Biol. 2020, 177, 121–131. [Google Scholar] [CrossRef]
  29. Galland, C.D.; Glesner, V.; Verheggen, F. Laboratory and field evaluation of a combination of attractants and repellents to control Drosophila suzukii. Entomol. Gen. 2020, 40, 263–272. [Google Scholar] [CrossRef]
  30. Katerinopoulos, H.E.; Pagona, G.; Afratis, A.; Stratigakis, N.; Roditakis, N. Composition and insect attracting activity of the essential oil of Rosmarinus officinalis. J. Chem. Ecol. 2005, 31, 111–122. [Google Scholar] [CrossRef]
  31. Barros, F.A.P.; Radünz, M.; Scariot, M.A.; Camargo, T.M.; Nunes, C.F.P.; de Souza, R.R.; Gilson, I.K.; Hackbart, H.C.S.; Radünz, L.L.; Oliveira, J.V.; et al. Efficacy of encapsulated and non-encapsulated thyme essential oil (Thymus vulgaris L.) in the control of Sitophilus zeamais and its effects on the quality of corn grains throughout storage. Crop Prot. 2022, 153, 105885. [Google Scholar] [CrossRef]
  32. Farag, S.M.; Moustafa, M.A.M.; Fónagy, A.; Kamel, O.; Abdel-Haleem, D.R. Chemical composition of four essential oils and their adulticidal, repellence, and field oviposition deterrence activities against Culex pipiens L. (Diptera: Culicidae). Parasitol. Res. 2024, 123, 110. [Google Scholar] [CrossRef] [PubMed]
  33. Han, Y.F. Fauna of Economic Insects in China (Thysanoptera); Science Press: Beijing, China, 1997. [Google Scholar]
  34. Mound, L.A.; Collins, D.W.; Hastings, A. Thysanoptera Britannica et Hibernica–Thrips of the British Isles; Lucidcentral.org, Identic Pty Ltd.: Queensland, Australia, 2018; Available online: https://keys.lucidcentral.org/keys/v3/british_thrips/index.html (accessed on 15 May 2024).
  35. Brenner, R.; Prischmann-Voldseth, D.A. Influence of a neonicotinoid seed treatment on a nontarget herbivore of soybean (twospotted spider mite) and diet switching by a co-occurring omnivore (western flower thrips). Environ. Entomol. 2020, 49, 461–472. [Google Scholar] [CrossRef] [PubMed]
  36. Pei, T.H.; Zhao, Y.J.; Wang, S.Y.; Li, X.F.; Sun, C.Q.; Shi, S.S.; Xu, M.L.; Gao, Y. Preliminary study on insecticidal potential and chemical composition of five Rutaceae essential oils against Thrips flavus (Thysanoptera: Thripidae). Molecules 2023, 28, 2998. [Google Scholar] [CrossRef] [PubMed]
  37. Baviskar, K.P.; Jain, D.V.; Pingale, S.D.; Wagh, S.S.; Gangurde, S.P.; Shardul, S.A.; Dahale, A.R.; Jain, K.S. A review on hyphenated techniques in analytical chemistry. Curr. Anal. Chem. 2022, 18, 956–976. [Google Scholar] [CrossRef]
  38. Smelcerovic, A.; Djordjevic, A.; Lazarevic, J.; Stojanovic, G. Recent advances in analysis of essential oils. Curr. Anal. Chem. 2013, 9, 61–70. [Google Scholar] [CrossRef]
  39. Huang, X.; Ge, S.Y.; Liu, J.H.; Wang, Y.; Liang, X.Y.; Yuan, H.B. Chemical composition and bioactivity of the essential oil from Artemisia lavandulaefolia (Asteraceae) on Plutella xylostella (Lepidoptera: Plutellidae). Fla. Entomol. 2018, 101, 44–48. [Google Scholar] [CrossRef]
  40. Zhang, Z.Q.; Sun, X.L.; Xin, Z.J.; Luo, Z.X.; Gao, Y.; Bian, L.; Chen, Z.M. Identification and field evaluation of non-host volatiles disturbing host location by the tea geometrid, Ectropis obliqua. J. Chem. Ecol. 2013, 39, 1284–1296. [Google Scholar] [CrossRef]
  41. Tang, Q.Y.; Zhang, C.X. Data Processing System (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Sci. 2013, 20, 254–260. [Google Scholar] [CrossRef]
  42. Zouirech, O.; El Moussaoui, A.; Saghrouchni, H.; Gaafar, A.R.Z.; Nafidi, H.A.; Bourhia, M.; Khallouki, F.; Lyoussi, B.; Derwich, E. Prefatory in silico studies and in vitro insecticidal effect of Nigella sativa (L.) essential oil and its active compound (carvacrol) against the Callosobruchus maculatus adults (Fab), a major pest of chickpea. Open Chem. 2023, 21, 20230133. [Google Scholar] [CrossRef]
  43. Elumalai, K.; Krishnappa, K.; Pandiyan, J.; Alharbi, N.S.; Kadaikunnan, S.; Khaled, J.M.; Barnard, D.R.; Vijayakumar, N.; Govindarajan, M. Characterization of secondary metabolites from Lamiaceae plant leaf essential oil: A novel perspective to combat medical and agricultural pests. Physiol. Mol. Plant Pathol. 2022, 117, 101752. [Google Scholar] [CrossRef]
  44. Palazzolo, E.; Laudicina, V.A.; Germanà, M.A. Current and potential use of citrus essential oils. Curr. Org. Chem. 2013, 17, 3042–3049. [Google Scholar] [CrossRef]
  45. Yang, X.; Han, H.; Li, B.L.; Zhang, D.Y.; Zhang, Z.L.; Xie, Y.J. Fumigant toxicity and physiological effects of spearmint (Mentha spicata, Lamiaceae) essential oil and its major constituents against Reticulitermes dabieshanensis. Ind. Crop. Prod. 2021, 171, 113894. [Google Scholar] [CrossRef]
  46. Yeom, H.J.; Lee, H.R.; Lee, S.C.; Lee, J.E.; Seo, S.M.; Park, I.K. Insecticidal activity of lamiaceae plant essential oils and their constituents against Blattella germanica L. adult. J. Econ. Entomol. 2018, 111, 653–661. [Google Scholar] [CrossRef] [PubMed]
  47. Stepanycheva, E.; Petrova, M.; Chermenskaya, T.; Pavela, R. Fumigant effect of essential oils on mortality and fertility of thrips Frankliniella occidentalis Perg. Environ. Sci. Pollut. Res. 2019, 26, 30885–30892. [Google Scholar] [CrossRef] [PubMed]
  48. Topuz, E. Insecticidal activity of Mentha pulegium essential oil against Thrips tabaci, Bemisia tabaci and Tuta absoluta adults. Int. J. Trop. Insect Sci. 2023, 43, 1475–1483. [Google Scholar] [CrossRef]
  49. Yi, C.G.; Choi, B.R.; Park, H.M.; Park, C.G.; Ahn, Y.J. Fumigant toxicity of plant essential oils to Thrips palmi (Thysanoptera: Thripidae) and Orius strigicollis (Heteroptera: Anthocoridae). J. Econ. Entomol. 2006, 99, 1733–1738. [Google Scholar] [CrossRef] [PubMed]
  50. Pumnuan, J.; Insung, A. Fumigant toxicity of plant essential oils in controlling thrips, Frankliniella schultzei (Thysanoptera: Thripidae) and mealybug, Pseudococcus jackbeardsleyi (Hemiptera: Pseudococcidae). J. Entomol. 2016, 40, 1–10. [Google Scholar] [CrossRef]
  51. Ni, Z.J.; Wang, X.; Shen, Y.; Thakur, K.; Han, J.Z.; Zhang, J.G.; Hu, F.; Wei, Z.J. Recent updates on the chemistry, bioactivities, mode of action, and industrial applications of plant essential oils. Trends Food Sci. Technol. 2021, 110, 78–89. [Google Scholar] [CrossRef]
  52. Russo, A.; Bruno, M.; Avola, R.; Cardile, V.; Rigano, D. Chamazulene-Rich Artemisia arborescens essential oils affect the cell growth of human melanoma cells. Plants 2020, 9, 1000. [Google Scholar] [CrossRef]
  53. da Silva, W.M.F.; Kringel, D.H.; de Souza, E.J.D.; Zavareze, E.D.; Dias, A.R.G. Basil essential oil: Methods of extraction, chemical composition, biological activities, and food applications. Food Bioprocess Technol. 2022, 15, 1–27. [Google Scholar] [CrossRef]
  54. Saleh, I.A.; El Gendy, A.N.G.; Afifi, M.A.; El-Seedi, H.R. Microwave extraction of essential oils from Senecio serpens GD rowly and comparison with conventional hydro-distillation method. J. Essent. Oil Bear. Plants. 2019, 22, 955–961. [Google Scholar] [CrossRef]
  55. Passos, B.G.; de Albuquerque, R.; Muñoz-Acevedo, A.; Echeverria, J.; Llaure-Mora, A.M.; Ganoza-Yupanqui, M.L.; Rocha, L. Essential oils from Ocotea species: Chemical variety, biological activities and geographic availability. Fitoterapia 2022, 156, 105065. [Google Scholar] [CrossRef]
  56. Kaur, H.; Bhardwaj, U.; Kaur, R. Cymbopogon nardus essential oil: A comprehensive review on its chemistry and bioactivity. J. Essent. Oil Res. 2021, 33, 205–220. [Google Scholar] [CrossRef]
  57. Ayub, M.A.; Goksen, G.; Fatima, A.; Zubair, M.; Abid, M.A.; Starowicz, M. Comparison of conventional extraction techniques with superheated steam distillation on chemical characterization and biological activities of Syzygium aromaticum L. essential oil. Separations 2023, 10, 27. [Google Scholar] [CrossRef]
  58. You, C.X.; Yang, K.; Wu, Y.; Zhang, W.J.; Wang, Y.; Geng, Z.F.; Chen, H.P.; Jiang, H.Y.; Du, S.S.; Deng, Z.W.; et al. Chemical composition and insecticidal activities of the essential oil of Perilla frutescens (L.) Britt. aerial parts against two stored product insects. Eur. Food Res. Technol. 2014, 239, 481–490. [Google Scholar] [CrossRef]
  59. Eliopoulos, P.A.; Hassiotis, C.N.; Andreadis, S.S.; Porichi, A.E.E. Fumigant toxicity of essential oils from basil and spearmint against two major pyralid pests of stored products. J. Econ. Entomol. 2015, 108, 805–810. [Google Scholar] [CrossRef]
  60. Shivaramu, S.; Parepally, S.K.; Byregowda, V.Y.; Damodaram, K.J.P.; Bhatnagar, A.; Naga, K.C.; Sharma, S.; Kumar, M.; Kempraj, V. Estragole, a potential attractant of the winged melon aphid Aphis gossypii. Pest Manag. Sci. 2023, 79, 2365–2371. [Google Scholar] [CrossRef]
  61. Sadeh, D.; Nitzan, N.; Shachter, A.; Chaimovitsh, D.; Dudai, N.; Ghanim, M. Whitefly attraction to rosemary (Rosmarinus officinialis L.) is associated with volatile composition and quantity. PLoS ONE 2017, 12, e0177483. [Google Scholar] [CrossRef]
  62. Blythe, E.K.; Tabanca, N.; Demirci, B.; Kendra, P.E. Chemical composition of essential oil from Tetradenia riparia and its attractant activity for mediterranean fruit fly, Ceratitis capitata. Nat. Prod. Commun. 2020, 15, 6. [Google Scholar] [CrossRef]
  63. Feng, Y.X.; Wang, Y.; You, C.X.; Guo, S.S.; Du, Y.S.; Du, S.S. Bioactivities of patchoulol and phloroacetophenone from Pogostemon cablin essential oil against three insects. Int. J. Food Prop. 2019, 22, 1365–1374. [Google Scholar] [CrossRef]
  64. van Tol, R.; James, D.E.; de Kogel, W.J.; Teulon, D.A.J. Plant odours with potential for a push-pull strategy to control the onion thrips, Thrips tabaci. Entomol. Exp. Appl. 2007, 122, 69–76. [Google Scholar] [CrossRef]
  65. Zvaríková, M.; Masarovic, R.; Zvarík, M.; Bagová, K.; Procházková, L.; Prokop, P.; Fedor, P. The effect of plant essential oils on the Banded Greenhouse Thrips (Hercinothrips femoralis O. M. Reuter 1891) (Thysanoptera: Thripidae: Panchaetothripinae). J. Plant Dis. Prot. 2023, 130, 747–755. [Google Scholar] [CrossRef]
  66. Koschier, E.H.; Sedy, K.A. Labiate essential oils affecting host selection and acceptance of Thrips tabaci lindeman. Crop Prot. 2003, 22, 929–934. [Google Scholar] [CrossRef]
  67. Li, X.W.; Zhang, Z.J.; Hafeez, M.; Huang, J.; Zhang, J.M.; Wang, L.K.; Lu, Y.B. Rosmarinus officinialis L. (Lamiales: Lamiaceae), a promising repellent plant for Thrips Management. J. Econ. Entomol. 2021, 114, 131–141. [Google Scholar] [CrossRef]
  68. Sanei-Dehkordi, A.; Hatami, S.; Zarenezhad, E.; Montaseri, Z.; Osanloo, M. Efficacy of nanogels containing carvacrol, cinnamaldehyde, thymol, and a mix compared to a standard repellent against Anopheles stephensi. Ind. Crop. Prod. 2022, 189, 115883. [Google Scholar] [CrossRef]
  69. Liu, S.Y.; Zhao, J.; Hamada, C.; Cai, W.L.; Khan, M.; Zou, Y.L.; Hua, H.X. Identification of attractants from plant essential oils for Cyrtorhinus lividipennis, an important predator of rice planthoppers. J. Pest Sci. 2019, 92, 769–780. [Google Scholar] [CrossRef]
  70. Diabate, S.; Martin, T.; Murungi, L.K.; Fiaboe, K.K.M.; Subramanian, S.; Wesonga, J.; Deletre, E. Repellent activity of Cymbopogon citratus and Tagetes minuta and their specific volatiles against Megalurothrips sjostedti. J. Appl. Entomol. 2019, 143, 855–866. [Google Scholar] [CrossRef]
  71. López, S.B.; López, M.L.; Aragón, L.M.; Tereschuk, M.L.; Slanis, A.C.; Feresin, G.E.; Zygadlo, J.A.; Tapia, A.A. Composition and anti-insect activity of essential oils from Tagetes L. Species (Asteraceae, Helenieae) on Ceratitis capitata Wiedemann and Triatoma infestans Klug. J. Agric. Food Chem. 2011, 59, 5286–5292. [Google Scholar] [CrossRef]
  72. Dukic, N.; Markovic, T.; Mikic, S.; Cutovic, N. Repellent activity of basil, clary sage and celery essential oils on Tribolium castaneum (Herbst). J. Stored Prod. Res. 2023, 103, 102150. [Google Scholar] [CrossRef]
  73. Jesser, E.; Yeguerman, C.; Stefanazzi, N.; Gomez, R.; Murray, A.P.; Ferrero, A.A.; Werdin-González, J.O. Ecofriendly approach for the control of a common insect pest in the food industry, combining polymeric nanoparticles and post-application temperatures. J. Agric. Food Chem. 2020, 68, 5951–5958. [Google Scholar] [CrossRef] [PubMed]
  74. Chatzidaki, M.D.; Demisli, S.; Zingkou, E.; Liggri, P.G.V.; Papachristos, D.P.; Balatsos, G.; Karras, V.; Nallet, F.; Michaelakis, A.; Sotiropoulou, G.; et al. Essential oil-in-water microemulsions for topical application: Structural study, cytotoxic effect and insect repelling activity. Colloid Surf. A-Physicochem. Eng. Asp. 2022, 654, 10. [Google Scholar] [CrossRef]
  75. Kotronia, M.; Kavetsou, E.; Loupassaki, S.; Kikionis, S.; Vouyiouka, S.; Detsi, A. Encapsulation of oregano (Origanum onites L.) essential oil in -cyclodextrin (-CD): Synthesis and characterization of the inclusion complexes. Bioengineering 2017, 4, 74. [Google Scholar] [CrossRef] [PubMed]
  76. Caetano, A.R.S.; Cardoso, M.D.; Haddi, K.; Campolina, G.A.; De Souza, B.M.; Da SilvaLunguinho, A.; De Souza, L.; Nelson, D.L.; De Oliveira, J.E. Rosmarinus officinalis essential oil incorporated into nanoparticles as an efficient insecticide against Drosophila suzukii (Diptera: Drosophilidae). Austral Entomol. 2022, 61, 265–272. [Google Scholar] [CrossRef]
  77. Gebaly, A.S.E.; Sofy, A.R.; Hmed, A.A.; Youssef, A.M. Combination of nanoparticles (NPs) and essential oils (EOs) as promising alternatives to non-effective antibacterial, antifungal and antiviral agents: A review. Biocatal. Agric. Biotechnol. 2024, 57, 103067. [Google Scholar] [CrossRef]
  78. Rodrigues, A.B.L.; Martins, R.L.; Rabelo, É.; Tomazi, R.; Santos, L.L.; Brandao, L.B.; Faustino, C.G.; Farias, A.L.F.; dos Santos, C.B.R.; Cantuária, P.D.; et al. Development of nano-emulsions based on Ayapana triplinervis essential oil for the control of Aedes aegypti larvae. PLoS ONE 2021, 16, e0254225. [Google Scholar] [CrossRef] [PubMed]
  79. Indriyani, N.N.; Al Anshori, J.; Permadi, N.; Nurjanah, S.; Julaeha, E. Bioactive components and their activities from different parts of Citrus aurantifolia (Christm.) swingle for food development. Foods 2023, 12, 2036. [Google Scholar] [CrossRef]
  80. Koschier, E.H. Essential oil compounds for thrips control—A review. Nat. Prod. Commun. 2008, 3, 1171–1182. [Google Scholar] [CrossRef]
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Figure 1. The control efficacy of four essential oils against Thrips flavus after one day of application in pot experiment. Different lowercase letters indicated significant differences (p < 0.05) among the control and essential oil treatments at the same concentration.
Figure 1. The control efficacy of four essential oils against Thrips flavus after one day of application in pot experiment. Different lowercase letters indicated significant differences (p < 0.05) among the control and essential oil treatments at the same concentration.
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Agronomy 14 01212 g002
Figure 2. The control efficacy of four essential oils against Thrips flavus after three days of application in pot experiment. Different lowercase letters indicated significant differences (p < 0.05) among the control and essential oil treatments at the same concentration.
Figure 2. The control efficacy of four essential oils against Thrips flavus after three days of application in pot experiment. Different lowercase letters indicated significant differences (p < 0.05) among the control and essential oil treatments at the same concentration.
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Agronomy 14 01212 g003
Figure 3. The control efficacy of four essential oils against Thrips flavus after seven days of application in pot experiment. Different lowercase letters indicated significant differences (p < 0.05) among the control and essential oil treatments at the same concentration.
Figure 3. The control efficacy of four essential oils against Thrips flavus after seven days of application in pot experiment. Different lowercase letters indicated significant differences (p < 0.05) among the control and essential oil treatments at the same concentration.
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Agronomy 14 01212 g004
Figure 4. Olfactory behavioral response of female adult Thrips flavus to four essential oils. The symbol “ns” indicated ‘no significance’ (p > 0.05), while an asterisk “*” indicated significance (p < 0.05).
Figure 4. Olfactory behavioral response of female adult Thrips flavus to four essential oils. The symbol “ns” indicated ‘no significance’ (p > 0.05), while an asterisk “*” indicated significance (p < 0.05).
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Agronomy 14 01212 g005
Figure 5. Olfactory behavioral response of male adult Thrips flavus to four essential oils. The symbol “ns” indicated ‘no significance’ (p > 0.05).
Figure 5. Olfactory behavioral response of male adult Thrips flavus to four essential oils. The symbol “ns” indicated ‘no significance’ (p > 0.05).
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Table 1. The toxicity of four essential oils to adult Thrips flavus.
Table 1. The toxicity of four essential oils to adult Thrips flavus.
Essential Oils95% Confidence IntervalLC50 (mg/mL)Regression EquationCorrelation Coefficientχ2df
Perilla leaf oil0.35~0.510.43y = 6.2134 + 3.3226x0.897.033
Marjoram oil0.17~0.600.41y = 6.5178 + 3.9312x0.8817.873
Clary sage oil0.35~0.480.42y = 6.1932 + 4.1952x0.990.943
Spearmint oil0.47~0.620.54y = 6.1934 + 4.4029x0.947.413
30% thiamethoxam0.0053~0.00950.0077y = 10.4813 + 2.5941x0.923.13473
Note: LC50 = concentration to kill 50% of thrips.
Table 2. Chemical constituents of marjoram oil (Origanum majorana L.).
Table 2. Chemical constituents of marjoram oil (Origanum majorana L.).
No.Retention Time (min)Retention IndexCompoundsRelative Percentage (%)
18.141085linalool24.52
23.308843leaf alcohol0.26
37.6371069methyl benzoate2.95
49.7651145benzyl acetate16.42
511.5751215ethyl phenylacetate4.31
611.961240nerol0.57
713.0121306methyl aminobenzoate2.95
813.13513172-tert-butylcyclohexanol3.09
913.3071332phenol, 2-methoxy-3-(2-propenyl)1.64
1013.57913554-tert-butylcyclohexanol5.78
1113.75813702,6,6-trimethyl-2,4-cycloheptadien-1-one0.29
1215.2261494butylated hydroxytoluene2.35
1316.931618methyl dihydrojasmonate4.65
1417.3681645cis-3-hexenyl salicylate0.94
1518.6661720α-hexylcinnamaldehyde14.28
1619.19817471-phenyl-1-nonen-3-one0.67
Table 3. Chemical constituents of clary sage oil (Salvia sclarea L.).
Table 3. Chemical constituents of clary sage oil (Salvia sclarea L.).
NumberRetention Time (min)Retention IndexCompoundsRelative Percentage (%)
114.5571438α-guaiene0.44
215.3481504α-bulnesene0.57
317.5181654patchouli alcohol1.10
46.1421013p-cymene2.23
54.554933α-pinene1.24
65.261973β-pinene0.37
714.3571420bicyclo[5.2.0]nonane, 4-ethenyl-4,8,8-trimethyl-2-methylene-0.45
86.33610211,8-cineole7.31
910.4821171terpinen-4-ol1.12
1010.7311179α-terpineol2.52
1112.0561246linalyl acetate20.07
1213.4761346geranyl acetate0.52
138.1321085linalool15.18
149.2861126DL-camphor4.13
1511.47912087-methoxy-3,7-dimethyloctanal1.20
1613.3821338linalyl anthranilate0.34
1713.6871364neryl acetate0.6
1818.8191728benzyl benzoate11.87
1920.4751813isopropyl myristate28.74
Table 4. Chemical constituents of perilla leaf oil (Perilla frutescens (L.) Britt.).
Table 4. Chemical constituents of perilla leaf oil (Perilla frutescens (L.) Britt.).
NumberRetention Time (min)RICompoundsRelative Percentage (%)
16.1391013p-cymene13.25
26.3751023(+)-limonene32.44
37.0971051γ-terpinene23.92
47.9561079terpinolene10.53
56.78310391,3,6-octatriene, 3,7-dimethyl-, (z)-2.34
67.210543-carene0.61
77.331059cis-linalool oxide0.59
87.6081068(-)-fenchone0.70
911.871234cinnamaldehyde15.61
Table 5. Chemical constituents of spearmint oil (Mentha spicata L.).
Table 5. Chemical constituents of spearmint oil (Mentha spicata L.).
Number.Retention Time (min)RICompoundsRelative Percentage (%)
14.557934α-pinene1.05
26.3731023(+)-limonene26.22
35.263973β-pinene1.19
410.38211673-p-menthol1.20
511.6141217(+)-carvone70.34
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Niu, Y.; Pei, T.; Zhao, Y.; Zhou, C.; Liu, B.; Shi, S.; Xu, M.-L.; Gao, Y. Exploring the Efficacy of Four Essential Oils as Potential Insecticides against Thrips flavus. Agronomy 2024, 14, 1212. https://doi.org/10.3390/agronomy14061212

AMA Style

Niu Y, Pei T, Zhao Y, Zhou C, Liu B, Shi S, Xu M-L, Gao Y. Exploring the Efficacy of Four Essential Oils as Potential Insecticides against Thrips flavus. Agronomy. 2024; 14(6):1212. https://doi.org/10.3390/agronomy14061212

Chicago/Turabian Style

Niu, Yulong, Tianhao Pei, Yijin Zhao, Changjun Zhou, Bing Liu, Shusen Shi, Meng-Lei Xu, and Yu Gao. 2024. "Exploring the Efficacy of Four Essential Oils as Potential Insecticides against Thrips flavus" Agronomy 14, no. 6: 1212. https://doi.org/10.3390/agronomy14061212

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