Efficacy of some Plant Essential Oils as Green Insecticides to Control Whitefly, Bemisia tabaci (Gennadius)

Efficacy of some Plant Essential Oils as Green Insecticides to Control Whitefly, Bemisia tabaci (Gennadius)
IJEN
Efficacy of some Plant Essential Oils as Green Insecticides
to Control Whitefly, Bemisia tabaci (Gennadius)
1Heba Youssif El-Sayed Ibrahim* and Mohamed El-Hoseiny Mostafa2
1,2Plant Protection Research Institute, Agriculture Research Center (ARC), Dokki, Giza, 12618, Egypt.
Ten plant essential oils were extracted and then tested for their activity as natural insecticides
against the whitefly, Bemisia tabaci (Gennadius). In-vitro bioassay, the contact toxicity of the
tested essential oils to eggs and 3rd
instar nymphs was determined. The most effective of tested
essential oils as ovicides were Artemisia absinthium, Cyperus articulates, and Thyme vulgaris
with LC50: 0.157, 0.305 and 0.334 ppm, respectively. Also, the most effective oils against 3rd
instar
nymphs were A. absinthium followed by C. articulates, and T. vulgaris with LC50: 7.268, 7.865 and
8.989 ppm respectively. Repellency effect and oviposition deterrency of the tested essential oils
were studied through choice and no-choice tests. The most repellents and anti-oviposition oils
were A. absinthium, T. vulgaris, C. articulates and Pluchea dioscoridis in both choice and no-
choice tests. Also, the efficacy of the most effective oils in the laboratorial experiments were
tested against B. tabaci in open field conditions. The most efficient one was A. absinthium which
showed great reduction percentage of B. tabaci populations (87.6%), followed by C. articulates
(85.0%), T. vulgaris (81.9%), Mentha longifolia (78.6%) then Syzygium aromaticum (51.7%).
Keywords: Bemisia tabaci, Essential oils, contact toxicity, repellency and oviposition deterrency.
INTRODUCTION
The sweet potato whitefly, Bemisia tabaci (Gennadius)
(Hemiptera: Aleyrodidae) is a polyphagous and multivoltine
insect pest in the field and greenhouses (Oliveira et al.,
2001) with great economic impacts on many crops such as
cotton, vegetables, fruit crops and ornamentals (Gerling,
1990 and Omid Bakhsh et al., 2010). Whiteflies damage
plants directly by sucking plant sap causing the silvering of
leaves, irregular colour of fruits and growth stunting
especially in young plants. And indirectly, whiteflies
transmit several plant viruses (Lapidot and Polston, 2006).
B. tabaci transmits plant viruses in seven distinct groups
including: potyviruses, geminiviruses, carlaviruses,
closteroviruses, nepoviruses, luteoviruses and DNA-
containing rod-shaped virus (Thompson, 2011). Also, they
excrete honeydew which stimulate the growth of sooty mold
hindering the photosynthesis process (Byrne and Bellows,
1991).
The excessive use of synthetic chemical insecticide led to
many environmental problems, besides developmnt of
insect resistance with subsequent population outbreaks
(Palumbo et al., 2001). Therefore, it became necessary to
seek for secure alternatives. Some plant derived
compounds showed promising efficiency against
insecticide-resistant insect pests (Ahn et al., 1997).
Essential oils play an important role as safe alternatives
having insecticidal activity against wide spectrum of insect
pests. They may act as repellents (Park et al., 2006,
Nagassoum et al., 2007 and Abd-Elhady, 2012),
antifeedants (Isman, 2002 and Hernandez-Lambrano et al.,
2014), molting and growth inhibitors (Athanassiou et al.
2014 and Aziza et al., 2014), fecundity inhibitors or toxins
(Enan, 2001; Isman, 2006; and Baldin et al., 2013). This
study aimed to test the efficacy of ten essential oils
extracted from local Egyptian available plants against
different stages of B. tabaci. The repellency effects of
female settlement and oviposition was also assessed.
*Corresponding author: Heba Youssif El-Sayed Ibrahim,
Plant Protection Research Institute, Agriculture Research
Center (ARC), Dokki, Giza, 12618, Egypt. Email:
hyei_youssif@yahoo.com
International Journal of Entomology and Nematology
Vol. 4(2), pp. 085-092, December, 2018. © www.premierpublishers.org. ISSN: 2326-7262
Research Article

Ibrahim and Mostafa 086
MATERIALS and METHODS
Plant Materials and Essential Oils Extraction
The seeds of Artemisia absinthium L. (Asteraceae); tubers
of Cyperus articulates L. (Cyperaceae); aerial parts of
Anethum graveolens L. (Apiaceae); Leaves of Pluchea
dioscoridis L. (Asteraceae), Mentha longifolia (L). Huds.
(Lamiaceae), Lantana camara L. (Verbenaceae); and
whole plant of Thyme vulgaris L. (Lamiaceae) were
collected from Mansoura University farm while roots of
Zingiber officinale Rosc. (Zingiberaceae); seeds pods of
Elettaria cardamomum maton. (Zingiberaceae); and buds
of Syzygium aromaticum (L.) Merr. & Perry (Myrtaceae)
were acquired from herbal markets of Mansoura, Egypt. All
plant materials were identified at Plant Department, Faculty
of Science, Mansoura University. Essential oils of different
plant materials were extracted by hydro-distillation for 4
hours in Clevenger-type apparatus. Then they were dried
over anhydrous sodium sulphate and kept frozen in dark
glass tubes until application. All essential oils were
formulated as emulsion in water and 0.1% triton X-100.
Four concentrations of each essential oil were tested
immediately after preparation.
Pure culture of Whitefly B. tabaci and Host Plants
A pure culture of B. tabaci biotype B was obtained from a
colony reared on cabbage, Brassica oleracea var. capitata
under glass greenhouse at Faculty of Agriculture,
Mansoura Univ. The whitefly strain was transferred to the
laboratory and reared on cabbage seedlings planted in
small pots 25cm (diameter) and kept under plastic
greenhouse conditions of 27±2 oC, 70±5 RH and 14:10
Light: Dark. For the in vitro bioassay experiments, cabbage
seeds were grown in plastic pots (15cm diameter) under
plastic greenhouse to avoid any insect infestation. The
seedlings were allowed to reach 20-25 cm high, with 4-5
fully expanded leaves.
In-vitro Bioassay
Bioassay for contact toxicity
All developmental stages of B. tabaci were obtained by
releasing adults (≈ 100 individuals per plant) on cabbage
seedlings free from any insect infestation in plastic cages,
and were allowed to deposit eggs. After 24 hours, adults
were removed, and the deposited eggs developed to the
suitable stages for assessment.
Thirty individuals of the tested developmental stages were
counted under dissecting microscope and marked with a
water proof pen to be considered as a replicate. Each
concentration had three replicates in addition to control
which was sprayed with water and 0.1% triton X-100 using
a hand sprayer. The sprayed leaves containing marked
developmental stages were individually placed in test tubes
filled with water to maintain leaves freshness along the
experiment, and kept under plastic cages with fine
polyester netting side panels for ventilation. All laboratorial
experiments were conducted in stable conditions of 27±2
oC, 70±5 RH and 14:10 L: D.
Effect of the tested essential oils on B. tabaci eggs
Immediately after adults’ removal, the fresh eggs were
counted, then treated with the tested essential oils
formulations and observed daily along 10 days until eggs
hatching was completed. The ovicidal effect was
determined by the number of unhatched eggs.
Effect of the tested essential oils on nymphal stage
When the hatched eggs developed to the third instar stage-
nymphs, they were treated with different concentrations of
the essential oils. The mortality percentages were
calculated after five days. Dried and shrunk brown nymphs
were considered as dead.
For contact toxicity, the average of mortality percentages of
B. tabaci was estimated and corrected using Abbott’s
formula (1925). The corrected mortality percentage of each
tested oil was statistically calculated according to Finney
(1971). The corresponding concentration probit lines (LC-p
lines) were estimated in addition to determination of 50 and
90% mortalities, slope values of the tested oils were also
estimated. In addition, the efficiency of different tested fungi
was measured by comparing the tested oils with the most
effective one by using Sun’s equation (1950).
Bioassay for repellency effect and oviposition
deterrency
Choice test
Twenty cabbage seedlings with three leaves were divided
into two equal groups. Each plant of the first group was
separately sprayed with one of the tested essential oils
formulations and the other group was sprayed only with
water and triton X-100 as a control. The repellency effect of
the essential oils was tested at concentration of LC90 of
nymphal stage. Each treated plant was placed with another
untreated one (control) in a net cage (60cm x 60cm x 60cm)
at 30cm distance of each other. After an hour of treatment,
100 adult whiteflies were released into the center of the
cage floor. The numbers of whiteflies settled on both sides
of leaves were counted at 12, 24 and 48 hours after
release. Also, the eggs deposited on leaves were counted
under dissecting microscope after 48 hrs. of release. The
experiment was repeated three times (three replicates)
under the same conditions of 27±2 Co, 70±5 RH and 14:10
L: D photoperiods. Repellence index (Baldin and Lara
2001; Baldin et al., 2013 and Schilick-Souza et al., 2011)
was calculated according to the equation: RI=2T / (T+C),
where T is the number of insects on treated plants and C is
the number of insects on the control plant. When RI values
<1, it indicated repellence of B. tabaci by treated plant
compared with the control; RI>1, that indicated
attractiveness of B. tabaci to the treated plant compared
with the control.

Int. J. Entomol. Nematol. 087
Also, oviposition deterrence index (ODI.) (Hang et al. 1982)
was calculated according to the equation: ODI= [(T-C)]/
(T+C)] x 100, where T is the number of eggs counted on
the treated plants, and C is the number of eggs counted on
the control plants. ODI values vary from +100 (very
attractive) to -100 (complete deterrence). RIs and ODIs
values of choice and no-choice test were separately
analyzed by Two-Way ANOVA using CoStat Software
(2004).
No choice test
Cabbage seedlings with three leaves were individually
placed in net cages (30 cm × 30 cm × 60 cm), and each
cage contained one cabbage plant. Three cages were used
as replicates for each oil treatment, in addition to three
cages as controls. The treated plants were sprayed with
LC90 of nymphal stage. Fifty adult whiteflies were released
into each cage after an hour of treatment. The adults were
counted at 12, 24, and 48 h after release. Also, the eggs
deposited were counted under a dissecting microscope at
48 h after the whiteflies release. Both RI and ODI were
calculated.
Field Bioassay
The five most efficient oils were tested against B. tabaci on
cabbage, B. oleraceae var. capitata in open field conditions.
The field was divided into equal blocks, and each oil was
sprayed on four blocks (four replicates) with invitro-LC90 of
3rd instar-nymphs in addition to another four replicates as
controls. The blocks were in completely random
arrangement. Thirty leaves from cabbage seedlings in each
replicate were examined directly for counting the adults and
under a dissecting microscope for counting the other
stages. The effect of the tested oils was observed daily till
3rd day after treatment. Efficiency of the tested essential oils
were calculated according to Henderson-Tilton (1955).
RESULTS AND DISCUSSION
Bioassay for contact toxicity
In vitro bioassay showed that all the tested oils significantly
suppressed the B. tabaci eggs hatchability by contact
toxicity. A. absinthium was the most efficient oil followed by
C. articulates, T. vulgaris, M. longifolia, S. aromaticum, A.
graveolens, E. cardamomum, L. camara, Z. officinal and P.
discoridis that showed the lowest activity. LC50, LC90 values
and toxicity index obtained from probit analysis for mortality
values are presented in Table 1. It was noticed that the oils
affected the eggs hatchability without any morphological
changes by disrupting or inhibiting embryogenesis and
making them unable to come out of the egg shells. Also,
the susceptibility of the 3rd instar of B. tabaci nymphs to the
tested essential oils was tested. It was found that A.
absinthium was the most efficient oil followed by C.
articulates, T. vulgaris, M. longifolia, S. aromaticum, A.
graveolens, Z. officina, L. camara, E. cardamomum, while,
P. discoridis showed the lowest activity. LC50, LC90 values
and toxicity index were mentioned in Table 2. Our results
about high contact toxicity of T. vulgaris essential oil against
B. tabaci biotype B. are agreed with those presented by
Yang et al. (2010) and Kim et al., (2011). Also, the present
results are in accordance with those presented by
Yarahmadi et al. (2013). They illustrated the contact toxicity
and significantly population reduction of Bemisia tabaci by
Artemisia essential oil.
Data clearly demonstrated that eggs were found to be more
susceptible to the tested essential oils than nymphs.
Moreover, the tested essential oils varied in their activity,
this may be due to variation of their chemical constituents.
Several studies pointed out the neurotoxic action of
essential oils by acetylcholinesterase (AChE) inhibition or
by blocking the octopamine receptors (Enan 2001).
Terpenoids, the major constituents of essential oils and the
responsible for their insecticidal toxicity, are highly selective
to insects since they are targeted to the insect-selective
octopaminergic receptor, a non-mammalian target. Also,
essential oils interfere with ˠ-aminobutyric acid (GABA) gate
chloride channels in insects (Priestley et al. 2003).
Bioassay for repellency effect and oviposition
deterrency
In choice test, the repellency of the tested essential oils
against B. tabaci adults were studied. It was observed that
almost all tested essential oils showed repellency effect
except two oils, S. aromaticum and L. camara that showed
slight attractant effect. There were high significant
differences among the tested oils (F: 1330.85; df: 9; p<
0.01).
Taking time after adults introduction into consideration,
(Fig. 1- 3), at 12 and 24 hours after adult introduction, A.
absinthium showed the highest repellency that followed by
C. articulates, T. vulgaris, P. discoridis, M. longifolia, A.
graveolens, E. cardamomum then Z. officina which showed
slight repellency effect. At 48 hours after adults-
introduction, observations showed that the repellency
effects of the tested oils decreased to some extent. Also,
the attraction effects of S. aromaticum and L. camara
decreased to values that were comparable to the control or
even less. There were high significant differences among
the experimental counting periods (F: 1198.97; df: 2; p<
0.01).
The oviposition deterrency of the tested essential oils was
tested against B. tabaci adults at 48 hours after adults-
introduction. The oviposition deterrency indices (ODIs)
(Fig. 4) indicated that A. absinthium showed high
deterrency and oviposition reduction effects (-63.41%)
followed by T. vulgaris (-42.58%) and P. discoridis (-
34.91%). The other essential oils except S. aromaticum, L.
camara and E. cardamomum, showed slight oviposition
deterrency whilst S. aromaticum, L. camara and E.

Table 1: Ovicidal effects of plant essential oils against B. tabaci eggs after 10 days of treatment.
Essential oils
Eggs
LC50 (ppm)
and confidence limits at 95%
LC90 (ppm)
and confidence limits at 95% Slope ± SE X2
Toxicity
index
A. absinthium
0.157 5.753
0.820± 0.186 1.20 100.00
0.036 0.342 2.311 41.692
T. vulgaris
0.334 7.640
0.943± 0.198 1.058 47.006
0.135 0.634 3.087 51.507
C. articulates
0.305 2.776
1.335± 0.277 0.618 51.475
0.163 0.505 1.378 11.925
M. longifolia
0.452 35.551
0.676± 0.171 3.759 34.735
0.095 1.171 8.9 1299.886
S. aromaticum
0.603 7.422
1.176± 0.194 0.424 26.036
0.336 1.004 3.685 24.986
Z. officinal
2.42 40.774
1.045± 0.191 1.73 6.488
1.384 4.864 15.078 289.579
A. graveolens
0.612 44.324
0.689± 0.166 0.624 25.654
0.21 1.37 11.014 1586.074
L. camara
1.085 32.453
0.868± 0.173 1.572 14.470
0.541 2.175 10.778 332.328
E. cardamomum
0.726 16.711
0.941± 0.177 0.223 21.625
0.361 1.342 6.578 104.749
P. discoridis
7.33 65.906
1.344± 0.323 1.251 2.142
4.341 18.928 23.423 993.05
Table 2: Toxicity of plant essential oils against 3rd instar nymphs of B. tabaci after 5 days of treatment.
Essential oils
3rd
instar
LC50 (ppm)
and confidence limits at 95%
LC90 (ppm)
and confidence limits at 95% Slope ± SE X2 Toxicity
index
A. absinthium
7.268 43.856
1.642± 0.390 1.578 100
3.816 10.343 26.652 146.109
T. vulgaris
8.989 37.337
2.072± 0.408 3.133 80.854
6.119 11.865 25.193 81.742
C. articulates
7.865 34.502
1.996± 0.411 2.133 92.409
4.998 10.551 23.194 77.845
M. longifolia
9.491 36.013
2.213± 0.415 1.98 76.578
6.75 12.331 24.90 72.943
S. aromaticum
12.825 43.5
2.416± 0.416 5.426 56.671
9.861 16.441 30.293 84.225
Z. officinal
17.667 88.044
1.837± 0.384 0.387 41.139
12.988 25.679 49.532 319.415
A. graveolens
16.339 118.929
1.487± 0.367 0.107 44.483
11.107 25.855 56.193 912.20
L. camara
21.383 108.436
1.818± 0.389 0.059 33.99
15.712 33.19 57.887 463.203
E. cardamomum
22.9 210.424
1.331± 0.367 0.064 31.738
15.236 48.401 78.930 4903.562
P. discoridis
36.996 135.29
2.276± 0.634 0.006 19.645
27.199 75.664 69.158 1195.897
cardamomum showed slight attractant effects. There were
high significant differences among the tested essential oils
ODI (F: 357.364; df: 9; p< 0.01). It was clear that there was
positive correlation between RI and ODI. This agreed with
Silva et al. 2012, who suggested that the repellency effect
is a factor of oviposition inhibition.
In no-choice test, all the tested essential oils showed
repellency effects and varied in repellency degree, (Fig. 5-
7). At 12h after adult`s introduction, A. absinthium showed
the highest repellency followed by P. discoridis, T. vulgaris,
C. articulates, A. graveolens, M. longifolia, E. cardamomum
then Z. officina, while S. aromaticum and L. camara hardly

showed slight repellency effect. All repellency effects of the
tested essential oils decreased at 24h after adults-
introduction and continued decreasing at 48h. It was
observed that almost all oils lose their repellency effects at
48 after adults-introduction except A. absinthium, T.
vulgaris, C. articulates and P. discoridis. There were
significant effects of the essential oils and time (F: 366.63;
df: 9; p< 0.01), (F: 694.94; df: 2; p< 0.01), respectively.
Previous data showed that repellency (RIs) of the tested
essential oils in no-choice test was less than that of choice
test. In no-choice test, there was no alternative nutrition
source for B. tabaci adults except for the plants treated with
essential oils, so, the adults forced themselves to settle on
the treated plants for feeding with frequent changing of
feeding sites.
All tested essential oils showed oviposition deterrency
against B. tabaci adults except S. aromaticum which
showed no effect. As shown in Fig. 8, the highest
oviposition deterrency effect was showed by A. absinthium
(-57.93%) followed by T. vulgaris (-38.98%) and P.
discoridis (-32.93%). There were high significant
differences of the tested essential oils ODI (F: 618.774; df:
9; p< 0.01).
Fig.1. Repellence indices of the tested essential oils at
12h after adults introduction in choice-test
Fig.4. Oviposition deterrence indices of the tested
essential oils at 48h after adults introduction in choice-
test
12h after adults introduction in no-choice test
-0.2
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
RepellenceIndex(RI)
Essential oils
0
0.2
0.4
0.6
0.8
1
1.2
1.4
REpellenceIndex(RI)
Essential oils
0
0.2
0.4
0.6
0.8
1
1.2
RepellenceIndex(RI)
Essential oils
-80
-60
-40
-20
0
20
OvipositionDeterrence
Index(ODI)
Essential oils
0
0.2
0.4
0.6
0.8
1
1.2
RepellenceIndex(RI)
Essential oils
0
0.2
0.4
0.6
0.8
1
1.2
RepellenceIndex(RI)
Essential oils

Fig.8. Oviposition deterrence indices of the tested
essential oils at 48h after adults introduction in no-choice
test
Table 3: Reduction % averages of B. tabaci treated with tested essential oils in open field conditions
Insecticide Pre-spray
Mean population per plant and percent reduction
Days after insecticide treatment
Overall Mean
1 2 3
Mean
No.
% Red. Mean No. % Red. Mean No. % Red.
Mean
No.
%
Red.
A. absinthium 592.3a 60.3c 90.3 68.5c 89.3 109.0d 83.3 79.3c 87.6
C. articulates 493.5a 57.5c 88.9 76.3c 85.7 105.8d 80.5 79.8c 85.0
T. vulgaris 542.3a 80.0c 85.9 99.8c 83.0 138.0cd 76.9 105.9c 81.9
M. longifolia 499.5a 80.5c 84.6 107.3c 80.1 158.0c 71.2 115.3c 78.6
S. aromaticum 515.3a 326.0b 39.6 212.8b 61.8 262.3b 53.7 267.0b 51.7
Control 525.8a 550.8a 567.8a a578.0 565.5a
LSD 0.05 134.9 61.6 40.6 44.8 61.2
Field Bioassay
The field experiment clarified the great suppression of B.
tabaci populations by application of essential oils as natural
insecticides. The pre-treatment counts recorded an hour
before spraying indicated that there was no significant
difference in the whitefly populations in all blocks. At the 1st
day after treatment, A. absinthium showed the highest
population reduction followed by C. articulates, T. vulgaris,
M. longifolia, and S. aromaticum with mean reduction %:
90.3, 88.9, 85.9, 84.6 and 39.6%, respectively as shown in
Table 3. At the 3rd day after treatment, the population
reduction was 83.3, 80.5, 76.9, 71.2 and 53.7%,
respectively. The average reduction percentages of the
selected essential oils were 87.6, 85.0, 81.9, 78.6 and
51.7%, respectively.
All tested essential oils except S. aromaticum, had the
same behavior of whitefly population reduction% that
decreased during the experiment period. S. aromaticum
had different behavior since it recorded the lowest reduction
at 1st day after treatment then it showed more reduction at
the 2nd day and the reduction% decreased again at 3rd day
after treatment. This was because S. aromaticum showed
contact toxicity to both eggs and immature stages but acted
as adults-attractant at the beginning, then it lost this
attraction property by time, which led to fluctuating
reduction% along the experiment period.
All previous data emphasized that essential oils are
promising factors that can act as insecticides, ovicides,
repellent and insect-oviposition deterrent. Therefore,
essential oils are worthy of further studies in order to
develop their application in wide scales as environmental-
friendly insecticides.
CONCLUSION
The present study highlighted the importance of the
essential oils as green insecticides. Our results illustrated
that A. absinthium, C. articulates and T. vulgaris showed
high contact toxicity, repellency effect and oviposition
deterrency against the whitefly, B. tabaci. Therefore, they
are recommended to be used in wide scales in B. tabaci
control.
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Accepted 3 December 2018
Citation: Ibrahim HYE, Mostafa ME (2018). Efficacy of
some Plant Essential Oils as Green Insecticides to Control
Whitefly, Bemisia tabaci (Gennadius). International Journal
of Entomology and Nematology, 4(2): 085-092.
Copyright: © 2018 Ibrahim and Mostafa. This is an open-
access article distributed under the terms of the Creative
Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided
the original author and source are cited.

Efficacy of some Plant Essential Oils as Green Insecticides to Control Whitefly, Bemisia tabaci (Gennadius)

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