Next Article in Journal
Capparis spinosa L. Cenopopulation and Biogeochemistry in South Uzbekistan
Previous Article in Journal
Gene Co-Expression Network Tools and Databases for Crop Improvement
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Chemical Diversity and Anti-Insect Activity Evaluation of Essential Oils Extracted from Five Artemisia Species

1
Beijing Key Laboratory of Traditional Chinese Medicine Protection and Utilization, Faculty of Geographical Science, Beijing Normal University, No.19 Xinjiekouwai Street, Beijing 100875, China
2
Department of Biomedical Science, Beijing City University, No. 269 North 4th Ring Middle Road, Beijing 100083, China
3
Department of Burns and Plastic Surgery, PLA Rocket Force Characteristic Medical Center, Beijing 100088, China
*
Authors to whom correspondence should be addressed.
Plants 2022, 11(13), 1627; https://doi.org/10.3390/plants11131627
Submission received: 18 May 2022 / Revised: 12 June 2022 / Accepted: 15 June 2022 / Published: 21 June 2022
(This article belongs to the Section Phytochemistry)

Abstract

:
As a source of aromatic plants, the genus Artemisia has long been considered to have the potential to develop plant pesticides. In this study, components of essential oils from A. dalai-lamae, A. tangutica, A. sieversiana, A. tanacetifolia and A. ordosica were identified by GC-MS. A total of 56 constituents were analysed, and each species consisted of 9 to 24 constituents. Principle component analysis (PCA) revealed that A. dalai-lamae, A. tangutica and A. tanacetifolia are characterised by monoterpene hydrocarbons and oxygenated monoterpenes. Hierarchical cluster analysis (HCA) showed the most remarkable similarity between A. sieversiana and A. ordosica, but the similarity was still lower than 50%. Contact toxicity and repellency of essential oils were evaluated by bioassays; A. ordosica oil exhibited the most substantial contact toxicity (LD50 = 52.11 μg/cm2) against Liposcelis bostrychophila, while A. tangutica oil showed the most potent contact toxicity (LD50 = 17.42 μg/adult) against Tribolium castaneum. Except for A. dalai-lamae, the other four species showed the same level (p > 0.05) of repellent activity as the positive control against both pests at high concentrations. The results indicated that these five Artemisia species had high chemical diversity and great potential to be developed into more effective and environmentally friendly anti-insect agents.

1. Introduction

Insecticides are an effective method of controlling storage pests, of which synthetic insecticides have been demonstrated to impact environmental protection and health safety negatively [1,2]. This phenomenon promoted the growing exploration of botanical pesticides. Plant secondary metabolites are important sources of botanical insecticides and have proven insecticidal [3,4] and repellent [5,6] effects in practice. Increasing studies have shown that essential oils mainly extracted from aromatic plants have great potential against arthropod species [7]. The genus Artemisia, one of the largest genera of the family Compositae, consists of nearly 500 species worldwide, and about 190 species are found in China. High concentrations and significant intraspecific variations of volatile terpenes in essential oil generated the strong and diverse odour of the Artemisia genus [8]. The compositional diversity of essential oils of several Artemisia species has been reported. A. dracunculus was rich in (Z)-anethole (81.0%) [9], A. scoparia was rich in α-thujone (81.7%) [10], while 67% of camphor was the main component of A. fragans [11].
The positive repellent and insecticidal activities of essential oils derived from Artemisia species have been in the limelight owing to the abundant volatile components [8,12]. Essential oils extracted from three Artemisia species, including A. absinthium, A. spicigera and A. santonicum, were toxic to Sitophilus granaries [13]. Oils from cultivated A. absinthium had better repellent activity against Trypanosoma cruzi and Leishmania infantum than the commercial ones [14]. A. capillaris and A. mongolica essential oils showed significant toxicity against Sitophilus zeamais [15].
Little research was conducted on A. dalai-lamae and A. tangutica, the endemic species in China. Terpenoids, lignans, flavonoids, and various compounds were isolated from A. sieversiana. Some of these components showed several biological activities such as anti-tumour, anti-inflammatory, anti-allergic, anti-hypertensive, and anti-hyperglycemic activities [16]. The methanolic extract of the leaves of A. tanacetifolia afforded several kinds of coumarins [17], and 5-O-caffeoylquinic acid was detected from the aerial parts of flowering A. tanacetifolia [18]. Essential oil from A. ordosica has the effectiveness of anti-inflammatory, haemostasis, treating rheumatoid arthritis, parotiditis, abdominal distension, intestinal obstruction and ischuria [19]. Although numerous studies have shown that Artemisia species has various pharmacological effects, still little is known concerning the insecticidal activity of these five Artemisia species.
In this study, we reported the essential oils from five species in the genera Artemisia (A. dalai-lamae, A. tangutica, A. sieversiana, A. tanacetifolia and A. ordosica) and provided a comparative investigation of these five species’ chemical composition, repellent, and contact potential for Liposcelis bostrychophila Badonnel and Tribolium castaneum Herbst adults.

2. Results

2.1. Chemical Composition of the Essential Oils

Essential oils of the five plants aerial parts were obtained by hydrodistillation and analysed by GC-MS. The major chemical compounds are presented in Table 1. The data of A. ordosica were drawn from Zhang et al. (2017) [20]. The yields of five Artemisia species essential oils ranged from 0.02% to 0.53% (v/w%, Table 2). The chemical composition of these oils is different. A. tanacetifolia essential oil contains substantial amounts of 3-carene (45.98%) and β-pinene (15.13%), which were absent in other samples. The major components of A. sieversiana are neryl propanoate (22.88%), β-nerol (11.01%) and β-cubebene (7.50%), whereas cineol (32.62%), 3,7-dimethyl-1,5,7-octatriene-3-ol (15.85%), and santolina triene (14.45%) are the major compounds of A. dalai-lamae. Unlike A. dalai-lamae, A. ordosica yielded oil which is rich in caryophyllene (17.81%), β-bisabolene (12.11%), spathulenol (10.56%) and β-caryophyllene oxide (8.67%). In addition, the five essential oils also have similar sets of main components: caryophyllene (0.91–17.81%), camphor (1.32–51.07%), linalool (0.56–1.34%), α-terpineol (0.92–3.69%), 4-terpineol (1.12–11.97%) and nerolidol (0.24–1.47%) existing in at least three oils.
Twenty-five compounds with a concentration > 3% (for these components were rich enough for describe the characteristics of essential oils) were selected to perform PCA. PCA was used to determine the impacts and differences of the most important compounds. The contributions to the first two components of each chemical are shown in Figure 1a. β-Elemene (23), caryophyllene (26), β-bisabolene (35), myristicine (37), β-caryophyllene oxide (41) and (E)-phytol (52) gave the contribution of over 10% to PC1; α-terpineol (18) β-cubebene (24) and elixene (29) gave over 10% of contribution to PC2; over 15% of contribution was contributed by β-pinene (5), sylvestrene (8) and germacrene D (33). The bi-plot of PCA is shown in Figure 1b. PC1 and PC2 described 62.45% of the total variances. PC1 had the highest positive correlation with 3-carene (3), and the highest negative correlation with camphor (14). PC2 was represented mainly by cineol (9) in the positive score. A. dalai-lamae, A. tangutica and A. tanacetifolia were characterised by monoterpene hydrocarbons and oxygenated monoterpenes. A. sieversiana was characterised by oxygenated monoterpenes, sesquiterpene hydrocarbons and neryl propanoate (28). Moreover, sesquiterpene hydrocarbons, oxygenated sesquiterpenes, and a diterpene, (E)-phytone, etc., could describe the chemical character of A. ordosica. A dendrogram of HCA revealed the similarity of these Artemisia species (Figure 2). A. sieversiana and A. ordosica had the greatest similarity, but the similarity rate was lower than 50%. A. tangutica was spread from the other four species with a minimum likeness.

2.2. Repellent Activity

The repellent rates at 2 and 4 h after exposure to essential oils derived from five Artemisia species against L. bostrychophila and T. castaneum are shown in Figure 3, respectively. The repellent effect of essential oils on both two pests showed various levels. When compared with the positive control, DEET, at both 2 and 4 h after exposure, all five oils possessed the same level of repellent activity (p > 0.05) at a testing concentration of 63.17 nL/cm2 for L. bostrychophila and 78.63 nL/cm2 for T. castaneum. The essential oil of A. tangutica, A. sieversiana, A. tanacetifolia and A. ordosica also showed comparable repellent levels with the positive control (p > 0.05) at the concentration of 12.63 nL/cm2 against L. bostrychophila and 15.73 nL/cm2 for T. castaneum adults. It is worth noting that A. tangutica and A. sieversiana were found to have attraction effects against these two insects at the lowest concentration. Among the oils, A. ordosica showed outstanding repellent activity and possessed the same (p > 0.05) with DEET at all five concentrations on both insects.

2.3. Contact Toxicity

The contact toxicities of essential oils from five Artemisia species against L. bostrychophila and T. castaneum adults are listed in Table 3 and Table 4. Except for A. tanacetifolia, others all exhibited contact effects against L. bostrychophila. Among them, the A. ordosica essential oil possessed the most potent contact toxicity (LD50 = 52.11 μg/cm2), about three times less than the positive control, pyrethrins. Compared with A. ordosica, A. tangutica essential oil showed slightly weaker activity with an LD50 value of 70.48 μg/cm2. In addition, both A. sieversiana and A. dalai-lamae essential oils exhibited moderate toxicities with LD50 values of 195.51 and 115.94 μg/cm2, respectively, while for the insect of T. castaneum adults, A. tangutica possessed the most substantial toxicity with an LD50 of 17.42 μg/adult, followed by A. ordosica, A. dalai-lamae and A. tanacetifolia, with LD50 values of 21.68, 25.70 and 41.90 μg/adult, respectively.

3. Discussion

The chemical composition of Artemisia species oils has high diversity. The oil has different protective effects due to various compositions, such as antibacterial activity, insecticidal effect, antiviral and repellent actions.
Only essential oil components from A. sieversiana and A. ordosica have been reported before. Reports of the chemical constitutions of essential oils from these two kinds of Artemisia species indicated the high diversity caused by geographic locations (which may affect precipitation, temperature, edatope, etc.). The compositions of essential oils of A. sieversiana gathered from different regions of China in the flowering stage had a high level of variability. When sampling from Beijing, the essential oil contained eucalyptol (9.2%), geranyl butyrate (9.1%), camphor (7.9%), borneol (7.9%) and germacrene D (5.5%) [27], whereas essential oils of A. sieversiana gathered from Tibet mainly consisted of α-bisabolol (34.47%), chamazulene (23.00%) and α-phellandrene (5.22%) [28]. In Ningxia, the oil was mainly chamazulene (29.61%), camphor (4.80%) and eucalyptol (4.32%) [29].
The essential oil extracted from A. ordosica collected from the southwestern boundary of Tengger Desert was mainly magnol (22.60%), trans-β-ocimene (11.60%), and acenaphthylene (11.00%) [30]. 2,5-Etheno[4.2.2]propella-3,7,9-triene (24.81%), trans-nerolidol (10.39%) and α-longipinene (8.82%) were the predominant compounds of the sample collected from the southeastern boundary of the Hopq desert [31]. In the Mu Us desert, β-pinene (11.17%), limonene (11.41%) and capillene (9.46%) were the major components [32].
In our tests, the main compounds of tested oils also were found in other Artemisia species. For example, camphor, linalool and 4-terpineol were the major compositions in A. haussknechtii [33], and spathulenol, β-elemene, germacrene D were found in A. campestris [34]. Caryophyllene was the main compound in A. lavandulaefolia and A. rubripes oils [35,36].
It has also been reported that changes in the composition of volatile oils can also occur during plant growth stages. For instance, monoterpenoids, the major composing components (69.5–77.7%) of Ocimum americanum oil, were found to be maximal (77.7%) in the vegetative growth stage followed in the seed setting period (76.8%) and full flowering stage (74.2%), with the minimum at the half-flowering stage (69.5%) [37].
Recently, thousands of plants have been deemed as potential sources of repellents. The repellent properties of essential oils from the genus Artemisia were also well documented. In our previous research, five Artemisia species, including A. anethoides, A. giraldii, A. roxburghiana and A. rubripes were evaluated for their repellent activities on T. castaneum [38]. The result indicated that the five essential oils were effective in repelling T. castaneum, and the sequence of their activity was A. rubripes > A. anethoides > A. roxburghiana = A. sacrorum = DEET (the positive control) > A. giraldii (p > 0.05). In another previous research, polyacetylenes were isolated from the essential oil of A. ordosica aerial parts. Although with low relative content, the three tested polyacetylenes (capillene, capillin and cis-dehydromatricaria ester) were proved to possess fair repellent and fumigant activities against T. castaneum adults. Additionally, A. lavandulaefolia essential oil and its six constituents were tested on Lasioderma serricorne [39]. At 2 h after exposure, the same level of repellency (p > 0.05) was observed at doses from 0.63 to 78.63 nL/cm2. In other reports, A. vulgaris essential oil presented high repellent activity against T. castaneum [40]. The essential oil extracted from A. scoparia had more marked repellent activity on Sitophilus oryzae and T. castaneum than Callosobruchus maculatus, but as a whole, the oil strongly repelled each species of tested pests [41]. Moreover, in our tests, the main constituents of the five Artemisia species were proved to have a repellent effect. For example, 3-carene had over 85% of PR values against L. bostrychophila and T. castaneum after 2 h exposure [22]. Caryophyllene had the PR values of 82% and 98% against T. castaneum after 2 h and 4 h exposure, respectively [22]. These major components were also confirmed to be toxic to other insects, such as Aedes aegypti, Semanstus japonicus and Lasioderma serricorne [42,43,44]. Therefore, this study and the previous reports proved that essential oils from the genus Artemisia have great potential to be developed as good repellent agents against storage insects.
The different toxicity effects could be found based on the LD50 values of five Artemisia species oils obtained in this study. The essential oils from A. ordosica and A. tangutica exhibited stronger contact toxicity than others against L. bostrychophila and T. castaneum. The essential oil of A. sieversiana possessed weak toxicity against L. bostrychophila with a LD50 value of 195.51 μg/cm2, and no insecticide effect was observed in tested concentrations to T. castaneum. In the previous report, A. sieversiana also possessed weak contact toxicity against Sitophilus zeamais adults with an LD50 value of 112.7 mg/adult [27]. No significant correlation was observed when combined with the LD50 values of principal components and essential oils. This is considered to be related to the content of components and the synergistic or antagonistic effect between compounds. Pavela et al. (2010) estimated the fumigant toxicity against Spodoptera littoralis larvae of 15 pairs of binary mixtures [45]. It showed that nine mixtures had a synergistic effect, five mixtures had an additive effect, and one mixture had an antagonistic effect. It was also identified that 138 synergistic/antagonistic effects were detected among 39 compounds in binary mixtures via topical application against Trichoplusia ni [46]. So it may need further study to reveal the relationship between the insecticidal activities of different compounds.
The mechanism of bio-action of essential oils was recorded. For contact toxicity, substances could permeate through the skin of insects to act on the insects. Some of the substances could cause neurological disorders, for example, the inhibition of the activity of acetylcholinesterase (AChE), which is an important enzyme to regulate synaptic transmission [47]. The inhibition of AChE could lead to hyperexcitation, causing locomotor behaviour alternation. High concentrations or combined use of substances may generate the knockdown effect, reflecting acute toxicity [48]. These phenomena make us care about the safety of applying essential oils and plant-derived substances. Although the potential toxicity to mammals or cells of these five Artemisia species has not been studied yet, the safety evaluation of some other species in Artemisia has been recorded. The water extracts of A. dracunculus showed a maximum tolerated dose to rodents at over 200 mL of extract (1:10)/kg bw [49]. Essential oil from A. nilagirica had a LD50 value of 7528.10 µL/kg for male mice [50]. The essential oil of A. herba-alba showed no significant cytotoxicity in macrophages at the concentrations of 1.25 µL/mL and no significant cytotoxicity to microglial cells and keratinocytes at concentrations up to 0.32 µL/mL [51]. Moreover, the safety of the major constituents, 1,8-cineole, camphor, 3-carene and caryophyllene, was evaluated. After acute oral administration of 1,8-cineole, the LD50 value was 3849 mg/kg, while no significant changes in body weight and relative organ weight were observed in the subacute toxicity study [52]. The natural form of camphor was not toxic at 100 mg·kg·b.w.−1 to mice [53]. For 3-carene, the exposure by inhalation at 0.0014 mg/day was believed to be safe, and it could cause eye irritation at about 2.39 mg/mL air [54,55]. Caryophyllene was not considered as a skin sensitiser, and the TTC (threshold of toxicological concern) of inhalation exposure was 0.012 mg/day, which is 117 times lower than the Cramer Class I TTC [56]. However, essential oils from some Artemisia species were confirm to have toxicity to human. For example, volatile oil extracted from A. argyi could cause hepatocellular harm to cause liver injury [57]. Although there was no direct evidence that these five essential oils are safe enough for use, combined with the toxicity of other essential oils from Artemisia and the major constituents, it can be assumed that these essential oils are at lower concentrations of safe use as insecticides.

4. Materials and Methods

4.1. Plant Material

Plant materials were included the aerial parts of A. dalai-lamae, A. tangutica, A. sieversiana, A. tanacetifolia and A. ordosica. They were collected in the Gansu, Xinjiang and Inner Mongolia provinces, China, respectively, and voucher specimens were deposited at the herbarium of Faculty of Geographical Science, Beijing Normal University. The species of plants were identified by Dr. Liu, Q.-R. (College of Life Sciences, Beijing Normal University, Beijing, China). Table 2 summarises the collecting information of these samples.

4.2. Extraction and GC-MS Analysis of Essential Oils

The plant materials were dried in the shade and coarsely ground. Then, the grounded materials were subjected to 6 h of hydrodistillation using a modified Clevenger type apparatus, and the cooled essential oils were dehydrated by anhydrous sodium sulphate. The final oils were stored in sealed containers in the refrigerator at 4 °C.
Gas chromatographic-mass spectrometry (GC-MS) analysis was performed with an Agilent 6890N gas chromatograph (Agilent Technologies, DE, USA) equipped with a flame ionisation detector (FID). A HP-5MS (30 m × 0.25 mm × 0.25 μm) capillary column was used to distinguish the compounds. A 1.0 mL/min flow rate helium was used as a carrier gas. Then, 1 μL of 1% essential oil–n-hexane solution was injected, and the injector temperature was 250 °C. The oven temperature was programmed as follows as 50 °C for 2 min, increased at 2 °C/min to 150 °C for 2 min, then increased at 10 °C/min to 250 °C for 5 min.
Constituents were identified by comparing their retention indices (RI) with those reported in the literature, and by matching their mass spectra with those stored in NIST 05, Wiley 275 libraries or literature [58]. The GC-FID peak area (%) was used to obtain the relative percentages of each individual component of the essential oils.

4.3. Insects

A 10:1:1(w/w/w) mixture of flour, milk powder and yeast was used to rear L. bostrychophila, whether T. castaneum was fed with wheat flour mixed with yeast (10:1, w/w). The colonies were maintained in the dark incubators at 28–29 °C and 70–80% RH. The mixed-sex adults used in repellent and contact assays were about 7 ± 2 days old. The edges of containers and the Petri dishes for L. bostrychophila were smeared with polytetrafluoroethylene to ensure escape-proofing.

4.4. Repellent Activity

The repellence assay was performed using the area preference method [59]. Five doses of 63.17, 12.63, 2.53, 0.51 and 0.10 nL/cm2 were made by serial dilution in n-hexane for the repellent assay applied against L. bostrychophila adults. Filter papers with a 5.5 cm diameter were cut in half. Each tested solution (150 μL) was applied to half-cut filter paper as the experimental group, and n-hexane (150 μL) was used in another half as the control group. The treated filter papers were air-dried to evaporate the solvent completely. Then, both semi-circular filter papers were attached to their opposite sides and placed in Petri dishes (Φ = 5.5 cm). Meanwhile, for T. castaneum, the filter papers and Petri dishes were prepared at 9 cm in diameter. The five tested concentrations were 78.63, 15.73, 3.15, 0.63 and 0.13 nL/cm2, and 500 μL of testing solution or n-hexane were treated on each semi-circular filter paper. Twenty insects were released at the centre of the Petri dishes and covered with lids for all tests. The dishes were then placed in the dark incubators in the same condition as raring. Five replications were used for each concentration. The positive control was conducted by DEET (N, N-diethyl-3-methylbenzamide, Dr. Ehrenstorfer, Germany). The numbers of insects present on different sides of the paper were recorded after 2 and 4 h.

4.5. Contact Toxicity

The contact toxicity of the essential oils was conducted as follows. The appropriate testing concentrations were determined for all bioassays based on range-finding studies. Then, the desired quantity of each sample was dissolved in n-hexane to obtain a series of concentrations as the testing solution. When it came to L. bostrychophila adults, 300 μL of the solutions of the essential oils were applied to a round filter paper of 5.5 cm in diameter. Then the treated filter paper was attached to the bottom of Petri dishes of the same size as the filter papers. Ten insects in each treatment were put in the Petri dishes. All the Petri dishes were covered by lids and kept in the incubator. For the bioassays with T. castaneum adults, 0.5 μL of solutions were applied to the insects’ dorsal thorax. Ten treated insects with the same solution were transferred into one vial, and reared in the incubator.
After 24 h, the number of deaths was checked and recorded. The n-hexane was used as the negative control, and pyrethrin (pyrethrin I and II, 37%) was used as the positive control. The experiments were replicated five times.

4.6. Statistic Analysis

Principle component analysis (PCA) was used to explain the dissimilarities between samples. Hierarchical cluster analysis (HCA) was used to evaluate the similarity of the samples based on the type and quantity of compounds from essential oils. PCA was conducted by R Studio (version 4.1.3) with FactoMineR [60] and factoextra [61] packages. HCA was performed with Minitab 17 by using the complete linkage and Euclidean distance measure methods. A dendrogram was constructed to express the result.
The percentage repellency (PR) was calculated to measure the repellent activity of essential oils, which was computed by the foluma as below [59]:
PR % = Nc Nt / Nc + Nt × 100
Nc and Nt are the numbers of insects in the negative control and treated half, respectively. Then the analysis of variance (one-way ANOVA) and Tukey’s test were conducted using SPSS 20.0.
For the contact toxicity test, LD50 was calculated by Probit analysis using SPSS 20.0. The 95% FL (fiducial interval), Slope ± SE, p-value and χ2 were also recorded.

5. Conclusions

The chemical composition, repellent activity and contact toxicity of five Artemisia species (A. dalai-lamae, A. tangutica, A. sieversiana, A. tanacetifolia and A. ordosica) essential oils extracted by hydrodistillation were compared by PCA and HCA. All the oils showed obvious repellent activity against both insects in repellent tests. As for contact toxicity, the obtained values of LD50 demonstrated that several of the evaluated essential oils possessed toxic effects on L. bostrychophila and T. castaneum adults. Among these oils, A. ordosica essential oil possessed the most potent contact toxicity (LD50 = 52.11 μg/cm2) against L. bostrychophila, and A. tangutica essential oil exhibited the most substantial toxicity (LD50 = 17.42 μg/adult) against T. castaneum. Hence, the results suggest that the above five Artemisia species have the potential to be further exploited as repellent and insecticide agents against storage pests.

Author Contributions

Conceptualisation, J.-W.Z.; Data curation, Y.Z.; Formal analysis, J.-W.Z. and B.-Y.L.; Investigation, Z.Z.; Methodology, X.-X.L.; Resources, S.-S.D.; Supervision, D.Z. and S.-S.D.; Validation, B.-Y.L.; Visualisation, J.-W.Z.; Writing—original draft, J.-W.Z.; Writing—review and editing, D.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Second Tibetan Plateau Scientific Expedition and Research Program, grant number 2019QZKK0608.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Isman, M.B. Perspective, botanical insecticides: For richer, for poorer. Pest. Manag. Sci. 2008, 64, 8–11. [Google Scholar] [CrossRef] [PubMed]
  2. Kotan, R.; Kordali, S.; Cakir, A.; Kesdek, M.; Kaya, Y.; Kilic, H. Antimicrobial and insecticidal activities of essential oil isolated from Turkish Salvia hydrangea DC. ex Benth. Biochem. Syst. Ecol. 2008, 36, 360–368. [Google Scholar] [CrossRef]
  3. Green, P.W.; Belmain, S.R.; Ndakidemi, P.A.; Farrel, L.W.; Stevenson, P.C. Insecticidal activity of Tithonia diversifolia and Vernonia amygdalina. Ind. Crop. Prod. 2017, 110, 15–21. [Google Scholar] [CrossRef]
  4. Rattan, R.S. Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot. 2010, 29, 913–920. [Google Scholar] [CrossRef]
  5. Guenther, E. The Essential Oils; Krieger Publishing Company: Malabar, Florida, USA, 1971. [Google Scholar]
  6. Park, B.S.; Choi, W.S.; Kim, J.H.; Lee, S.E. Monoterpenes from thyme (Thymus vulgaris) as potential mosquito repellents. J. Am. Mosq. Control Assoc. 2005, 21, 80–83. [Google Scholar] [CrossRef]
  7. Nerio, L.S.; Olivero-Verbel, J.; Stashenko, E. Repellent activity of essential oils: A review. Bioresour. technol. 2010, 101, 372–378. [Google Scholar] [CrossRef]
  8. Abad, M.J.; Bedoya, L.M.; Apaza, L.; Bermejo, P. The Artemisia L. genus: A review of bioactive essential oils. Molecules 2012, 17, 2542–2566. [Google Scholar] [CrossRef] [Green Version]
  9. Kordali, S.; Kotan, R.; Mavi, A.; Cakir, A.; Ala, A.; Yildirim, A. Determination of the chemical composition and antioxidant activity of the essential oil of Artemisia dracunculus and of the antifungal and antibacterial activities of Turkish Artemisia absinthium, A. dracunculus, Artemisia santonicum, and Artemisia spicigera essential oils. J. Agric. Food Chem. 2005, 53, 9452–9458. [Google Scholar] [CrossRef]
  10. Farzaneh, M.; Ahmadzadeh, M.; Hadian, J.; Tehrani, A.S. Chemical composition and antifungal activity of the essential oils of three species of Artemisia on some soil-borne phytopathogens. Commun. Agric. Appl. Biol. Sci. 2006, 71, 1327–1333. [Google Scholar]
  11. Shafaghat, A.; Noormohammadi, Y.; Zaifizadeh, M. Composition and antibacterial activity of essential oils of Artemisia fragans Willd. leaves and roots from Iran. Nat. Prod. Commun. 2009, 4, 279–282. [Google Scholar] [CrossRef] [Green Version]
  12. Pandey, A.K.; Singh, P. The Genus Artemisia: A 2012-2017 literature review on chemical composition, antimicrobial, insecticidal and antioxidant activities of essential oils. Medicines 2017, 4, 68. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Kordali, S.; Aslan, I.; Çalmaşur, O.; Cakir, A. Toxicity of essential oils isolated from three Artemisia species and some of their major components to granary weevil, Sitophilus granarius (L.) (Coleoptera: Curculionidae). Ind. Crops Prod. 2006, 23, 162–170. [Google Scholar] [CrossRef]
  14. Bailen, M.; Julio, L.F.; Diaz, C.E.; Sanz, J.; Martínez-Díaz, R.A.; Cabrera, R.; Burillo, J.; Gonzalez-Coloma, A. Chemical composition and biological effects of essential oils from Artemisia absinthium L. cultivated under different environmental conditions. Ind. Crops Prod. 2013, 49, 102–107. [Google Scholar] [CrossRef] [Green Version]
  15. Bachrouch, O.; Ferjani, N.; Haouel, S.; Jemâa, J.M.B. Major compounds and insecticidal activities of two Tunisian Artemisia essential oils toward two major Coleopteran pests. Ind. Crops Prod. 2015, 65, 127–133. [Google Scholar] [CrossRef]
  16. Liu, S.J.; Liao, Z.X.; Tang, Z.S.; Cui, C.L.; Liu, H.B.; Liang, Y.N.; Zhang, Y.; Shi, H.X.; Liu, Y.R. Phytochemicals and biological activities of Artemisia sieversiana. Phytochem. Rev. 2017, 16, 441–460. [Google Scholar] [CrossRef]
  17. Szabó, G.; Greger, H.; Hofer, O. Coumarin-hemiterpene ethers from Artemisia species. Phytochemistry 1985, 24, 537–541. [Google Scholar] [CrossRef]
  18. Olennikov, D.N.; Chirikova, N.K.; Kashchenko, N.I.; Nikolaev, V.M.; Kim, S.-W.; Vennos, C. Bioactive phenolics of the genus Artemisia (Asteraceae): HPLC-DAD-ESI-TQ-MS/MS profile of the Siberian species and their inhibitory potential against α-amylase and α-glucosidase. Front. Pharmacol. 2018, 9, 756. [Google Scholar] [CrossRef]
  19. New Medical College of Jiangsu. Dictionary of Traditional Chinese Medicine; Shanghai Science and Technology Publishing House: Shanghai, China, 1977; p. 909. [Google Scholar]
  20. Zhang, Z.; Guo, S.S.; Zhang, W.J.; Geng, Z.F.; Liang, J.Y.; Du, S.S.; Wang, C.F.; Deng, Z.W. Essential oil and polyacetylenes from Artemisia ordosica and their bioactivities against Tribolium castaneum Herbst (Coleoptera: Tenebrionidae). Ind. Crops Prod. 2017, 100, 132–137. [Google Scholar] [CrossRef]
  21. Liu, Z.L.; Zhao, N.N.; Liu, C.M.; Zhou, L.; Du, S.S. Identification of insecticidal constituents of the essential oil of Curcuma wenyujin rhizomes active against Liposcelis bostrychophila Badonnel. Molecules 2012, 17, 12049–12060. [Google Scholar] [CrossRef] [Green Version]
  22. Cao, J.Q.; Guo, S.S.; Wang, Y.; Pang, X.; Geng, Z.F.; Du, S.S. Toxicity and repellency of essential oil from Evodia lenticellata Huang fruits and its major monoterpenes against three stored-product insects. Ecotoxicol. Environ. Saf. 2018, 160, 342–348. [Google Scholar] [CrossRef]
  23. Liu, X.C.; Zhou, L.G.; Liu, Z.L.; Du, S.S. Identification of insecticidal constituents of the essential oil of Acorus calamus rhizomes against Liposcelis bostrychophila Badonnel. Molecules 2013, 18, 5684–5696. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Wang, Y.; You, C.X.; Wang, C.F.; Yang, K.; Chen, R.; Zhang, W.J.; Du, S.S.; Geng, Z.F.; Deng, Z.W. Chemical constituents and insecticidal activities of the essential oil from Amomum tsaoko against two stored-product insects. J. Oleo Sci. 2014, 63, 1019–1026. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Guo, S.S.; Geng, Z.F.; Zhang, W.J.; Liang, J.Y.; Wang, C.F.; Deng, Z.W.; Du, S.S. The chemical composition of essential oils from Cinnamomum camphora and their insecticidal activity against the stored product pests. Int. J. Mol. Sci. 2016, 17, 1836. [Google Scholar] [CrossRef] [PubMed]
  26. Guo, S.S.; Zhang, W.J.; Liang, J.Y.; You, C.X.; Geng, Z.F.; Wang, C.F.; Du, S.S. Contact and repellent activities of the essential oil from Juniperus formosana against two stored product insects. Molecules 2016, 21, 504. [Google Scholar] [CrossRef] [Green Version]
  27. Liu, Z.L.; Liu, Q.R.; Chu, S.S.; Jian, G.H. Insecticidal activity and chemical composition of the essential oils of Artemisia lavandulaefolia and Artemisia sieversiana from China. Chem. Biodivers 2010, 7, 2040–2045. [Google Scholar] [CrossRef]
  28. Li, H.L.; Chen, H.Q.; Xu, F.L.; Wang, W.L.; Li, J.L. Chemical composition, antimicrobial and antioxidant activities of the essential oil of Artemisia sieversiana. Food Sci. 2016, 37, 63–68. [Google Scholar]
  29. Zhang, C.; Wang, W.C.; Bai, L.; Shi, S.L.; Yang, L. Chemical composition and antimicrobial activity of the essential oil of Artemisia sieversiana in Ningxia. Chin. Agric. Sci. Bull. 2020, 36, 62–68. [Google Scholar]
  30. Yan, S.F.; Liang, B.; Li, J.B. Study on the trace elements and chemical constituents of essential oil of Artemisia ordosica. Chin. J. Anal. Lab. 1994, 3, 82–84+94. (In Chinese) [Google Scholar]
  31. Yang, X.L.; Deng, S.Q.; De Philippis, R.; Chen, L.Z.; Hu, C.Z.; Zhang, W.H. Chemical composition of volatile oil from Artemisia ordosica and its allelopathic effects on desert soil microalgae, Palmellococcus miniatus. Plant Physiol. Biochem. 2012, 51, 153–158. [Google Scholar] [CrossRef]
  32. Yu, F.L.; Ma, M.H.; Kong, L.S. Study on allelopathic effects of essential oil from Artemisia ordosica. Acta Phytoecol. Sin. 1999, 4, 58–63. [Google Scholar]
  33. Yoon, W.J.; Moon, J.Y.; Song, G.; Lee, Y.K.; Han, M.S.; Lee, J.S.; Ihm, B.S.; Lee, W.J.; Lee, N.H.; Hyun, C.G. Artemisia fukudo essential oil attenuates LPS-induced inflammation by suppressing NF-κB and MAPK activation in RAW 264.7 macrophages. Food Chem. Toxicol. 2010, 48, 1222–1229. [Google Scholar] [CrossRef] [PubMed]
  34. Judzentiene, A.; Badioene, J.; Butkiene, R.; Kupcinskiene, E.; Laffont-Schwob, I.; Masotti, V. Caryophyllene oxide-rich essential oils of Lithuanian Artemisia campestris ssp. campestris and their toxicity. Nat. Prod. Commun. 2010, 5, 1981–1984. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Cha, J.D.; Jeong, M.R.; Choi, H.J.; Jeong, S.I.; Moon, S.E.; Yun, S.I.; Kim, Y.H.; Kil, B.S.; Song, Y.H. Chemical composition and antimicrobial activity of the essential oil of Artemisia lavandulaefolia. Planta Med. 2005, 71, 575–577. [Google Scholar] [CrossRef] [PubMed]
  36. Dai, X.Y.; Dong, X.R. Chemical constituents of fresh Artemisia rubripes Nakai leaves. Acta Bot. Boreali-Occident. Sin. 2010, 30, 1259–1263. [Google Scholar]
  37. Padalia, R.C.; Verma, R.S.; Chauhan, A.; Chanotiya, C.S. Changes in aroma profiles of 11 Indian Ocimum taxa during plant ontogeny. Acta. Physiol. Plant 2013, 35, 2567–2587. [Google Scholar] [CrossRef]
  38. Liang, J.Y.; Gu, J.; Zhu, J.N.; Liu, X.T.; Zhang, X.X.; Bi, Y.; Yan, K.; Kong, W.B.; Du, S.S.; Zhang, J. Repellent activity of essential oils extracted from five Artemisia species against Tribolium castaneum (Coleoptera: Tenebrionidae). Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas 2017, 16, 520–528. [Google Scholar]
  39. Zhou, J.; Zou, K.X.; Zhang, W.J.; Guo, S.S.; Liu, H.; Sun, J.S.; Li, J.G.; Huang, D.Y.; Wu, Y.; Du, S.S.; et al. Efficacy of compounds isolated from the essential oil of Artemisia lavandulaefolia in control of the cigarette beetle, Lasioderma serricorne. Molecules 2018, 23, 343. [Google Scholar] [CrossRef] [Green Version]
  40. Wang, J.; Zhu, F.; Zhou, X.M.; Niu, C.Y.; Lei, C.L. Repellent and fumigant activity of essential oil from Artemisia vulgaris to Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). J. Stored Prod. Res. 2006, 42, 339–347. [Google Scholar] [CrossRef]
  41. Negahban, M.; Moharramipour, S.; Sefidkon, F. Chemical composition and insecticidal activity of Artemisia scoparia essential oil against three Coleopteran stored-product insects. J. Asia-Pac. Entomol. 2006, 9, 381–388. [Google Scholar] [CrossRef]
  42. Müller, G.C.; Junnila, A.; Butler, J.; Kravchenko, V.D.; Revay, E.E.; Weiss, R.W.; Schlein, Y. Efficacy of the botanical repellents geraniol, linalool, and citronella against mosquitoes. J. Vector. Ecol. 2009, 34, 2–8. [Google Scholar] [CrossRef]
  43. Yatagai, M.; Makihara, H.; Oba, K. Volatile components of Japanese cedar cultivars as repellents related to resistance to Cryptomeria bark borer. J. Wood Sci. 2002, 48, 51–55. [Google Scholar] [CrossRef]
  44. You, C.X.; Guo, S.S.; Zhang, W.J.; Yang, K.; Geng, Z.F.; Du, S.S.; Wang, C.F.; Deng, Z.W. Identification of repellent and insecticidal constituents from Artemisia mongolica essential oil against Lasioderma serricorne. J. Chem. 2015, 2015, 549057. [Google Scholar] [CrossRef] [Green Version]
  45. Pavela, R. Acute and synergistic effects of monoterpenoid essential oil compounds on the larvae of Spodoptera littoralis. J. Biopestic. 2010, 3, 573–578. [Google Scholar]
  46. Tak, J.H.; Isman, M. Penetration-enhancement underlies synergy of plant essential oil terpenoids as insecticides in the cabbage looper, Trichoplusia ni. Sci. Rep. 2017, 7, 42432. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  47. Spochacz, M.; Chowański, S.; Walkowiak-Nowicka, K.; Szymczak, M.; Adamski, Z. Plant-derived substances used against beetles-pests of stored crops and food-and their mode of action: A review. Compr. Rev. Food. Sci. Food Saf. 2018, 17, 1339–1366. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  48. Peter, R.; Josende, M.E.; da Silva Barreto, J.; da Costa Silva, D.G.; da Rosa, C.E.; Maciel, F.E. Effect of Illicium verum (Hook) essential oil on cholinesterase and locomotor activity of Alphitobius diaperinus (Panzer). Pest. Biochem. Physiol. 2022, 181, 105027. [Google Scholar] [CrossRef]
  49. Obolskiy, D.; Pischel, I.; Feistel, B.; Glotov, N.; Heinrich, M. Artemisia dracunculus L. (Tarragon): A critical review of its traditional use, chemical composition, pharmacology, and safety. J. Agric. Food Chem. 2011, 59, 11367–11384. [Google Scholar] [CrossRef] [Green Version]
  50. Abu-Darwish, M.S.; Cabral, C.; Gonçalves, M.J.; Cavaleiro, C.; Cruz, M.T.; Efferth, T.; Salgueiro, L. Artemisia herba-alba essential oil from Buseirah (south Jordan): Chemical characterisation and assessment of safe antifungal and anti-inflammatory doses. J. Ethnopharmacol. 2015, 174, 153–160. [Google Scholar] [CrossRef]
  51. Kumar, M.; Dwivedy, A.K.; Sarma, P.; Dkhar, M.S.; Kayang, H.; Raghuwanshi, R.; Dubey, N.K. Chemically characterised Artemisia nilagirica (Clarke) Pamp. essential oil as a safe plant-based preservative and shelf-life enhancer of millets against fungal and aflatoxin contamination and lipid peroxidation. Plant Biosyst. 2020, 154, 269–276. [Google Scholar] [CrossRef]
  52. Xu, J.; Hu, Z.Q.; Wang, C.; Yin, Z.Q.; Wei, Q.; Zhou, L.J.; Li, L.; Du, Y.H.; Jia, R.Y.; Li, M.; et al. Acute and subacute toxicity study of 1,8-cineole in mice. Int. J. Clin. Exp. Pathol. 2014, 7, 1495–1501. [Google Scholar]
  53. Zuccarini, P. Camphor: Risks and benefits of a widely used natural product. J. Appl. Sci. Environ. Manag. 2010, 13, 69–74. [Google Scholar] [CrossRef] [Green Version]
  54. Api, A.M.; Belmonte, F.; Belsito, D.; Botelho, D.; Bruze, M.; Burton, G.A.; Buschmann, J.; Dagli, M.L.; Date, M.; Dekant, W.; et al. RIFM fragrance ingredient safety assessment, δ-3-carene, CAS Registry Number 13466-78-9. Food Chem. Toxicol. 2018, 122, S771–S779. [Google Scholar] [CrossRef] [PubMed]
  55. Kasanen, J.P.; Pas, A.L. Evaluation of sensory irritation of 3-carene and turpentine, and acceptable levels of monoterpenes in occupational and indoor environment. J. Toxicol. Environ. Health Part A 1999, 57, 89–114. [Google Scholar] [CrossRef]
  56. Thakkar, Y.; Tokura, Y. RIFM fragrance ingredient safety assessment, β-caryophyllene, CAS Registry Number 87-44-5. Food Chem. Toxicol. 2022, 159, 112707. [Google Scholar] [CrossRef]
  57. Ma, X.; Peng, J.H.; Hu, Y.Y. Chinese herbal medicine-induced liver injury. J. Clin. Transl. Hepatol. 2014, 2, 170–175. [Google Scholar] [CrossRef] [Green Version]
  58. Adams, R.P. Identification of Essential Oil Components by Gas Chromatography/Quadrupole Mass Spectroscopy; Allured: Carol Stream, IL, USA, 2001. [Google Scholar]
  59. Liu, Z.L.; Ho, S.H. Bioactivity of the essential oil extracted from Evodia rutaecarpa Hook f. et Thomas against the grain storage insects, Sitophilus zeamais Motsch. and Tribolium castaneum (Herbst). J. Stored Prod. Res. 1999, 35, 317–328. [Google Scholar] [CrossRef]
  60. Lê, S.; Josse, J.; Husson, F. FactoMineR: An R Package for Multivariate Analysis. J. Stat. Softw. 2008, 25, 1–18. [Google Scholar] [CrossRef] [Green Version]
  61. Factoextra: Extract and Visualize the Results of Multivariate Data Analyses. Available online: https://CRAN.R-project.org/package=factoextra (accessed on 5 June 2022).
Figure 1. Principal component analysis (PCA) of five Artemisia species according to the major essential oil compositions (concentration > 3%). (a) the contribution (%) of chemical constituents to the first two principal components; (b) bi-plot of PCA. The serial numbers of components are consistent with those in Table 1.
Figure 1. Principal component analysis (PCA) of five Artemisia species according to the major essential oil compositions (concentration > 3%). (a) the contribution (%) of chemical constituents to the first two principal components; (b) bi-plot of PCA. The serial numbers of components are consistent with those in Table 1.
Plants 11 01627 g001
Figure 2. Dendrogram analysis based on essential oil components of five Artemisia species.
Figure 2. Dendrogram analysis based on essential oil components of five Artemisia species.
Plants 11 01627 g002
Figure 3. Percentage repellency (PR) value of five Artemisia species essential oil against L. bostrychophila (a,b) and T. castaneum (c,d) adults at 2 h (a,c) and 4 h (b,d) after exposure. Means in the same column followed by the same letters do not differ significantly (p > 0.05) in ANOVA and Tukey’s tests.
Figure 3. Percentage repellency (PR) value of five Artemisia species essential oil against L. bostrychophila (a,b) and T. castaneum (c,d) adults at 2 h (a,c) and 4 h (b,d) after exposure. Means in the same column followed by the same letters do not differ significantly (p > 0.05) in ANOVA and Tukey’s tests.
Plants 11 01627 g003
Table 1. Chemical composition of essential oils extracted from the five Artemisia species.
Table 1. Chemical composition of essential oils extracted from the five Artemisia species.
No.RI 1CompoundRelative Content (%) 2
ADAGASACAO 3
1800Octane1.24----
2908Santolina triene14.45----
3925α-Thujene---2.53-
4966β-Thujene---2.63-
5980β-Pinene---15.13-
610103-Carene---45.98-
71021α-Cymene1.51----
81027Sylvestrene---5.92-
910461,8-Cineole32.62-0.362.56-
1010743,5-Dimethylethylbenzene7.48----
111106Linalool--1.341.270.56
1211083,7-Dimethyl-1,5,7-octatriene-3-ol15.85----
131145Camphor-51.071.32-1.38
141160Borneol--6.97--
151164Pinocarvone0.46----
1611754-Terpineol2.0211.971.571.12-
171182Isocitral-9.20---
181190α-Terpineol-1.473.691.270.92
191232β-Nerol--11.01--
201250γ-Pironene----2.41
211267Geraniol--1.440.31-
221372Copaene----1.76
231388β-Elemene---1.545.56
241390β-Cubebene--7.50-0.76
2513963-Methyl-2-pent-2-enyl-cyclopent-2-enone--1.09--
261417Caryophyllene0.913.762.020.9817.81
2714251-Methyl-4-(1-methylethylidene)-2-(1-methylvinyl)-1-vinylcyclohexane---1.29-
281430Neryl propanoate--22.88--
291432Elixene--4.21-0.19
301441β-Farnesene--2.73-1.23
311464β-Humulene----1.74
321465γ-Muurolene----1.33
331480Germacrene D---8.793.36
341489Viridiflorene1.14----
351504β-Bisabolene----12.11
361508Himbaccol--1.21--
371513Myristicine----3.19
381517Capillene-2.57--4.04
391523δ-Cadinene -1.50-2.64
401557Germacrene B0.78-3.00--
411566β-Caryophyllene oxide----8.67
421576Nerolidol--0.490.241.47
431583Spathulenol2.19-1.04-10.56
441606Humulene oxide II-1.99---
451639τ-Cadinol--1.19--
461650α-Cadinol---0.431.70
471654Bisabolol oxide B-2.23---
481678Dillapiol----1.18
4916888-Cedren-13-ol--1.00--
5017341,4-Dimethyl-7-ethylazulene--2.76--
511846Phytone----2.79
522119(E)-Phytol----5.64
532632Tetracosanal-2.18---
1 RI, retention index of the chromatography determined on a HP-5MS column using the homologous series of 𝑛-hydrocarbons as reference; 2 AD, A. dalai-lamae; AG, A. tangutica; AS, A. sieversiana; AC, A. tanacetifolia; AO, A. ordosica; 3 Data from Zhang et al. [20].
Table 2. Collecting information of the five Artemisia species.
Table 2. Collecting information of the five Artemisia species.
SpeciesDateProvinceDistrictGeographic CoordinateLife FormSample Mass (kg)Yield (v/w%)
A. dalai-lamaeOctober 2016GansuLanzhou103°45′ E, 36°01′ NSubshrub2.700.35
A. tanguticaOctober 2016GansuLanzhou103°45′ E, 36°01′ NPerennial herb2.500.29
A. sieversianaJuly 2017HebeiBashang117°51′ E, 40°57′ NAnnual or biennial herb6.300.06
A. tanacetifoliaJuly 2017HebeiBashang117°51′ E, 40°57′ NPerennial herb3.100.20
A. ordosica 1October 2015Inner MongoliaKubuqi Desert109°44′ E, 40°17′ NShrub3.000.39
1 Data from Zhang et al. [20].
Table 3. Contact toxicity of the essential oils from five Artemisia species and major compounds against L. bostrychophila adults.
Table 3. Contact toxicity of the essential oils from five Artemisia species and major compounds against L. bostrychophila adults.
SamplesLD50 (μg/cm2)FL (μg/cm2)Slope ± SEp-Valueχ2
A. dalai-lamae115.94104.58–129.586.42 ± 0.950.19313.58
A. tangutica70.4868.20–73.8912.46 ± 1.450.37419.30
A. sieversiana195.51177.33–215.976.87 ± 0.940.8517.89
A. tanacetifolialess than 50% morality at concentration of 50%
A. ordosica52.1151.55–53.874.88 ± 0.500.66419.62
1,8-Cineole 11048.741021.95–1096.859.50 ± 0.91-11.76
Camphor 1207.26199.78–214.9913.81 ± 1.47-15.87
3-Carene 2223.62205.65–243.005.92 ± 0.62-8.52
Caryophyllene 252.5243.52–60.832.77 ± 0.39-9.62
Pyrethrins 318.7217.60–19.922.98 ± 0.400.9910.56
1 Data from Liu et al. [21]; 2 Data from Cao et al. [22]; 3 Data from Liu et al. [23].
Table 4. Contact toxicities of the essential oils from five Artemisia species and major compounds against T. castaneum adults.
Table 4. Contact toxicities of the essential oils from five Artemisia species and major compounds against T. castaneum adults.
SamplesLD50 (μg/adult)FL (μg/cm2)Slope ± SEp-Valueχ2
A. dalai-lamae25.7023.09–28.494.19 ± 0.450.68119.34
A. tangutica17.4215.17–19.983.38 ± 0.450.55316.57
A. sieversianaless than 50% morality at concentration of 50%
A. tanacetifolia41.9037.08–47.573.88 ± 0.450.9956.17
A. ordosica21.6819.86–23.595.41 ± 5.060.94413.34
1,8-Cineole 118.8317.13–20.694.86 ± 0.50-16.56
Camphor 2less than 50% morality at concentration of 50%
3-Carene 363.4357.16–70.754.11 ± 0.45-11.67
Caryophyllene 325.8622.61–30.242.97 ± 0.39-13.13
Pyrethrins 40.260.22–0.303.34 ± 0.320.9513.11
1 Data from Wang et al. [24]; 2 Data from Guo et al. [25]; 3 Data from Cao et al. [22]; 4 Data from Guo et al. [26].
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Zhang, J.-W.; Li, B.-Y.; Lu, X.-X.; Zheng, Y.; Wang, D.; Zhang, Z.; Zeng, D.; Du, S.-S. Chemical Diversity and Anti-Insect Activity Evaluation of Essential Oils Extracted from Five Artemisia Species. Plants 2022, 11, 1627. https://doi.org/10.3390/plants11131627

AMA Style

Zhang J-W, Li B-Y, Lu X-X, Zheng Y, Wang D, Zhang Z, Zeng D, Du S-S. Chemical Diversity and Anti-Insect Activity Evaluation of Essential Oils Extracted from Five Artemisia Species. Plants. 2022; 11(13):1627. https://doi.org/10.3390/plants11131627

Chicago/Turabian Style

Zhang, Jia-Wei, Bo-Ya Li, Xin-Xin Lu, Yu Zheng, Dan Wang, Zhe Zhang, Ding Zeng, and Shu-Shan Du. 2022. "Chemical Diversity and Anti-Insect Activity Evaluation of Essential Oils Extracted from Five Artemisia Species" Plants 11, no. 13: 1627. https://doi.org/10.3390/plants11131627

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