Chemical composition and biological activity against Tribolium castaneum (Coleoptera: Tenebrionidae) of Artemisia brachyloba essential oil

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Chemical composition and biological activity against Tribolium castaneum (Coleoptera: Tenebrionidae) of Artemisia brachyloba essential oil Junpeng Hu, Wenxia Wang, Jiali Dai, Liang Zhu

T

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School of Food Science and Engineering, South China University of Technology, Guangzhou, Guangdong Province, 510641, China

ARTICLE INFO

ABSTRACT

Keywords: Artemisia brachyloba Essential oil Tribolium castaneum Toxicity Biochemical assay

The aim of this study was to investigate the biological effects of essential oil from Artemisia brachyloba against Tribolium castaneum. The essential oil from the aerial parts of Artemisia brachyloba was obtained by hydrodistillation and analyzed by gas chromatography–mass spectrometry. The toxicity and repellency of the oil and its two major compounds were evaluated against Tribolium castaneum. The essential oil is rich in oxygenated monoterpenes (55.52%) and oxygenated sesquiterpenoids (16.47%); its major components are α-terpineol (21.74%) and davanone (10.67%). The LD50 values of the oil, α-terpineol, and davanone topically applied were 22.55–31.84, 17.09–29.16, and 43–56 μg/mg insect, respectively. The LD50 value of filter papers treated with the oil and α-terpineol was 15.29–23.74 μL/cm2, whereas that of filter papers treated with davanone was 66.3–256.57 μL/cm2. Fumigation with the oil, α-terpineol, and davanone had LD50 values of 13.75–22.26, 9.98–20.17, and 68.53–124.41 μL/L air, respectively. The repellent property of essential oil was 73.33%–96.67%, while the repellent property of α-terpineol of 0.315 μL/cm 2 was75.00%–100%. Moderate repellency (46.67%–61.67%) was achieved by 0.315 μL/cm2 davanone. Biochemical assays have revealed multiple mechanisms of A. brachyloba essential oil in regulating enzymatic activities, thereby reducing the overall tested enzyme activities of adults of T. castaneum even at high concentrations or during long exposure time. Furthermore, the biological activity of α-terpinol was similar to that of the oil, while davanone was quite different. The toxicity of A. brachyloba essential oils may be dependent on the cumulative or synergistic relationship between several phytochemical groups.

1. Introduction Insect infestation, mainly by beetles and moths, are major causes of the loss of grains and their products during storage. Stored grains and cereal products are frequently attacked by more than 600 species of coleopteran pests (Yadav et al., 2014), thereby causing a quantitative loss of approximately 20%–30% in tropical and subtropical zones (Rajendran, 2002). The continuous increasing pressure of the expanding human population has created a critical problem of food scarcity. Therefore, measures that safeguard stored food from insect contamination can increase the availability of food products. The red flour beetle Tribolium castaneum (Herbst,1797) (Coleoptera: Tenebrionidae) is commonly found in food facilities, such as mills, manufacturing plants, ware houses, and retail stores, where grain and grainbased products are processed and stored (Bingham et al., 2017; Popoviæ et al., 2013). This insect causes serious economic losses by attacking a wide range of stored grain and other food products, including broken grain, milled grain products, cereals, meal, crackers,

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beans, spices, pasta, cake mix, dried pet food, dried flowers, chocolate, and nuts (Via, 1999). To date, the control of stored grain pests has relied on the frequent strategic use of commercial synthetic pesticides. However, the constant use of such chemical products has led to the resistance of T. castaneum populations against synthetic pesticides (Bossou et al., 2015). Conversely, the residues of some persistent chemicals in the environment disturb the ecosystem, and other pesticides are toxic to humans (Hill, 1989). Thus, ecologically safe and target-specific pesticides must be developed to manage stored-product pests (Ahmadi et al., 2008). The essential oils of plants could be alternative sources for pest control because of their innate biodegradability, minimal effects on non-target organisms and the environment (Feldlaufer and Ulrich, 2015), and its different modes pesticide action (El-Wakeil, 2013). The acute toxic effects of various essential oils against insect pests have been evaluated. In particular, T. castaneum is reportedly sensitive to certain essential oils and their active components (Peixoto et al., 2015; Khiyari et al., 2014; Nenaah, 2014; Zapata and Smagghe, 2010). Botanical chemicals

Corresponding author at: School of Food Science and Engineering, South China University of Technology, Wushan Road 381, Guangzhou, 510641, China. E-mail address: [email protected] (L. Zhu).

https://doi.org/10.1016/j.indcrop.2018.10.076 Received 11 June 2018; Received in revised form 25 October 2018; Accepted 25 October 2018 0926-6690/ © 2018 Elsevier B.V. All rights reserved.

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affect metabolism and growth of insects through physiological processes and enzymatic activities (Senthil-Nathan, 2013). A variety of oxidases, reductases, esterases, epoxide hydrolases, and group transferases are used by insects to detoxify and eliminate toxic phytochemicals (Skrinjaric-Spoljar et al., 1971).Understanding of the biochemical effects of pesticides on insects may definitely provide safe control strategies of pests. Artemisia L. of the family Asteraceae (Compositae) is a genus of small herbs and shrubs that are common in temperate areas of mid to high latitudes in the northern hemisphere. Artemisia is a heterogeneous genus that includes over 500 diverse species (Martin et al., 2001). Several species of the genus have a high economic value as medicines, food, forage, ornamentals, or soil stabilizers in disturbed habitats (Tan et al., 1998). Most Artemisia species produce essential oils that are used in traditional and modern medicine as well as in the cosmetics and pharmaceutical industries (Abad et al., 2012). Artemisia brachyloba Franch. commonly known as "yenhao" in China is widespread in Northern Asia and is used in traditional Chinese medicine to treat inflammation, headaches and worm infestations. This plant is also used to drive away stored grain pest because of its unique smell in high altitude area of Wu-Tai Mountains. However, little is known about the phytochemical composition and biological activity of A. brachyloba. Therefore, the present study aims to determine the chemical composition of the essential oil of A. brachyloba and evaluate in vitro the toxic contact, fumigant and repellency activity of this essential oil and two of its major components.

The relative concentration of each compound in the oil was quantified on the basis of the peak area, which was integrated in the analysis program. 2.4. Insect culture An insect culture of the red flour beetle T. castaneum was established from an original strain that was reared for several generations at the Institute of Entomology of Sun Yat-sen University in Canton, China. T. castaneum colonies were maintained in the laboratory without exposure to any insecticidal contamination. The insects were reared in 5 L glass jars that were covered with muslin cloth for ventilation. Each jar contained a mixture of wheat flour and brewer’s yeast (10:1, w/w). The cultures were maintained in a growth cabinet set at 28 ± 2 °C temperature, 65% ± 5% relative humidity, and 14 h light:10 h dark photoperiod. 2.5. Contact toxicity based on the topical application bioassay The contact toxicity of the oil and the test compounds against T. castaneum was determined following the method described by Nenaah (2014). Range-finding studies were run to determine the appropriate testing concentrations. A stock solution (v/v) of each sample was prepared by dissolving the desired quantity of each material in acetone to obtain a graded series of six concentrations (5%, 11%, 17%, 23%, 29%, 35%) for each sample. Subsequently, a 0.5 μL aliquot of each sample with the appropriate dilution was topically applied onto the thorax of individual adults (7–14 d old, 1.8–2.1 mg weigh) by using a micropipette applicator (Burkard, United Kingdom). Insects treated with acetone alone served as the control. A total of 20 unsexed adults or second-instar larvae were used for each treatment or control group; each experiment was had six replicates. After the treatment, the insects were transferred into glass Petri dishes (9 cm diameter) containing culture media. The dishes were stored in the dark at 28 ± 2 °C and 68% ± 2% relative humidity. The corrected mortality percentages were recorded after 24, 48 and 72 h of treatment, until such a time that the number of dead insects had stabilized and no longer increased with time. The insects were considered dead when no leg or antennal movements were recorded. The contact toxicity was expressed in μL of essential oil per mg weight of insect. Bioassays were designed to assess the median lethal concentrations (LD50 and LD90 values).

2. Materials and methods 2.1. Plant material and chemicals The aerial parts of A. brachyloba were collected from the Wu-Tai Mountains, Shanxi Province, China in June 2012. The plant specimens were identified by A.P. Yin-zhang Zhou. The plants were dried under the shade (at room temperature). The voucher specimen (No. IBSC/ 0542982) was deposited to the South China Botanical Garden, Chinese Academy of Sciences. α-Terpineol and davanone were purchased from Sigma–Aldrich (St. Louis, USA). 2.2. Isolation of the essential oil The air-dried plant materials (2000 g) of A. brachyloba were chopped and subjected to hydrodistillation for 6 h with a Clevenger type apparatus. The obtained oil was dried over hydrous sodium sulfate for 24 h, filtered, and then stored at 4 °C in brown sealed glass vials until further tests.

2.6. Contact toxicity based on the treated-filter paper bioassay The toxicity of the oil and the test compounds against T. castaneum was determined by direct contact application using the impregnated filter paper bioassay (Khiyari et al., 2014). The oil and the test compounds were dissolved in acetone at concentrations of 2.5%, 5.0%, 10.0%, 20.0%, 40.0% and 80.0%. Subsequently, 8 mL of each solution was uniformly applied to a filter paper disk (Whatman No. 1; cut into 5.6 cm diameter pieces; 24.63 cm2) to obtain final concentrations of 8.12, 16.24, 32.48, 64.96, 129.92 and 259.85 μL/cm2. The treated filter paper was then placed in glass Petri dishes (6 cm diameter). Control filter papers were treated with acetone. After solvent evaporation, 20 unsexed adults (7–14 d old) were deposited onto each dish and stored in the dark at 28 ± 2 °C with 68% ± 2% relative humidity. Insects in dishes containing filter papers treated with acetone alone served as the control. All treatments were set up in six replicates along with the respective controls. The exposure of insects was continued for 24 h, before the insects were transferred back to clean vials containing the culture media and kept in the incubators under the same rearing conditions. The corrected mortality was recorded after 24, 48 and 72 h. Insects were considered dead when no leg or antennal movements were recorded. Bioassays were designed to assess median lethal concentrations (LD50 and LD90 values).

2.3. Gas chromatography–mass spectrometry (GC–MS) The essential oil was analyzed using a GC–MS 6890-5975 system (Agilent Technologies, Palo Alto, CA, USA) equipped with a HP-5 MS fused silica capillary column (30 m × 0.25 mm i.d.; 0.25 μm film thickness). An electron ionization system with an ionization energy of 70 eV was used for GC–MS detection. Helium gas was used as the carrier gas, with a constant flow rate of 1 mL/min. The injector and mass transfer line temperatures were set at 250 °C and 280 °C, respectively. The injection volume was 0.5 μL from the solution (1:100 of the oil in hexane) and analyzed under the following column conditions. : initial column temperature at 40 °C for 1 min, increased to 250 °C at a 3 °C/ min heating ramp, and maintained at 250 °C for 20 min. The Kovats indices of the volatile components were calculated by using a homologous series of n-alkanes (C8–C25) in an HP-5 MS column (Seifi et al., 2014; Shen et al., 2017). The major oil components were identified by co-injection with standards (whenever possible) and confirmed by comparing the Kovats indices against the Wiley (V. 7.0) and the National Institute of Standards and Technology (V. 2.0) GC–MS libraries. 30

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2.7. Repellent activity

30 s for 3 min at 37 °C and 340 nm with a microplate reader. The GST activity was determined from the extinction coefficient of 0.0096 for CDNB. MO activity assay. The reaction solution contained 20 μl of the homogenate, 80 μl of 0.0625 M potassium phosphate buffer pH 7.2, 200 μl of 2 mM TMBZ solution and 25 μl of 3% hydrogen peroxide. The absorbance was measured at 450 nm as an endpoint after incubating the plate at room temperature for 2 h. The enzyme contents were reported as equivalent units of cytochrome p450/mg protein corrected for the known heme content of cytochrome C and p450 using a standard curve of purified cytochrome C. Esterase assays assay. Reaction mixtures contained 20 μl of the homogenate and 200 μl of 0.03 mM α- or β-naphthyl acetate solution respectively. After incubating the mixtures at room temperature for 30 min, 50 μl of 6.4 mM fast blue solution was added to each well. After another incubation period at room temperature for 5 min, the absorbance was measured at 570 nm as an endpoint. The enzyme activities were reported as μM of product formed/min/mg protein. p-Nitrophenyl acetate (p-NPA) assay. The reaction mixtures contained 10 μl of the homogenate induplicate plus 200 μl of a working solution of 100 mM p-NPA in acetonitrile. The enzyme rates were kinetically measured at 405 nm for 2 min. The p-NPA activity was reported as μM of product formed/min/mg protein. Protein concentration was measured using the method of (Bradford, 1976) by adding 10 μl of larval homogenate to 200 μl of Bio-Rad reagent in duplicates. After incubation of the mixture for 5 min at room temperature, the absorbance was measured at 590 nm. Absorbance was converted into protein concentrations using a bovine serum albumin standard curve obtained with the same method and reagents.

The repellent effects of the treatments on beetle adults of T. castaneum were evaluated following the binary choice bioassay described by Giner et al. (2013). The essential oil and the test compounds were dissolved in acetone at concentrations of 2.0%, 1.0%, 0.5%, 0.25%, 0.125% and 0.0625%. Half of a piece of filter paper (Whatman No. 1; cut into 9 cm diameter pieces) was treated with 0.5 mL of the respective sample solution dissolved in acetone, whereas the other half was treated with 0.5 mL of acetone alone. Twenty unsexed adults were transferred into the center of each Petri dish after solvent evaporation. The percentage of repellence was scored at 2, 4 and 8 h after beginning the assay. One experiment consisted of six replicates per sample and dose (0.010, 0.020, 0.039, 0.079, 0.157 and 0.315 μg/cm2). And the experiment was repeated three times. The percentage of repellency (PR) was calculated as follows: PR = (C − T)/(C + T) × 100 (Liang et al., 2017), where C is the number of insects on the untreated area and T is the number of insects on the treated area. 2.8. Fumigant toxicity The fumigant toxicity of essential oil was tested following the method previously described (Nenaah, 2014). The oil and the test compounds were individually dissolved in acetone at concentrations of 2.0%, 1.0%, 0.5%, 0.25%, 0.125% and 0.0725%. Subsequently, 0.5 mL of the respective solution was uniformly applied onto a filter paper disk (Whatman No. 1; cut into 3.8 cm diameter pieces; 10.17 cm2). After solvent evaporation, the filter paper was attached to the bottom surface of the screw cap of a glass vial (4.0 cm diameter, 50 mL) to obtain equivalent fumigant concentrations of 200.0, 100.0, 50.0, 25.0, 12.5 and 6.25 μL/L air. Twenty unsexed adults (7–14 d old) were deposited into each vial, and the caps were screwed on. The vials were stored in the dark at 28 ± 2 °C and 68% ± 2% relative humidity. Insects in dishes containing filter papers treated with acetone alone served as the control. All treatments were set up in six replicates along with the respective controls. The insects were continuously exposed for 24 h before being transferred back into clean vials with culture media and incubated under the same rearing conditions. The corrected mortality was recorded after 24, 48 and 72 h. Insects were considered dead when no leg or antennal movements were recorded. Bioassays were designed to assess median lethal concentrations (LD50 and LD90 values).

2.10. Statistical analysis The average larval mortality data were subjected to a probit analysis for calculating the LD50, LD90, and other statistics at 95% fiducial limits of the upper and lower confidence limits. The χ2 values were calculated by using SPSS version 13.0 for Windows. The significance level was set at P < 0.05. The significance of mean differences between groups was statistically compared by ANOVA at the 5% probability level. Individual pairwise comparisons were performed by Duncan’s test with SPSS 13.0. 3. Results and discussion

2.9. Biochemical assays

3.1. Chemical composition of A. brachyloba essential oil

To measure in vivo enzymes activities, the method was modified from Bullangpoti et al. (2012). The adults of 24 h that survived treatment in fumigation assay following the above method were homogenised in buffer A. The homogenates were centrifuged at 13,000 rpm and 4 °C for 5 min and the resulting supernatant was used as the enzyme source for biochemical assays. The supernatant was used for acetylcholinesterase (AChE), glutathione S-transferase (GST), monooxygenase (MO), esterase assays. Other adults were continuously exposed to the oil, α-terpineol and davanone with LD50 concentrations for 12 h, 24 h, 48 h, 72 h and their homogenates were also used for biochemical assays. The procedure was repeated with three separate homogenates and the average values were taken. AChE activity assay. The homogenate was incubated for 30 min at 30 °C with TpS [10 mM of DTNB, 0.1 mM of EDTA, 100 mM of ASCh and 100 mM phosphate buffer (pH 7.2)]. The change in absorbance at 412 nm was measured in a microplate reader (Biotek Power wave XS microplate spectrophotometer, US), and the AChE activity was converted to nM of acetylthiocholine hydrolysed per min (ε412 nm = 1.36 × 104 M−1 cm−1). GST activity assay. The reaction solution contained 1 ml of enzyme solution, 2 ml of 50 mM potassium phosphate buffer (pH 7.3) and 0.1 ml of 150 mM CDNB. Optical density was recorded at intervals of

Steam distillation of dried plant material (2000 g) yielded 14.6 mL (0.73%, v/w) of yellow oil with a distinct smell. A total of 63 compounds amounting to 99.23% of A. brachyloba essential oil were identified. The oil was composed of 55.52% oxygenated monoterpene fraction, 16.47% oxygenated sesquiterpenoids fraction, 11.92% sesquiterpene hydrocarbons fraction, 9.98% monoterpene hydrocarbons fraction, 3.20% phenylpropanoids, and 2.12% other unclassified compounds (Table 1). The major components of the oil were α-terpineol (21.74%) and davanone (10.67%), followed by 1,8-cineole (6.21%), artemisia alcohol (4.09%), camphor (3.73%) and caryophyllene (3.21%). Other components included linalool, artemisia ketone, caryophyllene oxide, germacrene D, geraniol and trans-γ-cadinene. 3.2. Contact toxicity of the essential oil and tested compounds The essential oil and the two test compounds were toxic to T. castaneum adults. In the topical application bioassay, the LD50 of the test oil was 31.84 μg/mg insect after 24 h of exposure. This value decreased to 27.13 and 22.55 μg/mg insect after 48 and 72 h of exposure, respectively. T. castaneum a adults were susceptible to α-terpineol, with LD50 values of 29.16, 24.47 and 17.06 μg/mg insect after 24, 48 and 31

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c RI, retention index; MS, mass spectrum; Co, co-injection with authentic compound.

Table 1 Chemical composition of Artemisia brachyloba essential oil. Peak no.

RIa

1 2 3 4 5 6 7

922 927 937 952 973 978 987

8 9 10 11 12

992 1020 1030 1060 1088

13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31

1035 1064 1070 1085 1097 1101 1109 1148 1162 1168 1175 1190 1197 1208 1220 1230 1247 1258 1265

32 33 34 35 36 37 38 39 40 41

1349 1372 1376 1420 1446 1483 1497 1507 1514 1526

42 43 44 45 46 47 48 49 50 51

1533 1548 1578 1585 1589 1608 1630 1656 1684 1697

52 53 54 55 56

964 1045 1285 1305 1356

57 58 59 60 61 62 63

867 982 1052 1125 1206 1928 1996

a b

Component

%RAb

Monoterpene hydrocarbons Artemisia triene α-Thujene α-Pinene Camphene Sabinene β-Pinene Bicyclo[3.1.1]heptane, 6,6dimethyl-2-methylene-, (1S)Myrcene α-Terpinene Limonene γ-Terpinene α-Terpinolene Oxygenated monoterpenes 1,8-Cineole Artemisia ketone cis-Sabinene hydrate Artemisia alcohol trans-Sabinene hydrate Linalool cis-Thujone Camphor Pinocarvone Borneol Terpinen-4-ol α-Terpineol Myrtenol trans-Piperitol trans-Carveol Citronellol Carvone Geraniol Furomyrcenol Sesquiterpene hydrocarbons α-Cubebene Ylangene α-Copaene trans-Caryophyllene cis-β-Farnesene Germacrene D α-Muurolene α-Farnesene trans-γ-Cadinene δ-Cadinene Oxygenated sesquiterpenes Artedouglasia oxide A Nerolidol Globulol Caryophyllene oxide Davanone β-Oplopenone α-Acorenol α-Cadinol 8-Cedrene-13-ol Shyobunol Phenylpropanoids Benzaldehyde Benzene acetaldehyde Anethole Carvacrol Eugenol Others n-Hexanol 1-Octen-3-ol cis-Arbusculone Isophorone n-Decanal Methyl hexadecanoate Ethyl hexadecanoate Total compounds identified (%)

9.98 1.36 0.41 0.28 1.21 0.48 1.41 0.57 0.61 0.51 1.32 1.55 0.27 55.52 6.21 2.48 0.67 4.09 1.38 2.94 0.37 3.73 1.27 1.51 1.68 21.74 0.37 1.57 0.85 1.20 0.95 2.28 0.23 11.92 0.37 0.23 0.49 3.21 0.94 2.41 0.67 0.74 2.17 0.69 0.41 0.72 0.42 2.56 10.67 0.53 0.21 0.24 0.41 0.32 3.20 0.24 0.34 0.41 0.64 1.57 2.12 0.34 0.27 0.42 0.31 0.34 0.25 0.19 99. 23

Identification method c MS, MS, MS, MS, MS, MS, MS,

RI RI RI RI RI RI RI

MS, MS, MS, MS, MS,

RI RI RI RI RI

MS, MS, MS, MS, MS, MS, MS, MS, MS, MS, MS, MS, MS, MS, MS, MS, MS, MS, MS,

RI, RI RI RI, RI RI RI RI, RI RI RI RI, RI RI RI RI RI RI RI

MS, MS, MS, MS, MS, MS, MS, MS, MS, MS,

RI RI RI RI, Co RI RI RI RI RI RI

MS, MS, MS, MS, MS, MS, MS, MS, MS, MS,

RI RI RI, Co RI RI RI RI RI RI RI

MS, MS, MS, MS, MS,

RI RI RI RI RI

MS, MS, MS, MS, MS, MS, MS,

RI RI RI RI RI RI RI

72 h of exposure, respectively. Davanone showed minor effect than the essential oil and a-terpineol with LD50 values of 56.24, 49.92 and 43.05 μg/mg insect after 24, 48 and 72 h of exposure, respectively (Table 2). In the treated-filter paper bioassay, the LD50 values of the test oil against the adult insects were 23.74, 18.10. 15.29 μg/cm2 after 24, 48 and 72 h exposure, whereas those of α-terpineol were 23.23, 20.77 and 15.95 μg/cm2 after the same exposure periods, respectively. Davanone did not show high toxicity, with LD50 values of 256.37, 118.82 and 66.63 μg/cm2 after 24, 48 and 72 h of exposure, respectively (Table 3). 3.3. Repellency activity of the essential oil and tested compounds The repellent effect of the essential oil and its two major constituents on T. castaneum adults was tested using the area preference method (Guo et al., 2015) The essential oil and the tested compounds were strongly repellent to T. castaneum, and the concentration–response analyses were significant. The repellent activity of the samples was significantly influenced by the concentration applied. The activity also increased with prolonged exposure time. When applied at the concentration range of 0.010–0.315 μL/cm2, the essential oil had PR values within 13.33%–73.33%, 18.33%–93.33% and 21.67%–96.67% after 2, 4 and 8 h of exposure, respectively. The same trend was observed with α-terpineol, with PR values of 5%–63%, 15.00%–75.00%, 16.67%–95.00% and 25.00%–100.00% at the concentration range of 0.010‒0.315 μL/cm2 after 1–8 h of exposure. Davanone exhibited moderate repellency, with a PR value of 46.67%–61.67%, even at the highest concentration (Table 4).

Co Co

Co

Co

3.4. Fumigant toxicity of the essential oil and tested compounds During in vivo fumigant testing, α-terpineol had higher fumigant toxicity than the essential oil or davanone, with LD50 values of 20.17, 15.62 and 9.98 μL/L air against T. castaneum adults after 24, 48 and 72 h of exposure, respectively. The essential oil also exhibited a strong fumigant activity against T. castaneum adults, with LD50 values of 22.26, 16.72 and 13.75 μL/L air. Davanone was much less effective against T. castaneum, with LD50 values of 124.2, 91.14, and 68.53 μL/L air after 24, 48 and 72 h of exposure, respectively (Table 5). 3.5. Enzyme activities The effects contacted with different concentration of the oil and two compounds for 24 h on enzymes activities in adults of T. castaneum were analyzed and the results are showed in Fig. 1. In low concentration, the oil (6.25 and 12.5 μL/L air) can significantly activated the activity of MO (P < 0.05) and α-terpineol (6.25 μL/L air) can significantly activated the activity of AChE (P < 0.05). dovanone can significantly activated the activities of GST in the concentration of 6.25 and 12.5 μL/L air and significantly activated the activities of AChE (P < 0. 05) in every concentration. In high concentration (100 and 200 μL/L air), the activity of every enzyme significantly decreased by the oil and α-terpineol (P < 0. 05) dovanone can also inhibited the activities of GST, α-esterase, β-esterase and p-NPA, but these activities were not significantly different statistically. The effects contacted with LD50 concentration of the oil and two compounds for different time on enzymes activities in adults of T. castaneum were analyzed and the results are showed in Fig. 2. Davanone can significant activated the activities of AChE (P < 0.05) at each time. At 12 h, the oil and α-terpineol can significant activated the activities of AChE and MO (P < 0.05) and davanone can significant activated the activities of GST (P < 0.05). At 24 h, α-terpineol can significant activated the activities of AChE (P < 0.05). The oil can

Retention index relative to n-alkanes on HP-5 MS capillary column. Relative area (peak area relative to the total peak area). 32

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Table 2 Toxicity of Tribolium castaneum exposed to Artemisia brachyloba essential oil, α-terpineol, and davanone using the topical application bioassay. Test sample

Period (h)

Toxicity/stagea LD50 (95% CL)

LD90 (95% CL)

Slope ± S.E.

χ2 (df)

Essential oil

24 48 72 24 48 72 24 48 72

31.84 27.13 22.55 29.16 24.47 17.09 56.24 49.92 43.05

73.27 61.81 52.75 66.83 54.65 45.55 – – –

3.54 3.59 3.47 3.56 3.67 3.01 – – –

4.12 6.14 7.58 3.07 3.31 2.98 – – –

α-Terpineol Davanone

(29.53‒34.21) (22.00‒32.31) (16.83‒27.63) (26.97‒31.32) (22.49‒26.39) (14.93‒19.01) (51.88‒61.55) (43.67‒57.92) (37.11‒49.95)

(65.76‒83.93) (48.83‒95.41) (41.12‒85.07) (60.24‒76.01) (49.08‒62.65) (39.45‒55.56)

± ± ± ± ± ±

0.25 0.28 0.27 0.25 0.28 0.31

(4) (3) (3) (4) (3) (2)

Each datum represents the mean of six replicates, and each set-up had 20 individuals (n = 120). 95% CL = confidence interval at 95% confidence level. a Concentrations were expressed as μg/mg insect. Table 3 Toxicity of Tribolium castaneum exposed to Artemisia brachyloba essential oil, α-terpineol, and davanone using the treated-filter paper bioassay. Test sample

Period (h)

Toxicity/stagea LD50 (95% CL)

LD90 (95% CL)

Slope ± S.E.

χ2 (df)

Essential oil

24 48 72 24 48 72 24 48 72

23.74 (20.43‒27.24) 18.10 (12.92‒23.74) 15.29 (13.16‒17.45) 23.23 (20.10‒35.89) 20.77 (14.78‒27.40) 15.95 (13.80‒18.14) 256.37 (196.85‒365.25) 118.82 (98.79‒147.62) 66.63 (56.97‒78.70)

113.02 (92.88‒144.10) 80.36 (57.08‒125.74) 56.45 (47.38‒70.50) 106.45 (74.26‒186.56) 93.35 (65.51‒162.30) 57.48 (48.37‒71.49) – – –

1.89 2.07 2.26 1.95 1.95 2.30 – – –

5.93 8.21 1.65 8.50 8.46 3.92 – – –

α-Terpineol Davanone

± ± ± ± ± ±

0.13 0.15 0.18 0.13 0.14 0.18

(4) (4) (3) (4) (4) (3)

Each datum represents the mean of six replicates, and each set-up had 20 individuals (n = 120). 95% CL = confidence interval at 95% confidence level. a Concentrations were expressed as μL/cm2.

oxygenated sesquiterpenoids (16.47%). The major components of the oil were α-terpineol and davanone, which account for more than 10%. Previous reports on Artemisia species also showed that α-terpineol or davanone are the major compounds in their essential oils. α-Terpineol is the major component of essential oils from A. princeps (Lee et al., 2015), A. rupestris (Liu et al., 2013), A. amygdalina (Rather et al., 2012), A. annua (Bilia et al., 2008), A. feddei (Cha et al., 2007), A. lavandulaefolia (Cha et al., 2005), and A. vulgaris (Thao et al., 2004). Davanone is the major component of essential oils from A. aucheri (Asl et al., 2018), A. asiatica (Huang et al., 2018), A. vulgaris (Zhigzhitzhapova et al., 2016), A. herba-alba (Bachrouch et al., 2015; Dahmani-Hamzaoui and Baaliouamer, 2015), A. indica (Haider et al., 2014), A. sieberi (Bidgoli et al., 2014), A. ludoviciana (Lopes-Lutz et al., 2008), A. ciniformis (Rustaiyan et al., 2007), A. turanica (Firouznia et al., 2007), A. kopetdaghensis (Ramezani et al., 2006), A. khorassanica (Ramezani et al., 2004), A. pedemontana (Perez-Alonso et al., 2003), and A. pallens (Mallavarapu et al., 1999). Although α-terpineol and davanone are the major biochemical compounds of essential oils from Artemisia species rarely both are identified as predominant in the essential oil of a single plant. Artemisia essential oils exert insecticidal activities against insect pests. To the best of our knowledge, the present study is the first to reveal that A. brachyloba essential oil possesses significant contact and fumigant toxicity as well as repellent activity against T. castaneum adults. Accumulating studies have also reported that the essential oils from other (Artemisia) species, including A. ordosica (Zhang et al., 2017), A. monosperma (Abou-Taleb et al., 2015), A. annua (Goel et al., 2007), A. sieberi (Negahban et al., 2007), A. scoparia (Negahban et al., 2006), and A. vulgaris (Wang et al., 2006)), and A. vulgaris (Wang et al., 2006), showed acute toxicity, developmental damage, repellent and

significantly inhibited the activities of GST (P < 0.05) after 24 h, can significantly inhibited the activities of α-esterase and p-NPA (P < 0.05) after 36 h, an significantly inhibited the activities of β-esterase and AChE (P < 0.05) after 48 h, and can significantly inhibited the activities of MO (P < 0.05) after 60 h. α-Terpineol can significantly inhibited the activities of GST and (P < 0.05) after 24 h, can significantly inhibited the activities of MO, α-esterase and p-NPA (P < 0.05) after 36 h, can significantly inhibited the activities of β-esterase (P < 0.05) after 48 h, and can significantly inhibited the activities of AChE (P < 0.05) after 60 h. Dovanone can significantly inhibited the activities of α-esterase (P < 0.05) after 12 h, can significantly inhibited the activities of p-NPA (P < 0.05) after 36 h, can significantly inhibited the activities of β-esterase (P < 0.05) after 72 h. It is worth to mention that the essential oil, α-terpineol, and davanone did not induce significant changes in total proteins of T. castaneum adults. 4. Discussion Artemisia species have been widely used as herbal medicine to treat various diseases. Thus, many studies explored the chemical and biological activities of Artemisia. Over 260 Artemisia species have been investigated (Rustaiyan and Masoudi, 2011), and the essential oils from this genus have been extensively studied. Artemisia species synthetize essential oils, these metabolites are chemically complex mixtures that usually they can contain up to 100 individual components. The major components of the oils from Artemisia species are acyclic monoterpenes, bicyclic monoterpenes, oxygenated monoterpenes, bicyclic sesquiterpenes, and oxygenated sesquiterpenes (Abad et al., 2012). In the present study, the results of GC–MS analysis revealed that the essential oil of A. brachyloba is rich in oxygenated monoterpenes (55.52%) and 33

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nervous hyperactivity and intoxication, including restlessness, hyperexcitability, tremors, convulsions and paralysis, finally, leading to death (Rajashekar et al., 2014). AChE is known as a target enzyme for insect control chemicals, which can block the neurotransmitter acetylcholine at the synaptic cleft (Lopez and Pascual-Villalobos, 2010). Herein, it demonstrated that davanone is an activator of AChE. It also demonstrated that at lower concentrations or at early stages, the fumigant treatments with the oil or α-terpineol actually induced the activity of AChE. However, higher concentrations or longer exposure times reduced the enzymatic activity of AChE. Detoxification enzymes are generally demonstrated as the enzymatic defence against xenobiotic compounds that play an important role in maintaining physiological functions of insect (Riaz et al., 2014). GST play a central role in the detoxification of xenobiotic and endogenous compounds in insects (Mounsey et al., 2010) that catalyze the conjugation of endogenous reduced glutathione with electrophilic center in the molecules of xenobiotics or their metabolites. As a result of conjugation, the hydrophilicity of the molecules increases and in most case, facilitates the excretion (Ma et al., 2002). The cytochrome P450 superfamily comprises a wide variety of enzymes involved in both anabolic and catabolic metabolism (Plant, 2007). It is regarded as the most important enzymes involved in the initial steps of metabolic reactions facilitating elimination of lipophilic drugs and other xenobiotics from the body. Esterases represent a group of highly variable and multifactorial enzymes which are related to various physiological activities, such as regulation of juvenile hormone levels, digestive processes, reproductive behavior and nervous system functions (Galego et al., 2006). Esterases play a significant role in the metabolism and subsequent detoxification of many agrochemicals (Potter and Wadkins, 2006). The current study clearly demonstrates that the essential oil and α-terpineol can reduced overall detoxification enzyme activities in adults of T. castaneum in high concentrations or long exposure times. Davanone only can reduced activities of esterases, and the effect is weaker than the essential oil and α-terpineol. Thus, our combined results clearly illustrated that the mechanism of death in T. castaneum treated with the essential oil maybe endowed by the accumulative or synergistic relationship between several phytochemical groups because essential oil are a complex mixture of compounds that can interact with multiple molecular targets. In conclusion, A. brachyloba essential oil and its major compounds exhibited significant contact and fumigant toxicity as well as repellent activity against T. castaneum adults. the oil and α-terpinol against insect pests by inhibiting the activities of GST, α-esterase, β-esterase and pNPA which can protect T. castaneum adults from being died. the higher the concentration, the more obvious the effect. while davanone davanone was quite different. It can also inhibited the activities of GST, αesterase, β-esterase and p-NPA, but these activities were not significantly different statistically. In previous studies, the oil or its components are potential alternatives to synthetic pesticides for the control

Table 4 Repellent activity of Tribolium castaneum exposed to Artemisia brachyloba essential oil, α-terpineol, and davanone at different exposure times. Test sample

Dose (μL/ cm2)

Repellency (%) 2h

4h

8h

Essential oil

0.010 0.020 0.039 0.079 0.157 0.315

α-Terpineol

0.010 0.020 0.039 0.079 0.157 0.315

Davanone

0.010 0.020 0.039 0.079 0.157 0.315

13.33 ± 5.16a 23.33 ± 5.16b 36.67 ± 8.17c 50.00 ± 8.94d 56.67 ± 8.17d 73.33 ± 6.16e (F = 60.36; df = 5, 30; P < 0.001) 15.00 ± 8.37a 26.67 ± 5.16b 35.00 ± 5.48b 51.67 ± 7.53c 58.33 ± 7.53c 75.00 ± 8.37d (F = 48.08; df = 5, 30; P < 0.001) 8.33 ± 7.53a 16.67 ± 8.17ab 20.00 ± 6.32b 26.67 ± 8.17bc 33.33 ± 10.33c 46.67 ± 8.17d (F = 16.31; df = 5, 30; P < 0.001)

18.33 ± 7.53 a 33.33 ± 5.16 b 48.33 ± 7.52 c 56.67 ± 5.16 d 78.33 ± 7.52 e 93.33 ± 5.16 f (F = 111.59; df = 5, 30; P < 0.001) 16.67 ± 5.16a 36.67 ± 5.16b 53.33 ± 8.17c 65.00 ± 5.47d 86.67 ± 8.17e 95.00 ± 5.48f (F = 129.03; df = 5, 30; P < 0.001) 10.00 ± 6.32a 29.33 ± 7.53b 38.33 ± 9.83bc 43.33 ± 10.33cd 53.33 ± 10.33de 55.00 ± 8.37e (F = 21.60; df = 5, 30; P < 0.001)

21.67 ± 4.08 a 38.33 ± 7.53 b 56.67 ± 5.16 c 65.00 ± 5.47 d 83.33 ± 8.17 e 96.67 ± 5.16 f (F = 124.55; df = 5, 30; P < 0.001) 25.00 ± 5.48a 43.33 ± 5.16b 60.00 ± 6.32c 70.00 ± 8.94d 91.67 ± 7.52e 100.00 ± 0.00f (F = 125.14; df = 5, 30; P < 0.001) 13.33 ± 5.16a 31.67 ± 7.52b 40.00 ± 10.96bc 46.67 ± 8.17cd 55.00 ± 8.37de 61.67 ± 7.53e (F = 27.37; df = 5, 30; P < 0.001)

abcde

Means within the same column followed by the same letter are not significantly different. ANOVA, LSD (P > 0.05).

feeding deterrents to T. castaneum. Furthermore, the present study showed that α-terpinol, the most abundant compound in A. brachyloba essential oil had an effective biological activity against T. castaneum. Therefore, this compound might play a critical role in the bioactivity of the essential oil, which was comparable to the reported insecticidal activities of α-terpineol. To illustrate, α-terpineol exhibited contact toxicity against Liposcelis bostrychophila with an LD50 value of 140.30 m ug/cm2 (Liu et al., 2013), fumigant toxicity against Sitophilus zeamais adults with an LC50 value of 7.45 mg/L air (Chu et al., 2013), and mosquitocidal activity against the fourth-instar larvae of Aedes aegypti with an LC50 value of 331.7 mg/kg (Pandey et al., 2013). To the best of our knowledge, the present study was the first to evaluate davanone's insecticidal activity, which was lower than essential oil Acetylcholine is the neurotransmitter found at all nervemuscle junctions and at many other sites in the nervous system (Rajashekar et al., 2014). The accumulation of acetylcholine in synapses causes

Table 5 Toxicity of Tribolium castaneum exposed to Artemisia brachyloba essential oil, α-terpineol, and davanone using the fumigation bioassay. Test sample

Period (h)

Toxicity/stagea LD50 (95% CL)

LD90 (95% CL)

Slope ± S.E.

χ2 (df)

Essential oil

24 48 72 24 48 72 24 48 72

22.26 (14.34‒31.24) 16.72 (10.25‒23.64) 13.75 (5.60‒21.75) 20.17 (13.46‒27.56) 15.62 (13.35‒17.92) 9.98 (8.13‒11.69) 124.21 (103.81‒153.37) 91.14 (76.49‒111.11) 68.53 (57.44‒83.00)

141.94 (90.16‒307.27) 68.85 (44.89‒158.91) 46.49 (27.78‒283.21) 120.53 (80.26‒232.54) 62.07 (51.64‒78.47) 36.93 (32.40‒51.04) – – –

1.59 2.08 2.42 1.65 2.14 2.26 – – –

9.45(4) 7.69 (3) 5.32 (2) 8.17 (4) 3.34 (3) 2.41 (2) – – –

α-Terpineol Davanone

Each datum represents the mean of six replicates, and each set-up had 20 individuals (n = 120). 95% CL = confidence interval at 95% confidence level. 34

± ± ± ± ± ±

0.12 0.17 0.22 0.12 0.17 0.23

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Fig. 2. Activities of enzymes in adult T. castaneum treatment with LD50 value of tested samples at different time. *Denote significant different at P < 0. 05 compared to the control.

Fig. 1. Activities of enzymes in adult T. castaneum treatment with tested samples at different concentrations. *Denote significant different at P < 0. 05 compared to the control.

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of storage pests. However, further studies are necessary to determine the mode of action and insecticidal efficiency of the essential oil under practical outdoor storage conditions.

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