Toxicity and repellency of essential oil from Evodia lenticellata Huang fruits and its major monoterpenes against three stored-product insects

Ecotoxicology and Environmental Safety 160 (2018) 342–348

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Toxicity and repellency of essential oil from Evodia lenticellata Huang fruits and its major monoterpenes against three stored-product insects Ju-Qin Caoa,b, Shan-Shan Guoa, Yang Wanga, Xue Panga, Zhu-Feng Genga,c, Shu-Shan Dua,

T

⁎

a

Beijing Key Laboratory of Traditional Chinese Medicine Protection and Utilization, Faculty of Geographical Science, Beijing Normal University, No. 19, Xinjiekouwai Street, Haidian District, Beijing 100875, China b Medical Chemistry Department, School of Basic Medical Sciences, Ningxia Medical University, Yinchuan 750004, China c Analytical and Testing Center, Beijing Normal University, Beijing 100875, China

A R T I C LE I N FO

A B S T R A C T

Keywords: Evodia lenticellata Fumigant toxicity Contact toxicity Repellency Monoterpenes Stored-product insects

In this work, the essential oil (EO) was extracted from the fruits of Evodia lenticellata, and the fumigant toxicity, contact toxicity and repellency against three stored-product insect species were evaluated for the obtained EO and several of its chemical components. The target insects were the adults of Tribolium castaneum (Coleoptera: Tenebrionidae), Lasioderma serricorne (Coleoptera: Anobiidae) and Liposcelis bostrychophila (Psocoptera: Liposcelididae). The EO was obtained with hydrodistillation and its chemical components were analyzed with the gas chromatography-mass spectrometry (GC-MS). Twenty-seven compounds, accounting for 83.1% of the total amount of the oil, were identified from the EO sample. The main compounds included linalool (12.0%), βpinene (11.5%), 3-carene (9.6%), caryophyllene oxide (8.7%) and β-caryophyllene (7.9%). Among them, the amounts of monoterpenes and sesquiterpenes were as high as 52.7% and 22.7% to the total amount of EO respectively. The results of bioactivity test showed that the EO and its testing compounds had interspecific toxicity and repellent activity. So that, it might be expected that the EO extracted from the fruits of E. lenticellata could be developed to a new type of eco-friendly natural insecticide or repellent for the control of stored-product insects.

1. Introduction The damage caused by stored-product insects includes weight loss, nutrient loss, contamination and health risks to consumers (Hagstrum and Subramanyam, 2006). In this work, Tribolium castaneum (Coleoptera: Tenebrionidae), Lasioderma serricorne (Coleoptera: Anobiidae) and Liposcelis bostrychophila (Psocoptera: Liposcelididae) were selected as the target insects. T. castaneum is an important cosmopolitan pest with short life cycle and high fecundity. It feeds and reproduces on a wide range of grains and value-added food products across the storage system and supply chain (Richards et al., 2008). L. serricorne is one of the most varied taste storage insect. It breeds on stored cereals, tobacco, seeds, dried fruits and even animal matter (Howe, 1957). L. bostrychophila is a worldwide distributed insect pest as reported. This specie has a remarkable reproductive capacity owing to its parthenogenetic charact eristic (Bryan, 1994). Synthetic insecticides have been used as one of the popular control method for stored-product insects. However, they have long been considered to be replaced due to their

unexpected toxicity on non-target organisms, endangerment on human health and the environment safety (Arthur, 1996; Isman, 2000). Botanical insecticides have been considered as suitable alternatives to conventional insecticides for pest control owing to insecticidal potential of their secondary chemicals inspired by plant-insect chemical interactions (Miresmailli and Isman, 2014). Meanwhile, they are relatively low toxic to environment and human health contrasted to synthetic chemical insecticides (Isman, 2006). Essential oils are one of the major types of botanical products which have been used for insect control, owing to their low risk to the environment and non-target insects. This is because their volatile nature leads minimal residual activity (Isman, 2006). Another benefit of the EOs would be the slowly developed resistance owing to the complex mixtures of the compounds (Koul et al., 2008). Essential oils are usually mixtures of monoterpenes, sesquiterpenes, aromatic and aliphatic compounds with small-molecular-weight and high volatility (Bassolé and Juliani, 2012). Most of the compounds in essential oils are nontoxic to mammals, birds, and fishes (Stroh et al., 1998). Monoterpenes are usually cited as one of the

Abbreviations: E. lenticellata, Evodia lenticellata; EO, essential oil; T. castaneum, Tribolium castaneum; L. serricorne, Lasioderma serricorne; L. bostrychophila, Liposcelis bostrychophila; RI, Retention Index; MS, mass spectrum; DEET, N, N-diethyl-3-methyl-benzamide ⁎ Corresponding author. E-mail address: [email protected] (S.-S. Du). https://doi.org/10.1016/j.ecoenv.2018.05.054 Received 28 December 2017; Received in revised form 6 April 2018; Accepted 22 May 2018 0147-6513/ © 2018 Elsevier Inc. All rights reserved.

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essential oil were obtained by averaging the GC-FID peak area% reports.

dominant factors responsible for biological activities of EOs (Habtemariam, 2017). They are used as contact toxicants, fumigants, attractants or repellents to control insect pests (Miresmailli and Isman, 2014). Evodia of family Rutaceae were reported to possess insecticidal and repellent activity against stored-product insects. e.g., Essential oil of Evodia rutaecarpa unripe fruits showed fumigant toxicity against Sitophilus zeamais and T. castaneum adults with LC50 values of 36.89 and 24.57 mg/L air (Liu and Du, 2011). E. rutaecarpa unripe fruits is officially listed in the Chinese Pharmacopoeia and used as an analgesic, antiemetic, anti-inflammatory, astringent agents and treatment of hypertension (Tang and Eisenbrand, 1992). The major compounds isolated from E. rutaecarpa were identified as dehydroevodiamine, evodiamine and rutaecarpine, displaying biological activities related to inflammatory (Tang and Eisenbrand, 1992). Evodia lenticellata, mainly distributed in Southwest Shannxi province of China, belonging to family Rutaceae, has similar morphology and medicinal effects as the fruit of Evodia rutaecarpa (Ma, 2016). Evodiamine and rutaecarpine have also been isolated from E. lenticellata fruits as major active constitutes which exhibit similar activities as E. rutaecarpa fruits (Ma, 2016). Besides, EOs from Evodia calcicola and Evodia trichotoma leaves were also reported exhibit strong repellency to T. castaneum, L. serricorne and L. bostrychophila (Yang et al., 2014b). These prompt us to conduct a systematic investigation on bioactivity of this genus against stored-product insects. Hence, in this research, we focus our attention on this overlooked local traditional medicine herbs, E. lenticellata, which is selected as a source of compounds showing insecticidal activity against three target stored-product insect adults, T. castaneum, L. serricorne and L. bostrychophila. Meanwhile, no published studies so far have evaluated the insecticidal activity of E. lenticellata fruit EO on stored-product insects. Thus, it is reasonable to hypothesize that EO of E. lenticellata fruit may also exhibit insecticidal and repellent activity against stored-product insects.

2.3. Insects culture The insects are reared in glass containers (0.5 L) with incubators (29 ± 1 °C and 65% ± 5% relative humidity) that are kept in permanent darkness. The red flour beetles (T. castaneum) and cigarette beetles (L. serricorne) are reared on wheat flour mixed with additional 10% yeast. L. bostrychophila was reared with the mixture of flour, milk powder and yeast (the mass ratio is 10:1:1). The unsexed adults of all species used in the tests were two weeks post-emergence. 2.4. Bioactivity 2.4.1. Fumigant toxicity The five concentrations of essential oil and individual compounds were determined by pre-experiments (maximum concentration, 50%, V/V). The testing samples were dissolved separately in acetone to prepare serials of testing solutions. The treatments were experimented as the method described by Liu and Ho (1999). A Whatman filter paper (diameter 2.0 cm) was laid at the bottom of the screw cap and impregnated with 10 μL dilution. The solvent was allowed to evaporate for 20 s before the cap was placed tightly on the glass vial (diameter 2.5 cm, height 5.5 cm, volume 25 mL), each of which contained 10 insects inside. The negative control was acetone. Five replications were performed for each treatment. After 24 h, record the number of dead insects. 2.4.2. Contact toxicity Contact toxicity test method of essential oil and compounds against T. castaneum and L. serricorne are similar to that described by Liu and Ho (1999). The samples were serially diluted with acetone to a suit of concentrations according to the pre-experiments (maximum concentration, 50%, V/V). Volume of 0.5 μL prepared solution was applied to dorsal thorax of each insect. The control group was treated only with acetone. The treated insects were then transferred to clean glass vial and kept in the aforementioned incubator. Each treatment was replicated five times. After 24 h, the mortality was recorded. The test of L. bostrychophila was run as described (Zhao et al., 2012). A serial dilution of the EO and compounds (five concentrations) were prepared in acetone (the highest concentration of pre-experiment is 5%, V/V). The filter paper disks (5.5 cm in diameter) were treated with 300 μL of the diluted solution and then adhered to the bottom of the same size Petri dish. Twenty booklice were introduced at the center of the filter paper by using a hair brush then the Petri dish was covered with lid. Controls received only acetone. Five replications were run for each concentration. Mortality of insects was observed after 24 h.

2. Materials and methods 2.1. Essential oil extraction The E. lenticellata ripe fruits were collected from Hanzhong, Shannxi Province, China (Latitude 32°08'–33°53' N, Longitude 105°30'–108°16' E) in November 2017. The sample was identified by Dr. Liu, Q.R. and the voucher specimen (BNU-dushushan-20171208) was deposited at the Herbarium (BNU) of College of Resources Science and Technology, Beijing Normal University. The fruits were air-dried. The sample was weighted and ground to powder, then transferred into a modified Clevenger-type apparatus for 6 h. The extracted essential oil was dehydrated with anhydrous sodium sulfate and stored in airtight containers at 4 °C.

2.4.3. Repellency tests The area preference method (Zhang et al., 2011) was used to evaluate repellency of the EO and compounds against T. castaneum and L. serricorne. The filter paper disk (9 cm in diameter) was cut into semicircles. One half was treated with 500 μL of acetone solutions of the samples (0.13–78.63 nL/cm2) and the other half was treated with acetone as control. Reassemble the two halves into disk again after the solvent was evaporated (85 s), and then attach them at the bottom of the same size Petri dish. Twenty adults were introduced at the center of the filter paper then the Petri dish was covered with a lid. As for L. bostrychophila, the same method was used. The differences are the diameter of filter paper disk (5.5 cm in diameter), concentrations of the samples (0.10–63.17 nL/cm2) and the volume of the solution used to treat the semicircles (150 μL). Each treatment was replicated five times and numbers of insects presented on the control (Nc) and the testing (Nt) halves were recorded after 2 and 4 h, respectively. A commercial repellent, N, N-diethyl-3-methylbenzamide (DEET), was used as a

2.2. Gas chromatography and mass spectrometry GC-MS analysis was performed on a Thermo Finnigan Trace DSQ instrument coupled with a flame ionization detector (FID) and a capillary column of HP-5MS (30 m × 0.25 mm×0.25 µm). The GC-MS settings were programmed as follows: initial oven temperature was held at 50 °C for 2 min, rising to 150 °C at 2 °C/min and increased to 250 °C at 10 °C/min, then kept for 5 min. Injector temperature was maintained at 250 °C and the volume injected was 1 μL of 1% solution (diluted in nhexane). Carrier gas used was helium at a flow rate of 1.0 mL/min. Spectra were scanned from 50 to 550 m/z. Under the same operating conditions, the retention indices were determined in relation to a homologous series of n-alkanes (C5-C36). Further identification was made by comparing their mass spectra with those stored in NIST 05 (Standard Reference Data, Gaithersburg, MD) and Wiley 275 libraries (Wiley, New York, NY) or with mass spectra from literature (Adams, 2001). Relative percentages of the individual components of the 343

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to exhibit fumigant toxicity against L. bostrychophila at the highest concentration (5%, V/V). Linalool was the most toxic one among five compounds against T. castaneum and L. bostrychophila with LC50 values of 11.60 and 0.82 mg/L air, respectively. Caryophyllene oxide and β-caryophyllene were not so effective on three insects as fumigants, as well as 3-carene on L. bostrychophila. After 24 h, we found the dead body of insects turned black and the beetles dead with opened waings. We could speculate the insecticidal mechanism of EO and its compounds according to these symptoms.

positive control. The value of percent repellency (PR) was calculated as follows:

PR(%) = [(Nc − Nt)/(Nc + Nt) × 100 The mean values are then assigned to different classes (0 to V), using the scale suggested by Liu and Ho (1999): Class 0, PR < 0.1; Class Ⅰ, PR = 0.1–20.0; Class Ⅱ, PR = 20.1–40.0; Class Ⅲ, PR = 40.1–60.0; Class Ⅳ, PR = 60.1–80.0; Class Ⅴ, PR = 80.1–100.0. 2.5. Statistical analysis

3.3. Contact toxicity of the essential oil and major compounds The data are analyzed using the Statistical Package of Social Science (SPSS) version 20.0 (IBM Corp., Armonk, NY, USA) for Windows 7. LC50, LD50, their 95% fiducial limits, chi-square values and related parameters are calculated by using probit analysis.

Twenty-seven compounds of the essential oil from E. lenticellata fruits were identified (Table 1), accounting for 83.1% of the total oil. The main compounds included linalool (12.0%), β-pinene (11.5%) and 3-carene (9.6%), followed by caryophyllene oxide (8.7%) and β-caryophyllene (7.9%). Among them, monoterpenes (52.7%) and sesquiterpenes (22.7%) give a contribution of 75.4% to the total essential oil.

Three seleted monoterpenes showed high mortality at the same concentration on T. Castaneum and L. serricorne (Table 4). The essential oil exhibited different levels of contact toxicity against three insects with LD50 values of 89.70 μg/adult, 17.09 μg/adult and 57.22 μg/cm2, respectively (Table 5). Among the compounds, β-pinene, linalool and caryophyllene oxide showed the strongest contact toxicity against T. castaneum, L . serricorne and L. bostrychophila, respectively. Low mortality was observed when topical application was performed on T. castaneum with caryophyllene oxide at the highest concentration (50%, v/v). Typical neurotoxic symptoms were observed in experiments, e.g., tremors, lack of coordination (walked backward), wings opened and dead body turned black. We could speculate that the EO act on the insects as neuro-toxicants.

3.2. Fumigant toxicity of the essential oil and major compounds

3.4. Repellent activity

Essential oil from the fruits of E. lenticellata were toxicity to three target insect species in a dose dependent manner, with monoterpenes generally more toxic than sesquiterpenes (Table 2). The EO exhibited fumigant toxicity against T. castaneum and L. serricorne with LC50 values of 46.95 mg/L air and 32.22 mg/L air, respectively (Table 3), but failed

The essential oil was strongly repellent to T. castaneum and L. bostrychophila with the PR over 80% at 2 h (Table 6). Compared with the positive control DEET, the EO, β-pinene, 3-carene, caryophyllene oxide and β-caryophyllene showed the same level of repellency against T. castaneum at 2 h. The EO and its compounds showed fair repellency

3. Results 3.1. Extraction and chemical composition of the essential oil

Table 1 Chemical composition of essential oil from E. lenticellata fruits. No.

Compound name

RIa

Molecular formula

Content [%]b

Mode of identificationc

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

β-Thujene 4-Hydroxybenzenephosphonic acid D-Limonene β-Pinene 3-Carene β-Ocimene Linalool m-Cresol Propene, 2-methyl-1-(trimethylcyclopropylidene)Sabina ketone p-Ethylphenol 2,4-Dimethylphenol α-Terpineol Phellandral p-Ethylguaiacol Cuminol 1,6-Methano[10]annulene p-Vinylguaiacol β-Caryophyllene Neryl propionate Aromadendrene Germacrene D α-Selinene δ-Cadinene linalyl valerate Spathulenol Caryophyllene oxide Total

966 970 975 979 1010 1044 1100 1105 1140 1160 1168 1181 1191 1273 1280 1291 1300 1315 1423 1430 1466 1485 1491 1528 1548 1582 1589

C10H16 C6H7O4P C10H16 C10H16 C10H16 C10H16 C10H18O C7H8O C10H16 C9H14O C8H10O C8H10O C10H18O C10H16O C9H12O2 C10H14O C11H10 C9H10O2 C15H24 C13H22O2 C15H24 C15H24 C15H24 C15H24 C15H26O2 C15H24O C15H24O

4.4 0.6 5.3 11.5 9.6 5.0 12 1.0 0.6 1.5 0.6 0.3 1.0 2.5 1.1 0.8 0.6 0.8 7.9 1.2 1.0 1.3 1.0 0.6 0.5 1.7 8.7 83.1

MS; MS MS MS; MS; MS; MS; MS; MS MS; MS; MS; MS; MS; MS; MS; MS MS; MS; MS; MS; MS; MS; MS; MS MS; MS;

a b c

Retention index (RI) relative to the homologous series of n-hydrocarbons on the HP-5MS capillary column. Relative area (peak area relative to the total peak area). MS = mass spectrum. 344

RI

RI RI RI RI RI RI RI RI RI RI RI RI RI RI RI RI RI RI RI RI RI

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Table 2 Motality of T. castaneum (TC), L.serricorne (LS) and L . bostrychophila (LB) in fumigation tests at 24 h. Insect

TC

LS

LB

Essential Oil

β-Pinene

Linalool

3-Carene

Caryophyllene oxide

β-Caryophyllene

C (%) (V/ V)

M (%) ± SD

C (%) (V/ V)

M (%) ± SD

C (%) (V/ V)

M (%) ± SD

C (%) (V/ V)

M (%) ± SD

C (%) (V/ V)

M (%) ± SD

C (%) (V/ V)

M (%) ± SD

33.3 22.2 14.8 9.9 6.6 22.2 14.8 9.9 6.6 4.4 5.0 – – – –

87 ± 5.8 77 ± 5.8 57 ± 5.8 33 ± 5.8 3 ± 5.8 93 ± 5.8 80 ± 10 53 ± 5.8 23 ± 5.8 0±0 0±0 – – – –

6.7 4.4 3.0 2.0 1.3 33.8 22.5 15.0 10.0 6.7 5.0 3.3 2.2 1.5 1

82 ± 4.5 66 ± 5.5 46 ± 8.9 26 ± 5.5 6 ± 5.5 98 ± 4.5 80 ± 7.1 52 ± 8.4 34 ± 5.5 10 ± 7.1 98 ± 4.5 76 ± 5.5 34 ± 8.9 20 ± 7.1 6 ± 5.5

10.0 6.7 4.4 3.0 2.0 20.0 13.3 8.9 5.9 4.0 5.0 – – – –

100 ± 0 78 ± 8.4 50 ± 10 32 ± 8.4 4 ± 5.5 98 ± 4.5 80 ± 7.1 56 ± 8.9 34 ± 5.5 2 ± 4.5 63 ± 5.8 – – – –

10.0 6.7 4.4 3.0 2.0 20 13.3 8.9 5.9 4.0 5.0 – – – –

92 ± 4.5 76 ± 5.5 66 ± 5.5 32 ± 8.4 4 ± 5.5 94 ± 5.5 80 ± 7.1 64 ± 5.5 36 ± 5.5 4 ± 5.5 0±0 – – – –

50.0 10.0 – – – 50.0 – – – – 5.0 – – – –

60 27 – – – 23 – – – – 20 – – – –

50.0 – – – – 50.0 – – – – 5.0 – – – –

0±0 – – – – 0±0 – – – – 43 ± 5.8 – – – –

± 10 ± 5.8

± 5.8

±0

C=Concentration (%, V/V); M=Mortality of treated insects; SD=Standard Deviation.

(Class Ⅲ-Class Ⅴ) to T. castaneum and L. bostrychophila at the highest concentration of 78.63 nL/cm2 and 63.17 nL/cm2 after 2 h exposure, respectively. However, the situation seems different to L. serricorne. The EO and its major compounds provided varying degrees of repellence against L. serricorne at all test concentrations.

Zhao, 2010). The authors collected E. lenticellata leaves from Shannxi province as well. The main components of the EO were measured to be (Z)-β-ocimene (40.2%), (E)-β-ocimene (9.0%), β-myrcene (6.7%), βcaryophyllene (6.0%) and linalool (2.7%). The composition and content are different from our result. The components of the EOs in the same plant species can be varied, as a result of the different ecological conditions like type of soil, climate, degree of maturity and physiological development of plant (Ishaaya, 2007; Araújo et al., 2017).

4. Discussion 4.1. Chemical composition of the essential oils

4.2. Fumigant toxicity During our screening program for new natural insecticides from local wild plants and Chinese medicinal herbs, the essential oils of several evodia samples, including E. lenticellata fruits, E. lenticellata leaves and E. daniellii fruits, were extracted with the yield (v/w) of 0.30%, 0.12% and 0.14%, respectively. The EO from fruits of E. lenticellata possessed a relatively high extraction yield. The composition analysis of EO from E. lenticellata fruits have been reported (Fu and

In fumigant toxicity assays, the essential of E. lenticellata fruits possessed fair toxicity against T. castaneum and L. serricorne with the value of 46.95 mg/L air and 32.22 mg/L air respectively. In the previous report, EO from E. rutaecarpa unripe fruits possessed fumigant activity to T. castaneum adults with LC50 values of 24.57 mg/L air (Liu and Du, 2011). Compared with their results, the EO of E. lenticellata

Table 3 Fumigant toxicity of E. lenticellata fruits essential oil and major compounds against T. castaneum (TC), L. serricorne (LS) and L. bostrychophila (LB) adults at 24 h. Insects

Samples

LC50 (mg/L air) (95% Fiducial Limits)

LC90 (mg/L air) (95% Fiducial Limits)

Slope ± SE

Chi-Square (χ2)

TC

E. lenticellata Linalool β-Pinene 3-Carene Caryophyllene oxide β-Caryophyllene MeBr a E. lenticellata Linalool β-Pinene 3-Carene Caryophyllene oxide β-Caryophyllene Phosphine b E. lenticellata Linalool β-Pinene 3-Carene Caryophyllene oxide β-Caryophyllene Dichlorvos c

46.95 (40.33-54.41) 11.60 (10.26-13.21) 14.51 (13.18-15.95) 14.10 (12.64-15.66) > 50.0 (mortality 60% ± 10%) > 50.0 (mortality 0% ± 0%) 1.7 32.22 (28.47-36.40) 46.93 (42.21-52.02) 28.50 (25.88-31.31) 27.25 (24.48-30.17) > 50.0 (mortality 23% ± 6%) > 50.0 (mortality 0% ± 0%) 9.23×10-3 (7.13×10-3-11.37×10-3) > 5.0 (mortality 0% ± 0%) 0.82 (0.74-0.90) > 5.0 (mortality 63% ± 6%) > 5.0 (mortality 0% ± 0%) > 5.0 (mortality 20% ± 0%) > 5.0 (mortality 43% ± 6%) 1.35×10-3

103.88 (83.97-146.95) 28.36 (22.91-39.27) 26.84 (23.47-32.38) 29.19 (25.05-36.27) – – – 58.83 (50.00-75.43) 94.78 (81.57-117.28) 52.65 (46.14-63.26) 54.62 (47.25-66.99) – – – – 1.52 (1.32-1.84) – – – – –

3.72 ± 0.54 3.30 ± 0.40 4.80 ± 0.50 4.05 ± 0.44 – – – 4.90 ± 0.65 4.20 ± 0.45 4.81 ± 0.50 4.24 ± 0.46 – – 2.12 ± 0.27 – 4.78 ± 0.49 – – – – –

5.77 5.80 13.02 11.01 – – – 5.78 9.32 12.23 10.91 – – 11.96 – 13.07 – – – – –

LS

LB

The mortality of the negative control was 0 for the three insects. a Data from Liu & Ho (1999). b Data from Yang et al. (2014b). c Data from Liu et al. (2013). 345

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Table 4 Motality of T. castaneum (TC), L.serricorne (LS) and L. bostrychophila (LB) in contact tests at 24 h. Insect

TC

LS

LB

Essential oil

β-Pinene

Linalool

3-Carene

Caryophyllene oxide

β-Caryophyllene

C (%) (V/ V)

M (%) ± SD

C (%) (V/ V)

M (%) ± SD

C (%) (V/ V)

M (%) ± SD

C (%) (V/ V)

M (%) ± SD

C (%) (V/ V)

M (%) ± SD

C (%) (V/ V)

M (%) ± SD

50 33.3 22.2 14.8 9.9 6.6 5.5 4.6 3.8 3.2 0.9 0.7 0.6 0.5 0.4

100 ± 0 83 ± 5.8 47 ± 5.8 20 ± 0 0±0 97 ± 5.8 83 ± 5.8 67 ± 5.8 47 ± 5.8 0±0 100 ± 0 90 ± 0 67 ± 11.5 43 ± 5.8 0±0

33.3 22.2 14.8 9.9 6.6 15.0 10.0 6.7 4.4 3.0 0.8 0.7 0.6 0.5 0.4

100 ± 0 82 ± 8.4 64 ± 5.5 54 ± 5.5 22 ± 8.4 98 ± 4.5 80 ± 7.1 48 ± 8.4 28 ± 4.5 8 ± 8.4 92 ± 4.5 54 ± 5.5 38 ± 8.4 20 ± 7.1 4 ± 5.5

33.3 22.2 14.8 9.9 6.6 22.5 15.0 10.0 6.7 4.4 4.2 3.5 2.9 2.4 2

96 ± 5.5 84 ± 5.5 66 ± 5.5 54 ± 11.4 20 ± 7.1 84 ± 5.5 66 ± 11.4 52 ± 8.4 36 ± 8.9 8 ± 8.4 98 ± 4.5 88 ± 8.4 44 ± 5.5 36 ± 8.9 4 ± 5.5

30 20 13.3 8.9 5.9 15.0 10.0 6.7 4.5 3.0 5.0 3.3 2.2 1.5 1

96 ± 5.5 62 ± 8.4 38 ± 8.4 22 ± 5.5 6 ± 5.5 90 ± 7.1 52 ± 8.4 24 ± 8.9 16 ± 5.5 2 ± 4.5 100 ± 0 84 ± 5.5 60 ± 7.1 22 ± 8.4 2 ± 4.5

50.0 – – – – 15.0 10.0 6.7 4.4 3.0 0.7 0.4 0.3 0.2 0.1

10 ± 0 – – – – 86 ± 5.5 68 ± 8.4 36 ± 5.5 20 ± 7.1 4 ± 5.5 94 ± 5.5 76 ± 8.9 52 ± 8.4 26 ± 5.5 6 ± 5.5

10.0 6.7 4.4 3.0 2.0 22.5 15 10 6.7 4.4 1.5 1 0.7 0.4 0.3

76 ± 8.9 52 ± 8.4 44 ± 5.5 24 ± 13.4 4 ± 5.5 96 ± 5.5 70 ± 7.1 48 ± 8.4 34 ± 5.5 8 ± 8.4 94 ± 5.5 80 ± 7.1 62 ± 8.4 58 ± 8.4 26 ± 5.5

C=Concentration (%, V/V); M=Mortality of treated insects; SD=Standard Deviation. Table 5 Contact toxicity of E. lenticellata fruits essential oil and major compounds against T. castaneum (TC), L. serricorne (LS) and L. bostrychophila (LB) adults at 24 h. Insects

Samples

LD50 (μg/adult; μg/cm2) (95% Fiducial Limits)

LD90 (μg/adult; μg/cm2) (95% Fiducial Limits)

Slope ± SE

Chi-Square (χ2)

TC

E. lenticellata Linalool β-Pinene 3-Carene Caryophyllene oxide β-Caryophyllene Pyrethrins a E. lenticellata Linalool β-Pinene 3-Carene Caryophyllene oxide β-Caryophyllene Pyrethrins a E. lenticellata Linalool β-Pinene 3-Carene Caryophyllene oxide β-Caryophyllene Pyrethrins a

89.70 (80.55-99.95) 45.96 (39.91-51.79) 46.18 (39.86-52.26) 63.43 (57.16-70.75) > 50.0 (mortality 10% ± 0%) 25.86 (22.61-30.24) 0.26 (0.22-0.30) 17.09 (16.08-18.07) 27.41 (24.80-30.27) 44.45 (38.87-50.88) 36.09 (32.70-40.17) 37.56 (33.71-42.13) 43.79 (39.16-48.93) 0.24 (0.16-0.35) 57.22 (54.36-60.08) 68.35 (65.27-71.97) 304.77 (291.94-317.92) 223.62 (205.65-243.00) 35.40 (32.01-39.28) 52.52 (43.52-60.83) 18.72 (17.60-19.92)

145.26 (126.43-179.67) 106.19 (89.74-136.44) 110.68 (92.96-143.62) 130.00 (110.15-165.12) – 69.85 (53.60-107.17) – 22.70 (21.09-25.41) 53.07 (45.98-64.88) 117.93 (93.88-168.47) 69.69 (59.46-87.62) 79.94 (66.94-103.63) 94.78 (80.00-121.26) – 71.63 (67.33-78.78) 94.94 (87.79-106.36) 400.36 (377.34-434.90) 368.01 (328.83-430.03) 71.29 (61.23-88.27) 152.54 (122.69-216.45) –

6.12 ± 0.83 3.52 ± 0.44 3.38 ± 0.42 4.11 ± 0.45 – 2.97 ± 0.39 3.34 ± 0.32 10.40 ± 1.43 4.47 ± 0.47 3.02 ± 0.38 4.49 ± 0.49 3.91 ± 0.43 3.82 ± 0.43 1.31 ± 0.20 13.16 ± 1.82 9.00 ± 1.00 10.81 ± 1.13 5.92 ± 0.62 4.23 ± 0.45 2.77 ± 0.39 2.98 ± 0.40

4.59 10.58 9.68 11.67 – 13.13 13.11 11.33 10.92 11.58 13.09 7.49 11.82 17.36 7.21 13.28 16.95 8.52 7.69 9.62 10.56

LS

LB

a

e)

Data from Yang et al. (2014b).

concentration. It is worth noting that linalool and β-pinene exhibited fair toxicity (0.82 mg/L air, 63% mortality) against L. bostrychophila, but the EO failed at the same concentration. Hassall (1983) found pyrethroids, as botanical insecticides, can be partially detoxified by microsomal mono-oxygenases from L. bostrychophila body. It would be advisable to consider the use of synergized EO with higher content of toxic constituents on L. bostrychophila control. Interestingly, two weeks old insects in our tests showed comparative survivability as one week old insects (Guo et al., 2016; Yang et al., 2014a). But on the contrary, linalool exhibited 2⁓3 times less fumigant toxicity against two weeks old L. serricorne compared to one week old. Besides, the fumigant toxic level of monoterpenes would be different even for the same tested insects. e.g., the values of LC50 for linalool against S. oryzae were 14 μL·litre−1 and 39.2 μL·litre−1, respectively (Coats et al., 1991; Lee et al., 2001). This might be due to the different strains of cultured insects and any uncontrolled factors not considered.

fruits exhibited more than two times less toxic against T. castaneum adults. This might be due to the different content of monoterpenes (52.7% in E. lenticellata fruits and 80.8% in E. rutaecarpa unripe fruits) which are usually considered to be one of the active ingredients of the EOs (Ibrahim, 2001). Among the five tested compounds, the highest toxicity against T. castaneum and L. bostrychophila were shown by linalool (11.60and 0.82 mg/L air, respectively). Monoterpenes (account for 33.1% of the EO) with the property of volatility which allow the insecticide act on target insects in gaseous phase. In our tests, excited behaviors and black dead body with unfold wings of the treated insects indicated that the EO and its compounds might acted as neuro-toxicants on target insects. The small monoterpene molecules may block the tracheae of insects or bind to target sites on receptors that modulate nervous activity and interrupt normal neurotransmission leading to paralysis and death (Hollingworth et al., 1984; Liu and Ho, 1999). In contrast to monoterpenes, sesquiterpenes were found to be less toxic against the target insects (0⁓60% mortality). Caryophyllene oxide and β-caryophyllene are sesquiterpenes with higher molecular weight and less volatility. This might be one of the reasons for their relatively weak fumigant toxicity against three target insects at the tested

4.3. Contact toxicity The essential oil from E. lenticellata fruits exhibited different levels 346

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Table 6 Repellency of the essential oils and their major compounds against T. castaneum (TC), L. serricorne (LS) and L. bostrychophila (LB). Treatment TC E. lenticellata Linalool β-Pinene 3-Carene Caryophyllene oxide β-Caryophyllene DEET LS E. lenticellata Linalool β-Pinene 3-Carene Caryophyllene oxide β-Caryophyllene DEET LB E. lenticellata Linalool β-Pinene 3-Carene Caryophyllene oxide β-Caryophyllene DEET a

2 h (% ± SE, N = 20) a

78.63 90 ± 5 58 ± 20 80 ± 10 88 ± 5 98 ± 2 82 ± 8 100 ± 0 78.63a 72 ± 6 76 ± 12 20 ± 18 60 ± 18 36 ± 17 42 ± 13 88 ± 7 63.17a 88 ± 3 64 ± 4 72 ± 12 88 ± 7 92 ± 7 56 ± 19 100 ± 0

a

15.83 94 ± 4 48 ± 19 70 ± 18 50 ± 20 98 ± 2 48 ± 20 96 ± 3 15.83a − 24 ± 16 84 ± 11 32 ± 18 68 ± 14 12 ± 11 − 22 ± 20 76 ± 14 12.63a 78 ± 5 46 ± 13 32 ± 18 52 ± 18 80 ± 8 26 ± 18 96 ± 4

4 h (% ± SE, N = 20) a

3.15 72 ± 15 50 ± 17 26 ± 18 46 ± 20 82 ± 8 34 ± 19 74 ± 16 3.15a − 34 ± 19 42 ± 20 − 16 ± 19 82 ± 16 14 ± 10 10 ± 17 28 ± 7 2.53a 38 ± 15 8 ± 19 40 ± 19 44 ± 19 48 ± 18 − 22 ± 7 92 ± 7

a

0.63 92 ± 5 80 ± 18 52 ± 19 50 ± 20 36 ± 10 22 ± 20 66 ± 9 0.63a 20 ± 20 24 ± 18 52 ± 19 − 50 ± 6 2±7 42 ± 19 20 ± 14 0.51a 40 ± 15 6 ± 19 18 ± 20 6 ± 20 38 ± 19 28 ± 17 90 ± 10

a

0.13 84 ± 10 64 ± 13 18 ± 14 48 ± 20 56 ± 17 22 ± 16 18 ± 16 0.13a 68 ± 15 16 ± 17 30 ± 20 − 28 ± 20 0±9 − 48 ± 13 16 ± 7 0.10a 36 ± 15 10 ± 20 40 ± 18 − 16 ± 15 − 16 ± 18 10 ± 18 92 ± 7

78.63a 80 ± 5 44 ± 20 94 ± 6 68 ± 11 94 ± 4 98 ± 2 94 ± 6 78.63a 60 ± 16 48 ± 20 32 ± 19 64 ± 19 40 ± 20 34 ± 17 98 ± 2 63.17a 72 ± 4 14 ± 18 80 ± 13 68 ± 12 96 ± 4 80 ± 13 90 ± 6

15.83a 80 ± 7 54 ± 19 78 ± 14 36 ± 13 98 ± 2 72 ± 19 80 ± 10 15.83a 26 ± 17 50 ± 18 46 ± 19 60 ± 18 46 ± 13 18 ± 13 78 ± 9 12.63a 64 ± 2 20 ± 15 38 ± 20 26 ± 19 100 ± 0 20 ± 20 74 ± 9b

3.15a 58 ± 20 72 ± 13 44 ± 19 62 ± 19 92 ± 8 50 ± 20 46 ± 17 3.15a − 34 ± 18 42 ± 18 − 22 ± 20 54 ± 19 32 ± 12 12 ± 8 58 ± 16 2.53a 68 ± 8 4 ± 19 − 14 ± 13 26 ± 7 40 ± 19 44 ± 18 72 ± 19

0.63a 88 ± 10 58 ± 20 56 ± 18 20 ± 14 − 36 ± 19 − 46 ± 19 − 2 ± 20 0.63a 30 ± 18 34 ± 20 14 ± 19 6 ± 20 24 ± 4 56 ± 15 56 ± 14 0.51a 38 ± 18 52 ± 19 40 ± 19 10 ± 20 28 ± 20 54 ± 19 30 ± 10

0.13a 60 ± 18 78 ± 5 40 ± 16 50 ± 5 56 ± 19 − 20 ± 20 − 8 ± 20 0.13a 76 ± 15 − 12 ± 20 34 ± 19 14 ± 18 16 ± 12 − 46 ± 12 46 ± 7 0.10a 24 ± 15 12 ± 8 − 12 ± 8 − 6 ± 20 18 ± 19 30 ± 18 32 ± 7

Concentration (nL/cm2); N: number of insects.

of contact toxicity against three insects with LD50 values of 89.70 μg/ adult, 17.09 μg/adult and 57.22 μg/cm2, respectively. Compared with positive control, pyrethrins, the EO demonstrated 345, 71 and 3 times less toxicity against three target insects, respectively. Caryophyllene oxide caused moderate mortality (10%) against T. castaneum at the highest concentration (50%, V/V). During the experiment, we found that the crystal of caryophyllene oxide was very easy to precipitate out. This might be due to poorly cuticle perviousness of T. castaneum and low solubility of caryophyllene oxide. Three monoterpenoids (linalool, β-pinene and 3-carene) exhibited fair contact toxicity against T. castaneum and L. serricorne respectively. e.g., linalool showed 177, 114 and 4 times less toxicity to T. castaneum, L . serricorne and L. bostrychophila when compared to pyrethrins. Monoterpenoids from plants are considered to have anticholinesterasic properties which cause high levels of mortality of insects when higher concentrations were used (López & Pascual-Villalobos, 2010). For instance, linalool exhibited contact toxicity with LC50 values of 66.74 μg/cm2 and 105.63 μg/cm2 against S. oryzae and T. castaneum, respectively (Samir et al., 2009). Herein, we observed tremors and lack of coordination of moribund insects. These are typical neurotoxic symptoms which demonstrated the neurotoxicity of the major compounds. The neurotoxic compounds exhibit their insecticidal activity as acetylcholinesterase inhibitors and octopamine receptor blockers (Jukic et al., 2007; Khanikor et al., 2013). For L. serricorne and L. bostrychophila, the EO showed comparatively stronger toxicity than most of its major compounds. Synergistic effect of compounds in the EO may play an important role in the level of insecticidal activity (Pavela, 2014). But the opposite happened to T. castaneum. EO from Evodia lepta root barks possessed contact toxicity against T. castaneum adults with LD50 value of 166.94 μg/adult (Jiang et al., 2012). The toxicity of α-pinene with the highest content of 26.68% seemed to be weakened by other constituents. Antagonistic interaction of compounds was considered to be a possible affecting factor. Besides, the toxicity affecting factors include physical and chemical properties, penetration rate, reaction mechanism and metabolism. Thus, the hydrophobicity of the individual compounds may facilitate the penetration through the cuticle of insects (Habtemariam, 2017; Resende et al., 2016). Because the epicuticle of insects is mainly consist of hydrocarbons, proteins and lipids. Furthermore, the thickness and composition of the cuticle might be other important factor affecting insecticidal

effect, because the acting rate of detoxification enzymes is partially decided by the penetration rate of insecticide molecules (Balabanidou et al., 2018). E. lenticellata fruits have been used as Chinese medical herb (Ma, 2016). There are no toxicity data for this plant available on human consumption. 4.4. Repellent activity Essential oil from E. lenticellata fruits provided strong repellent efficiency against T. castaneum, after 2 h exposure, attaining Class Ⅴ at concentration of 78.63, 15.83, 0.63, and 0.13 nL/cm2. The PR became lower after 4 h exposure. But overall the repellent effect was basically stable (Class Ⅲ-Ⅴ). Except linalool, the other four compounds exhibited similar repellency against T. castaneum. As for L. serricorne, only EO and linalool showed 72% and 76% (Class Ⅳ) at the highest concentration, and no strong repellency (Class Ⅴ or Class Ⅳ) against L. serricorne were found from other treatments. Moreover, frequent attractive effect was observed during the whole testing time. Interestingly, Hori (2003) reported that linalool and β-caryophyllene attracted L. serricorne female at the dose of 0.1 μL and 1 μL, respectively (tested by olfactometer). This means that the attractive effect of these two compounds in our tests might be due to the dosage of the compounds. The mechanism of this phenomenon is still unknown, so the further study is needed. Against L. bostrychophila, the effective repellents (Class Ⅳ and Class Ⅴ) were recorded for the highest dose of 63.17 nL/cm2 at 2 h and 4 h. For all the treatments on L. bostrychophila, the repellency decreased with the decrease of concentration by and large. It is noteworthy that although the monoterpenes were more toxic than EO, the same was not observed for repellency activity. However, most of the monoterpenes showed repellent effect on three insects. The major pure metabolites, like linalool, 3-carene, caryophyllene oxide and limonene were also demonstrated to be effective repelling compounds against mosquitoes and beetles (Omolo et al., 2004; Odalo et al., 2005; Nerio et al., 2009; Tabari et al., 2017). Interestingly, caryophyllene oxide and β-caryophyllene exhibited moderate fumigant toxic effect but strong repellency to T. castaneum and L. bostrychophila adults. Among sesquiterpenes, β-caryophyllene was reported as a strong repellent against A. aegypti and S. zeamais (Gillij et al., 2008; Bougherra et al., 2014), and caryophyllene oxide showed strong repellency (more than 83%) to T. castaneum 347

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(Soonil et al., 2010). The lower volatility and molecular structural differences of these two compounds may account for the significant differences in insecticidal efficacy. Olfactory responses of insects depend on the interaction of chemicals with antennal sensillae (Yoon et al., 2011). A computational model revealed that the positive end is more favorable for receptor interactions (Wang et al., 2008). C = C maybe responsible for the repellent activity of these two compounds. Overall, insecticidal activity and repellency of E. lenticellata fruit essential oil against three stored-product insects, T. castaneum, L . serricorne and L. bostrychophila were tested in our present work. The results demonstrate that the E. lenticellata fruit EO or blends of linalool, βpinene, 3-carene, caryophyllene oxide and β-caryophyllene have potential for development of eco-friendly natural insecticides.

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