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Industrial Crops and Products 23 (2006) 140–146

Insecticidal and acaricidal effect of three Lamiaceae plant essential


oils against Tetranychus urticae Koch and Bemisia tabaci Genn.
Önder Çalmaşur, İrfan Aslan ∗ , Fikrettin Şahin
Atatürk University, Faculty of Agriculture, Plant Protection Department, 25240 Erzurum, Turkey

Received 30 June 2004; accepted 19 May 2005

Abstract

Tetranychus urticae Koch (Acari: Tetranychidae) and Bemisia tabaci Genn. (Homoptera: Aleyrodidae) are two economically
important pests of greenhouse vegetables and ornamentals. The management is commonly done based on repetitive applications
of chemicals, resulting in environmental pollution and resistance in pest population.
In the present study, essential oil vapours from Micromeria fruticosa L., Nepeta racemosa L. and Origanum vulgare L.
(Lamiaceae) were tested for toxicities against the nymphs and/or adults of T. urticae and the adults of B. tabaci. Amounts of the
essential oils applied were 2, 4, 6 and 8 ␮l in each of the desiccators with 4 l capacity, corresponding to 0.5, 1, 1.5 and 2 ␮l/l air.
The essential oil vapours of all three plant species caused the highest mortality in 2 ␮l/l air doses and at 120 h of exposure in both
of two pests’ species. In general, higher mortality was observed as the doses of essential oils and exposure period increased. T.
urticae was more tolerant than B. tabaci at all doses of essential oils in all times. The data may suggest that essential oils of all
three plants have potential to be used for management of T. urticae and B. tabaci pests in greenhouse conditions.
© 2005 Elsevier B.V. All rights reserved.

Keywords: Tetranychus urticae; Bemisia tabaci; Essential oil; Natural insecticide; Natural acaricide

1. Introduction monly controlled by applications of the synthetic insec-


ticides and acaricides (Choi et al., 2004). However,
Tetranychus urticae Koch (Acari: Tetranychidae) it is difficult to manage both of these pests in green-
and the white fly, Bemisia tabaci Genn. (Homoptera: house and/or fields by chemical applications due to
Aleyrodidae) are the major pests of greenhouse plants resistance. In addition, the use of different synthetic
in the world including Turkey. These pests are com- insecticides and acaricides as a pest control method,
in order to increase yields and protect stored prod-
∗ Corresponding author. Tel.: +90 442 231 1468;
ucts, may involve serious health hazards for Mammalia.
fax: +90 442 231 1469.
These insecticides and acaricides are often associ-
E-mail addresses: iaslan@atauni.edu.tr, aslanir@hotmail.com ated with residuals that are dangerous for the con-
(İ. Aslan). sumer and the environment (Lamiri et al., 2001). In

0926-6690/$ – see front matter © 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.indcrop.2005.05.003
Ö. Çalmaşur et al. / Industrial Crops and Products 23 (2006) 140–146 141

addition, the risk of developing insect resistance and the positions of essential oils from many medicinal plants
high cost–benefit ratio of synthetic pesticides pushed species including M. fruticosa, N. racemosa and O. vul-
research towards investigating alternative insecticides. gare plants collected from the eastern Anatolia region
The number of confirmed resistant insect and mite of Turkey (Bourrel et al., 1993; Güllüce et al., 2004;
species to synthetic pesticides has continued to rise, Şahin et al., 2004). In addition, some other biological
apart from risks associated with the use of these chem- activities of these plants species such as antimicrobial
icals (Campos et al., 1995; White, 1995). Therefore, and antioxidant properties have been studied up to now
in the current scenario, there is an urgent need to (Lamiri et al., 2001; Şahin et al., 2004; Güllüce et al.,
develop safer, environmentally friendlier and efficient 2004). However, there have been no attempts to study
alternatives that have potential to replace synthetic the toxicity of essential oils from these plants species
pesticides and are convenient to use. In the search on economically important pests in the greenhouses or
for alternatives to conventional pesticides, essential open field conditions.
oils extracted from aromatic plants have been widely The objective of this study was to assess in more
investigated. Their toxicities, arresting and repel- details the potential of essential oils to control pests of
lent effects to stored-product insects and greenhouse greenhouse crops. Greenhouses, like storehouses and
pests have been of special interest during the last beehives, are closed spaces where essential oil vapours
decade (Huang et al., 1997; Ho et al., 1997; Obeng- can be applied as fumigants. The toxicity of essential oil
Ofori and Reichmuth, 1997; Tunc and Sahinkaya, vapours obtained from three plant species, M. fruticosa,
1998; Landolt et al., 1999; Tunç et al., 2000; N. racemosa and O. vulgare to T. urticae and B. tabaci
Tripathi et al., 2000; Choi et al., 2003, 2004; Aslan was investigated.
et al., 2004).
In Turkey, aromatic plants widely separated and
there are a very rich and diversified flora, are famous 2. Material and methods
for their nutritional and medicinal characteristic.
They are used in various industries such as cos- 2.1. Plant material
metics, perfumes, detergents, as well as in pharma-
cology and food flavoring. In the world, to these M. fruticosa, N. racemosa and O. vulgare plants
rapidly evolving traditional sectors, a new industrial at flowering stage were collected from various local-
development could be added in the plant protection ities of Erzurum province in Turkey in the summer of
field. 2002. Plant taxonomists in the Department of Biology
Micromeria, Origanum and Nepeta are well known at Atatürk University, Erzurum, confirmed the taxo-
genera in the Lamiaceae family, and are typical nomic identification of plant species. Collected plant
Mediterranean plants. These genera are generally used materials were dried in shadow, and the leaves of plant
as traditional remedy to treat various ailments such were separated from the stem, and ground in a grinder
as a spasmodic, antimicrobial, insecticides, repellents, with a 2 mm diameter mesh. The voucher specimens
expectorant carminative and aromatic for whooping have been deposited at the herbarium of the Department
and convulsive coughs, digestive disorders and men- of Plant Protection at Atatürk University, Erzurum,
strual problems sedative, anesthetic, antiseptic, abor- Turkey.
tifacient, antirheumatic, CNS stimulant in addition to
the treatment of heart disorders and colds (Ietswaart, 2.2. Isolation of the essential oil
1980; Wollenweber, 1982; Kishore and Dwivedi, 1992;
Hallahan et al., 1998; Guner et al., 2000; Tabanca et al., The air-dried and ground aerial parts of plants col-
2001; Aligiannis et al., 2001; Lamiri et al., 2001; Şahin lected were submitted for 3 h to water-distillation using
et al., 2004). a Clevenger-type apparatus (yield 1.85%, v/w). The
Nepeta racemosa, Origanum vulgare and Microme- obtained essential oil (EO) was dried over anhydrous
ria fruticosa are three wild medicinal plants distributed sodium sulphate and, after filtration, stored at +4 ◦ C
mainly in the eastern Anatolia region of Turkey. In pre- until tested. For all plants were made the same as
vious studies, it has been determined the chemical com- replicate.
142 Ö. Çalmaşur et al. / Industrial Crops and Products 23 (2006) 140–146

2.3. Biological material ferences in the appearance of treated plants compared


with healthy controls were considered as the indication
T. urticae and B. tabaci were obtained from cultures of phytotoxicity.
maintained in the Plant Protection Department, Faculty
of Agriculture, Atatürk University and were reared on 2.6. Data analysis
tomato and bean plants (5-week-old), Phaseolus vul-
garis L., at 25 ± 1 ◦ C and 65 ± 5% r.h. and L13:D11. In order to determine if there is a statistically sig-
Tests were also carried out under the same conditions. nificant difference in toxicity among the insecticidal
and acaricidal activities and time, two-way using SPSS
2.4. Bioassays 10.0 software package carried out analyses of variance
(ANOVA).
Desiccators with a capacity of 4 l were used as test
chambers. Adults and/or nymphs of T. urticae and
adults of B. tabaci on fresh leaves of bean were exposed 3. Results
separately to the essential oils of M. fruticosa, N. race-
mosa and O. vulgare. A fine brush was used to transfer The insecticidal and acaricidal effects of three essen-
the nymphs and adults of T. urticae onto leaves. The tial oil vapours obtained from M. fruticosa, N. race-
leaves infested with B. tabaci were brought to desicca- mosa and O. vulgare against T. urticae and B. tabaci
tors. In order to maintain turgor of leaves, their petioles were summarized in Table 1 and Fig. 1. The results
were dipped through a hole made in a rubber cap fit- showed that all three essential oil have toxic effect
ted to 15 ml capacity glass vials filled with tap water. on both T. urticae and B. tabaci. There were signifi-
The control consisted of a similar setup but without cant differences between the mortality levels of both
essential oils. pests in terms of the essential oil concentrations and
Each replicate consisted of 20 T. urticae adults exposure times at P < 0.01 (Table 1). In general, higher
and/or nymphs and 20 B. tabaci adults placed on dif- mortality was observed as the doses of essential oils
ferent leaves. For each dose and exposure time com- and exposure period increased (Table 1 and Fig. 1).
bination, three replicates were used. The essential oils The mortality rates of T. urticae adult and/or nymph
were applied with an automatic pipette on a blotting with the treatment of M. fruticosa, N. racemosa and
paper strip (6 cm × 3 cm) attached to the bottom of the O. vulgare essential oils at highest doses (2 ␮l/l) for
desiccators. Initial testing was establishing appropriate 120 h exposure time were found to be 96.7, 95 and
dose and exposure time ranges. The amounts of essen- 95%, respectively. In the case of B. tabaci, all the adults
tial oils applied were 2, 4, 6, 8 ␮l in each desiccators, (100%) were dead at the highest concentration of all
corresponding to 0.5, 1, 1.5, 2 ␮l/l air. No material was essential oils tested (Table 1 and Fig. 1).
applied to the control desiccators. Exposure periods
were 24, 48, 96 and 120 h.
In order to determine mortalities in each exposure 4. Discussion
time, leaves with two-spotted spider mites or white flies
were removed from the desiccators and prodded with The results of the present study showed that essen-
a fine brush, if they did not move or fly, respectively, tial oils obtained from three aromatic plant species
they were considered to be dead. tested efficiently killed adults and/or nymphal stages
of T. urticae and adults B. tabaci. The acaricidal and
2.5. Phytotoxicity insecticidal activities were relatively enhanced with
increasing amount of doses and exposure times for all
Phytotoxicity of essential oils obtained from tested essential oils (Table 1 and Fig. 1). These results sug-
plants was determined by exposing tomato and bean gesting that essential oils of M. fruticosa, N. racemosa
plants to the highest dose (2 ␮l/l air) and the longest and O. vulgare may have great potential to be used for
exposure period (120 h) used in the test. Each plant effective managements of T. urticae and B. tabaci. A
species was exposed separately in desiccators. The dif- further study is also necessary to determine the toxicity
Table 1
The results of multiple comparison with mean and standard error of exposure time and dose of essential oil
Time (h) Dose Bemisia tabaci Tetranychus urticae Grand
(␮l/l air) Mean ± S.E.
M. fruticosa N. racemosa O. vulgare Mean ± S.E. M. fruticosa N. racemosa O. vulgare Mean ± S.E.
24 0.5 18.3 ± 2.0 23.3 ± 2.0 23.3 ± 2.2 21.76 ± 1.2 16.7 ± 2.0 18.3 ± 2.0 18.3 ± 2.2 17.8 ± 1.2 19.7 ± 0.8
1 30.0 ± 2.0 33.3 ± 2.0 35.0 ± 2.2 32.8 ± 1.2 28.3 ± 2.0 30.0 ± 2.0 28.3 ± 2.2 28.9 ± 1.2 30.8 ± 0.8

Ö. Çalmaşur et al. / Industrial Crops and Products 23 (2006) 140–146


1.5 48.3 ± 2.0 53.3 ± 2.0 55.0 ± 2.2 52.2 ± 1.2 51.7 ± 2.0 53.3 ± 2.0 51.7 ± 2.2 52.2 ± 1.2 52.2 ± 0.8
2 65.0 ± 2.0 68.3 ± 2.0 68.3 ± 2.2 67.2 ± 1.2 65.0 ± 2.0 60.0 ± 2.0 63.3 ± 2.2 62.8 ± 1.2 65.0 ± 0.8
Cont. 0.0 ± 2.0 0.0 ± 2.0 0.0 ± 2.2 0.0 ± 1.2 0.0 ± 2.0 0.0 ± 2.0 0.0 ± 2.2 0.0 ± 1.2 0.0 ± 0.8
Mean ± S.E. 32.3 ± 6.1d 35.7 ± 6.4d 36.3 ± 6.4d 34.8 ± 0.6 32.3 ± 6.3d 32.3 ± 6.0d 32.3 ± 6.2d 32.3 ± 0.6 33.5 ± 2.5
48 0.5 36.6 ± 2.0 38.3 ± 2.0 36.7 ± 2.2 37.2 ± 1.2 36.7 ± 2.0 38.3 ± 2.0 36.7 ± 2.2 37.2 ± 1.2 37.2 ± 0.8
1 46.6 ± 2.0 48.3 ± 2.0 48.3 ± 2.2 47.8 ± 1.2 45.0 ± 2.0 48.3 ± 2.0 46.7 ± 2.2 46.7 ± 1.2 47.2 ± 0.8
1.5 73.3 ± 2.0 75.0 ± 2.0 76.7 ± 2.2 75.0 ± 1.2 75.0 ± 2.0 76.7 ± 2.0 73.3 ± 2.2 75.0 ± 1.2 75.0 ± 0.8
2 83.3 ± 2.0 90.0 ± 2.0 86.7 ± 2.2 86.7 ± 1.2 86.7 ± 2.0 88.3 ± 2.0 83.3 ± 2.2 86.1 ± 1.2 86.4 ± 0.8
Cont. 0.0 ± 2.0 0.0 ± 2.0 0.0 ± 2.2 0.0 ± 1.2 0.0 ± 2.0 0.0 ± 2.0 0.0 ± 2.2 0.0 ± 1.2 0.0 ± 0.8
Mean ± S.E. 48.0 ± 7.9c 50.3 ± 8.4c 49.7 ± 8.3c 49.3 ± 0.6 48.7 ± 8.2c 50.3 ± 8.3c 48.0 ± 7.9c 49.0 ± 0.6 49.2 ± 3.2
96 0.5 58.3 ± 2.0 63.3 ± 2.0 58.3 ± 2.2 60.0 ± 1.2 63.3 ± 2.0 63.3 ± 2.0 63.3 ± 2.2 63.3 ± 1.2 61.7 ± 0.8
1 75.0 ± 2.0 76.7 ± 2.0 75.0 ± 2.2 75.5 ± 1.2 75.0 ± 2.0 76.7 ± 2.0 75.0 ± 2.2 75.5 ± 1.2 75.5 ± 0.8
1.5 91.7 ± 2.0 91.7 ± 2.0 90.0 ± 2.2 91.1 ± 1.2 83.3 ± 2.0 86.7 ± 2.0 85.0 ± 2.2 85.0 ± 1.2 88.1 ± 0.8
2 96.7 ± 2.0 96.7 ± 2.0 96.7 ± 2.2 96.6 ± 1.2 91.7 ± 2.0 88.3 ± 2.0 88.3 ± 2.2 89.4 ± 1.2 93.1 ± 0.8
Cont. 6.7 ± 2.0 6.7 ± 2.0 6.7 ± 2.2 6.7 ± 1.2 0.0 ± 2.0 0.0 ± 2.0 0.0 ± 2.2 0.0 ± 1.2 3.3 ± 0.8
Mean ± S.E. 65.7 ± 8.7b 67.0 ± 8.7b 65.3 ± 8.7b 66.0 ± 0.6 62.7 ± 8.8b 63.0 ± 8.7b 62.3 ± 8.7b 62.7 ± 0.6 64.3 ± 3.5
120 0.5 71.7 ± 2.0 71.7 ± 2.0 70.0 ± 2.2 71.1 ± 1.2 68.3 ± 2.0 66.7 ± 2.0 66.7 ± 2.2 67.2 ± 1.2 69.2 ± 0.8
1 85.0 ± 2.0 85.0 ± 2.0 86.7 ± 2.2 85.5 ± 1.2 86.7 ± 2.0 86.7 ± 2.0 83.3 ± 2.2 85.5 ± 1.2 85.5 ± 0.8
1.5 98.3 ± 2.0 98.3 ± 2.0 96.7 ± 2.2 97.8 ± 1.2 91.7 ± 2.0 90.0 ± 2.0 90.0 ± 2.2 90.5 ± 1.2 94.2 ± 0.8
2 100.0 ± 2.0 100.0 ± 2.0 100.0 ± 2.2 100.0 ± 1.2 96.7 ± 2.0 95.0 ± 2.0 95.0 ± 2.2 95.5 ± 1.2 97.8 ± 0.8
Cont. 10.0 ± 2.0 10.0 ± 2.0 10.0 ± 2.2 10.0 ± 1.2 11.7 ± 2.0 11.7 ± 2.0 11.7 ± 2.2 11.7 ± 1.2 10.8 ± 0.8
Mean ± S.E. 73.0 ± 8.9a** 73.0 ± 8.9a** 72.7 ± 8.9a** 72.9 ± 0.6 71.0 ± 8.4a** 70.0 ± 8.2a** 69.3 ± 8.1a** 70.1 ± 0.6 71.5 ± 3.4
Grand Mean ± S.E. 54.7 ± 4.4 56.5 ± 4.4 56.0 ± 4.4 55.8 ± 0.3 53.7 ± 4.3 53.9 ± 4.3 53.0 ± 4.2 53.5 ± 0.3 54.6 ± 1.7
** P < 0.01.

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Ö. Çalmaşur et al. / Industrial Crops and Products 23 (2006) 140–146
Fig. 1. Mortality (%) of adult Bemisia tabaci and Tetranychus urticae at different doses and exposure times.
Ö. Çalmaşur et al. / Industrial Crops and Products 23 (2006) 140–146 145

of these essential oils on other economically important terpinene, thymol, carvacrol, linalool, eugenol, methyl
pests in greenhouse conditions where pest management eugenol and methyl chavicol, which were reported to be
depends on chemical applications, which is causing poisonous to insect and mite pests (Isman et al., 2001;
environmental pollution and resistance in pest popu- Nostro et al., 2001; Pascual-Villalobus and Ballesta-
lation in nature (Lamiri et al., 2001). Acosta, 2003; Şahin et al., 2003, 2004; Güllüce et al.,
Our data demonstrated that the acaricidal and insec- 2004).
ticidal activities were relatively enhanced with increas- These results also suggested that for reasonable effi-
ing amount of doses and exposure times for all essential cacy on estimated amount of 2.5–3.5 l of M. fruticosa,
oils (Table 1 and Fig. 1). Similar findings were also N. racemosa and O. vulgare essential oils would be
reported in other studies showing the toxic effects of necessary for per 1000 m2 area of a greenhouse with-
essential oils obtained from some other aromatic plants out heating and cooling.
against insect and mite (Tunç et al., 2000; Tripathi et al., In conclusion, the essential oils from M. fruticosa, N.
2000; Choi et al., 2003, 2004). Essential oils obtained racemosa and O. vulgare may have potential to be used
from Satureja hortensis, Thymus vulgaris and Ocimum in sustainable management of T. urticae and B. tabaci
basilicum species efficiently killed adult and/or nymph in the greenhouses. However, further studies need to
stages of Tetranychus urticae and adult of Bemisia be conducted to evaluate the cost and efficacy of these
tabaci (Aslan et al., 2004). Tunc and Sahinkaya (1998) essential oils on wide range of pests in commercial
obtained 100% mortality with vapours of essential oils greenhouses.
from anise, cumin and oregano against the spider mite,
Tetranychus cinnabarinus, and aphids, Aphis gossypi
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