Journal of Entomological and Acarological

Journal of Entomological Research

and Acarological 2023; 2012;
Research volume 55:11670
volume 44:e

STORED PRODUCT PEST

Efficacy of Eucalyptus citriodora and Syzygium aromaticum essential oil

as insecticidal, antiovipositant, and fumigant against Callosobruchus
maculatus F (Coleoptera: Bruchidae)
Agus Kardinan,1 Paramita Maris,1 Ireng Darwati,1 Zakiah Mustapha,2 Norhayati Ngah2,3
1Research Center for Horticultural and Estate Crops, Nasional Research and Innovation Agency, Cibinong, Indonesia; 2Faculty of
Bioresources and Food Industry, Universiti Sultan Zainal Abidin, Besut Terengganu, Malaysia; 3East Coast Environmental
Research Institute, Universiti Sultan Zainal Abidin, Gong Badak Campus, Kuala Terengganu, Terengganu, Malaysia

done to identify the active ingredient of essential oils in

Abstract Eucalyptus citriodora and Syzygium aromaticum and to evaluate

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the effectiveness of those essential oils in controlling C. macula-

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Callosobruchus maculatus is the most pernicious pest of tus. The results of gas chromatography/mass spectrometry analy-
stored grain worldwide. Even though synthetic insecticides are sis indicated that the essential oil extracted from the leaves of S.
commonly used to eliminate this insect pest, the negative effect aromaticum are rich in Eugenol and β caryophyllene as much as

e
of this pest management method on humans and the environment 81% and 14.65% consecutively, while E. citriodora oil contains
raises concern among people around the world. This study was
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86% of Citronella. According to the bioassay results, increasing
the essential oil concentration from 1% to 3% resulted in a sig-
nificant increase in insect mortality rate, oviposition deterrence,
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and fumigant toxicity. Additionally, S. aromaticum has signifi-
cantly shown a higher insecticidal performance compared to E.
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Correspondence: Ireng Darwati, Research Center for Horticultural and citriodora. However, there are no synergistic effects observed on
Estate Crops, Nasional Research and Innovation Agency, Cibinong, the use of essential oil of both plant species on C. maculatus.
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Indonesia. These results suggest that S. aromaticum and E. citriodora

E-mail: [email protected]
essential oils could be potential candidates as a natural insecti-
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Key words: E. citriodora; S. aromaticum; C. maculatus; insecticidal; cide in managing C. maculatus in stored products.
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ovipositant; fumigant.

Acknowledgments: we would like to thank Nurbeti Tarigan and Galih Introduction

Perkasa, the technicians of the Entomology Laboratory in Indonesia
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Spices and Medicinal Research Institute who have assisted the research Cowpea seed beetle Callosobruchus maculatus F
from preparation and observation to completion. (Coleoptera: Bruchidae) is the major insect pest that causes both
on

qualitative and quantitative losses of grain legumes during stor-

Conflict of interest: the authors declare no potential conflict of interest.
age (Devi & Devi, 2014). Infestation of this insect pest will
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Funding: none. reduce the nutritional quality of grains and cause food contami-
nation due to insect residue. The eggs and adults present on the
Received: 21 August 2023. grain, but larvae and pupae live within the seed. Its larvae make
Accepted: 4 September 2023. a hole in the grains and feed on the endosperm (Ahuchaogu &
Ojiako, 2020). Feeding is done during the larval stage, the
Publisher’s note: all claims expressed in this article are solely those of the adults-only mate and oviposit (Nisar et al., 2021). The age
authors and do not necessarily represent those of their affiliated organi- of adults is between 10 to 14 days, after which they will die
zations, or those of the publisher, the editors and the reviewers. Any prod-
(Beck & Blumer, 2011). Callosobruchus maculatus are able to
uct that may be evaluated in this article or claim that may be made by its
complete their life cycle in several generations per year (Kebe et
manufacturer is not guaranteed or endorsed by the publisher.
al., 2020).
©Copyright: the Author(s), 2023 The estimated post-harvest losses caused by this insect to the
Licensee PAGEPress, Italy pulses ranged from 30 to 40% within 6 months and when left unat-
Journal of Entomological and Acarological Research 2023; 55:11670 tended losses could be up to 100% (Mahendran & Mohan, 2002;
doi:10.4081/jear.2023.11670 Thein et al., 2020). The pest management techniques in control-
ling this insect pest are generally done by using insecticide, fumi-
This article is distributed under the terms of the Creative Commons gation (Phospine or Methyl bromide), or by radiation. However,
Attribution-NonCommercial International License (CC BY-NC 4.0)
which permits any noncommercial use, distribution, and reproduction in
these control methods are not environmentally friendly and are
any medium, provided the original author(s) and source are credited. considered to have a negative impact on the environment and con-
sumer health.

[Journal of Entomological and Acarological Research 2023; 55:11670] [page 19]

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There is an increasing demand from grain buyers and con- Extraction and chemical analysis of the essential oil
sumers toward zero tolerance to contamination by insects in grains
(Sarwar, 2012; Kaliramesh et al., 2013). Owing to the negative Essential oils of E. citriodora and S. aromaticum
impacts caused by previous control techniques, there is a need for were obtained from the distillation process of the leaves. The
environmentally friendly control measures for C. maculatus by leaves of E. citriodora and S. aromaticum were harvested and
using natural products. The efficacy of some natural products has dried indoors for 24 hours prior to distillation by steaming. The
been reported against C. maculatus, such as Neem (Azadirachta steam that came out flowed through the condenser and became
indica), Garlic (Allium sativum), West African pepper (Piper liquid and was accommodated. The liquid consisted of both
guineense), Drum Stick (Moringa oleifera), African Basil water and oil, with the oil floating on top and taken for further
(Ocimum gratissimum), Moss plant (Barbula indica) and Clausena research. The active chemical content in the essential oil was
anisata which is indicating to have potentials of controlling C. analysed using Gas Chromatography (Agilent 6890 N) with an
maculatus in the store (Muhammad et al., 2017). advanced electronic pneumatic control containing a Carbowax
The use of garlic powder has significantly decreased egg lay- 20 M high polarity capillary column of 3 meters long and 0.25
ing, larval penetration and adult emergence as compared to turmer- mm in diameter. The temperature was programmed to rise to
ic powder (Sharma & Kaur, 2017). Otikai (Alphitonia sp.) leaf 60°C and then to 200°C at 3°C/ minute with injector and detec-
extract and pinang (Areca catechu) fruit extract also has the poten- tor temperatures at 220°C and 250°C, respectively. The detector
tial as natural insecticide material to control Callosobruchus sp. in was a flame ionization detector and nitrogen was used as a car-
rier gas at a flow rate of 1ml/minute and the injection volume
the store (Gobaia et al., 2015). While ginger oil, nutmeg oil, and
was 0.2 μl. The chemical constituents were identified by com-
clove oil have also affected the mortality of C. maculatus (Astuthi
paring their relative retention indices and mass spectra, with
et al., 2012). Piper guineense fruits, Dennittia tripetala fruits,
those published in the literature, and supplemented with
Allium sativum bulbs, and Zingiber officinale rhizomes powders
NIST 1.7 and Wiley 7 gas chromatography/mass spectrometry

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were also effective in controlling insect infestation by showing sig-
libraries. The relative proportion of the essential oil constituent
nificantly higher mortality, reduction in the number of eggs laid,

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was computed in each case from the gas chromatography
and suppression of the development and emergence of adult prog-
peak areas.
enies from the treated mung bean seeds (Emeasor & Chukwu,
2019). Clove essential oil (Syzygium aromaticum) is toxic to C.

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Insecticidal activities of E. citriodora and
maculatus (Bao et al., 2015) followed by cinnamon
(Cinnamomum sp), lengkuas (Alpinia galanga), citronella
(Cymbopogon nardus), and kaffir lime (Citrus hystrix) essential oil
us
S. aromaticum essential oil on C. maculatus
A number of 100 mung bean seeds were sprayed with 0.2ml of
(Thein et al., 2020).
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10 different essential oil treatments (Table 1) and then air-dried in
Eucalyptus (Family: Myrtaceae) is an Australian native, repre-
the same place for approximately 10 minutes. After drying, 10
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sented by around 700 species of tall, evergreen and magnificent

females were introduced to each treatment to observe their mortal-
trees cultivated around the world for their oil, pulp, timber, and
ity rate on a daily basis for 4 days.
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medicine value. The essential oil found in its foliage possesses a

broad spectrum of biological activity including anti-microbial,
Oviposition deterrents and egg hatching
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fungicidal, insecticidal/insect repellent, herbicidal, acaricidal, and

nematicidal (Daizy et al., 2008).
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A plastic box (20 cm ｘ 15 cm) was divided by paper into

Another species of Eucalyptus such as Eucalyptus citriodora 12 similar segments. Each segment was filled with 20 mung
containing essential oil (Citronellal - 64.7% and citronellol - beans that had been treated with 10 different treatments of essen-
10.9%) has the potential to be used as bioherbicide and can consti-
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tial oil (Table 1) while 2 segments in the middle were emptied

tute an alternative process of weed control (Benchaa et al., 2018). for storing 20 pairs of C. maculatus. The number of eggs laid
Eucalyptus essential oil has the potential as a repellent and
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on the surface of the seeds was recorded after 4 days of applica-

antiovipositant against stored product insects of Ephestia cautella tion. Oviposition deterrent was calculated based on Meena and
(Hasyim et al., 2014). Nevertheless, there are only limited reports Gupta (2013).
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on the insecticidal activity of S. aromaticum and E. citriodora

either in single or in combination against C. maculatus. Therefore, Fumigant toxicity bioassay
the objective of this study is to identify the main active ingredient
of essential oils in E. citriodora and S. aromaticum and to evaluate The fumigant toxicity bioassay was done for 4 different treat-
the efficiency of these essential oils as insecticidal, antiovipositant, ments of essential oil (Table 2) using the fumigation testing tool
and fumigant against cowpea weevil C. maculatus. consisting of a 170 cm3 petri dish that was divided by screen
cloth into lower and upper parts. 10 insects of C. maculatus were
placed on the lower side and 0.1 ml of essential oil was dropped
Materials and Methods onto the cotton cloth on the upper side. The mortality rate of C.
maculatus was recorded after 24 hours of incubation.
Biological materials
Statistical analysis
The dried leaves of E. citriodora and S. aromaticum were
obtained from the Manoko Experimental Station, Bogor All experiments were arranged in a completely randomized
Indonesia. Meanwhile, the colony of C. maculatus was reared on design. The experiment for insecticide bioassay oviposition deter-
mung bean (Vigna radiata) seeds at Entomology Laboratory, rents and egg hatching bioassay were done for 3 replications using
ISMCRI. The insects were kept in the closed rearing box with 10 different treatments (Table 1). While 6 replications with 4 dif-
ambient temperature at 28°C (±1ºC) and relative humidity of ferent treatments were designed for the experiment of fumigant
68% (±5%) for further use. toxicity bioassay (Table 2).

[page 20] [Journal of Entomological and Acarological Research 2023; 55:11670]

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tively. A total of 43 components from the essential oil of

Results E. citriodora were separated. Based on Gass Chromatography
analysis, the main active ingredient of E. citriodora
Chemical constituents of E. citriodora and is Citronellal as much as 86.69% (Figure 1). Meanwhile,
S. aromaticum essential oil A total of 52 components from the essential oil of S. aroma-
ticum were separated and the main active ingredient content
The yield of the essential oil from E. citriodora and S. aro- was 81.04% Eugenol and 14.65% β caryophyllene
maticum were 1.2% and 1.5% (v/w based on dry weight) respec- (Figure 2).

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Figure 1. Retention time gas chromatogram (flame ionization detector) E. citriodora. FID, flame ionization detector.
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Table 1. Treatment details for the experiment of insecticide bioassay and oviposition deterrents and egg hatching bioassay.
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Treatment Details
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1 E. citriodora – 1% (10 ml EO/L water)

2 E. citriodora – 2% (20 ml EO/L water)
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3 E. citriodora – 3% (30 ml EO/L water)

4 S. aromaticum – 1% (10 ml EO/L water)
5 S. aromaticum – 2% (20 ml/L water)
6 S. aromaticum – 3% (30 ml/L water)
7 E. citriodora + S. aromaticum (1 : 1) – 1% (10 ml/L water)
8 E. citriodora + S. aromaticum (1 : 1) – 2% (20 ml/L water)
9 E. citriodora + S. aromaticum (1 : 1) – 3% (30 ml/L water)
10 Control/water

Table 2. Treatment details for the experiment of fumigant toxicity bioassay.

Treatment Details
1a E. citriodora oil (0.1 ml/170 cm3)
2a S. aromaticum oil (0.1 ml/170 cm3)
3a E. citriodora + S. aromaticum oil (0.1 ml/170 cm3, 1:1)
4a Control/water (0.1 ml/170 cm3)

[Journal of Entomological and Acarological Research 2023; 55:11670] [page 21]

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Insecticide bioassay icant for S. aromaticum essential oil at concentrations of 1%, 2%,
and 3% (Treatment 4, 5, and 6) causing 43.3%, 50%, and 56.6%
The result showed that on the first day after application, there insect mortality respectively. Meanwhile, a combination of E. cit-
was no significant effect of E. citriodora and S. aromaticum essen- riodora and S. aromaticum essential oil (Treatment 7, 8, and 9)
tial oil on the mortality of the tested insect. On the second day after showed lower results compared to the use of a single application
application, S. aromaticum essential oil at concentrations of 2% of essential oil. Mortality rates of C. maculatus for Treatment 7,
and 3% (Treatment 5 and 6) began to show its effect on insects as 8, and 9 showed not much difference and were not significant to
much as 13% to 16% of mortality (Table 3) and the results are sig- the treatment with single usage of E. citiriodora essential oil
nificant compared to control. Other treatments have not yet shown (Treatment 1, 2, and 3).
their effect on the insect's mortality on day 2 after treatment.
All treatments showed mortality of C. maculatus after 3 days Oviposition deterrent and egg-hatching
of application. E. citriodora essential oil at concentrations of 1%,
2%, and 3% (Treatment 1, 2, and 3) caused mortality to the tested The different types and concentrations of essential oil oviposi-
insect as many as 16.6%, 23.3%, and 26.6% respectively. S. aro- tion deterrence activity in the females of C. maculatus are shown
maticum essential oil at 2% and 3% (Treatment 5 and 6) showed in Table 4. The oil’s oviposition deterrence increased with
higher and significant mortality rates compared to other treat- increased concentrations of the oil. The results showed that the
ments. On the fourth day after treatment, the results were signif- number of eggs laid by the females decreased as concentrations of

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Figure 2. Retention time gas chromatogram (flame ionization detector) S. aromaticum. FID, flame ionization detector.
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Table 3. Effect of E. citriodora and S. aromaticum essential oil on the mortality of C. Maculatus.
Treatment Mortality rate (%)
Day 1 Day 2 Day 3 Day 4
1 0.0 a 3.3 a 16.6 b 32.6 b
2 0.0 a 6.3 a 23.3 c 30.0 b
3 0.0 a 6.6 a 26.6 c 33.3 b
4 0.0 a 10.0 ab 23.3 c 43.3 c
5 0.0 a 16.6 b 30.0 cd 50.0 cd
6 3.3 a 13.3 b 43.3 d 56.6 d
7 0.0 a 0.0 a 26.6 c 33.3 b
8 0.0 a 6.6 a 23.3 c 30.0 b
9 3.3 a 3.0 a 22.0 c 30.0 b
10 0.0 a 0.0 a 0.0 a 0.0 a
Numbers with the same letters in the same column are not significantly different at 5% Duncan’s multiple range test.

[page 22] [Journal of Entomological and Acarological Research 2023; 55:11670]

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the oil were increased. S. aromaticum essential oil had better The results from the insecticide bioassay showed that S. aro-
oviposition deterrent ability compared to the use of single or in maticum has significantly killed an average of 56% and 59%
combination with E. citriodora. The oviposition deterrent ability more insects compared to the use of E. citriodora alone or in
of S. aromaticum was 46-54.9%, E. citriodora was 27-41% and the combination with S. aromaticum respectively after 4 days of
mixture of both essential oils was 35% to 42%. treatment. It was the same as in oviposition deterrent ability
assay where S. aromaticum showed an average of 43% and 26%
Fumigant toxicity test respectively higher results compared to E. citriodora alone or in
combination with S. aromaticum. The number of eggs hatching
The data for fumigant toxicity was collected after 24 hours of also decreased as the concentration of every essential oil
application and presented in Table 5. The result showed that all treat- increased either alone or in a combination. However, the result
ments gave a significantly different fumigant toxicity ability. E. cit- from fumigant toxicity showed that E. citriodora gave signifi-
riodora essential oil (Treatment 1a) gave the highest insect mortality cantly 22% and 75% higher mortality rates respectively com-
(93.3%), followed by the combination of the two essential oils pared to the use of S. aromaticum either alone or in combination
(Treatment 3a) with 76.6% insect mortality while S. aromaticum with E. citriodora. Thus, the results from the three bioassays
(Treatment 2a) showed the lowest mortality rates of 53.3%. showed that there are no synergism effects between S. aro-
maticum and E. citriodora essential oils against C. maculatus
attacks on mung beans.
Discussion A combination of essential oils usually will produce synergis-
tic effects. However, it depends on a vigorous set of criteria
Legumes are rich in proteins, vitamins, and minerals (Shevkani including the dose of the oils and the complexity of chemical
et al., 2019). These characteristics attract insect attacks that are molecules each of which can act on different targets (Kachkoul et
usually interested in seeds that contain carbohydrates and protein. al., 2021). The mixture of essential oils compounds does not nec-

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The process of damage and loss of green beans stored in the ware- essarily always synergism because antagonism can occur as well

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house by warehouse pests C. maculatus begins when insects lay as potentiation both situations can exist depending on the dose,
eggs on the surface of the seeds. The shape and size of the seeds application and properties of the oils (Harris, 2002). The major
and the presence of certain substances on the surface of the seeds and minor components of essential oil could also be the factor

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will influence insect pests to choose places for laying eggs, includ- that affects their effectiveness such as in the case of the antimi-
ing avoiding them (Kaliramesh et al., 2013). The presence of S.
aromaticum and E. citriodora essential oil on the surface of mung
bean seeds has significantly decreased the oviposition of the insect
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crobial property of Eucalyptus species where the major compo-
nents are often relatively inactive but the minor components that
actually the main synergists (Zakaraya et al., 1993). These fac-
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on the surface of mungbean. This is in line with Bao et al. (2015) tors may be contributing to the results obtained in this study
statement that clove oil (Syzygium aromaticum) was toxic to C. where there is no synergism effect recorded for the combination
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maculatus. While Eucalyptus essential oil has the potential as an of E. citriodora and S. aromaticum on insecticidal, oviposition,
insecticidal repellent and antiovipositant against stored product and fumigant effects on C. maculatus.
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insect (Daizy et al., 2008; Hasyim et al., 2014). Many essential oils extracted from different plant spices have
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Table 4. Effect of E. citriodora and S. aromaticum essential oil as oviposition deterrent.

Treatment Number of eggs laid Oviposition deterrent (%)
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1 44.0 c 27.4 d
2 37.3 bc 38.4 bc
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3 35.6 b 41.2 b
4 32.6 ab 46.2 ab
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5 31.0 ab 48.8 ab
6 27.3 a 54.9 a
7 39.3 bc 35.1 cd
8 35.0 b 42.2 b
9 35.0 b 42.2 b
10 60.6 d 0e
Numbers with the same letters in the same column are not significantly different at 5% Duncan’s multiple range test.

Table 5. Effect of E. citriodora and S. aromaticum essential oil as fumigant against C. maculatus after 24 hours of treatment.
Treatment Mortality of insect (%)
1a 93.3 a
2a 53.3 c
3a 76.6 b
4a 3.3 d
Numbers with the same letters in the same column are not significantly different at 5% Duncan’s multiple range test.

[Journal of Entomological and Acarological Research 2023; 55:11670] [page 23]

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already been screened for toxicity as potential insecticides

against C. maculatus. Essential oils are generally broad spectrum References
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on

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