Next Article in Journal
Linoleic Acid-Enriched Diet Increases Mitochondrial Tetralinoleoyl Cardiolipin, OXPHOS Protein Levels, and Uncoupling in Interscapular Brown Adipose Tissue during Diet-Induced Weight Gain
Previous Article in Journal
Comprehensive Transcriptome Analysis of Different Skin Colors to Evaluate Genes Related to the Production of Pigment in Celestial Goldfish
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Biology
Volume 12
Issue 1
10.3390/biology12010008
biology-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

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

Chemical Composition, Larvicidal and Repellent Activities of Wild Plant Essential Oils against Aedes aegypti

by
Muhammad Ghazanfar Abbas
1,
Abdullah Haris
1,
Muhammad Binyameen
1,†,
Abdul Nazir
2,
Raimondas Mozūratis
3,4,*,† and
Muhammad Azeem
5,*,†
1
Laboratory of Insect Chemical Ecology, Department of Entomology, Faculty of Agricultural Sciences & Technology, Bahauddin Zakariya University, Multan 60800, Pakistan
2
Department of Environmental Sciences, Abbottabad Campus, COMSATS University Islamabad, Abbottabad 22060, Pakistan
3
Department of Zoology, Stockholm University, 10691 Stockholm, Sweden
4
Laboratory of Chemical and Behavioural Ecology, Institute of Ecology, Nature Research Centre, LT-08412 Vilnius, Lithuania
5
Department of Chemistry, Abbottabad Campus, COMSATS University Islamabad, Abbottabad 22060, Pakistan
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Biology 2023, 12(1), 8; https://doi.org/10.3390/biology12010008
Submission received: 8 November 2022 / Revised: 14 December 2022 / Accepted: 17 December 2022 / Published: 21 December 2022
(This article belongs to the Section Zoology)
Browse Figures
Versions Notes

Abstract

:

Simple Summary

Mosquitoes are the deadliest insects alive due to the transmission of pathogens that cause diseases. Plant essential oils are considered an alternative to synthetic repellents for controlling mosquitoes. We have investigated the repellent and larvicidal activity of six plant essential oils against adult female mosquitos and the larvae of yellow fever mosquitos, Aedes aegypti. The essential oils extracted from Mentha longifolia, Zanthoxylum armatum, Erigeron bonariensis, and E. canadensis have the potential to manage Ae. aegypti at the larval stage. Moreover, M. longifolia, E. canadensis, E. bonariensis, and Salsola imbricata essential oils exhibited prolonged mosquito-repellent activity against adult female Ae. Aegypti; these oils might be used to develop formulations that are efficient and cost-effective as mosquito repellents without harming humans and the environment.

Abstract

Bio-degradable and eco-friendly essential oils (EOs) extracted from Mentha longifolia, Salsola imbricata, Erigeron bonariensis, E. canadensis, Ailanthus altissima, and Zanthoxylum armatum were investigated for their repellent and larvicidal potential against Aedes aegypti mosquitoes. The EOs of M. longifolia, S. imbricata, E. bonariensis, E. canadensis, A. altissima, and Z. armatum exhibited 99.0%, 96.8%, 40.2%, 41.7%, 29.1%, and 13.2% repellency against mosquitoes at a tested dose of 33.3 μg/cm2, respectively. In time span bioassays, the EOs of M. longifolia, S. imbricata, E. bonariensis, and E. canadensis showed more than 40% repellency for 60 min at a tested dose of 330 μg/cm2. Larvicidal bioassays revealed that larvae of Ae. aegypti were the most susceptible to M. longifolia (LC50, 39.3 mg/L), E. bonariensis (LC50, 26.0 mg/L), E. canadensis (LC50, 35.7 mg/L), and Z. armatum (LC50, 35.9 mg/L) EOs upon 48 h exposure. The most abundant constituents in the EOs of M. longifolia, S. imbricata, E. bonariensis, E. canadensis and A. altissima were piperitone oxide (45.5%), carvone (39.9%), matricaria ester (43.1%), (31.7%) and eugenol (24.4%), respectively. Our study demonstrates that EOs of M. longifolia, S. imbricata, E. bonariensis, and E. canadensis might be used to control Ae. aegypti mosquitoes without harming humans or the environment.

Graphical Abstract

1. Introduction

Mosquitoes are the deadliest insects [1] due to the transmission of pathogens, causing diseases such as the West Nile virus, filariasis, dengue, chikungunya, Japanese encephalitis, and malaria in humans [2]. The yellow fever mosquito, Aedes aegypti L. (Diptera: Culicidae) is a primary vector of the Zika virus, chikungunya, yellow fever, and dengue viruses [2]. Moreover, it is listed as a major vector threat in the world due to its proliferation ability [3]. In the last few decades, the incidence of diseases spread by Ae. aegypti increased all around the world. In 1969, the epidemic of dengue was present in 9 countries, but now it has spread to more than 100 countries. The incidence of dengue has increased dramatically, and about half the population of the world is at risk of contracting this virus from the yellow fever mosquito [4]. Asia suffers more than 70% of the global burden of diseases due to dengue mosquitoes [2], and the people of Pakistan are at risk due to dengue. Dengue infections in Pakistan are mostly reported in September and October [5,6]. Dengue is considered a dangerous disease due to difficulty in control and diagnosis [7]. Therefore, one of the means to battle this disease is a reduction in Ae. aegypti populations.
Synthetic insecticides like deltamethrin, temephos, acetamiprid, metofluthrin, and cypermethrin have been found to be effective against Ae. aegypti [8,9,10,11]. However, resistance in Ae. aegypti has also been reported against permethrin, deltamethrin, and temephos [12,13,14,15]. Chemical insecticides are a danger to non-target organisms [16,17] causing endocrine, reproductive, and carcinogenic problems in humans [18,19]. N, N’-diethyl-3-methylbenzamide (DEET) is a common mosquito repellent [20]. However, the extensive use of DEET has also resulted in harmful effects like allergic reactions and skin irritation, and is also responsible for causing brain disease—encephalopathy—in children [21,22]. Keeping in mind the problems associated with chemical insecticides, synthetic repellents, and diseases spread by Ae. aegypti, there is a need to find natural chemical sources to develop new plant-based mosquito repellents and insecticides.
Plants-based products are not only safe to use but are also not harmful to humans and animals [23]. Furthermore, plant-based materials have proven very effective against blood-seeking insects. For example, some components of plant-based essential oils like safrole, myristicin, terpinolene, and α-terpineol showed higher efficiency against these insects than DEET [24]. Some other essential oils have also proven to be very effective in killing and repelling the Aedes species [19,25,26]. Plant essential oils are considered an alternative for controlling insect pests. In the market, plant-based chemicals represent an estimated USD seven hundred million and forty-five thousand tons of the total world pesticide production. Furthermore, due to their degradability, these are safe to use for humans and the environment [27].
The present study reports the repellent and larvicidal activity of six plant essential oils (EOs), derived from Mentha longifolia, Salsola imbricata, Erigeron bonariensis, E. canadensis, Ailanthus altissima, and Zanthoxylum armatum, against adult females and larvae of Ae. aegypti.

2. Materials and Methods

2.1. Collection of Plant Material

Leaves and stems of M. longifolia, S. imbricata, E. bonariensis, E. canadensis, A. altissima, and Z. armatum were collected from the Bio-Park at Bahauddin Zakaria University, Multan and from a hilly area of Abbottabad, Pakistan during September–October. The species of the plants were identified by a plant taxonomist at COMSATS University Islamabad, Abbottabad Campus, Abbottabad, Pakistan as well as using the Plant-Net Identifier Software, Version 2.0, (Sydney, Australia).

2.2. Extraction of Essential Oils

The steam distillation method was used to extract essential oils from fresh parts of identified plants on the same day as their collection. The steam distillation method is described in detail by Azeem et al. [28,29]. Briefly, about 2 kg of fresh plant biomass was cut into small pieces and placed into the distillation apparatus. Two litres of distilled water were added to the bottom of the distillation apparatus and plant material was loaded above the water level. The distillery was heated by using an electric heating mantle. The distillate, comprising water and plant volatiles, was collected in a separating funnel for 4 h. The distillate was extracted in HPLC-grade n-hexane (70 mL × 3). The extracted organic layer was dried by the addition of anhydrous MgSO4. After filtration, the solvent was evaporated with a low-pressure rotary evaporator at 25 °C. The mass of extracted essential oil was compared with the mass of fresh plant materials to calculate the percentage yield of extracted essential oil. The essential oil was stored in screw-capped glass vials at −20 °C until use for chemical analysis and bioassays.

2.3. Rearing of Ae. aegypti

The Ae. aegypti colony was reared in the laboratory, using the method described by Johnson [30] and Zheng et al. [31]. The larval population of Ae. aegypti was taken from Health Department, Multan, Pakistan. Larvae were placed in a plastic container (20 × 16 × 4 cm) filled with water. A fish diet (Osaka green fish food) consisting of 3% crude fat, 4% crude fibre, and 28% crude protein was used for larval feeding. The pupae collected daily from the larval container were transferred to plastic cups (350 mL capacity) filled with distilled water (200 mL). They were then placed in a separate Plexiglass cage (30 × 30 × 30 cm), with 3 meshes (one on the upper side and one on each lateral side) as well as an opening hole (18 cm diameter) covered with a muslin cloth fastened by a rubber band. Cotton soaked with a 10% sugar solution was kept in the cages as a food for adults. Ae. aegypti were used to mate after 3–4 days of emergence, and therefore the adult females were fed on the blood of constrained pigeons. The plastic cups (350 mL capacity), lined with 10 cm long wax paper and filled with 120 mL of water, were placed in the adult cage of blood-fed female mosquitoes for oviposition. Egg laying was observed after 3–5 days of mating. The eggs laid by the female mosquitoes were either placed in a larval container filled with water for hatching or stored in a dry place for whenever eggs may be needed for use [32]. Only mated females and larvae of Ae. aegypti were used in the repellent and larvicidal bioassays, respectively. Rearing as well as experiments were performed in a climatic chamber where the relative humidity was 70 ± 10%, the temperature was 28 ± 2 °C, and a photoperiod of 14:10 h light: dark was maintained.

2.4. Mosquito Repellency Bioassay

The repellency of extracted essential oils was investigated by using the human bait method against female Ae. aegypti before the scotophase period. The essential oils solutions at concentrations of 1, 5, and 10% were prepared in ethanol to evaluate their repellency against adult female mosquitoes. Thirty mated and blood-starved four-to-five day-old female mosquitoes were separated in an adult cage (30 × 30 × 30 cm) 24 h before the repellency experiment. Before the start of the bioassay, the hands of the subject were washed with scent-free soap and then dried. Afterwards, gloves were worn on the hands to cover the entire hands, except for a circular area of 30 cm2 on the dorsal side of the hands. A 100 μL aliquot of solvent or solution of the test substance was applied on the exposed area of the hand in each replication of treatments, giving doses of 33.3 µg/cm2, 166.5 µg/cm2, and 330 µg/cm2 when 1%, 5%, and 10% concentrations of EO were used. After 3 min drying at room temperature, the solvent or substance-treated hands were exposed to female Ae. aegypti in the experimental units for five min. The number of female Ae. aegypti landings on the negative control and test-treated exposed area of hands were counted. The human subjects (volunteers) were informed about the test procedure and consent was obtained before conducting repellency bioassays, moreover, permission regarding human subject use was also obtained from the Ethical and Biosafety Committee of Bahauddin Zakariya University. The percentage repellency was calculated by adopting the formula reported by Azeem et al. [29]: percentage repellency = [(Mc − Mt)/Mc] × 100, where Mc is the number of mosquito landings on the negative control (solvent) treated hand and Mt is the number of mosquito landings on the test substance treated hand. The essential oils that showed more than 60% repellency against Ae. aegypti at each tested dose and were further investigated to evaluate the time span repellency (repellent longevity). The time span bioassay was carried out in the same way as the repellency bioassay described above, except this time using the same treated hand after each 15 min period and counting females landing for 5 min until the number of mosquito landings on the control and treated hands became equal. All the repellency bioassays were repeated five times, randomly, to minimize the error in the experiment.

2.5. Larvicidal Activity Bioassay

The larvicidal activity of selected essential oils was tested against the second-instar larvae of Ae. aegypti by following the protocol explained by Ali et al. [33], with some modifications. Briefly, five second-instar larvae of Ae. aegypti were added to each portion of the ice tray (50 mL capacity), which had 20 mL water. The larvicidal activity of the essential oils was evaluated at different concentrations where it remained effective. Different dilutions of essential oils were prepared in DMSO, and 50 µL essential oil solution or DMSO was added to each well. Thus, the final concentration of essential oil in wells was 6.25 mg/L to 1600 mg/L (6.25, 12.5, 25, 50, 100, 200, 400, 800, 1600 mg/L) with twofold dilution at each step. DMSO was used as the negative control and its concentration in test media never exceed 0.25%. The larvae were exposed to essential oils or the negative control for 24 and 48 h to evaluate susceptibility. A fish diet was also provided to larvae during the exposure period. After the exposure period, larvae mortality was checked by using a camel hairbrush, and the larvae that did not show any movement were considered dead. At least seven replicates of each concentration of different essential oils and control were employed.

2.6. Chemical Analysis of the Essential Oils

Essential oils that showed good repellency against Ae. aegypti were investigated further, using a Hewlett Packard gas chromatography-mass spectrometry (GC–MS) system (Agilent Technologies Inc., Santa Clara, CA, USA), to detect the main components of the essential oils. The 6890N GC was equipped with a 30 m long capillary column with 0.25 mm internal diameter and 0.25 μm stationary phase film thickness. The stationary phase of the GC column was 95% dimethylpolysiloxane and 5% diphenyl (DB-5, Agilent Technologies Inc., Santa Clara, CA, USA). The injector of GC was constantly operated at a temperature of 235 °C. The temperature of the GC oven was set as follows: initially, it was kept constant at 40 °C for 2 min, then raised to 240 °C at a constant rate of 4 °C/min and finally was programmed isothermally at 240 °C for 8 min. Helium (gas) was used as a mobile phase at a constant flow of 1 mL/min. An aliquot of 1 µL dilute solution of essential oil was injected into GC in the splitless mode for 30 s. The mass spectrometer parameters were programmed as follows: electron energy for ionization was maintained at 70 eV, ion source temperature was set at 180 °C, and the range of mass spectra scan was set at 30–400 amu. To calculate the composition (%) of compounds in essential oils, a total ion chromatogram was used. Separated compounds were initially identified through the comparison of mass spectra with the NIST-2008 MS library. In addition, the retention indices of separated compounds were compared to published data and the NIST online library. To calculate retention indices of separated compounds, the standard mixture of n-alkanes (C9–C24) was analyzed using the same GC-MS parameters as were used for essential oils. A final verification of the compounds was carried out by injecting the solution of pure available standard compounds at the same conditions used for essential oils analysis. The standard compounds were purchased from Sigma-Aldrich (St. Louis, MI, USA) or Alfa Aesar (Haverhill, MA, USA) chemical suppliers, or otherwise purified in a laboratory at the same parameters used for essential oils analysis.

2.7. Statistical Analysis

General Linear Model (GLM) was used to evaluate the EO type and dose effect on the repellency of mosquitoes in repellency bioassay as well as EO type and time effect on the repellency in time span experiments. In all models, experimental replication was treated as a random variable. If a significant effect was determined, pairwise comparisons of group means by Tukey’s post hoc test at the significance threshold (alpha = 0.05) were used. The statistical analysis was performed by Statistica software version 14.0.1.25 (TIBCO Software Inc, Palo Alto, CA, USA). For larvae mortality data, the Abbott formula [34] was used to calculate corrected mortality. The different lethal concentrations LC50 and LC90 were calculated by using probit analysis through the Polo-Plus software. The LC50 values of the two bioassays were considered significantly different when their fiducial limits did not overlap [35].

3. Results

3.1. Yield of Essential Oils

The Z. armatum leaves were the richest in essential oil and yielded 0.76%, whereas the least amount of essential oil was obtained from S. imbricata and A. altissima, which produced yields of 0.01% and 0.04%, respectively (Table 1).

3.2. Repellency of Essential Oils

A statistical data evaluation by GLM revealed that the EO type (df = 6, F = 1178, p < 0.001) and dose (df = 2, F = 5423, p < 0.001) significantly affected the repellency of mosquitoes. Pairwise comparisons of group means by Tukey’s post hoc test at the significance threshold (alpha = 0.05) revealed that the essential oil of M. longifolia showed high repellent activities, comparable to those of DEET, at the lowest dose of 33.3 µg/cm2 (Figure 1). EO of S. imbricate had a good repellent effect as well, while essential oils of E. bonariensis, E. canadensis, and A. altissima demonstrated from 30% to 40% of DEET efficiency. The essential oil of Z. armatum showed the lowest repellency compared to all tested essential oils. At the medium dose of 166.5 µg/cm2, the essential oils of A. altissima and Z. armatum were significantly weaker repellents compared to the rest of the samples, whose activities did not differ significantly from each other. The repellent activity of six essential oils did not differ significantly from DEET tested directly after application at a dose of 330 µg/cm2 concentration (Figure 1).

3.2.1. Time Span Repellency at a Dose of 33.3 µg/cm2

The GLM model showed significant effects of EO type (df = 2, F = 2970, p < 0.001) and time (df = 2, F = 4239, p < 0.001) on the repellency effect. EO of M. longifolia and S. imbricata showed repellency comparable to DEET immediately after application. However, their repellency decreased drastically after 15 and 30 min of application (Figure 2). S. imbricata exhibited 63% repellency after 15 min, which was significantly higher than the repellency of M. longifolia. However, after 30 min, both plants’ essential oils exhibited similar activity (Figure 2).

3.2.2. Time Span Repellency at a Dose of 166.5 µg/cm2

GLM analyses revealed significant effects of EO type (df = 4, F = 8625, p < 0.001) and time (df = 4, F = 8559, p < 0.001) on the repellency effect. Four out of six plants’ essential oils exhibited 100% repellency at a dose of 166.5 µg/cm2 when tested immediately after application. However, their repellencies decreased when tested after 15 or 30 min. A. altissima and Z. armatum exhibited significantly lower repellency compared to all other essential oils or the positive control (Figure 3). The essential oil of M. longifolia proved best in repellency at a dose of 166.5 µg/cm2 and showed 33% repellency after 45 min of treatment, which was significantly higher than that of all other essential oils, but significantly lower than that of DEET (Figure 3).

3.2.3. Time Span Repellency at a Dose of 330 µg/cm2

GLM analyses showed significant effects of EO type (df = 6, F = 2803, p < 0.001) and time (df = 5, F = 11813, p < 0.001) on the repellency effect. All the tested plants showed 100% repellency towards female Ae. aegypti when tested immediately after application, except for A. altissima essential oil, which showed 96.5% repellency (Figure 4). Furthermore, DEET provided complete protection for 45 min, while E. bonariensis, E. canadensis, and S. imbricata showed complete repellency until 30 min, against Ae. aegypti. However, A. altissima showed repellency for up to only 30 min (Figure 4). At this dose, the most active plant essential oils were M. longifolia, S. imbricata, E. bonariensis, and E. canadensis, which exhibited 70% or higher repellence for more than 45 min. After 75 min post-treatment, the repellency of DEET declined to 79%, M. longifolia, S. imbricata, E. bonariensis, and E. canadensis essential oils showed 7–22% repellency, whereas M. longifolia exhibited significantly higher repellence (p < 0.05) compared to all essential oils (Figure 4).

3.3. Larvicidal Activity of Essential Oils

All the tested essential oils showed larvicidal effects against the second-instar larvae of Ae. aegypti. There was no statistically significant difference among toxicity of E. canadensis, Z. armatum, M. longifolia, and E. bonariensis but their toxicities were significantly different from that of S. imbricata and A. altissima based on non-overlapping of fiducial limits after 24 and 48 h of post-treatment (Table 2). Furthermore, there was also a significant difference between the toxicity of S. imbricata and A. altissima based on non-overlapping of the fiducial limits after 24 and 48 h of post-treatment. The LC50 value of E. bonariensis was 28.48 mg/L after 24 h of larvae exposure which decreased to 26.03 mg/L after 48 h of post-treatment (Table 2). The tested larvae showed the least susceptibility, statistically, towards the exposure of A. altissima as compared to all the tested essential oils (Table 2).

3.4. Composition of Essential Oils

Piperitone oxide (45.5%), piperitenone oxide (30.1%), and limonene (4.6%) were the most abundant compounds in the M. longifolia essential oil. The major compounds in S. imbricata essential oil were 20% camphor, 39.9% carvone, and 6.9% piperitone, which constituted about 70% of the oil (Table 3). The E. bonariensis essential oil comprised trans-β-farnesene (10.2%), cis-lachnophyllum ester (24.9%), and matricaria ester (43.1%), whereas the major compounds of E. canadensis were limonene (28.4%), cis-lachnophyllum ester (16.3%), and matricaria ester (31.7%). The most abundant compounds in the essential oil of A. altissima were eugenol (24.4%) methylugenol (16.5%) and capillin (19.3%), comprising 60.2% of the essential oil (Table 3).

4. Discussion

Products derived from plants can be used as repellents against mosquitoes. However, their potential varies, depending upon their chemical compounds [36,37]. In the present study, essential oils of six aromatic plants, including M. longifolia, S. imbricata, E. bonariensis, E. canadensis, A. altissima, and Z. armatum, were assessed for their repellent and larvicidal effects against Ae. aegypti. All the essential oils showed repellency and larvicidal effects against adult females and second-instar larvae of Ae. aegypti, respectively. The essential oils which showed strong repellency at a dose of 33.3 µg/cm2 were further investigated for their longevity at tested at doses of 33.3 µg/cm2, 166.5 µg/cm2, and 330 µg/cm2.
The essential oil of M. longifolia showed the highest repellency at the lowest tested dose; moreover, these samples showed the most prolonged activity in the time span repellency bioassay. A previous study reported the repellent effect of M. longifolia essential oil for 65 min against Culex pipiens at a tested dose of 1 µL/cm2 (approx. 1000 µg/cm2), where the major compounds were 74.9% pulegone, 6.6% menthone, and 7.4% 1-8-cineole [38]. A previous study from Pakistan reported 68% repellent activity of M. longifolia against Sitophilus oryzae [39]. M. longifolia has also proven very effective against Sitophilus zeamais and showed 100% repellency [40]. Motazedian et al. [41] demonstrated that the essential oil of M. longifolia possessed killing and repellent ability against Tetranychus urticae. Koc et al. [42] reported the repellent effect (73.8%) of M. longifolia against Ochlerotatus caspius. The study of Saeidi and Moharramipour [43] also demonstrated the repellence activity of M. longifolia against Tribolium confusum.
In our study, 45.5% piperitone oxide and 30% piperitenone oxide were the major components of the M. longifolia essential oil and possibly contributedtowards the higher repellency of this EO against Ae. aegypti. Furthermore, the lower volatility of these compounds could be the reason behind the long-lasting repellency. Previously, essential oils with trans-piperitone oxide have shown toxic effects against Cx. pipiens [44]. In previous studies, piperitenone oxide has been proven as an excellent repellent against Anopheles stephensi [45] and Ae. albopictus [46]. Though the repellency of piperitone oxide against Ae. albopictus was moderate, its combined effect was significant in the case of essential oil, which contained 23% piperitone oxide and 41% piperitenone oxide [46]. A study from India reported the presence of 32.4% piperitone oxide and 41.5% piperitenone oxide in Plectranthus incanus essential oil that showed excellent repellency against Anopheles stephensi and Culex fatigans [47]. Thus, the synergetic effects of different components of M. longifiolia essential oil make it a potent repellent for Ae. aegypti.
The essential oil of E. bonariensis did not show good activity at the lowest tested dose. However, it showed 100% repellency against the tested population of mosquitoes at higher doses, such as 166.5 µg/cm2 and 333 µg/cm2. Matricaria ester, cis-lachnophyllum ester, and trans-β-farnesene were the most abundant compounds in the essential oil of E. bonariensis. The presence of these major compounds along with others could be the reason for prolonged repellency at the higher concentrations. Previously, matricaria ester has shown lethal effects on Heliothis virescens moths [48]. The presence of matricaria ester might contribute towards the repellency of E. bonariensis against Ae. aegypti.
The essential oil of E. canadensis showed excellent repellency at the tested doses of 166.5 µg/cm2 and 333 µg/cm2. Interestingly, in our previous study, this plant’s essential oil showed about 85% repellence at 33 µg/cm2 [29], whereas in the present study the essential oil of this plant species showed about 42% repellence at a similar dose. The difference in bioactivity could be attributed to the chemistry of the essential oils, as the plant samples from each study were collected from different locations. In the current study, cis-lachnophyllum ester (16.3%), limonene (28.4%), and matricaria ester (31.7%) were the most abundant compounds in the essential oils of E. canadensis, whereas Azeem et al. [29] reported results of 41.3% limonene, 10.3% of each of germacrene D and matricaria ester, and 6.5% cis-lachnophyllum ester. From the comparison of both studies, it could be concluded that plants growing on different soil types could have different chemistries and hence, varied bioactivity. The essential oil of E. canadensis also showed strong larvicidal potential against Ae. aegypti having LC50 of 35.75 mg/L. Another study from Vietnam described that E. canadensis essential oil possessed strong insecticidal activity against three different species of mosquitoes including Ae. aegypti (LC50 9.80 mg/L) and Ae. albopictus (LC50 = 18.0 mg/L), indicating the toxic effect of E. canadensis [49]. The difference in LC50 values against Ae. aegypti in the previous and current studies might be due to a difference in the chemical composition of E. canadensis.
The essential oil of Z. armatum showed low-to-moderate repellency against adult Ae. aegypti. Previously, essential oil from Z. armatum leaves containing α-pinene and linalool as major compounds depicted strong repellency against Plodia interpunctella [50]. Additionally, Z. armatum EO with a binary mixture of some other essential oils also showed good repellency against stable fly, Stomoxys calcitrans. Furthermore, major components of Z. armatum EO, including cumin aldehyde, cuminyl alcohol, limonene, and methyl cinnamate showed 82%, 74%, 74%, and 64% repellency for 30 min, respectively, against stable fly [51]. In another study, Z. armatum EO consisting of sylvestrene, monomethyl cinnamate, 2-tridecanone, E-caryophyllene, vinyl decanoate, phytol, caryophyllene oxide has shown strong toxic effects against mosquitoes [52].
Essential oils of S. imbricata showed good-to-excellent repellency against Ae. aegypti at each tested concentration. Carvone was the most abundant compound (39.9%) of S. imbricata. Previously, carvone has shown repellence activity against Hylobius abiet is [53] and Arion lusitanicus [54]. Camphor was the second most abundant constituent (20%) of S. imbricata EO, which has previously shown repellency activity, ranging from 80–100% against beetles Sitophilus granarius, S. zeamais, Tribolium castaneum, and Prostephanus truncates [55,56]. The presence of these compounds, along with other compounds, might contribute towards the repellence activity of S. imbricata against Ae. aegypti.
A. altissima showed quite good repellency against Ae. aegypti at higher tested doses, albeit for a shorter period. A previous study from China has also demonstrated the repellent effects of A. altissima against four stored grain pests: Tribolium castaneum, Oryzaephilus surinamensis, Sitophilus oryzae, and Liposcelis paeta [57]. A. altissima showed insecticidal properties against Sitophilus zeamaise [58]. The high volatility and absence of pungent smell in the components of A. altissima might contribute towards repellency for short period against Ae. aegypti. Furthermore, in the present study eugenole (24.4%), capillin (19.3%), and methyleugenole (16.5%) were the major constituents of A. altissima, while in a previous study the main constituents of A. altissima were apocarotenoids (17.2%), oxygenated sesquiterpenes (42.1%) caryophyllene oxide (22.7%) [59]. In another study, the main compounds of A. altissima were α-curcumene, α-gurjunene, γ-cadinene, α-humulene β-caryophyllene, caryophyllene oxide, and germacrene D [60]. The change in a major chemical compound of A. altissima in the present study and previous studies might be due to a change in the location of plants of A. altissima.
In the larvicidal bioassays, the LC50 results depicted the second-instar larvae of Ae. aegypti to be more sensitive to the essential oils of E. bonariensis, M. longifolia, E. canadensis, and Z. armatum, as compared to those of S. imbricata and A. altissima. The LC50 value for E. bonariensis was 28.28 mg/L and 26.03 mg/L after 24 h and 48 h exposure, respectively. The presence of major compounds, such as matricaria ester and cis-lachnophyllum ester with high toxicity, might be contribute to the highest larvicidal activity, but the effects of other major and minor compounds cannot be ruled out. In a previous study from Vietnam, the Conyza (Syn: Erigeron) bonariensis essential oil exhibited LC50 values of 69.71 mg/L and 63.85 mg/L after 24 h and 48 h exposure, respectively [49], results which differ from the data presented here. The reason for this clear difference could be due to the difference in the chemical composition reported in the two different studies.
The LC50 value of E. canadensis was 35.7 mg/L after 48 h, which demonstrated good larvicidal potential against Ae. aegypti. Both E. bonariensis and E. canadensis consisted of a similar ratio of major compounds, for example, matricaria ester and cis-lachnophyllum ester. However, there was the one exception of limonene that was present in abundance only in E. canadensis. The slight difference in their bioactivity could be attributed to the difference in this chemical composition. Hoi et al. [49] reported that the LC50 of E. canadensis essential oil and pure limonene against Ae. aegypti was 6.09 mg/L and 17.43 mg/L, respectively. The larvicidal activity reported by Hoi et al. [49] is higher than that we found in the current study. The difference in bioactivity could be explained based on differences in the chemistry of the essential oils as well as differences in the mosquito populations. Another previous study demonstrated that E. canadensis essential oil exhibited quite good LD50 of 14.42 mg/10 g rice against adult T. castaneum [28]. The relative proportions of limonene, determined in the studies carried out by Azeem et al. [28] and Hoi et al. [49], were similar.
The LC50 values for S. imbricata and A. altissima were 124.2 and 333.6 mg/L, respectively. In a previous study, the essential oil of A. altissima proved toxic against aphids, having an LC50 of 340.06 µg/cm [61]. However, it only showed good toxic effects against C. quinquefasciatus, and Ae. aegypti at the higher concentrations of extracts, like at 75 and 100% [62]. In our study, it showed rather good toxicity towards mosquitoes, as compared to the results of Wallace et al. [62]. This might be due to a change in the chemical composition of A. altissima.
The essential oil of M. longifolia showed strong larvicidal activity (LC50 39.29 mg/L) against second-instar larvae, in addition to strong deterrence activity against adult female Ae. aegypti. The compounds in M. longifolia might be toxic, which might contribute to the larvicidal activity of M. longifolia. In a previous study, the essential oil of M. longifoliam having pipertenone (43.9%) as a major compound, showed insecticidal activity against T. castaneum (flour beetle) and Callosobruchus maculatus with LC50 of 13.05 µL/L [63]. In another study, M. longifolia having trans-piperitone epoxide and piperitenone oxide as major compounds provided a toxic effect against the larvae of Cx. pipiens [44].
The essential oil of Z. armatum showed strong larvicidal activity against Ae. Aegypti, having LC50 of 35.92 mg/L. In the previous study, Z. armatum (monoterpenes as major constituents) revealed insecticidal activity against three mosquito species, including Ae. aegypti (LC50 54 mg/L), An. stephensi (LC50 58 mg/L), and Cx. quinquefasciatus (LC50 49 mg/L) [64]. Previously, Z. armatum (2-undecanone as a major compound) has shown larvicidal activity against An. anthropophagus (LC50 36 mg/L), An. sinensis (LC50 38.56) [62], T. castaneum with (LC50—25.64 mg/L) [65], and Lasioderma serricorn (LC50—13.3 mg/L) [66], showing toxic effects of Z. armatum similar to the toxic effects showed against Ae. aegypti in the present study. The essential oil of S. imbricata showed good larvicidal activity against Ae. Aegypti, having a LC50 value of 124.2 mg/L, and previously also proved toxic against aphid with LC50 340 µg/cm2 [62], and Cx. pipiens with LC50 = 79.1 μg/mL [67]. The change in the toxic effects of S. imbricata against Ae. aegypti and Cx. pipiens might be due to a difference in the chemical composition in the S. imbricata or due to a difference in the tested species of the mosquito.

5. Conclusions

The essential oils extracted from M. longifolia, Z. armatum, E. bonariensis, and C. canadensis have the potential to manage Ae. aegypti at the larval stage. M. longifolia, E. canadensis, E. bonariensis, and S. imbricata essential oils exhibited prolonged mosquito-repellent activity against adult female Ae. aegypti. These essential oils could be used to develop cost-effective and efficient mosquito-repellent formulations for personal protection, without harming humans and the environment.

Author Contributions

Conceptualization, M.A. and M.B.; conducted experiments and collected data M.A., M.G.A., R.M., A.H. and A.N.; data analysis M.A. and R.M.; visualization, M.A. and M.G.A.; writing—original draft preparation, M.A. and R.M.; writing—review and editing al authors; project administration, M.A. and M.B.; funding acquisition, M.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by International Foundation for Science (IFS), Sweden, grant number I-1-F-6041-1 to MA and by the Lithuanian state grant through Nature Research Centre, program 2 Climate and Ecosystems, Vilnius, Lithuania available to RM.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the ethics committee of Bahauddin Zakariya University, Multan.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

Data presented in this study are available on request from the corresponding authors.

Acknowledgments

We thank Fawad Ali, Muhammad Abubakar, Muhammad Umar Bashir, Mahar Muhammad Imran Sharif, and Muhammad Amjad for their assistance during the study. We thank William Walker for English language editing.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Dehghani, R.; Mousavi, G.A.; Ghasemi, B.; Ghasemi, M.; Saheb, M.; Mohamadi, R. A survey on residential areas infestation to house pests (Arthropods) in Kashan. Sci. Inf. Database 2013, 15, 36–39. [Google Scholar]
  2. WHO. Dengue and severe dengue. Available online: https://www.who.int/news-room/fact-sheets/detail/dengue-and-severe-dengue. (accessed on 13 November 2020).
  3. Silva, N.M.; Santos, N.C.; Martins, I.C. Dengue and Zika viruses: Epidemiological history, potential therapies, and promising vaccines. Trop Med. Infect. Dis. 2020, 5, 150. [Google Scholar] [CrossRef]
  4. Stanaway, J.D.; Shepard, D.S.; Undurraga, E.A.; Halasa, Y.A.; Coffeng, L.E.; Brady, O.J.; Hay, S.I.; Bedi, N.; Bensenor, I.M.; Castañeda-Orjuela, C.A. The global burden of dengue: An analysis from the global burden of disease study 2013. Lancet Infect. Dis. 2016, 16, 712–723. [Google Scholar] [CrossRef] [Green Version]
  5. Khan, J.; Anwar, F.; Shah, S.S.; Qamar, Z.; Ullah, W.; Ali, A.; Hussain, M.; Ali, I.; Ali, F.; Ullah, F. Dengue virus epidemics: A recent report of 2018 from district Swat, Khyber-Pakhtunkhwa Pakistan. Int. J. Mosquito Res. 2021, 8, 105–108. [Google Scholar]
  6. Imran, M.; Hamid, Y.; Mazher, A.; Ahmad, S.R. Geo-spatially modelling dengue epidemics in urban cities: A case study of Lahore, Pakistan. Geocarto Int. 2021, 36, 197–211. [Google Scholar] [CrossRef]
  7. Wharton-Smith, A.; Green, J.; Loh, E.C.; Gorrie, A.; Omar, S.F.S.; Bacchus, L.; Lum, L.C.S. Using clinical practice guidelines to manage dengue: A qualitative study in a Malaysian hospital. BMC Infect. Dis. 2019, 19, 45. [Google Scholar] [CrossRef] [Green Version]
  8. Al Zahrani, M.R.; Gharsan, F.N.; Al-Ghamd, K.M.; Mahyoub, J.A.; Alghamdi, T.S. Toxicity of two groups of pesticides against the mosquito Aedes aegypti. GSC GSC Biol. Pharm Sci. 2020, 13, 148–155. [Google Scholar] [CrossRef]
  9. Junkum, A.; Intirach, J.; Chansang, A.; Champakaew, D.; Chaithong, U.; Jitpakdi, A.; Riyong, D.; Somboon, P.; Pitasawat, B. Enhancement of temephos and deltamethrin toxicity by Petroselinum crispum oil and its main constituents against Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 2021, 58, 1298–1315. [Google Scholar] [CrossRef]
  10. Devine, G.J.; Vazquez-Prokopec, G.M.; Bibiano-Marín, W.; Pavia-Ruz, N.; Che-Mendoza, A.; Medina-Barreiro, A.; Villegas, J.; Gonzalez-Olvera, G.; Dunbar, M.W.; Ong, O. The entomological impact of passive metofluthrin emanators against indoor Aedes aegypti: A randomized field trial. PLoS Negl. Trop Dis. 2021, 15, e0009036. [Google Scholar] [CrossRef]
  11. Samal, R.R.; Kumar, S. Cuticular thickening associated with insecticide resistance in dengue vector, Aedes aegypti L. Int. J. Trop. Insect Sci. 2021, 41, 809–820. [Google Scholar] [CrossRef]
  12. Dos Santos, C.R.; de Melo Rodovalho, C.; Jablonka, W.; Martins, A.J.; Lima, J.B.P.; dos Santos Dias, L.; da Silva Neto, M.A.C.; Atella, G.C. Insecticide resistance, fitness and susceptibility to Zika infection of an interbred Aedes aegypti population from Rio de Janeiro, Brazil. Parasit Vectors 2020, 13, 293. [Google Scholar] [CrossRef] [PubMed]
  13. Dos Santos, E.; Cohren, S.; Costa, R. Epidemiological profile of diseases caused by Aedes aegypti in sanitary districts of São Luis, Brazil. Eur. J. Public Health 2020, 30, ckaa166-141. [Google Scholar] [CrossRef]
  14. Fernando, H.S.D.; Saavedra-Rodriguez, K.; Perera, R.; Black, W.C.; De Silva, B.N.K. Resistance to commonly used insecticides and underlying mechanisms of resistance in Aedes aegypti (L.) from Sri Lanka. Parasit Vectors 2020, 13, 407. [Google Scholar] [CrossRef] [PubMed]
  15. Rahman, R.U.; Cosme, L.V.; Costa, M.M.; Carrara, L.; Lima, J.B.P.; Martins, A.J.J.P.n.t.d. Insecticide resistance and genetic structure of Aedes aegypti populations from Rio de Janeiro State, Brazil. PLoS Neglec. Tropic. Dis. 2021, 15, e0008492. [Google Scholar] [CrossRef] [PubMed]
  16. Zhao, Q.; De Laender, F.; Van den Brink, P.J. Community composition modifies direct and indirect effects of pesticides in freshwater food webs. Sci. Total Environ. 2020, 739, 139531. [Google Scholar] [CrossRef]
  17. Ali, S.; Ullah, M.I.; Sajjad, A.; Shakeel, Q.; Hussain, A. Environmental and health effects of pesticide residues. In Sustainable Agriculture; Springer: Berlin/Heidelberg, Germany, 2021; pp. 311–336. [Google Scholar]
  18. Uwaifo, F.; John-Ohimai, F. Dangers of organophosphate pesticide exposure to human health. Matrix Sci. Med. 2020, 4, 27. [Google Scholar] [CrossRef]
  19. Pratiwi, M.A.M. The repellent activity test of rosemary leaf (Rosmarinus officinalis L) essential oil gel preparations influence on Aedes aegypti mosquito. In Proceedings of Journal of Physics: Conference Series; IOP Publishing: Bristol, UK, 2021; p. 012016. [Google Scholar]
  20. Afify, A.; Potter, C. Insect repellents mediate species-specific olfactory behaviours in mosquitoes. Malar. J. 2020, 19, 127. [Google Scholar] [CrossRef] [Green Version]
  21. Qiu, H.; Jun, H.W.; Dzimianski, M.; McCall, J. Reduced transdermal absorption of N, N-diethyl-m-toluamide from a new topical insect repellent formulation. Pharm. Dev. Technol. 1997, 2, 33–42. [Google Scholar] [CrossRef]
  22. Calafat, A.M.; Baker, S.E.; Wong, L.-Y.; Bishop, A.M.; Morales-A, P.; Valentin-Blasini, L. Novel exposure biomarkers of N, N-diethyl-m-toluamide (DEET): Data from the 2007–2010 National Health and Nutrition Examination Survey. Environ. Int. 2016, 92, 398–404. [Google Scholar] [CrossRef]
  23. Oftadeh, M.; Sendi, J.J.; Ebadollahi, A.; Setzer, W.N.; Krutmuang, P. Mulberry protection through flowering-stage essential oil of Artemisia annua against the lesser mulberry pyralid, Glyphodes pyloalis Walker. Food Addit. Contam. 2021, 10, 210. [Google Scholar] [CrossRef]
  24. Wong, C.; Crystal, K.; Coats, J. Three molecules found in rosemary or nutmeg essential oils repel ticks (Dermacentor variabilis) more effectively than DEET in a no-human assay. Pest. Manage. Sci. 2020, 77, 1348–1354. [Google Scholar] [CrossRef] [PubMed]
  25. Rizvi, S.A.H.; Ling, S.; Zeng, X. Seriphidium brevifolium essential oil: A novel alternative to synthetic insecticides against the dengue vector Aedes albopictus. Environ. Sci Pollut Res. Int. 2020, 27, 31863–31871. [Google Scholar] [CrossRef] [PubMed]
  26. Stappen, I.; Wanner, J.; Tabanca, N.; Bernier, U.R.; Kendra, P.E. Blue Tansy Essential Oil: Chemical Composition, Repellent Activity Against Aedes aegypti and Attractant Activity for Ceratitis capitata. Nat. Prod.Commun. 2021, 16, 1–8. [Google Scholar] [CrossRef]
  27. Tripathi, A.K.; Upadhyay, S.; Bhuiyan, M.; Bhattacharya. A review on prospects of essential oils as biopesticide in insect-pest management. J. Pharm. Phytother. 2009, 1, 52–63. [Google Scholar]
  28. Azeem, M.; Zaman, T.; Abbasi, A.M.; Abid, M.; Mozūratis, R.; Alwahibi, M.S.; Elshikh, M.S. Pesticidal potential of some wild plant essential oils against grain pests Tribolium castaneum (Herbst, 1797) and Aspergillus flavus (Link, 1809). Arab J. Chem. 2022, 15, 103482. [Google Scholar] [CrossRef]
  29. Azeem, M.; Zaman, T.; Tahir, M.; Haris, A.; Iqbal, Z.; Binyameen, M.; Nazir, A.; Shad, S.A.; Majeed, S.; Mozūraitis, R. Chemical composition and repellent activity of native plants essential oils against dengue mosquito, Aedes aegypti. Ind Crops Prod. 2019, 140, 111609. [Google Scholar] [CrossRef]
  30. Johnson, H. Notes on the continuous rearing of Aedes aegypti in the laboratory. Public Health Rep. 1937, 52, 1177–1179. [Google Scholar] [CrossRef]
  31. Zheng, M.-L.; Zhang, D.-J.; Damiens, D.D.; Lees, R.S.; Gilles, J.R. Standard operating procedures for standardized mass rearing of the dengue and chikungunya vectors Aedes aegypti and Aedes albopictus (Diptera: Culicidae)-II-Egg storage and hatching. Parasit Vectors. 2015, 8, 1–7. [Google Scholar]
  32. Morlan, H.B.; Hayes, R.O.; Schoof, H.F. Methods for mass rearing of Aedes aegypti (L.). Public Health Rep. 1963, 78, 711. [Google Scholar] [CrossRef]
  33. Ali, A.; Wang, Y.-H.; Khan, I.A. Larvicidal and biting deterrent activity of essential oils of Curcuma longa, ar-turmerone, and curcuminoids against Aedes aegypti and Anopheles quadrimaculatus (Culicidae: Diptera). J. Med. Entomol. 2015, 52, 979–986. [Google Scholar] [CrossRef]
  34. Abbott, W.S. A method of computing the effectiveness of an insecticide. J. Med. Entomol. 1925, 18, 265–267. [Google Scholar] [CrossRef]
  35. Litchfield, J.j.; Wilcoxon, F. A simplified method of evaluating dose-effect experiments. J. Pharmacol. Exp. Ther. 1949, 96, 99–113. [Google Scholar]
  36. Hassan, E.M.; El Gendy, A.E.-N.G.; Abd-ElGawad, A.M.; Elshamy, A.I.; Farag, M.A.; Alamery, S.F.; Omer, E.A. Comparative chemical profiles of the essential oils from different varieties of Psidium guajava L. Molecules 2021, 26, 119. [Google Scholar] [CrossRef]
  37. Nezhadasad Aghbash, B.; Dehghan, G.; Movafeghi, A.; Talebpour, A.H.; Pouresmaeil, M.; Maggi, F.; Sabzi Nojadeh, M. Chemical compositions and biological activity of essential oils from four populations of Satureja macrantha CA Mey. J. Essent. Oil. Res. 2021, 33, 1–10. [Google Scholar] [CrossRef]
  38. Al-Sarar, A. Chemical Composition, Adulticidal and Repellent Activity of Essential Oils From Mentha longifolia L. and Lavandula dentata L. against Culex pipiens L. Plant. Prot. Pathol. 2014, 5, 817–826. [Google Scholar] [CrossRef]
  39. Saljoqi, A.U.R.; Afridi, M.K.; Khan, S.A. Effects of six plant extracts on rice weevil Sitophilus oryzae L. in the stored wheat grains. J. Agric. Biol Sci. 2006, 1, 1–5. [Google Scholar]
  40. Odeyemi, O.; Masika, P.; Afolayan, A. Insecticidal activities of essential oil from the leaves of Mentha longifolia L. subsp. capensis against Sitophilus zeamais (Motschulsky)(Coleoptera: Curculionidae). Afr. Entomol. 2008, 16, 220–225. [Google Scholar] [CrossRef]
  41. Motazedian, N.; Ravan, S.; Bandani, A. Toxicity and repellency effects of three essential oils against T etranychus urticae Koch (Acari: Tetranychidae). J. Agric. Sci Technol. Health Care. 2012, 14, 275–284. [Google Scholar]
  42. Koc, S.; Oz, E.; Cetin, H. Repellent activities of some Labiatae plant essential oils against the saltmarsh mosquito Ochlerotatus caspius (Pallas, 1771)(Diptera: Culicidae). Parasitol Res. 2012, 110, 2205–2209. [Google Scholar] [CrossRef]
  43. Saeidi, M.; Moharramipour, S. Insecticidal and repellent activities of Artemisia khorassanica, Rosmarinus officinalis and Mentha longifolia essential oils on Tribolium confusum. J. Crop. Prot. 2013, 2, 23–31. [Google Scholar]
  44. Koliopoulos, G.; Pitarokili, D.; Kioulos, E.; Michaelakis, A.; Tzakou, O. Chemical composition and larvicidal evaluation of Mentha, Salvia, and Melissa essential oils against the West Nile virus mosquito Culex pipiens. Parasitol. Res. 2010, 107, 327–335. [Google Scholar] [CrossRef] [PubMed]
  45. Tripathi, A.K.; Prajapati, V.; Ahmad, A.; Aggarwal, K.K.; Khanuja, S.P. Piperitenone oxide as toxic, repellent, and reproduction retardant toward malarial vector Anopheles stephensi (Diptera: Anophelinae). J. Med. Entomol. 2004, 41, 691–698. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Giatropoulos, A.; Kimbaris, A.; Michaelakis, A.; Papachristos, D.P.; Polissiou, M.G.; Emmanouel, N. Chemical composition and assessment of larvicidal and repellent capacity of 14 Lamiaceae essential oils against Aedes albopictus. Parasitol. Res. 2018, 117, 1953–1964. [Google Scholar] [CrossRef] [PubMed]
  47. Pal, M.; Kumar, A.; Tewari, K.S. Chemical composition and mosquito repellent activity of the essential oil of Plectranthus incanus link. Facta Univ. Ser. Phys. Chem. Technol. 2011, 9, 57–64. [Google Scholar] [CrossRef]
  48. Binder, R.G.; Chan, B.G.; Elliger, C.A. Antibiotic Effects of C10–C12 Fatty Acid Esters on Pink Bollworm, Bollworm and Tobacco Budworm. Agric. Biol. Chem. 1979, 43, 2467–2471. [Google Scholar] [CrossRef] [Green Version]
  49. Hoi, T.M.; Huong, L.T.; Chinh, H.V.; Hau, D.V.; Satyal, P.; Tai, T.A.; Dai, D.N.; Hung, N.H.; Hien, V.T.; Setzer, W.N. Essential oil compositions of three invasive Conyza species collected in Vietnam and their larvicidal activities against Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus. Molecules 2020, 25, 4576. [Google Scholar] [CrossRef]
  50. Brari, J.; Kumar, V. Insecticidal efficacy of essential oils from Artemisia maritima L. and Zanthoxylum armatum DC. and their two major constituents against Plodia interpunctella (Hubner). Int. J. Life Sci. Res. 2021, 9, 71–79. [Google Scholar]
  51. Hieu, T.T.; Kim, S.I.; Kwon, H.W.; Ahn, Y.J.J.P.m.s. Enhanced repellency of binary mixtures of Zanthoxylum piperitum pericarp steam distillate or Zanthoxylum armatum seed oil constituents and Calophyllum inophyllum nut oil and their aerosols to Stomoxys calcitrans. Pest. Manage. Sci. 2010, 66, 1191–1198. [Google Scholar] [CrossRef]
  52. Singh, A.; Dhami, A.; Palariya, D.; Prakash, O.; Kumar, R.; Kumar, R.; Pant, A. Methyl nonyl ketone and linalool rich essential oils from three accessions of Zanthoxylum armatum (DC.) and their biological activities. Int. J. Herb. Med. 2019, 7, 20–28. [Google Scholar]
  53. Schlyter, F.; Smitt, O.; Sjödin, K.; Högberg, H.E.; Löfqvist, J. Carvone and less volatile analogues as repellent and deterrent antifeedants against the pine weevil, Hylobius abietis. J. Appl. Entomol. 2004, 128, 610–619. [Google Scholar] [CrossRef]
  54. Frank, T.; Biert, K.; Speiser, B. Feeding deterrent effect of carvone, a compound from caraway seeds, on the slug Arion lusitanicus. Ann. Appl. Biol. 2002, 141, 93–100. [Google Scholar] [CrossRef]
  55. Obeng-Ofori, D.; Reichmuth, C.; Bekele, A.; Hassanali, A. Toxicity and protectant potential of camphor, a major component of essential oil of Ocimum kilimandscharicum, against four stored product beetles. Int. J. Pest. Manag. 1998, 44, 203–209. [Google Scholar] [CrossRef]
  56. Chen, Z.-Y.; Guo, S.-S.; Cao, J.-Q.; Pang, X.; Geng, Z.-F.; Wang, Y.; Zhang, Z.; Du, S.-S. Insecticidal and repellent activity of essential oil from Amomum villosum Lour. and its main compounds against two stored-product insects. Int. J. Food Prop. 2018, 21, 2265–2275. [Google Scholar] [CrossRef] [Green Version]
  57. Lu, J.; Wu, S. Bioactivity of essential oil from Ailanthus altissima bark against 4 major stored-grain insects. Afr. J. Microbiol. Res. 2010, 4, 154–157. [Google Scholar]
  58. Haroon, M.; Maduka, U.; Sujarajini, V. Insecticidal effects of plant extracts of some medicinal plants against Sitophilus zeamaise mostchulsky on stored maize. In Abstracts of the 7th Annual Science Research Sessions (ASRS); Faculty of Applied Science, South Eastern University of Sri Lanka: Oluvil, Sri Lanka, 2018. [Google Scholar]
  59. El Ayeb-Zakhama, A.; Ben Salem, S.; Sakka-Rouis, L.; Flamini, G.; Ben Jannet, H.; Harzallah-Skhiri, F. Chemical composition and phytotoxic effects of essential oils obtained from Ailanthus altissima (Mill.) swingle cultivated in Tunisia. Chem. Biodivers 2014, 11, 1216–1227. [Google Scholar] [CrossRef]
  60. Kozuharova, E.; Benbassat, N.; Berkov, S.; Ionkova, I. Ailanthus altissima and Amorpha fruticosa–invasive arboreal alien plants as cheap sources of valuable essential oils. Pharmacia 2020, 67, 71. [Google Scholar] [CrossRef]
  61. Khani, A.; Ordouni, F.; Sahebzadeh, N.J.E.a.B. Qualitative phytochemical screening and mortality effect of ethanolic extract of Salsola imbricata on Aphis gossypii. Exp. Anim. Biol. 2018, 7, 89–96. [Google Scholar]
  62. Wallace, J.R.; Wylie, C.D.; Wagner, R.L. Plant extract efficacy on mosquito mortality: Preliminary studies on the effect of Ailanthus altissima extract on adult Aedes aegypti and Culex quinquefasciatus. Great Lakes Entomol. 2021, 54, 8. [Google Scholar]
  63. Khani, A.; Asghari, J. Insecticide activity of essential oils of Mentha longifolia, Pulicaria gnaphalodes and Achillea wilhelmsii against two stored product pests, the flour beetle, Tribolium castaneum, and the cowpea weevil, Callosobruchus maculatus. J. Insect Sci. 2012, 12, 73. [Google Scholar] [CrossRef] [Green Version]
  64. Tiwary, M.; Naik, S.; Tewary, D.K.; Mittal, P.; Yadav, S.J.J.o.v.b.d. Chemical composition and larvicidal activities of the essential oil of Zanthoxylum armatum DC (Rutaceae) against three mosquito vectors. J. Vector. Borne Dis. 2007, 44, 198. [Google Scholar]
  65. Zhang, W.; Wang, Y.; Geng, Z.; Guo, S.; Cao, J.; Zhang, Z.; Pang, X.; Chen, Z.; Du, S.; Deng, Z. Antifeedant activities of lignans from stem bark of Zanthoxylum armatum DC. against Tribolium castaneum. Molecules 2018, 23, 617. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Wang, C.-F.; Zhang, W.-J.; You, C.-X.; Guo, S.-S.; Geng, Z.-F.; Fan, L.; Du, S.-S.; Deng, Z.-W.; Wang, Y.-Y. Insecticidal constituents of essential oil derived from Zanthoxylum armatum against two stored-product insects. J. Oleo Sci. 2015, 64, 861–868. [Google Scholar] [CrossRef] [PubMed]
  67. Abutaha, N.; Al-Mekhlafi, F.A.; Al-Keridis, L.A.; Farooq, M.; Nasr, F.A.; Al-Wadaan, M. Larvicidal potency of selected xerophytic plant extracts on Culex pipiens (Diptera: Culicidae). Entomol. Res. 2018, 48, 362–371. [Google Scholar]
Biology 12 00008 g001 550
Figure 1. Repellency exhibited by DEET and essential oils, tested at the doses of 33.3 µg/cm2, 166.5 µg/cm2, and 330 µg/cm2 against Ae. aegypti female. Bars, indicated by different letters, denote significant differences (p < 0.05) among different treatments when tested at the same concentration by ANOVA post hoc Tukey test. Error bars denote the standard error (n = 5).
Figure 1. Repellency exhibited by DEET and essential oils, tested at the doses of 33.3 µg/cm2, 166.5 µg/cm2, and 330 µg/cm2 against Ae. aegypti female. Bars, indicated by different letters, denote significant differences (p < 0.05) among different treatments when tested at the same concentration by ANOVA post hoc Tukey test. Error bars denote the standard error (n = 5).
Biology 12 00008 g001
Biology 12 00008 g002 550
Figure 2. Time-based repellency of DEET and two essential oils tested at a dose of 33.3 µg/cm2 against Ae. aegypti. Bars having different letters depict significant differences (p < 0.05) among the repellency of different tested substances at 0, 15, and 30 min of post-treatment when compared independently by ANOVA post hoc Tukey test. Error bars denote the standard error (n = 5).
Figure 2. Time-based repellency of DEET and two essential oils tested at a dose of 33.3 µg/cm2 against Ae. aegypti. Bars having different letters depict significant differences (p < 0.05) among the repellency of different tested substances at 0, 15, and 30 min of post-treatment when compared independently by ANOVA post hoc Tukey test. Error bars denote the standard error (n = 5).
Biology 12 00008 g002
Biology 12 00008 g003 550
Figure 3. Time-based repellency of DEET and essential oils at a dose of 166.5 µg/cm2 against Ae. aegypti. Bars having different letters depict significant differences (p < 0.05) among the repellency of different tested substances at different periods of post-treatment that were compared for each period independently by ANOVA post hoc Tukey test. Error bars denote the standard error (n = 5).
Figure 3. Time-based repellency of DEET and essential oils at a dose of 166.5 µg/cm2 against Ae. aegypti. Bars having different letters depict significant differences (p < 0.05) among the repellency of different tested substances at different periods of post-treatment that were compared for each period independently by ANOVA post hoc Tukey test. Error bars denote the standard error (n = 5).
Biology 12 00008 g003
Biology 12 00008 g004 550
Figure 4. Time-based repellency of DEET and essential oils at a dose of 330 µg/cm2 against Ae. aegypti. Bars having different letters depict significant differences (p < 0.05) among the repellency of different tested substances at different time periods of post-treatment that were compared for each period independently by ANOVA post hoc Tukey test. Error bars denote the standard error (n = 5).
Figure 4. Time-based repellency of DEET and essential oils at a dose of 330 µg/cm2 against Ae. aegypti. Bars having different letters depict significant differences (p < 0.05) among the repellency of different tested substances at different time periods of post-treatment that were compared for each period independently by ANOVA post hoc Tukey test. Error bars denote the standard error (n = 5).
Biology 12 00008 g004
Table
Table 1. Plant material and yield of essential oils used in the study.
Table 1. Plant material and yield of essential oils used in the study.
Scientific NameFamilyPart UsedCollection CoordinatesElevation (m)Yield
(%)
Mentha longifolia LamiaceaeLeaves, stems34°11′48.9″ N
73°14′51.7″ E		12360.36
Salsola imbricata AmaranthaceaeLeaves, stems30°15′59.6″ N
71°30′40.2″ E		1240.01
Erigeron bonariensis AsteraceaeLeaves, stems30°16′13.5″ N
71°30′44.6″ E		1240.21
Erigeron canadensis AsteraceaeLeaves, stems30°15′52.9″ N
71°30′04.0″ E		11830.21
Ailanthus altissima SimaroubaceaeLeaves, stems30°15′52.9″ N
71°30′04.0″ E		1240.04
Zanthoxylum armatum RutaceaeLeaves34°11′48.4″ N
73°15′43.0″ E		13700.76
Table
Table 2. Toxicity of essential oils tested against second-instar larvae of Aedes aegypti.
Table 2. Toxicity of essential oils tested against second-instar larvae of Aedes aegypti.
Essential OilsExposure TimeLC50 (mg/L)95% CI (mg/L)LC90 (mg/L)95% CI (mg/L)Slope ± SEChi-Square (df)
M. longifolia 24 h46.7 a30.41–73.3995.9a61.87–169.26.04 ± 0.863.28 (5)
S. imbricata 132.3 b83.94–208.4294.0 b187.8–516.757.83 ± 1.100.31 (5)
E. bonariensis 28.5 a18.30–44.3063.3a40.87–110.35.37 ± 0.490.33 (5)
E. canadensis 37.9 a23.92–59.9784.2 a53.53–148.75.83 ± 0.790.34 (5)
A. altissima 356.1 c231.3–551.2791.4 b513.62–13769.42 ± 1.290.99 (5)
Z. armatum 46.5 a29.99–72.95103.3 a66.33–183.036.16 ± 0.884.30 (5)
M. longifolia 48 h39.3 a20.6–71.6120.0 a67–792.64 ± 0.305.94 (5)
S. imbricata 124.2 b106–145223.9 b185–3045.00 ± 0.782.41 (5)
E. bonariensis 26.1 a21–31.6163.6 a49–953.30 ± 0.402.41 (5)
E. canadensis 35.7 a29.9–41.863.9 a52–905.07 ± 0.900.64 (5)
A. altissima 333.6 c161–631909.5 c517–77922.94 ± 0.407.20 (5)
Z. armatum 35.9 a18.6–74.797.6 a59–3212.95 ± 0.3014.0 (5)
LC50 and LC90: lethal concentrations at which a chemical(s) will kill 50% and 90% of tested individuals exposed to it, respectively; CI: confidence interval; SE: standard error, df: degree of freedom; different lower-case letters in the columns depict significant differences (p < 0.05) between the LC50 and LC90 values based on the non-overlapping of the fiducial limits for 24 h and 48 h separately.
Table
Table 3. Composition (expressed as %) of plant essential oils based on total ion chromatogram of GC-MS.
Table 3. Composition (expressed as %) of plant essential oils based on total ion chromatogram of GC-MS.
RICompoundCAS
Number		 M. longifolia S. imbricata E. bonariensis E. canadensis A. altissima
929α-Pinene *80-56-80.41.1
970Sabinene3387-41-50.30.6 1.1
972β-Pinene *127-91-30.5
990β-Myrcene *123-35-32.00.70.10.7tr
1003α-Phellandrene99-83-2 0.2 0.1
10083-Carene13466-78-9 0.3
1026Limonene *138-86-34.62.22.128.40.5
1028Eucalyptol *470-82-61.12.30.5 1.7
1038cis-β-Ocimene *3338-55-40.5
1047trans-β-Ocimene *3779-61-10.1 0.85.0
1056γ-Terpinene99-85-4tr0.2 0.1
1086Terpinolene586-62-90.10.1 0.1
1099Linalool *78-70-60.30.2 0.3
1103Nonanal124-19-6 0.5 0.5
1141Camphor *76-22-20.120.4tr 0.1
1163Borneol *507-70-00.21.4 0.1
11754-Terpineol562-74-3 0.8tr 0.1
1189α-Terpineol98-55-50.10.3tr 0.1
1194cis-Dihydrocarvone3792-53-8 1.1
1237Pulegone *89-82-7 4.1
1242Carvone *99-49-0tr39.90.1 0.5
1252Piperitone89-81-6 6.9 0.1
1260Piperitone oxide57130-28-645.5
1272Isopiperitenone529-01-10.2
1285Bornyl acetate76-49-3 0.2
1290Piperitenone oxide # 2.6
1293Thymol *89-83-80.20.2tr 0.9
12982-Hydroxypiperitone490-03-90.40.2 0.3
13122-Methoxy-4-vinylphenol7786-61-0 2.1 0.2
1337δ-Elemene20307-84-0 0.2
1342α-Guaiene3691-12-1 0.2
1349α-Cubebene17699-14-8 0.10.20.2
1358Eugenol *97-53-0 0.2 29.9
1378Piperitenone oxide *35178-55-330.1 0.3
1389β-Cubebene13744-15-5 0.20.2
1391β-Elemen515-13-90.10.20.20.4
1404Methyleugenol93-15-2 0.6 20.3
1414p-Menthane-1,2,3-triol22555-61-93.6
1418trans-β-Caryophyllene *87-44-51.80.31.90.72.8
1436trans-α-Bergamotene13474-59-4 0.23.6
1452α-Humulene6753-98-6 1.10.30.6
1458trans-β-Farnesene18794-84-8 10.22.5
1476γ-Muurolene30021-74-0 0.20.2
1480Germacrene D23986-74-5 0.34.66.46.5
1485β-Selinene17066-67-03.9 0.2
1496Capilline520-74-1 3.70.623.7
1508trans-α-Farnesene502-61-4 0.90.31.3
1516cis-Lachnophyllum ester505-01-1 0.124.916.3
1523δ-Cadinene483-76-1 0.4
1526Matricaria ester505-02-2 43.131.7
1549Hedycaryol21657-90-9 2.6
1563Nerolidol142-50-7 0.30.3
1576Spathulenol77171-55-2 0.32.0tr0.4
1582Caryophyllene oxide1139-30-6 0.4 0.3
1646α-Eudesmol473-16-5 0.3 1.2
1654Juniper camphor473-04-1 3.5
1715Pentadecanal2765-11-9 0.4 0.2
1817Hexadecanal629-80-1 1.9
Total Identified 98.794.498.298.895.5
RI: retention index of a separated compound, which was calculated relative to the retention time of C9–C26 hydrocarbons using DB-5 gas chromatographic column, and the same parameters were applied for analyses of essential oils. CAS Chemical Abstract Service.* Identification of compounds was verified by comparing mass spectrum and retention index with those recorded from the injection of standard compounds. # CAS number of this Piperitenone oxide was not found. The data shown in table are approximate relative compositions, expressed as %, where tr stands for trace amount < 0.1%.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Abbas, M.G.; Haris, A.; Binyameen, M.; Nazir, A.; Mozūratis, R.; Azeem, M. Chemical Composition, Larvicidal and Repellent Activities of Wild Plant Essential Oils against Aedes aegypti. Biology 2023, 12, 8. https://doi.org/10.3390/biology12010008

AMA Style

Abbas MG, Haris A, Binyameen M, Nazir A, Mozūratis R, Azeem M. Chemical Composition, Larvicidal and Repellent Activities of Wild Plant Essential Oils against Aedes aegypti. Biology. 2023; 12(1):8. https://doi.org/10.3390/biology12010008

Chicago/Turabian Style

Abbas, Muhammad Ghazanfar, Abdullah Haris, Muhammad Binyameen, Abdul Nazir, Raimondas Mozūratis, and Muhammad Azeem. 2023. "Chemical Composition, Larvicidal and Repellent Activities of Wild Plant Essential Oils against Aedes aegypti" Biology 12, no. 1: 8. https://doi.org/10.3390/biology12010008

APA Style

Abbas, M. G., Haris, A., Binyameen, M., Nazir, A., Mozūratis, R., & Azeem, M. (2023). Chemical Composition, Larvicidal and Repellent Activities of Wild Plant Essential Oils against Aedes aegypti. Biology, 12(1), 8. https://doi.org/10.3390/biology12010008

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

Article Metrics

Back to TopTop