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Toxicity of Plant Essential Oils and Their Components Against

Lycoriella ingenua (Diptera: Sciaridae)

Article  in  Journal of Economic Entomology · March 2008

DOI: 10.1603/0022-0493(2008)101[139:TOPEOA]2.0.CO;2 · Source: PubMed

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 HORTICULTURAL ENTOMOLOGY

Toxicity of Plant Essential Oils and Their Components Against

Lycoriella ingenua (Diptera: Sciaridae)
IL-KWON PARK,1 JUNHEO N. KIM, YEON-SUK LEE, SANG-GIL LEE,
YOUNG-JOON AHN,2 AND SANG-CHUL SHIN
Division of Forest Insect Pests and Diseases, Korea Forest Research Institute, Seoul 130-012, Republic of Korea

J. Econ. Entomol. 101(1): 139Ð144 (2008)

ABSTRACT Plant essential oils from 20 plant species were tested for their insecticidal activity against
larvae of Lycoriella ingenua (Dufour) (Diptera: Sciaridae) by using a fumigation bioassay. Good
insecticidal activity (⬎90%) against larvae of L. ingenua was achieved with essential oils of caraway
seed [Carum carvi (L.)], lemongrass [Cymbopogon citratus (D.C.) Stapf.], mandarine (Citrus retic-
ulate Blanco), nutmeg (Myristica fragrans Houtt), cade (Juniperus oxycedrus L.), spearmint (Mentha
spicata L.), cumin (Cuminum cyminum L.), and thyme red [Thymus vulgaris (L.)] oils at 30 ⫻ 10⫺3
mg/l air. Among them, caraway seed, spearmint, cumin, and thyme red essential oils were highly
effective against L. ingenua at 20 ⫻ 10⫺3 mg/ml air. Analysis by gas chromatography-mass spectrometry
led to identiÞcation of 4, 9, 8, and 17 compounds from caraway seed, spearmint, cumin, and thyme
red oils, respectively. These compounds were tested individually for their insecticidal activities against
larvae of L. ingenua, and compared with the toxicity of dichlorvos. Carvacrol, thymol, linalool,
cuminaldehyde, p-cymen, terpinen-4-ol, and carvone was effective at 10 ⫻ 10⫺3 mg/l. The insecticidal
activity of dichlorvos was 60% at 10 ⫻ 10⫺3 mg/ml. Effects of four selected plant essential oils on growth
of oyster mushroom, Pleurotus ostreatus, also were investigated.

KEY WORDS plant essential oils, Lycoriella ingenua, fumigant

Six species of mushroom-infesting ßies have been re-
ported so far, including Lycoriella ingenua (Dufour)
(Diptera: Sciaridae) and Bradysia sp. in Korea (Kim
and Hwang 1996, Lee et al. 1999). Among them, L.
ingenua is the most serious pest of the commercial
mushroom industry. Flies of the family Sciaridae occur
almost worldwide (Lewandowski et al. 2004). Great
economic losses caused by various sciarid species in
the mushroom industry have been reported from Aus-
tralia (Clift 1979), the United States (Cantelo 1979,
White 1985), the United Kingdom (White 1985), and
South Korea (Kim and Hwang 1996).
Control of L. ingenua primarily depends on contin-
ued applications of synthetic pesticides such as diazi-
non, chlorpyrifos, carbofuran, dißubenzuron, and
methoprene (Kalberer and Vogel 1977, Cantelo and
McDaniel 1978, Kim et al. 2001). However, there are
environmental and human health concerns with syn-
thetic pesticides. To avoid these environmental and
health problems, there is a trend to search for naturally
occurring toxicants from plants. Plant essential oils
may provide potential alternatives to currently used L.
ingenua control agents because they constitute a rich
source of bioactive chemicals and they are commonly
1Corresponding author, e-mail: parkik1@forest.go.kr.
2College of Agricultural & Life Science, Seoul National University,
Seoul, Republic of Korea.
used as fragrances and ßavoring agents for foods and
beverages (Isman 2006). Commercial mushrooms are
cultivated in closed area such as a greenhouse in Ko-
rea. Because of high volatility, plant essential oils
would be more effective than nonvolatile pesticides to
control mushroom arthropod pests. In this study, we
selected 20 commercially available plant essential oils
widely used as fragrances and ßavoring agents and we
assessed their fumigant toxicity against larvae of L.
ingenua by using a fumigation bioassay.
Materials and Methods
Sources of Insects and Chemicals. Adult L. ingenua
were collected, by use of aspirators, in a mushroom
growing room at the Korea Forest Research Institute
(Seoul, Korea) in January 2005. They were then put
into petri dishes (87 mm in diameter) Þlled with Pleu-
rotus ostreatus grown on PDA medium. Flies were left
for 48 h at 22 ⫾ 1⬚C and 80% RH, and a photoperiod
of 16:8 (L:D) h to lay eggs. Hatching larvae were
reared with P. ostreatus under the same conditions.
S-(⫹)-carvone (purity 96%), R-(⫺)-carvone (purity
98%), 1,8-cineole (purity 99%), cuminaldehyde (pu-
rity 99%), (⫹)-limonene (purity 97%), trans-anethole
(purity 99%), and myrcene (purity 95%) were pur-
chased from Sigma-Aldrich (St. Louis, MO). Camphor
(purity 99%), p-cymene (purity 95%), ␥-terpinene

0022-0493/08/0139Ð0144$04.00/0 䉷 2008 Entomological Society of America

140 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 101, no. 1

Table 1. List of plant essential oils tested diameter, Whatman, Maidstone, United Kingdom),
and the treated Þlter paper was placed in the bottom
Oil Plant source Family lid of a glass cylinder (5 cm in diameter ⫻ 10 cm) with
Bay Pimenta racemosa Myrtaceae a wire sieve Þtted at 3.5 cm above the bottom after
Bergamot Citrus bergamia Rutaceae which lids were tightly sealed with sealing Þlm (What-
Cade Juniperus oxycedrus Cupressaceae
Caraway seed Carum carvi Apiaceae
man). Test insects were placed on the sieve. This
Citronella java Cymbopogon nardus Gramineae prevented direct contact of insects with the test plant
Cumin Cuminum cyminum Apiaceae oils and compounds. Twenty larvae (7Ð10 d old) were
Cypress Cupressus sempervirens Cupressaceae used in each replicate. A disk (1 cm in diameter) of P.
Geranium Pelargonium graveolens Geraniaceae
Grape fruit Citrus paradisi Rutaceae
ostreatus grown on PDA medium was supplied as food
Lavender Lavendula officinalis Lamiaceae for larvae. Controls received acetone. Treated insects
Lemongrass Cymbopogon citratus Gramineae were held at 22⫾1 ⬚C and 80% RH, and a photoperiod
Mandarine Citrus reticulata Rutaceae of 16:8 (L:D) h. Mortality was determined 1 d after
Nutmeg Myristica fragrans Myristicaceae
Palmarosa Cymbopogon martini Gramineae
treatment. All treatments were replicated Þve times.
Sage spanish Salvia officinalis Lamiaceae Nominal concentrations in the air in the glass cylinder
Spearmint Mentha spicata Lamiaceae were calculated using an assumption that all of the oils
Thyme red Thymus vulgaris Lamiaceae or compounds volatilized off the Þlter paper.
Vetiver haiti Vetiveria zizaniodes Gramineae
Wormwood Artemisia absinthium Asteraceae
Effect on Mycelial Growth of P. ostreatus. Effect of
Ylang ylang Canagaa odorata Annonaceae four essential oils on the mycelial growth of P. ostreatus
were examined by the method of Alvarez-Castellanos
et al. (2001). PDA plates were prepared using plastic
(purity 97%), terpinen-4-ol (purity 99%), and thymol petri dishes (87 mm in diameter). Agar-mycelial plugs
(purity 99%) were purchased from Fluka (Buchs, (7 mm in diameter) of P. ostreatus were inoculated at
Switzerland). Borneol (purity 70%), ␣-pinene (purity the center of the dish. The petri dishes were placed
95%), camphene (purity 80%), ␣-phellandrene (pu- with the lid upside down. Essential oil dissolved in
rity 98%), ␤-caryophyllene (purity 90%), carvacrol acetone were introduced onto a paper disc (8 mm in
(purity 95%), and ␤-pinene (purity 94%) were pur- diameter, Advantec, Tokyo, Japan), and the disc was
chased from Tokyo Kasei (Tokyo, Japan). Linalool placed on the lid without agar. Controls received ac-
(purity 98%) was from Wako Pure Chemicals (Osaka, etone. The treatments were incubated at 28⬚C in the
Japan). Dichlorvos (purity 99.5%) was purchased dark. Colony growth diameter was measured after the
from Chem Service (West Chester, PA). fungal growth in the control treatment had completely
Essential Oil. Plant species used are listed in Table covered the petri dishes. All treatments were repli-
1. Twenty plant samples were purchased from Jin cated four times.
Aromaticis (Anyang, Kyunggi Province, Korea). Growth inhibition of treatment against control was
Gas Chromatography-Mass Spectrometry. The es- calculated by percentage, using the following formula:
sential oils of caraway seed [Carum carvi (L.)], spear-
% Inhibition ⫽ C ⫺ T/C ⫻ 100
mint (Mentha spicata L.), cumin (Cuminum cyminum
L.), and thyme red [Thymus vulgaris (L.)] were an- where C is an average of four replicates of hyphal
alyzed on a gas chromatograph (model 6890N)-mass extension (millimeters) in control, and T is an average
spectrometer (model 5973N MSD) (Agilent Technol- of four replicates of hyphal extension (millimeters) of
ogies, Palo Alto, CA) equipped with a DB-5MS column plates treated with either the essential oil or an indi-
(30 m ⫻ 0.25 mm i.d., 0.25-␮m Þlm thickness, J & W vidual compound.
ScientiÞc, Folsom, CA). The oven temperature was Statistical Analysis. Larval mortality and mycelial
programmed as follows: isothermal at 40⬚C for 1 min, growth inhibition were transformed to arcsine square
then raised to 250⬚C at 6⬚C /min and held at this root values for analysis of variance (ANOVA). Treat-
temperature for 4 min. Helium was used as the carrier ment means were compared and separated by Schef-
gas at the rate of 1.5 ml/min. Efßuent of the GC féÕs test (SAS Institute 1999).
column was introduced directly into the source of the
MS via a transfer line (280⬚C). Ionization was obtained
Results
by electron impact (70 eV, source temperature
230⬚C). Scan range was 25Ð 800 amu. Compounds were Insecticidal Activity of Plant Essential Oils. When
tentatively identiÞed by comparison of mass spectra of 20 plant essential oils were bioassayed, mortalities
each peak with those of authentic samples in the NIST varied according to dose (Table 2). Of these, seven
MS library. Retention times for comparison with au- essential oils gave ⱖ90% mortality at 30 ⫻ 10⫺3 mg/ml
thentic compounds were measured with DB-1MS and air. At 20 ⫻ 10⫺3 mg/ml air, caraway seed, spearmint,
DB-FFAP column (30 m ⫻ 0.25 mm i.d., 0.25-␮m Þlm cumin, and thyme red gave ⬎90% mortality. Caraway
thickness, J & W ScientiÞc). The GC temperature seed oil exhibited 94% mortality at 10 ⫻ 10⫺3 mg/ml
conditions were the same as described above. air, whereas the insecticidal activity of the oil was
Bioassay. Insecticidal activity was evaluated using a signiÞcantly lower at 5 ⫻ 10⫺3 mg/ml air. Spearmint
fumigation bioassay. An appropriate concentration of oil showed 98 and 28% mortality at 10 and 5 ⫻ 10⫺3
each plant essential oil dissolved in acetone was ap- mg/ml air, respectively. Thyme red oil gave 92 and
plied to a Þlter paper (Whatman no. 2, 4.5 cm in 70% mortality at 10 and 5 ⫻ 10⫺3 mg/ml air, respec-
February 2008 PARK ET AL.: TOXICITY OF PLANT ESSENTIAL OILS 141

Table 2. Fumigant activity of various concentrations (10ⴚ3 mg/ml air) of plant essential oils against larvae of L. ingenua

Mortality (mean ⫾ SE, %)

Essential oil
30 20 10 5 2.5
Bay 2 ⫾ 0.20f
Bergamot 66 ⫾ 0.24b
Cade 94 ⫾ 0.40a 8 ⫾ 0.58c
Caraway seed 100a 100a 94 ⫾ 0.24a 22 ⫾ 0.58b
Citronella java 48 ⫾ 0.58bc
Cumin 100a 92 ⫾ 0.49a 40 ⫾ 0.55b 20b
Cypress 16 ⫾ 0.24def
Geranium 26 ⫾ 0.24de
Grape fruit 36 ⫾ 0.40cde
Lavender 62 ⫾ 0.37b
Lemongrass 98 ⫾ 0.20a 48 ⫾ 0.49b
Mandarine 100a 42 ⫾ 0.58b
Nutmeg 100a 38 ⫾ 0.80b
Palmarosa 4 ⫾ 0.24f
Sage spanish 42 ⫾ 0.49cd
Spearmint 100a 100a 98 ⫾ 0.20a 28 ⫾ 0.37b
Thyme red 100a 100a 92 ⫾ 0.37a 70 ⫾ 0.45a 34 ⫾ 0.40a
Vetiver haiti 0f
Wormwood 24 ⫾ 0.24de
Ylang ylang 0f
Control 0f 0c 0c 0c 0b

Means within a column followed by same letters are not signiÞcantly different (P ⫽ 0.05; ScheffÕs test).

tively, but mortality decreased to 34% at 2.5 ⫻ 10⫺3
mg/ml air. Insecticidal activity of lemongrass [Cym-
bopogon citratus (D.C.) Stapf.] and cumin was ⬍50%
at 10 ⫻ 10⫺3 mg/ml air.
Chemical Components of Four Essential Oils. Fig.
1 shows a chromatogram of four active essential oils by
using a DB-1MS fused silica capillary column (30 m ⫻
0.25 mm i.d., 0.25-␮m Þlm thickness, J & W ScientiÞc).
Main components of caraway seed oil were ␤-pinene
(0.13%), myrcene (0.22%), limonene (43.4%), and (⫹)-
carvone (53.6%). The most abundant compound in
cumin oil was p-cymene (27.92%) followed by ␥-ter-
pinene (23.57%), cuminaldehyde (19.08%), ␤-pinene
(11.26%), trans-anethole (2.66%), ␣-phellandrene
(0.91%), ␣-pinene (0.89%), and myrcene (0.77%).
Nine compounds such as ␣-pinene (0.17%), ␤-pinene
(0.43%), myrcene (1.3%), 1,8-cineole (1.8%), li-
monene (19.3%), ␥-terpinene (0.47%), terpinen-4-ol
(1.12%), (⫺)-carvone (63.2%), and ␤-caryophyllene
(1.18%) were identiÞed in spearmint oil. Total 17 com-
pounds were identiÞed in thyme red oil. Thymol
(47.36%) was the most abundant followed by
p-cymene (19.59%), ␥-terpinene (7.67%), linalool
(4.12%), carvacrol (3.31%), and borneol (2.32%). The
other compounds were contained ⬍2%.
Insecticidal Activity of Individual Compounds. In-
secticidal activity of compounds identiÞed in four ac-
tive essential oils and dichlorvos are shown in Table 3.
Among test compounds, carvone, terpinen-4-ol,
p-cymene, cuminaldehyde, linalool, carvacrol, and
thymol showed very strong activity, but the other test
compounds showed ⬍50% mortality at 10 ⫻ 10⫺3
mg/ml air. Mortality of carvacrol was high at 2.5 ⫻
10⫺3 mg/ml air, but decreased to 2% at 1.25 ⫻ 10⫺3
mg/ml air. Insecticidal activity of carvone, terpinen-
4-ol, linalool, and cuminaldehyde was ⬍20% at 2.5 ⫻
10⫺3 mg/ml air. Carvacrol, carvone, cuminaldehyde,
p-cymene, linalool, terpinen-4-ol, and thymol were
more effective than dichlorvos at 10 ⫻ 10⫺3 mg/ml air.
However, only carvacrol was more effective than di-
chlorvos at 2.5 ⫻ 10⫺3 mg/ml air.
Inhibition Effect on Growth of P. ostreatus. Effects
of four active essential oils on the mycelial growth of
P. ostreatus are shown in Table 4. Inhibition rates of
caraway seed oil was 0% at 79 ⫻ 10⫺3 mg/ml air.
Spearmint and cumin oils did not inhibit the mycelial
growth of P. ostreatus at 39 ⫻ 10⫺3 mg/ml air. Among
test oils, thyme red oil inhibits the mycelial growth of
P. ostreatus at lowest concentration.
Discussion
Plant essential oils have potential for L. ingenua
control because many of them have no or little harmful
effects on environment and human, and they may be
applied in the same way as conventional insecticides.
Many plant essential oils are known to posses ovicidal,
repellent, and insedicidal activities against arthropod
pests (Isman 2000). Additionally, some plant essential
oils were highly effective against L. ingenua larvae
(Park et al. 2006a, 2006b). In the current study, potent
insecticidal activity was observed with caraway seed,
cumin, spearmint, and thyme red oil. These essential
oils might be good candidates for naturally occurring
L. ingenua control agents because of low cost, a result
of their extensive worldwide use as fragrances and
ßavoring. Furthermore, there is a potential that these
oils could be used for the control of greenhouse pests
(Isman 2006).
Chemical components of caraway seed, cumin,
spearmint, and thyme red oils have been well studied
(Kokkini et al. 1996. Bailer et al. 2001, šipailienė 2006,
Gachkar et al. 2007). Similar results were obtained in
our analysis, although there was some difference in
142 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 101, no. 1

Fig. 1. Gas chromatograms of four active essential oils. Caraway seed (A): 1, ␣-pinene (0.13%); 2, myrcene (0.22%); 3,
limonene (43.44%), 4, (⫹)-carvone (53.66%). Cumin (B): 1, ␣-pinene (0.89%); 2, ␤-pinene (11.26%); 3, myrcene (0.77%);
4, ␣-phellendrene (0.91%); 5, p-cymene (27.92%); 6, ␥-terpinene (23.57%); 7, cuminaldehyde (19.08%); 8, trans-anethole
(2.66%). Spearmint (C): 1, ␣-Pinene (0.17%); 2, ␤-pinene (0.43%); 3, myrcene (1.34%); 4, 1,8-cineole (1.82%); 5, limonene
(19.37%); 6, ␥-terpinene (0.47%); 7, terpine-4-ol (1.12%); 8, (⫺)-carvone (63.22%); 9, ␤-caryophyllene (1.18%). Thyme red
(D): 1, ␣-pinene (1.40%); 2, camphene (1.27%); 3, ␤-pinene (0.27%); 4, myrcene (1.87%); 5, ␣-phellendrene (0.19%); 6,
␣-terpinene (1.43%); 7, p-cymene (19.59%); 8, 1,8-cineole (0.63%); 9, limonene (0.59%); 10, ␥-terpinene (7.67%); 11, linalool
(4.12%); 12, camphor (1.12%); 13, borneol (2.32%); 14, terpinen-4-ol (1.10%); 15, thymol (47.36%); 16, carvacrol (3.31%); 17,
␤-caryophyllene (1.47%).

ratio of some chemicals. Ogihara and Takeda (1990)
already reported that the essential oil content can vary
markedly, depending on growing conditions. In fumi-
gation test with individual compound identiÞed in
caraway seed, cumin, spearmint, and thyme red oils,
there was a big difference in insecticidal activity
among functional groups. Phenol, alcohol, aldehyde,
and ketone compounds were generally more toxic
than hydrocarbons. Two phenols (carvacrol and thy-
mol) showed strong insecticidal activity at 10 ⫻ 10⫺3
mg/ml air, but there was a big difference in insecti-
cidal activity at 5 ⫻ 10⫺3 mg/ml air. The position of
hydroxyl group is the only difference in chemical
structure of two phenols. This result indicates that
February 2008 PARK ET AL.: TOXICITY OF PLANT ESSENTIAL OILS 143

Table 3. Fumigant activity of various concentrations (10ⴚ3 mg/ml air) compounds identified in four essential oils against larvae of
L. ingenua

Mortality (mean ⫾ SE, %)

Compounda
10 5 2.5 1.25
Borneol 30 ⫾ 0.32de
Camphene 16 ⫾ 0.24e
Camphor 0f
Carvacrol 100a 100a 92 ⫾ 0.37a 2 ⫾ 0.20a
(⫹)-Carvone 100a 100a 16 ⫾ 0.24bc
(⫺)-Carvone 100a 100a 12 ⫾ 0.20bc
␤-Caryophyllene 0f
1,8-Cineole 2 ⫾ 0.20f
Cuminaldehyde 100a 98 ⫾ 0.20a 12 ⫾ 0.20bc
p-Cymene 100a 4 ⫾ 0.24c
Linalool 100a 100a 12 ⫾ 0.49bc
Myrcene 2 ⫾ 0.20f
␣-Phellendrene 0f
␣-Pinene 0f
␤-Pinene 32 ⫾ 0.58cde
␥-Terpinene 48 ⫾ 0.37bc
Terpinen-4-ol 100a 100a 2 ⫾ 0.20c
Thymol 84 ⫾ 0.51a 10 ⫾ 0.63c
Dichlorvos 60 ⫾ 0.32b 42 ⫾ 0.37b 24 ⫾ 0.24b 0b

Means within a column followed by same letters are not signiÞcantly different (P ⫽ 0.05; ScheffÕs test).
a
Limonene and trans-anethole were not tested because their activity against L. ingeuea was obtained previously (Park et al. 2006a, 2006b).

position of hydroxyl group is closely related to the
activity. There is no difference in activity of (⫹)- and
(⫺)-carvone.
Kalberer and Vogel (1977) reported that carbofu-
ran decreased the output of Agaricus bisporus when it
was applied for control of Lycoriella auripila (Fitch).
Cantelo (1981) investigated the effect of seven com-
mercial pesticides on mushrooms growth. In our
study, caraway seed oil did not inhibit the mycelial
growth of P. ostreatus at 79 ⫻ 10⫺3 mg/ml air. Inhi-
bition rates of spearmint and cumin oil were 34.5 and
73.6% at 79 ⫻ 10⫺3 mg/ml air, respectively, but no
inhibition was observed at 39 ⫻ 10⫺3 mg/ml air. These
three plant essential oil showed 100% insecticidal ac-
tivity at 30 ⫻ 10⫺3 mg/ml air, and this result indicates
that caraway seed, spearmint and cumin oils might be
useful for control of L. ingenua without any deleterious
effect on the mycelial growth of P. ostreatus. Thyme
red oil did not inhibit the mycelial growth of P. os-
treatus at 9 ⫻ 10⫺3 mg/ml air, but inhibition rate
increased to 100% at 19 ⫻ 10⫺3 mg/ml air. Proper
Table 4. Effect of four essential oils on the growth of P.
ostreatus
Conc., 10⫺3
Essential oil
mg/l
Caraway seed 79
Spearmint 158
79
39
Cumin 158
79
39
Thyme red 19
9 0d
Means within a column followed by same letters are not signiÞ-
cantly different (P ⫽ 0.05; ScheffÕs test).
concentration of thyme red oil should be applied to
minimize deleterious effect on the mycelial growth of
P. ostreatus when applied in greenhouse.
Results of our study indicate that some plant essen-
tial oils could be useful as fumigants for L. ingenuea.
For the practical use of these oils as novel fumigants,
further study is necessary on the safety of these ma-
terials to humans and on development of formulations
to improve efÞcacy and stability, and to reduce cost.
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