BIOLOGICAL
AND
MICROBIAL CONTROL
Insecticidal Potential of Clove Essential Oil and Its Constituents on Cacopsylla chinensis (Hemiptera: Psyllidae) in Laboratory and Field BAO-LIANG TIAN,1 QI-ZHI LIU,2 ZHI-LONG LIU,1 PENG LI,1 AND JIE-WEN WANG1
J. Econ. Entomol. 108(3): 957–961 (2015); DOI: 10.1093/jee/tov075
ABSTRACT Cacopsylla chinensis (Yang and Li) (Hemiptera: Psyllidae) is an important pest of pear in China. As an alternative to conventional chemical pesticides, botanicals including essential oils and their constituents could provide an eco-friendly and nonhazardous control method. In this study, the essential oil of clove buds (Syzygium aromaticum) was obtained by hydrodistillation. Five constituents, accounting for 99.89% of the oil, were identified by gas chromatography-mass spectrometry, and the major constituents were eugenol (88.61%) and eugenol acetate (8.89%), followed by b-caryophyllene (1.89%). In a laboratory bioassay, clove essential oil, commercial eugenol (99.00%) and b-caryophyllene (98.00%) exhibited strong contact toxicity against the summerform adults of C. chinensis with LD50 values of 0.730, 0.673, and 0.708 mg/adult, and against the nymphs with LD50 values of 1.795, 1.668, and 1.770 mg/nymph, respectively. In contrast, commercial eugenol acetate (98%) had LD50 values of 9.266 mg/adult and 9.942 mg/nymph. In a field trial, clove essential oil caused significant population reductions of 73.01% (4.80 mg/ml), 66.18% (2.40 mg/ml) and 46.56% (1.20 mg/ml), respectively. Our results demonstrated that clove essential oil and its constituents have potential as a source of natural insecticides. KEY WORDS pear psylla, Syzygium aromaticum, eugenol, contact toxicity Pear psylla, Cacopsylla chinensis (Yang and Li) (Hemiptera: Psyllidae) has been one of more important pests of commercial pears in Palearctic and Nearctic Region since it can suck the sap from young leaves, shoots, and buds (Luo et al. 2012). The most notable morphological characteristic of the adults is seasonal dimorphism (Horton et al. 1994), that is, they are small, light-colored (summer form) during growing season, then become large and dark in later autumn and winter (winter form) (Butt and Stuart 1986). High-density populations of C. chinensis can cause premature leaf drop, diminish plant growth, and reduce fruit size by sucking the sap of leaves, shoots, and fruits. In addition, they are also considered vectors of pear pathogens such as Erwinia amylovora Burrill (Hildebrand et al. 2000) and Candidatus Phytoplasma pyri (Carraro et al. 1998). Their honeydew promotes sooty mould on leaves and fruits (Shaltiel-Harpaz et al. 2014). At present, the traditional control of C. chinensis mainly depends on heavy usage of synthetic chemical insecticides, especially during the growing season. However, there are many drawbacks, such as toxic residues on fruits, disruption of the natural biological control systems and widespread development of resistance as well as undesirable effects on nontarget organisms (Isman 2000). It is urgent to look for new materials to
1 Department of Entomology, College of Agriculture and Biotechnology, China Agricultural University, Beijing, 100193, China 2 Corresponding author, e-mail:
[email protected]
control C. chinensis in an environmentally safe way. Previous studies suggested that plant essential oils and their constituents can be alternative sources for insect control, not just because they are selective, but also they can biodegrade to nontoxic products and have no negative effects on nontarget organisms and the environment (Isman 2006, Jiang et al. 2012, Liu et al. 2012). According to recent research, several botanicals, including essential oils and their constituents, have demonstrated good potential as natural insecticides against C. chinensis. These include garlic (Allium sativum) essential oil (Zhao et al. 2013), rapeseed oil (Marcˇic´ et al. 2009a), and crude alkaloids from the aerial parts of Macleaya cordata (Willd.) (Sun et al. 2004). During our mass screening program, the preliminary data suggests that essential oil of clove, Syzygium aromaticum (L.) Merrill and Perry (Myrtales: Myrtaceae), exhibits insecticidal activity against C. chinensis. Clove essential oil has been widely studied for its insecticidal and repellent activities against many species of pests (Chaieb et al. 2007, Kafle and Shih 2013, Corte´s-Rojas et al. 2014), such as Asian citrus psyllid (Mann et al. 2010); fire ants (Appel et al. 2004); termites (Pandey et al. 2012); cockroaches (Omara et al. 2013, Sharawi et al. 2013); mosquitoes (Trongtokit et al. 2005, Sutthanont et al. 2010); aphids (Rani 2004, Kareem et al. 2012); weevils (Ho et al. 1994, Kerdchoechuen et al. 2010, Mishra et al. 2013); moths (Oparaeke 2006, Birah et al. 2010). However, there is no report on the bioactivity against C. chinensis. So this study aims to evaluate the acute toxicity of clove essential oil and its major constituents against C. chinensis in the
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laboratory as well as the effectiveness of the crude oil in a field trial. Materials and Methods Source of Insects. C. chinensis were collected from 10-yr-old trees in a Whangkeumbae pear orchard, Shahe village, Daxing District, Beijing, China (39 370 N, 116 240 E, altitude 22 m) in June and early July, 2013. Adults were collected by sweep net, and nymphs were collected by collecting leaves. All the insects were fed with fresh pear leaves in an incubator [28 C, 90% relative humidity (RH), and a photoperiod of 15:9 L:D] for 24 h before experiment. Essential Oil and Chemicals. Each flask of 3,000 ml was filled with 500 g of dried clove buds purchased from Anguo Chinese Medicinal Herbs Market (Anguo, 071200, Hebei Province, China). After hydrodistillation for 6 h, the distillate was extracted with 1,000 ml of n-hexane. And then the hexane layer was further heated at 40 C on a water bath to concentrate the oil after which it was dehydrated with anhydrous sodium sulfate. The concentrated oil was kept in a refrigerator (4 C) for subsequent use. Eugenol (99.00%), eugenol acetate (98.00%), bcaryophyllene (98.00%), and abamectin (1.80%) were purchased from Aladdin-Reagent Company (Shanghai, China). Clove Essential Oil Analysis. Clove essential oil was analyzed by gas chromatography-mass spectrometry (GC-MS) on an Agilent 7890 instrument with split stream injector at 270 C. The HP-5 capillary column was 30 m 0.32 mm with a 0.25 mm film of a crosslinked methyl (95%) phenyl (5%) polysiloxane stationary phase. The initial oven temperature was held at 60 C for 1 min and increased at 10 C/min to 180 C held for 1 min and then ramped at 20 C/min to 280 C maintained for 15 min. The injection volume was 1ml (diluted 1:100 in acetone), and the split ratio was 1:10. The carrier gas was helium at a flow rate of 1.0 ml/min. GC-MS analysis was performed on a GC-MS 6890N gas chromatograph hooked to a 5973N mass selective detector. The GC conditions and capillary column were the same as earlier. The spectra were scanned from 20 to 550 m/z at two scans per second. Most constituents were identified by GC by comparison of retention indices with those found in the literature or those of authentic compounds. The retention indices were determined in relation to a homologous series of nalkanes (C8-C24, Sigma-Aldrich, St. Louis, and MO) under the same operating conditions. Further identification was made by comparing their mass spectra with those stored in NIST 05 and Wiley 275 libraries or with mass spectra from the literature. Relative percentages of the individual components of the essential oil were obtained by averaging the GC-flame ionization detector peak area% reports (Zhao et al. 2013). Laboratory Bioassay. Range-finding studies were run to determine the appropriate concentrations of the clove essential oil and its constituent compounds for determining LD50 values. Five concentrations of clove essential oil and its two constituents (eugenol and
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b-caryophyllene) were selected for adults (0.25–4.00 mg/ml) and nymphs (0.95–15.20 mg/ml). Five concentrations of eugenol acetate were used for adults and nymphs test at the range of 2.35–37.60 mg/ ml. Five concentrations of abamectin (0.01–0.16 mg/ml) were used for both the adults and nymphs as a positive control, and acetone alone was used as a negative control. Five replicates were prepared for each dose level. Petri dishes (9 cm diameter) were prepared with a wet paper disc and a fresh 8 cm diameter pear leaf. Groups of 10 third-fifth instar nymphs of C. chinensis were transferred directly into a prepared Petri dish by a fine camel’s hair brush as one replication. The adults were anesthetized by ether and transferred into a glass Petri dish which was placed on ice. An aliquot (0.5 ml) of oil or each component dilution was applied topically to the dorsal thorax of nymphs and adults using Burkard Arnold micro applicators (Burkard Scientific Supply, Rickmansworth, UK). Then the treated nymphs were kept in the prepared Petri dish. Groups of 10 treated adults were transferred into a prepared Petri dish as one replication as well. All the Petri dishes were put into an incubator with 28 C, 90% RH, and a long-day photoperiod of 15:9 (L:D). Mortality was recorded after 24 h. Adults and nymphs were considered dead if they failed to respond when probed with a fine camel’s hair brush. Field Trials. The field trial was also conducted in a Shahe pear orchard (1 ha) in July, 2013. There were a total of 21 plots for the 7 treatments (one blank control, three concentrations of clove essential oil, and detergent, respectively), and each plot consisted of 15 trees (3 rows 5 trees). There were three replications in each treatment (Erler et al. 2014). The clove essential oil was diluted to three different concentrations (1.20, 2.40, and 4.80 mg oil/ml) with tap water after being dissolved in detergent (1:1 v:v; as a surfactant, purchased from Beijing goldfish technology Co., LTD, Beijing, China). The same concentrations of detergent alone served as a negative control, and tap water was used as a blank control. The solutions were applied (about 1.5 liters per tree) in a completely randomized block design by atomizer (purchased from Alibaba, China) and the trees in one plot constituted a single treatment. The three trees in the center of each plot were chosen to look for live nymphs (first-fifth instar). Four branches (each branch has ca 25 leaves in 80 cm long) on each tree were observed randomly using a handheld magnifier (10) before treatment as well as 3 d after treatment. The percentages of nymphs’ corrected reduction (R%) by clove essential oil was calculated by using Henderson and Tilton’s equation (1955). R% ¼ ½1–ðNta =Nca Þ ðNcb =Ntb Þ 100 N ¼ number of nymphs per shoot; t ¼ treated plots; c ¼ control plots; a ¼ after treatment; b ¼ before treatment. Data Analysis. The relative mortality in the laboratory bioassay was corrected by control using Abbott’s
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formula. Results from all the replicates were subjected to probit analysis by using IBM SPSS Statistics 20.0 software to determine LD50 values. The field application data were analyzed using oneway Analysis of Variance (ANOVA) and presented as mean 6 SEM (standard error mean). The data of R% among control and treatments within concentrations were analyzed by ANOVA, followed by Duncan multiple mean separation techniques using IBM SPSS Statistics 20.0 software.
Results and Discussion Essential Oil Constituents. Five constituents were detected in the essential oil by GC-MS, accounting for 99.89%, and the major constituents were eugenol (88.61%), eugenol acetate (8.89%) and b-caryophyllene (1.89%) (Table 1). Chaieb et al. (2007), who found eugenol (88.58%), eugenyl acetate (5.62%), and b-caryophyllene (1.39%) in clove essential oil (Chaieb et al. 2007). Furthermore, Sigma-Aldrich Chemical Co. Ltd (Poole, England) indicate that the oil mainly contains eugenol (78.00%) and b-caryophyllene (13.00%) (Prashar et al. 2006). The difference may be caused by the variation of vegetative state, growing season and the places of origin (Srivastava et al. 2005, Fu et al. 2007, Samarasekera et al. 2008), Constituents of clove bud oils from India and Madagascar differ significantly with respect to eugenol (70.00 and 82.60%), b-caryophyllene (19.50 and 7.20%), and eugenyl acetate (2.10 and 6.00%), respectively (Srivastava et al. 2005). The clove essential oil we used was purchased from Nanyang, Henan Province of China, containing 68.52% eugenol, 19.00% b-caryophyllene, and 10.15% phenol acetate (Fu et al. 2007). Even though the constituents in clove bud oils can differ, there is no doubt that eugenol is the major constituent in clove essential oil in all places (Chaieb et al. 2007). Bioassay in Laboratory. Clove essential oil exhibited toxicity against the summerform adults of C. chinensis with an LD50 value of 0.730 mg/adult. Eugenol and b-caryophyllene had similar LD50 values of 0.673 and 0.708 mg/adult, respectively. Eugenol acetate possessed weaker toxicity with an LD50 value of 9.266 mg/ adult (Table 2). As to the nymphs, the essential oil, eugenol and b-caryophyllene possessed contact toxicity with LD50 values of 1.795, 1.668, and 1.770 mg/nymph, respectively and eugenol acetate had an LD50 value of 9.942 mg/nymph (Table 3). Consequently, the adults were more susceptible to the essential oil than the nymphs. However, compared with abamectin (LD50 ¼ 0.017 mg/adult and 0.021 mg/nymph), the currently used commercial insecticide (Tables 2 and 3), the clove essential oil was 43 times less toxic against the adults of C. chinensis and 84 times less toxic against the nymphs of C. chinensis. Moreover, eugenol was about 40 and 79 times less toxic than the positive control against summerform adults and nymphs of C. chinensis, respectively. Although the adults and nymphs were more susceptible to the positive control, clove essential
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Table 1. Chemical constituents of the essential oil derived from Syzygium aromaticum Peak 1 2 3 4 5 Total
Compound b
Eugenol b-Caryophylleneb a-Caryophyllene Eugenolacetateb Caryophyllene oxide
RIa
Peak area (%)
1,356 1,420 1,454 1,552 1,578
88.61 1.89 0.24 8.89 0.26 99.89
a RI (retention indice), determined on an HP-5MS column using the homologous series of n-hydrocarbons. b Identification by co-injection of authentic compounds.
Table 2. Probit analysis of the insecticidal activity of the clove essential oil and its constituents against the summer adults of Cacopsylla chinensis Treatment Clove essential oil Eugenol Eugenol acetate b-Caryophyllene Abamectin
LD50 (mg/adult)
95% Fiducial limit
Slope 6 SE
v2
P value
0.730 0.673 9.266 0.708 0.017
0.676–0.755 0.657–0.705 8.340–10.295 0.641–0.799 0.015–0.018
1.742 6 0.101 1.641 6 0.183 1.135 6 0.252 1.186 6 0.166 1.770 6 0.172
3.191 4.313 15.465 7.966 9.923
1.000 1.000 0.894 0.999 0.992
Table 3. Probit analysis of the insecticidal activity of the clove essential oil and its constituents against the nymphs of C. chinensis Treatment Clove essential oil Eugenol Eugenol acetate B-Caryophyllene Abamectin
LD50 95% (mg/nymph) Fiducial limit 1.795 1.668 9.942 1.770 0.021
1.782–1.819 1.410–1.842 8.911–10.987 1.595–1.941 0.019–0.023
Slope 6 SE
v2
1.092 6 0.141 5.983 0.253 6 0.133 7.233 0.932 6 0.230 16.914 1.241 6 0.133 6.432 1.363 6 0.166 9.475
P value 1.000 0.999 0.892 1.000 0.994
oil may be better for C. chinensis control because of its environmental safety (Chaieb et al. 2007). There are also other botanical essential oils with control potential, such as garlic oil (A. sativum) which possessed contact toxicity (LD50 ¼ 1.42 mg/adult) to overwintering adults of C. chinensis (Zhao et al. 2013) and AkseBio2 (a natural botanical essential oil mixture of thyme, oregano, anise, sesame oil, and maize oil plus a natural emulgator and a fluorescent bacterium, Pseudomonas fluorescens, TR 97) which showed strong activity against the nymphs of pear psylla, Cacopsylla pyri, with 87.40% mortality of younger nymph (first and second instars) and 62.10% mortality of the older (third-fifth instars) during 7 d at a concentration of 0.10% in laboratory (Erler 2004). Field Trial. Three days after treatment there were 46.56, 66.18, and 73.01% fewer C. chinensis nymphs with the essential oil at concentrations of 1.20, 2.40, and 4.80 mg/ml (1,200; 2,400; 4,800 ppm) in a field trial, respectively (Fig. 1). The result revealed that clove essential oil treatment could reduce the numbers of C. chinensis nymphs in a concentration-dependent manner. Although there was no significant difference between 2.40 and 4.80 mg/ml treatments (F ¼ 3.80, df ¼ 1, 17; P > 0.05), both produced greater reductions in nymph populations than in the 1.20 mg/ml treatment. Clove essential oil exhibited similar effects after 3 d to novaluron (750 ppm), which caused 62–70% nymph mortality of pear psylla (C. pyri) after 7 d
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The corrected percentage reduction of C. chinensis nymphs ( % )
80 a
Detergent Clove essential oil a
60
b
40
20 c c c
0 1.20
2.40
4.80
1.20
2.40
4.80
Concentration ( mg/ml )
Fig. 1. The corrected reduction rate of C. chinensis nymphs by foliar spray of clove essential oil or detergent in a field trial. Values shown in means 6 SE, calculated according to the equation of Henderson and Tilton. Means with the same letter were not significantly different (P < 0.05) in Duncan’s multiple range test (DMRT).
treatment (Erler et al. 2014), and AkseBio2 which caused 81.10% mortality of young nymphs and 52.70% mortality of older nymphs at 700 ppm after 7 d (Erler et al. 2007). But the clove essential oil was less active than azadirachtin (100 ppm), abamectin (13.5 ppm), and diflubenzuron (120 ppm), which were highly efficacious against nymphs (94.30–100%) (Marcˇic´ et al. 2009b). In conclusion, as a natural insecticide, the clove essential oil could be exploited in developing more effective strategies to prevent and control pear psylla. Furthermore, as clove essential oil is widely used as an herbal medicine and spice, it is generally recognized as safe to human health (Zheng et al. 1992, Naveena et al. 2006) and no phytotoxicity was observed in our pear trees even at 10,000 ppm (B.-L., unpublished data). The positive attributes of these constituents warrant further research into their potential development as an eco-friendly insecticide for pear psylla control in fruit production. Acknowledgments We would like to thank the support of China Agriculture Research System (CARS-29).
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