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Efficacy of Elettaria cardamomum L.

(Zingiberaceae) essential oil on the two spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae)

Samaneh Fat emikia â , Habib Abbasipour â , Jaber Karimi â , Ayat allah Saeedizadeh â & Aziz Sheikhi Gorj an ^b

a Facult y of Agricult ural Sciences, Depart ment of Plant Prot ect ion , Shahed Universit y , Tehran , Iran

b Depart ment of Pest icides , Inst it ut e of Plant Prot ect ion of Iran , Tehran , Iran

Published online: 21 Aug 2013.

To cite this article: Archives Of Phyt opat hology And Plant Prot ect ion (2013): Ef f icacy of Elet t aria cardamomum L. (Zingiberaceae) essent ial oil on t he t wo spot t ed spider mit e, Tet ranychus urt icae Koch (Acari: Tet ranychidae), Archives Of Phyt opat hology And Plant Prot ect ion, DOI:

10. 1080/ 03235408. 2013. 828858

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Ef ﬁ cacy of Elettaria cardamomum L. (Zingiberaceae) essential oil on the two spotted spider mite, Tetranychus urticae Koch (Acari:

Tetranychidae)

Samaneh Fatemikiaâ, Habib Abbasipourâ*, Jaber Karimiâ, Ayatallah Saeedizadehâ and Aziz Sheikhi Gorjan^b

aFaculty of Agricultural Sciences, Department of Plant Protection, Shahed University, Tehran, Iran;^bDepartment of Pesticides, Institute of Plant Protection of Iran, Tehran, Iran

(Received 16 July 2013;ﬁnal version received 22 July 2013)

Two-spotted spider mite, Tetranychus urticae Koch is the major pest of various plants worldwide. Now the control is dependent on the use of chemical pesticides.

Plant compounds are recently known as biopesticides. Essential oil of Elettaria cardamomum was researched on repellent and oviposition inhibition of T. urticae.

The LC50values of fumigant toxicity of this oil on adults and eggs of the two spotted spider mite were 7.26 and 8.82μL/L air, respectively. Also LT50value of essential oil at 45μL/L air was 23.86 h and LT₅₀value of essential oil at 60μL/L air was 9.01 h. In addition, different concentrations of the essential oil of E. cardamomum signiﬁcantly affected oviposition deterrence and repellency of adults. The results of this study indicated that essential oil of E. cardamomum may be considered as a biopesticide to control two spotted spider mites.

Keywords:Elettaria cardamomum; essential oil;Tetranychus urticae; LC50

oviposition deterrence; repellency

Introduction

The two spotted spider mite, Tetranychus urticae Koch (Acarina: Tetranychidae) is a serious pest and it infests many crops causing reduction in plant productivity or even kills the host plants (Nachman & Zemek 2002; Zhang 2003). It attacks numerous greenhouse plantations causing a great problem. The ideal areas for spider mites are greenhouses that they can complete a generation in one week (Duzgunes & Cobanoglu 1983). Conventional synthetic pesticides such as chlorinated hydrocarbons, organophos- phates, carbamates and pyrethroids showed a temporary success in controlling this mite pest but late posed serious problems like pesticide resistance (Brattsten et al. 1986), secondary pest outbreak (Elzen 2001), pest resurgence and toxic residues in the environment (Frank et al. 1990) as well as effect on non-target organisms (Croft 1990).

Spider mites have evolved resistance to more than 80 acaricides to date, and resistance has been reported from more than 60 countries (DARP 2004). Plants have acquired effective defence mechanisms that ensure their survival under adverse environmental factors. In addition to morphological mechanisms, plants have also developed chemical defence mechanisms towards organisms such as insects and mites that affect the

*Corresponding author. Email: [email protected] Archives of Phytopathology and Plant Protection, 2013 http://dx.doi.org/10.1080/03235408.2013.828858

Ó2013 Taylor & Francis

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biochemical and physiological functions (Prakash & Rao 1997). The cardamom, Elettaria cardamomum (Zingiberaceae) is a pungent aromatic herbaceous perennial plant growing to 2–4 m in height. The leaves are alternate in two ranks, linear-lanceo- late, 40–60 cm long, with a long pointed tip. As well as in its native range, it is also grown in Nepal, Vietnam, Thailand, and Central America. In India, the states of Sikkim and Kerala are the main producers of cardamom; they rank highest both in cultivated area and in production. It was ﬁrst imported into Europe around 1300 BC (Abbasipour 2012). One of the alternative approaches, within pest control, which may be suitable for greenhouses, is using natural fumigants, because of their safety and capability to each every point in high-density plantation. Fumigant toxicity of several volatile oils was investigated against different pests (Stamopoulos 1991; Regnault-Roger & Hamraoui 1994; Don-Pedro 1996; Sammataro et al. 1998; Kim et al. 2004; Abbasipour et al.

2010; Abbasipour et al. 2011a, 2011b).

Up to now there are no published reports on acaricidal activity of the essential oil of E. cardamomum. Being a part of systematic evaluation of the acaricidal potential of the plants, the objective of this work investigated acaricidal properties of E.

cardamomum leaves essential oil. They included fumigant bioassay on eggs and adults, oviposition deterrence and repellency activity againstT. urticae.

Materials and methods Essential oil extraction

The seeds of the E. cardamomum were commercially prepared for extraction of the essential oil. The seeds were dried under indoor condition and were subjected to hydrodistillation using Clevenger type distiller (Cavalcanti et al. 2004). For extraction of essential oils, 50 g of air-dried plant materials was put in water (1:12 w:v) for distillation during 4 h. Extracted essential oils were dried via anhydrous sodium sulphate and stored at 4 °C in darkness. For fumigant bioassay tests, pure essential oil was used.

Tested mites

The strain of the two spotted spider mite,T. urticaeKoch was supplied from Acarology laboratory in Agriculture Faculty of University of Tehran. It was reared as a test strain as the following: lima bean (Phaseolus vulgariscv. Akhtar) seeds were planted in plastic jars (15 cm in diameter) at a rate of 4–5 seeds per jar, and incubated under muslin cage to prevent any infestation. Jars containing lima bean seedlings (15–20 cm long) were taken to the laboratory, then infested leaves ofT. urticaewere transferred to these plants and left to reproduce under laboratory condition at 25 ± 1 °C. This colony was supplied with fresh lima bean plants from time to time according to necessity.

Calculating LC₅₀and LT₅₀values of the oil

The fumigant toxicity of essential oil on T. urticae was tested in plastic vials (140 mL) and in each of them 30 adults of mite (1–3 days old) was released on the leaves of lima bean. Filter paper discs (Whatman No. 1) were cut into 2 cm diameter and were then attached to undersurface of screw caps of plastic vials. Filter papers were impregnated with series of concentrations ofE. cardamomumessential oil. After 24 h, the dead mites were recorded. Three replications were run for each concentration and for control groups. All tests were carried out in the growth chamber at 25 ± 1 °C and 70 ± 5% RH 2 S. Fatemikia et al.

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with a 16L:8D h photoperiod. To investigate the lethal time (LT50) of T. urticae, high concentrations of the essential oil was obtained and used from bioassay tests (60 and 45μL/L air). Selected concentrations similar to the mentioned method for bioassay test were tested and for each dose, three replications were performed. The mortality of mites was counted after 3, 6, 9, 12, 15, 18, 21 and 24 h and after that in 3 h intervals, mortality recording continued until 100% mortality was reached.

Toxicity of oil to the eggs

For contact toxicity assay with eggs,ﬁve individuals of T. urticaefemales were allowed to oviposit for 24 h on the 3 cm diameter of lima bean leaf discs resting on wet cotton pads in a Petri dish (9 cm in diameter). Then they were removed and the eggs were counted. The leaf discs containing 30 eggs were put in plastic vials and for 24 h submit- ted to different concentrations. The method of this test was similar to the one used for the adulticidal assay.

Oviposition deterrence

To investigate the effect of essential oil on the oviposition reduction, four concentrations (1500, 3000, 4500 and 7000 mg/L) of essential oil ofE. cardamomumwere prepared in mix of water and ethanol (70:30). For each treatment, 20:1 of various ethanol-water solutions was applied on the surface of leaves (3 cm in diameter). After evaporation of water and ethanol, two pairs (2 males and 2 females) of adults (3-old-days) ofT. urticae for each concentration and control were selected and were placed inside a plastic vial (140 mL). For control, only ethanol and water were separately used. For each concentration, 4 replications were performed.

The number of laid eggs was recorded after 24 h and oviposition deterrence was calculated with formulae as follows (Pascual-Villalobos & Robledo 1998).

%Oviposition deterrence¼ 1 NEt NEc

100

NEt = Number of eggs in treatment, NEc = Number of eggs in control.

Repellency test of oil

The repellency test of oil was made according to the method described by Kogan and Goeden (1970). Leaf discs of lima bean of 3 cm diameter were used to evaluate the repellency of the oil. Half of the disc was immersed into an ethanolic solution of the oil in four concentrations (1500, 300, 4500 and 7000 mg/L) for 5 s and after drying, the other half of the disc was immersed in the ethanol and water solution, which served as the control. Ten mite males and females were placed on each disc (ﬁve mites on each half of the leaf disc) and each treatment was repeated 4 times. The evaluation was made after 24 h when the numbers of mites present in each half of the leaf were counted. The repellency percentage (%R) of the oils was calculated according to the following equation:

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%R¼C T N 100

T= mite number in the treatment, C= number of mites in the control, N= number of used mites in the test.

Statistical analysis

The lethal concentrations (LC50 and LC90) and lethal time (LT50) values of mortality were assessed by probit analysis using SAS software (SAS-Institute 1997). The data from oviposition deterrence and repellency percentage were subjected to one-way ANOVA (p< 0.05) after checking for normality. Means were compared by Duncan’s new multiple Range Test, admitting signiﬁcant differences p< 0.05. The SAS software was used for all analyses (SAS-Institute 1997).

Results

Acaricidal activities of the essential oil

The LC50values of fumigant assay of E. cardamomumessential oil on adults and eggs of the two spotted spider mite after 24 h are indicated in Table 1. Values of LC50 bioassay on eggs and adults were 7.26 and 8.82μL/L air, respectively (Table 1).

Lethal time of mortality (LT⁵⁰)

Lethal time of mortality (LT50) of oil ofE. cardamomumonT. urticaeadults was 23.86 h for 45μL/L air concentration and was 9.01 h for 60μL/L air concentration (Table 2).

Oviposition deterrence of essential oil

Percentage of oviposition deterrence of various water concentrations and ethalonic solutions of E. cardamomum essential oil of on adults of T. urticae are shown in Table 3.

Table 2. Values of lethal time of mortality (LT50) ofE. cardamomum essential oil on adults of T. urticaeafter 24 h.

Concentration

(μL/L air) N df LT₅₀(h) LC₉₀(h) Slope ± SE χ² p-value

Adult 60 540 6 9.01 (7.04–10.86) 33.09 (24.60–56.00) 2.26 ± 0.36 0.30 0.96 Eggs 45 540 6 23.86 (18.25–43.12) 118.76 (56.72–920.53) 1.83 ± 0.45 0.28 0.92 Table 1. Fumigant toxicity of essential oil of E. cardamomum against eggs and adults of T. urticaeafter 24 h.

Stage N df LC50(μL/L air) LC90(μL/L air) Slope ± SE χ² p-value Adult 540 4 7.26 (6.88–7.68) 12.83 (11.36–15.52) 5.17 ± 0.61 2.62 0.62 Eggs 540 4 8.82 (8.56–9.15) 12.03 (11.19–13.41) 9.51 ± 0.94 1.08 0.89 4 S. Fatemikia et al.

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There were signiﬁcant differences between different tested concentrations (df = 3, F= 168.3,p< 0.0001) (Table 3). The highest reduction in oviposition rate was observed at 7000 mg/L.

Repellency effect of essential oil

Table 4 shows the repellency effect of E. cardamomum essential oil on adults of the two spotted spider mite. Essential oil had a signiﬁcant repellency on adults of T. urticae. Efﬁcacy of the high dose (7000 mg/L) was more than others (df = 2, F= 205.77,p= 0.0001) (Table. 4).

Discussion and conclusion

Efficacy of plant materials (extracts and essential oils) on various pests was reported in previous studies (Viglianco et al. 2008; Abbasipour et al. 2011a, 2011b). Many research- ers investigated efficiency of volatile oils from different families of plants against different mite species. In the current study, effect of essential oil of E. cardamomum on the adults, eggs, oviposition inhibition and detergency ofT. urticaewere investigated. Tunç and Şahinkaya (1998) proved the toxic effect of vapour of the essential oil of cumin, Cuminum cyminum L. to the carmine spider mite,Tetranychus cinnabarinus. They also reported that greenhouse pests were much more sensitive to the vapours of essential oils than stored-product pests. Oils from Artemisia absinthiumand Tanacetum vulgare were toxic against T. urticae (Chiasson et al. 2001). Cavalcanti et al. (2004) reported that materials of essential oil of Lippia sidoides Cham. had good efficiency on T. urticae.

Calmasur et al. (2006) investigated the acaricidal activity of Micromeria fruticosa L., Nepeta racemosaL. andOriganum vulgareL. (Lamiaceae).

Efﬁcacy tests ofE. cardamomum on adults and eggs of the two spotted spider mites show that this oil has a good vapour fumigant effect on this important pest. This is the ﬁrst study on the toxicity of E. cardamomum on a mite pest, although the essential oil Table 3. Percentage (±SE) of oviposition deterrence ofE. cardamomum essential oil on adults ofT. urticae.

Concentrations of essential oil (mg/L)

1500 3000 4500 7000

Mean of laid eggs 7.1 ± 0.43 a 19.9 ± 0.8 b 24.2 ± 0.9 c 30.6 ± 0.9 d Note: Means marked with the different letters are signiﬁcantly different (p< 0.05; Duncan) (df = 3,F= 168.3, p= 0.0001).

Table 4. Percentage (±SE) of repellency ofE. cardamomumessential oil on adults ofT. urticae.

Concentrations of essential oil (mg/L)

1500 3000 4500 7000

Mean of repellency 41.4 ± 0.68 a 52.9 ± 1.01 b 59.6 ± 0.35 b 67.9 ± 0.92 c Note: Means marked with the different letters are signiﬁcantly different (p< 0.05; Duncan) (df = 3,F= 205.77, p= 0.0001).

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was tested on the some insects in a few reports. Abbasipour et al. (2011b) stated that that essential oil of E. cardamomum toxic to the bruchid beetle, Callosobruchus maculatus Fabricius (Coleoptera: Bruchidae), the redflour beetle, Tribolium castaneum Herbst (Coleoptera: Tenebrionidae), and the flour moth, Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Adults of E. kuehniella were more sensitive than the Coleoptera and essential oil of E. cardamomum had a good efficacy on oviposition deterrence of C. maculatus females, too. Mahmoudvand, Abbasipour, Rastegar et al.

(2011) stated that essential oil of E. cardamomum had fumigant toxicity on Sitophilus granarius. Huang et al. (2000) demonstrates different responses of the egg stage and active stages of stored product insects to theE. cardamomumessential oil.

The tested essential oil in this study could be considered as potential alternative for synthetic miticides as their structures could lead to the development of a new type of miticidal compounds. However, further studies need to be conducted to evaluate the mode of action and cost-efﬁcacy of these essential oils on wide range of pests in commercial greenhouses.

Acknowledgement

This work was supported by Faculty of Agricultural Sciences, Shahed University, Tehran, Iran.

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