Insecticidal Activities

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Journal of Stored Products Research 39 (2003) 375384

Insecticidal activities of constituents identified in the essential

oil from leaves of Chamaecyparis obtusa against

Callosobruchus chinensis (L.) and Sitophilus oryzae (L.)

Il-Kwon Parka, Sang-Gil Leeb, Don-Hwa Choib,

Ji-Doo Parkb

, Young-Joon Ahna,

*aSchool of Agricultural Biotechnology, Seoul National University, Suwon 441-744, South Korea

bKorea Forest Research Institute, Seoul 130-712, South Korea

Accepted 12 March 2002

Abstract

Analysis by gas chromatographymass spectrometry led to the identification of 20 volatiles from the

steam distilled oil of the leaves from Chamaecyparis obtusa Siebold et Zuccarni. Seven constituents of the

oil were tested for contact and fumigant activity against adults of Callosobruchus chinensis (L.) andSitophilus oryzae (L.). Responses varied with compound and dose rather than increasing exposure time

beyond 1 or 2 days. In the impregnated-paper test with the constituents [bornyl acetate, (+)-limonene,

myrcene, a-phellandrene, a-pinene, sabinene and terpinolene], at 0.1 mg/cm2, bornyl acetate,

a-phellandrene and terpinolene caused 97%, 97% and 87% mortality, respectively, against C. chinensis

adults 1 day after treatment. At 0.05 mg/cm2, moderate activity was achieved with bornyl acetate (56%

mortality), a-phellandrene (75%) and terpinolene (55%). Against S. oryzae adults, at 0.26 mg/cm2,

terpinolene caused 93% mortality 2 days after treatment, whereas 80% mortality 4 days after treatment was

observed with bornyl acetate and a-phellandrene. The toxicity of these compounds was significantly

decreased at 0.18 mg/cm2. In a fumigation test with S. oryzae adults, bornyl acetate and terpinolene were

much more effective in sealed containers than in open ones, indicating that the insecticidal activity of these

compounds was largely attributable to fumigant action. These naturally occurring materials derived from

leaves of Chamaecyparis could be useful for managing populations of C. chinensis and S. oryzae. r 2002Elsevier Science Ltd. All rights reserved.

Keywords: Natural insecticide; Natural fumigant; Callosobruchus chinensis; Sitophilus oryzae; Chamaecyparis obtusa;

Essential oil; Bornyl acetate; a-phellandrene; Terpinolene

*Corresponding author. Tel.: +82-31-290-2462; fax: +82-31-296-1650.

E-mail address: [email protected] (Y.-J. Ahn).

0022-474X/02/$ - see front matterr 2002 Elsevier Science Ltd. All rights reserved.

PII: S 0 0 2 2 - 4 7 4 X ( 0 2 )0 0 0 3 0 - 9


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1. Introduction

The rice weevil, Sitophilus oryzae (L.) and the adzuki bean weevil, Callosobruchus chinensis (L.),

are two of the most widespread and destructive primary insect pests of stored cereals andstored legumes, respectively. Control of these insect populations around the world is

primarily dependent upon continued applications of organophosphorus and pyrethroid

insecticides and the fumigants methyl bromide and phosphine. These are still the most effective

treatments for the protection of stored food, feedstuffs and other agricultural commodities

from insect infestation. Although effective, their repeated use for decades has disrupted

biological control by natural enemies and led to outbreaks of other insect species and sometimes

resulted in the development of resistance. It has had undesirable effects on non-target organisms,

and fostered environmental and human health concerns (Champ and Dyte, 1976; Subramanyam

and Hagstrum, 1995; White and Leesch, 1995). The use of methyl bromide will be prohibited in

the near future because of its ozone depletion potential and high toxicity (Anonymous, 1993).These problems have highlighted the need for the development of selective insect-control

alternatives with fumigant action.

Many plant extracts and essential oils may be an alternative source of stored-product insect-

control agents (Hill and Schoonhoven, 1981; Konstantopoulou et al., 1992; Desmarchelier, 1994;

Shaaya et al., 1997) because they constitute a rich source of bioactive chemicals. Much effort has,

therefore, been focused on plant-derived materials as potential sources of commercial insect-

control agents. In a preliminary test, steam distilled oil of the leaves from Chamaecyparis obtusa

Siebold et Zuccarni, belonging to the family Cupressaceae, revealed good adulticidal activity

against S. oryzae and C. chinensis.

In the laboratory study described herein, we have examined the essential oil of C. obtusa leaves

for insecticidal constituents active against adults of S. oryzae and C. chinensis as well as for itsinsecticidal mode of action.

2. Materials and methods

2.1. Chemicals

Bornyl acetate, (+)-limonene, a-phellandrene, a-pinene and terpinolene were purchased from

Tokyo Kasei (Tokyo, Japan). Myrcene and sabinene were supplied by Aldrich (Milwaukee, WI,USA). All other chemicals were of reagent grade.

2.2. Insects

Cultures of the rice weevil, S. oryzae and the adzuki bean weevil, C. chinensis, were maintained

in the laboratory without exposure to any insecticide. They were reared on rice grain and adzuki

bean, respectively, in plastic containers (26 30 20cm3) at 25711C, 5060% r.h., and a 16:8

light:dark photoperiod.

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2.3. Sample preparation

The healthy, mature leaves ofC. obtusa were obtained from mature plants grown in Hongneung

Arboretum, Korea Forest Research Institute (Seoul, Korea) on August 1999, brought to thelaboratory, and analyzed the day after arrival. The leaves were cut into pieces (12 cm). They were

diluted with distilled water (800 ml) in a 2 l flask and steam distilled (1001C). Distillation

continued for 3 h, yielding 39 ml of white distillate. The distillate was extracted with 20 ml of

hexane.

2.4. Gas chromatographymass spectrometry

The essential oil of the Chamaecyparis leaves was analyzed on a gas chromatograph (HP6890)

mass spectrometer (JMS-600W, JEOL) (GCMS). The GC column was a 60 m 0.25 mm i.d.

DB-WAX (0.25mm film) fused silica capillary column (J&W Scientific, Folsom, CA, USA). TheGC conditions were as follows: injector temperature, 2101C; column temperature, isothermal at

501C for 15 min, then programmed to 2001C at 21C/min and held at this temperature for 15 min;

ion source temperature, 2001C. Helium was used as the carried gas at the rate of 0.8 ml/min. The

effluent of the GC column was introduced directly into the source of the MS. Spectra were

obtained in the EI mode with 70 eV ionization energy. The sector mass analyzer was set to scan

from 50 to 800 amu for 2 s. Compounds such as bornyl acetate, camphene, (+)-limonene,

myrcene, a-phellandrene, a-pinene, sabinene and terpinolene were identified by comparison with

retention times and the mass spectra obtained with the authentic standards on the GCMS system

used for analysis. When an authentic sample was not available, the identification was carried out

by comparison of mass spectra with those in the mass spectra library (The Wiley Registry of Mass

Spectral Data, 6th ed.).

2.5. Bioassay

The contact activities of seven of the constituents of the Chamaecyparis leaf essential oil against

adults of S. oryzae and C. chinensis were determined in impregnated-paper assays. Appropriate

amounts of each test compound in 100 ml methanol were applied to filter papers (Whatman No. 2,

5 cm diameter). Adults ofC. chinensis and S. oryzae were exposed to treatments for 1 day, and 2, 3

and 4 days, respectively. Controls received 100 ml methanol. After drying under a fume hood for

2 min, each filter paper was placed in the bottom of a vial (5 cm diameter 3.5 cm), and then 20

adults of S. oryzae (1014 days old) and 20 adults of C. chinensis (35 days old) were placed ineach vial and covered with a lid.

In a separate experiment, susceptibility of S. oryzae adults to the fumigant action of test

compounds was investigated according to the method of Kim and Ahn (2001) with a slight

modification. A filter paper (Whatman No. 2, 4.5 cm diameter) treated with 0.6 mg/cm2 of each

test compound in 100ml methanol was placed in the bottom lid of a plastic cylinder (5 cm

diameter 9 cm) with a wire sieve fitted at 3.5 cm above the bottom after which the lid was sealed.

Twenty adult weevils were placed on the sieve. This prevented direct contact of the weevils with

the test compounds. Each plastic cylinder was then either sealed with a lid, method A, or left

unsealed, method B. The insects were exposed for 24 days. Controls received 100 ml methanol.

I.-K. Park et al. / Journal of Stored Products Research 39 (2003) 375384 377


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Treated insects were held at 25711C, 5060% r.h., and a 16:8 light:dark photoperiod.

Cumulative mortalities were determined 1, 2, 3 and 4 days after treatment. All treatments were

replicated five times.

2.6. Statistical analysis

The percentage mortality was determined and transformed to arcsine square-root values for

analysis of variance (ANOVA). Treatment means were compared and separated by Scheffes test

at P 0:05 (SAS, 1990). Means (7SE) of untransformed data are reported.

3. Results

3.1. Composition of C: obtusa leaf essential oil

Fig. 1 shows a typical chromatogram of C. obtusa leaf volatiles using a DB-WAX fused silica

capillary column. The substances identified by GCMS in the leaf essential oil are represented in

Table 1. Analysis led to identification of 20 volatiles from the Chamaecyparis leaf oil. The main

constituents were (+)-limonene (13.4%), a-pinene (9.1%), bornyl acetate (8.8%), a-terpinyl

acetate (7.6%), myrcene (6.8%), elemol (6.6%), sabinene (6.4%), terpinolene (4.3%) and

widdrene (3.6%).

Fig. 1. Capillary gas chromatogram of C. obtusa leaf volatiles obtained by steam distillation with subsequent hexane

extraction. Temperature programmed from 501C (15 min isothermal) to 2001C at 21C/min on a 60 m 0.25 mm i.d. DB-

WAX column. The peak numbers correspond to the numbers in Table 1.



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3.2. Insecticidal activity with treated filter paper

The toxicity of the essential oil from the Chamaecyparis leaves against adults ofC. chinensis and

S. oryzae exposed to direct contact with the chemicals is recorded in Table 2. Responses varied

Table 1

Volatile compounds in steam-distilled oil of the leaves from C. obtusa identified by gas chromatographymass

spectrometry

Peak numbera Compound Mass spectral datab Retention time (min) Relative (%)

1 Camphene 93, 121, 41, 27, 79 16:11 1.6

2 Sabinene 93, 77, 41, 27, 121 21:12 6.4

3 Myrcene 93, 41, 69, 27, 53 25:06 6.8

4 (+)-2-Carene 93, 121, 136, 79, 105 26:14 5.5

5 Limonene 68, 93, 39, 27, 53 28:00 13.4

6 a-Pinene 93, 77, 41, 27, 121 31:58 9.1

7 Terpinolene 93, 121, 136, 79, 41 34:53 4.3

8 a-Cedrene 119, 93, 105, 204, 41 54:90 2.2

9 Bornyl acetate 43, 93, 121, 136, 79 55:34 8.8

10 Widdrene 121, 133, 105, 189, 204 57:57 3.6

11 d-Cadinene 161, 134, 204, 119, 105 58:59 1.6

12 a-Phellandrene 93, 77, 136, 41, 27 61:10 2.1

13 a-Terpinyl acetate 43, 121, 93, 136, 196 62:57 7.6

14 a-Elemene 161, 204, 119, 41, 105 63:50 3.2

15 b-Himachalene 119, 204, 134, 105, 93 64:37 1.5

16 a-Cadinene 161, 134, 204, 119, 105 66:21 2.3

17 Elemol 59, 93, 161, 81, 41 82:31 6.6

18 d-Selinene 189, 204, 161, 105, 91 86:31 2.4

19 a-Eudesmol 204, 149, 161, 189, 222 88:58 1.9

20 b-Eudesmol 59, 149, 164, 108, 41 89:25 1.5

aThe peak numbers correspond to the numbers in Fig. 1.bMajor fragmentation ions, base peak (listed first) and other ions in decreasing order of relative abundance.

Table 1

Table 2

Contact activities of essential oil of C. obtusa leaves against adults of C. chinensis and Sitophilus oryzae, using

impregnated-paper assaysa

Dose (mg/cm2) Mortality (%) mean7SEb, n 5

C. chinensisc S. oryzaed

0.26 9772a 8072a

0.13 6572b 3273b

0.06 2973c 672c

aEach datum represents the mean of five replicates, each set up with 20 adults.bMeans within a column followed by the same letter are not significantly different at P 0:05 (Scheffes test).cExposed for 24 h.dExposed for 48 h.

Table 2



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according to insect and dose. In a test with C. chinensis adults, the Chamaecyparis essential oil at

doses of 0.26 and 0.13 mg/cm2, caused 97% and 65% mortality, respectively. Against S. oryzae

adults, the oil gave 80% mortality at 0.26 mg/cm2, and the insecticidal activity of the oil was

significantly decreased at 0.13 mg/cm2. No mortality was obtained in the untreated controls.Table 3 shows the contact toxicity of seven constituents from the Chamaecyparis leaf essential

oil on C. chinensis adults. At a dose of 0.1 mg/cm2, bornyl acetate, a-phellandrene, terpinolene and

(+)-limonene caused 97%, 97%, 87% and 60% mortality, respectively. However, the insecticidal

activity of these compounds was significantly decreased at 0.05 mg/cm2. At a dose of 0.1 mg/cm2,

little or no insecticidal activity was achieved with myrcene, a-pinene and sabinene. There was no

mortality in the untreated controls.

Table 3

Contact activities of constituents of essential oil from C. obtusa leaves against C. chinensis female adults, using

impregnated-paper assaysa

Compoundb Dose (mg/cm2) Mortality (%) mean7SEc, n 5

Bornyl acetate 0.1 9772a

0.05 5672c

0.03 4572c

(+)-Limonene 0.1 6073c

0.05 1572d

0.03 371de

Myrcene 0.1 371de

0.05 0e

0.03 0e

a-Phellandrene 0.1 9772a

0.05 7572c

0.03 4674c

a-Pinene 0.1 0e

0.05 0e

0.03 0e

Sabinene 0.1 271de

0.05 0e

0.03 0e

Terpinolene 0.1 8774ab

0.05 5572c

0.03 1572d

aEach datum represents the mean of five replicates, each set up with 20 adults.bExposed for 24 h.cMeans within a column followed by the same letter are not significantly different at P 0:05 (Scheffes test).



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Data on the contact toxicity of the test compounds on S. oryzae adults are given in Table 4.

Responses varied according to compound and dose. Increasing the exposure time beyond 2 days

resulted in smaller increases in mortality. At a dose of 0.26 mg/cm2, terpinolene caused 93% and

95% mortality 2 and 4 days after treatment. Bornyl acetate and a-phellandrene gave 76% and70% mortality 2 days after treatment, respectively, and 80% mortality 4 days after treatment. At

0.18 mg/cm2, terpinolene gave 72% mortality 4 days after treatment, whereas toxicity of bornyl

acetate and a-phellandrene was significantly decreased. At 0.26 mg/cm2, weak or no contact

activity was obtained with (+)-limonene, myrcene, a-pinene and sabinene. No mortality was

obtained in the untreated controls.

3.3. Fumigant activity

The response ofS. oryzae adults to the fumigant action of terpinolene and bornyl acetate varied

with treatment method (Table 5). After 2 days exposure there was a significant difference(Po0:05) in the fumigant activity of terpinolene between exposure in a sealed cylinder (method A)

which resulted in 100% mortality and an open cylinder (method B) which resulted in 2%

Table 4

Contact activities of C. obtusa leaf essential oil-derived constituents against S. oryzae adults, using impregnated-paper

assaysa

Compound Dose (mg/cm2) Mortality (%) mean7SEb, n 5

Days after treatment

2 3 4

Bornyl acetate 0.26 7672b 8072a 8072b

0.18 3873de 4273bcd 5074cde

(+)-Limonene 0.26 3672de 5274bc 6173bcd

0.18 0h 0h 672h

Myrcene 0.26 1072fg 1472efg 2472fg

0.18 271gh 872fg 1272gh

a-Phellandrene 0.26 7073bc 8073a 8073b

0.18 472gh 1072efg 1872fgh

a-Pinene 0.26 1873ef 3073cde 3672def

0.18 0h 472gh 672h

Sabinene 0.26 871fg 2271def 3271efg

0.18 0h 672gh 1273gh

Terpinolene 0.26 9372a 9372a 9572a

0.18 5273cd 5673b 7273bc

aEach datum represents the mean of five replicates, each set up with 20 adults.bMeans within a column followed by the same letter are not significantly different at P 0:05 (Scheffes test).



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mortality. Similar differences in the response of S. oryzae adults to bornyl acetate vapor in

treatments A and B were observed. There was no mortality in the untreated controls.

4. Discussion

In East Asia, Chamaecyparis obtusa has long been considered to have natural medicinal

properties attributable to various compounds such as bornyl acetate, (+)-limonene, a-pinene, a-

terpinyl acetate, sesquiterpenes, sesquiterpene alcohols and hinokiic acid (Namba, 1993). Little

work has been done on its potential value for the management of stored-product insects, althoughthe antifungal activity of the essential oil of the Chamaecyparis leaves was noted (Kang et al.,

1993).

It has been recognized that some plant-derived insect-control agents could be developed into

products suitable for integrated pest management because they are selective to pests, have no or

little harmful action against non-target organisms or the environment. They act in many ways on

various types of pest complex and may be applied to the plant in the same way as other

agricultural chemicals (Arnason et al., 1989a; Schmutterer, 1992; Hedin et al., 1997). Many plant

extracts such as neem extract and essential oils are known to possess ovicidal, repellent and

insecticidal activities against various stored-product insects (Hill and Schoonhoven, 1981;

Desmarchelier, 1994; Shaaya et al., 1997). The insecticidal constituents of many plant extracts andessential oils against stored-product insects are mainly monoterpenoids such as (+)-limonene,

linalool, terpineol, carvacrol and myrcene (Coats et al., 1991; Regnault-Roger and Hamraoui,

1995; Ahn et al., 1998). Additionally, some plant-derived materials are highly effective against

insecticide-resistant insect pests (Arnason et al., 1989b; Ahn et al., 1997). In our study with seven

constituents of the Chamaecyparis leaf essential oil, the terpenoids bornyl acetate and terpinolene

revealed good adulticidal activity against C. chinensis and S. oryzae and this confirms their

usefulness as candidates for the control of insect pests in stored products. Bornyl acetate and

terpinolene are known to possess antifeeding activity against Hylobius pales (Herbst) (Salom et al.,

1994), larval growth-inhibiting effects against Choristoneura occidentalis (Freeman) (Zou and

Table 5

Fumigant activities of bornyl acetate and terpinolene against S. oryzae adultsa

Method Mortality (%) mean7SEb, n 5

Terpinolenec Bornyl acetatec

Days after treatment

2 3 4 2 3 4

A, vapor in closed container 100a 100a 100a 6674a 100a 100a

B, vapor in open container 271b 271b 1271b 0b 1072b 2072b

aEach datum represents the mean of five replicates, each set up with 20 adults.bMeans within a column followed by the same letter are not significantly different at P 0:05 (Scheffes test).cExposed to 0.6 mg/cm2.

Table 5



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Cates, 1997) and pheromonal effects against Periplaneta americana (L.) (Manabe and Nishino,

1983).

El-Nahal et al. (1989) stated that the exposure period appeared to be the more important factor

affecting the toxic effects of the vapors of Acorus calamus L. essential oil on adults of five stored-product insect species rather than the dosage. Similar results have been reported for the toxicity of

(Z)-asarone to adults of S. oryzae and Lasioderma serricorne (F.) (Park, 2000). However, the

adulticidal activity of (E)-anethole, fenchone and estragole against S. oryzae, C. chinensis and

L. serricorne is dependent upon both dose and exposure time (Kim and Ahn, 2001). In our study,

the adulticidal activity of bornyl acetate, a-phellandrene and terpinolene varied according to the

dose rather than the exposure time.

Volatile compounds of many plant extracts and essential oils are composed of alkanes,

alcohols, aldehydes and terpenoids, especially monoterpenoids, and exhibit fumigant activity

(Coats et al., 1991; Shaaya et al., 1997; Ahn et al., 1998; Kim and Ahn, 2001). The monoterpene

carvacrol is highly toxic to nymphs of Reticulitermes speratus (Kolbe) and adults of S. oryzae,C. chinensis and L. serricorne, and acts as a fumigant (Ahn et al., 1998). The phenylpropenes

(E)-anethole and estragole and the monoterpene fenchone have fumigant action against adults of

S. oryzae, C. chinensis and L. serricorne (Kim and Ahn, 2001). In our study, terpinolene and

bornyl acetate were much more effective against S. oryzae adults in sealed containers than in open

ones. These results indicate that the insecticidal mode of action of the compounds may be largely

attributable to fumigant action: they may be toxic by penetrating the insect body via the

respiratory system.

Results of this and earlier studies indicate that C. obtusa leaf essential oil-derived materials

might be useful for managing populations of S. oryzae and C. chinensis in enclosed spaces such as

storage bins, glasshouses, or buildings because of their fumigant action, provided that a carrier

giving a slow release of active material can be selected or developed.

Acknowledgements

This work was supported by grants from the Ministry of Agriculture and Forestry through the

R&D Promotion Center for Agriculture and Forestry and the Ministry of Education (Brain

Korea 21 Project) to Young-Joon Ahn.

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