Parasitol Res (2013) 112:11551161

DOI 10.1007/s00436-012-3246-6

ORIGINAL PAPER

Larvicidal and repellent activity of the essential oil of Coriandrum

sativum L. (Apiaceae) fruits against the filariasis vector Aedes
albopictus Skuse (Diptera: Culicidae)
Giovanni Benelli & Guido Flamini & Giulia Fiore &
Pier Luigi Cioni & Barbara Conti

Received: 1 December 2012 / Accepted: 10 December 2012 / Published online: 24 December 2012
# Springer-Verlag Berlin Heidelberg 2012

Abstract The essential oils of many Apiaceae species have

been already studied for their insecticidal and repellent
properties against insect pests. In this research, the essential
oil (EO) extracted from the fruits of Coriandrum sativum L.
(Apiaceae) was evaluated for the first time for its larvicidal
and repellent activities against the most invasive mosquito
worldwide, Aedes albopictus Skuse (Diptera: Culicidae).
The chemical composition of C. sativum EO was investigated by gas chromatography with electron impact mass
spectrometry analysis. Coriander EO was mainly composed
by monoterpene hydrocarbons and oxygenated monoterpenes, with linalool (83.6 %) as the major constituent. C.
sativum EO exerted toxic activity against A. albopictus
larvae: LC50 was 421 ppm, while LC90 was 531.7 ppm.
Repellence trials highlighted that C. sativum EO was a
good repellent against A. albopictus, also at lower dosages: RD50 was 0.0001565 L/cm2 of skin, while RD90
was 0.002004 L/cm2. At the highest dosage (0.2 L/
cm2 of skin), the protection time achieved with C.
sativum essential oil was higher than 60 min. This study
adds knowledge about the chemical composition of C.
sativum EO as well as to the larvicidal and repellent
activity exerted by this EO against A. albopictus. On
this basis, we believe that our findings could be useful
for the development of new and safer products against
the Asian tiger mosquito.
G. Benelli : G. Fiore : B. Conti (*)
Entomology SectionDepartment of Agriculture, Food
and Environment, University of Pisa,
Via del Borghetto 80, 56124 Pisa, Italy
e-mail: bconti@agr.unipi.it
G. Flamini : P. L. Cioni
Department of Pharmacy, University of Pisa,
Via Bonanno 33, 56126 Pisa, Italy

Introduction
Since the Middle Ages, plant extracts have been widely
employed for bactericidal, virucidal, fungicidal, parasiticide,
insecticidal, medicinal, and cosmetic applications (Amer
and Mehlhorn 2006a; Bakkali et al. 2008 and references
therein). In this context, previous researches on natural
compounds from Apiaceae highlighted their toxic activity
against a wide range of arthropod pests, including mites
[e.g., Dermatophagoides farinae, Dermatophagoides pteronyssinus (Acari: Pyroglyphidae)] (Kwon and Ahn 2002),
whiteflies [e.g., Bemisia tabaci (Gennadius) (Homoptera:
Aleyrodidae)] (Ateyyat et al. 2009), foodstuffs beetles
[e.g., Lasioderma sericorne F. (Coleoptera: Anobiidae),
Sitophilus oryzae L. (Coleoptera: Curculionidae)] (Kim et
al. 2003), moths [e.g., Ephestia kuehniella Zeller
(Lepidoptera: Pyralidae)] (Tunc et al. 2000), midges [e.g.,
Mayetiola destructor Say (Diptera: Cecidomyiidae)]
(Lamiri et al. 2001), drosophillids [e.g., Drosophila melanogaster Meigen (Diptera: Drosophilidae)] (Tsukamoto et
al. 2005), and mosquitoes [e.g., Aedes aegypti L., Anopheles
stephensi Meigen, and Culex quinquefasciatus Say (Diptera:
Culicidae)] (Amer and Mehlhorn 2006a; Conti et al. 2010;
for a recent review see Evergetis et al. 2012).
The Asian tiger mosquito, Aedes albopictus Skuse
(Diptera: Culicidae) is currently considered the most
invasive mosquito species in the world (Benedict et al.
2007). Thanks to its huge ecological and physiological
plasticity, A. albopictus is able to rapidly adapt to
different anthropogenic environments. In recent decades,
it has completely invaded many countries, spreading
rapidly to Europe, North and South America, the
Caribbean, Africa, and the Middle East (Paupy et al.
2009; Caminade et al. 2012). The medical significance
of the Asian tiger mosquito is mainly due to its

1156

aggressive daytime human-biting behavior, as well as to

its ability to serve as a vector for many viruses (e.g.,
dengue, yellow fever, West Nile, Japanese encephalitis
and chikungunya; Benedict et al. 2007; Paupy et al.
2009), and filariasis (e.g., Dirofilaria immitis Leidy,
Dirofilaria repens Railliet & Henry, and Setaria labiatopapillosa Perroncito; Paupy et al. 2009). The vector
control still remains the key tool for the prevention of
these diseases, since there are no vaccines or drugs
against the main pathogens transmitted by A. albopictus.
On this purpose, control strategies against mosquito
larval instars are based on organophosphates and insect
growth regulators (e.g., diflubenzuron and methoprene)
and their use can lead to the development of resistant
vector strains or to undesirable effects on nontarget
organisms, to the environment, and to human health
(Robert and Olson 1989; Severini et al. 1993).
Alternative biological control strategies based on the
release of larvivorous organisms still require further
studies (Lapied et al. 2009). Against adult mosquitoes,
the use of the skin repellent N,N-diethyl-3-methylbenzamide is recognized as one of the most efficient tools.
However, this molecule is irritating for mucous membranes (Klun et al. 2006) and can be toxic to humans,
especially to children and elders (Sudakin and Trevathan
2003). Therefore, further research is still needed to find
alternatives to synthetic insecticides. In latest years,
consistent efforts have been carried out in order to
investigate the efficacy of natural products against a
huge range of arthropod pests (Amer and Mehlhorn
2006b; Fichi et al. 2007a, 2007b; Elango et al. 2011;
Govindarajan et al. 2011; Benelli et al. 2012a, 2012b;
Govindarajan and Sivakumar 2012). In detail, essential
oils are known as toxic agents against mosquitoes, acting as larvicidal (Kamsuk et al. 2007; Mathew et al.
2009; Conti et al. 2010; Hafeez et al. 2011), ovicidal,
oviposition deterrents, growth and/or reproduction inhibitors (Rajkumar and Jebanesan 2005; Pushpanathan et al.
2006), and/or adult repellents (Gleiser et al. 2011;
Koliopoulos et al. 2010). Among these products, the essential
oil obtained from Coriandrum sativum L. (Apiaceae) fruits
was tested against several mosquito species for its larvicidal
(Chantraine et al. 1998; Amer and Mehlhorn 2006a; Knio et
al. 2008; Sedaghat et al. 2011), oviposition deterrent (Consoli
et al. 1989), and repellent properties (Kang et al. 2009).
To the best of our knowledge, nothing has been reported
about the activity of the essential oil from C. sativum fruits
against A. albopictus. On this basis, this research investigates the larvicidal and repellent properties of this essential
oil against the Asian tiger mosquito. The chemical composition of the tested essential oil was also investigated by gas
chromatography coupled with electron impact mass spectrometry (GC-EIMS) analysis.

Parasitol Res (2013) 112:11551161

Materials and methods

Essential oil extraction and GC-EIMS analysis
C. sativum fruits were originally from Warsaw (Poland) and
were provided by Webb James (Livorno, Italy). Fruits were
hydrodistilled in a Clevenger-type apparatus for 2 h. GC
analyses were carried out with an HP-5890 Series II instruments equipped with HP-WAX and HP-5 capillary columns
(30 m0.25 mm, 0.25 m film thickness), working with
this temperature program: 60 C for 10 min, ramp of 5 C/
min up to 220 C; injector and detector temperatures 250 C;
carrier gas was helium (2 ml/min); detector dual FID; split
ratio 1:30; injection of 0.5 l (10 % hexane solution).
Components identification was carried out, for both columns, by comparing their retention times with those of pure
authentic samples and by means of their linear retention
index (LRI), relative to the series of n-hydrocarbons.
Gas chromatography-electron impact mass spectroscopy
(GC-EIMS) analyses were performed with a Varian CP3800 gas chromatograph, equipped with a HP-5 capillary
column (30 m0.25 mm; coating thickness, 0.25 m) and a
Varian Saturn 2000 ion trap mass detector. Analytical conditions: injector and transfer line temperatures 220 and 240 C,
respectively; oven temperature programmed from 60 to
240 C at 3 C/min; carrier gas helium at 1 ml/min; injection
of 0.2 l (10 % hexane solution); split ratio of 1:30.
Constituents identification was based on comparison of retention times with those of authentic samples; this implied comparing their LRIs with the series of n-hydrocarbons and using
computer matching against commercial (NIST 98 and
ADAMS) and home-made library mass spectra (built up from
pure substances and components of known oils and mass
spectra literature data (Stenhagen et al. 1974; Massada 1976;
Jennings and Shibamoto 1980; Swigar and Silverstein 1981;
Davies 1990; Adams 1995). Moreover, molecular weights
of all identified substances were confirmed by gas
chromatography-chemical ionization mass spectrometry, using methanol as the chemical ionization ionizing gas.
A. albopictus rearing conditions
Adults of A. albopictus originated from field-collected eggs,
deposited by wild females on bars of masonite placed outdoors in dark vases containing water. Eggs batches were
daily collected and kept moist for 24 h. Then they were
placed in laboratory conditions (251 C, 455 % RH,
natural summer photoperiod) in 250 cm3 beakers and submerged in mineral water for hatching. Newly emerged larvae were reared in groups of 150 specimens in 500 cm3
beakers, with mineral water and a small amount of cat food
until they reached the pupal stage, when they were introduced in the bioassay cage. Emergent adults were

Parasitol Res (2013) 112:11551161

maintained (300 specimens/cage; sex ratio, 1:1) at 251 C,

655 % RH, natural summer photoperiod, and supplied
with 10 % sucrose solution on a cotton wick (Conti et al.
2012a, 2012b).
C. sativum larvicidal activity
The newly emerged larvae were isolated in glass tubes with
mineral water and a small amount of cat food. Larvae were
daily controlled until they reached the fourth instar. Then,
four groups of 10 fourth-instar larvae were isolated in
250 ml beakers and exposed for 24 h to dosages of 50,
100, 200, 250, 300, 350, 400, 450, 500, 550, and 600 ppm
of C. sativum essential oil in mineral water containing 0.1 %
of Tween 80; 250 ml beakers with the same number of
larvae (for four replicates) and mineral water with 0.1 % of
Tween 80 were used as control. Mortality was recorded
after 24 h, at the end of the test, during which no food was
given to the larvae (WHO 1981; Conti et al. 2010, 2012a).
Larval mortality was reported as an average of four
replicates. Data were also used to calculate the LC50 and
LC90 values. Since no mortality was registered in the control
treatment, the mortality percentage rates were not corrected.
C. sativum repellent activity
The repellence of the essential oil of C. sativum was evaluated using the human-bait technique, to simulate the condition of human skin on which repellents will be applied
(Conti et al. 2012b, 2012c). Experiments were conducted
during summer 2012. Groups of 150 nulliparous, nonbloodfed, starved female of A. albopictus (812 days old) were
placed into Plexiglas cylindrical laboratory cages (diameter,
35 cm; length, 60 cm). Each cage had a cotton stockinet
access sleeve on the front. Since A. albopictus is a daybiting mosquito, testing period was between 09:00 and
16:00 hours. Ten volunteers were chosen among susceptible
to mosquito bites and non-allergic subjects. They had no
contact with lotions, perfumes, oils, or perfumed soaps on
the day of the bioassay. After cleaning their hands with
distilled water, they protected their forearms with a thick
fabric sleeve and wore a latex surgical glove where a dorsal
square area (55 cm) was cut out. Mosquito-exposed
skin was treated with 100 L of ethanol as a negative
hand control. The other hand was treated with 100 L
of essential oil in ethanol solution (dosages ranging
from 0.004 to 0.2 L/cm2 of skin, refer to Table 3).
All concentrations were replicated five times on different volunteers. First, the control hand was exposed in
the cage for 3 min, during which the number of probing
mosquitoes was recorded. Immediately after, the other
hand was treated with repellent formulation and exposed
to mosquitoes in the same test cage. The number of

1157

probing mosquitoes in a further 3 min exposure period

was recorded. The percentage of repellence obtained
from five replicatesexpressed as percentage protective
efficacy (PE%)was calculated at each dosage using
this formula: PE%=[(number probing untreated hand
number probing treated hand)/number probing untreated
hand]100 (Fradin and Day 2002).
To calculate the full protection time (PT), the test was
repeated every 15 min until either two probings occurred in
a single exposure period or one bite occurred in each of two
consecutive exposure periods. The period of time between
repellent application and the first two probings in a single
exposure, or two probings in successive observations, was
recorded as the complete protection time. Each PT is given
as average of five replicates. Each concentration has been
tested for a total of 120 min. During each test, the control
and the treated hand were regularly interchanged to verify
the mosquitoes readiness to bite. On rare occasions, when
no mosquito attempted to probe the untreated hand, trial was
discarded and test repeated with a new mosquitos cage, to
ensure that the lack of bites was due to repellence and not to
mosquitoes being unwilling to have a blood meal at the
time. To calculate the RD50 and RD90 values, the essential
oil was tested at dosages of 0.00002, 0.00004, 0.00012,
0.0002, 0.0004, 0.002, 0.004, and 0.008 Lcm2 of skin
(WHO 2009).
Statistical analysis
Larvicidal activity data were transformed into arcsineproportion values before statistical analysis. Data were
processed with JMP, using a general linear model
(GLM; JMP SAS, 1999) with one factor, the dosage:
yj =+Dj +ej, in which yj is the observation, is the
overall mean, Dj the dosage (j=111), and ej the residual error. Averages were separated by TukeyKramer
HSD test. Only probability level P<0.05 was used, for
the significance of differences between means, to simplify statistical analysis.
Repellence data was analyzed using a GLM with two factors
with interactions, dosage, and time: yj =+Dj +Tj +Dj Tj +ej in
which yj is the observation, is the overall mean, Dj the dosage
(j=16), Tj the time (j=18), Dj Tj the interaction between
dosage and time, and ej the residual error in the interaction
between oil and dosage. Protection time data were analyzed
using a GLM with one factor, the dosage: yj =+Dj +ej,
in which yj is the observation, is the overall mean, Dj
the dosage (j=16), and ej the residual error.
LC50, LC90, RD50, and RD90 were calculated using
Prism 5 (GraphPad software, San Diego, CA, USA).
Bottom and top parameters were fixed to 0 (0 % mortality and no repellence) and 100 (100 % mortality and
full repellence).

1158

Parasitol Res (2013) 112:11551161

Results and discussion

The GC-EIMS analysis on the essential oil obtained
from the fruits of C. sativum led to the identification
of 18 compounds, representing 99.3 % of the whole oil
(Table 1). This essential oil was almost entirely composed by terpene derivatives, in particular monoterpene
hydrocarbons (nine molecules, 6.9 % of the whole oil)
and oxygenated monoterpenes (eight molecules, 92.4 %
of the whole oil); the only nonterpene component was
decanal, detected at trace levels. The major constituent
of this essential oil was linalool (83.6 % of the whole
oil). This latter compound was identified in a comparable amount (87.54 %) also in the EO extracted from C.
sativum fruits from Tunisia (Msaada et al. 2007) while
in Korean C. sativum fruits, it was present in a lower
quantity (53.79 %; Nagella et al. 2012). Interestingly,
linalool was present in very little amounts in the EO
extracted from the coriander leaves and stems (e.g., only
0.32 % in leaves) (Matasyoh et al. 2009; Chung et al.
2012) and this is probably be due to peculiar metabolic
and accumulation pathways of C. sativum.
Concerning the larvicidal activity of C. sativum essential
oil, results demonstrated that this EO exerted toxic activity
against A. albopictus larvae. LC50 was 421 ppm (95 % confidence interval, 402.4442.2 ppm; regression equation, y=
0.2346x32.846), while LC90 was 531.7 ppm (95 % confidence interval, 459.6615.0 ppm). Significant differences in
mortality rates as a function of dosage were detected (F=
Table 1 Chemical
composition of the essential oil from C. sativum fruits used in the
toxicity assays

LRI Linear Retention

Index, tr traces

Constituents

LRI

-Pinene
Camphene
Sabinene
-Pinene
Myrcene
p-Cymene
Limonene
-Terpinene
Trans-linalool oxide
Terpinolene
Linalool
Camphor
Borneol
4-Terpineol
-Terpineol

939
954
977
980
991
1,027
1,031
1,062
1,073
1,088
1,099
1,144
1,166
1,178
1,190

1.3
0.2
0.1
0.1
0.4
0.7
1.0
2.8
tr
0.3
83.6
5.0
0.2
0.3
0.4

Decanal
Geraniol
Geranyl acetate
Total

1,205
1,256
1,384

tr
1.7
1.2
99.3

43.96, df=10, P<0.0001; Table 2). At the highest dosages

(500, 550, and 600 ppm), no differences on mortality were
highlighted, with rates ranging from 100 and 87.50 %. At
dosages ranging from 300 to 400 ppm, mortality rates were
lower (from 37.50 to 55.00 %, respectively) and did not differ
from each other. To the best of our knowledge, these data
represent the first evidence of the efficacy of the essential oil
of C. sativum fruits against the Asian tiger mosquito. In
agreement with our results, it was recently observed that the
ether extract of C. sativum seeds was toxic against A. albopictus larvae, since it exerted a comparable LD50 (363.7 ppm)
(Bilal et al. 2012). Similarly, methanol and ethyl acetate
extracts of coriander seeds were toxic against larvae of A.
stephensi and C. quinquefasciatus (Kamaraj et al. 2011).
Also the petroleum ether extract from Korean coriander fruits
showed toxic effects against A. aegypti larvae (LC50 =
20.57 ppm) (Nagella et al. 2012). More generally, the larvicidal properties of C. sativum EO against other mosquito
species are widely recognized. For instance, C. sativum fruits
EO from Lebanon was toxic against the seaside mosquito,
Ochlerotatus caspius Lynch-Arriblzaga, with a LD50 of
156 g/mL after 24 h (Knio et al. 2008). Essential oil from
coriander fruits collected in Iran showed consistent larvicidal
activity against A. stephensi (LC50 =120.95 ppm; Sedaghat et
al. 2011). Lastly, essential oils extracted from coriander leaves
and stems were very effective against A. aegypti larvae, with a
LD50 of 26.93 and 29.39 ppm, respectively (Chung et al.
2012). On the other hand, Chantraine et al. (1998) reported a
low mortality of A. aegypti larvae treated with EO from
Bolivian C. sativum EO (100 mg/L achieved 25 % of larval
mortality). We suppose that these discrepancies could be due
to differences in the constituents of the tested EOs, since it is

Table 2 Mortality obtained in larvicidal test conducted with essential

oil from C. sativum fruits against fourth instar larvae of Aedes albopictus. Each datum represents the mean of four replicates, each setup
with ten larvae. Each mean was followed by a standard deviation. Data
followed by the same letters are not statistically different (P<0.05,
GLM, TukeyKramer HSD test)
Dosage (ppm)

Mortality (%SD)

600
550
500
450
400
350
300
250
200
100
50

1000 a
92.505.00 a
87.509.57 a
60.0021.60 b
55.0012.91 bc
40.0011.55 bcd
37.505.00 bcd
27.5012.58 cde
22.509.57 de
7.505.00 ef
00 f

1159

l
l
l
l
l
l
00
00
00
00
00
00
00 l
00 l
00 l
00 l
0.982.20
31.9718.38 ghijk
00 l
00 l
00 l
1.433.19 l
19.4018.89 ijkl
54.954.38 cdefghi
00 l
00 l
00 l
39.1320.14 fghij
40.5710.42 fghij
88.105.10 abc
46.4723.46 fghi
79. 5023.63 bcd
73.5815.08 cdef
89.1429.06 ab
92.243.25 ab
1000 a
0.004
0.012
0.024
0.040
0.080
0.200

75.698.82 cde
80.7615.58 abc
1000 a
1000 a
1000 a
1000 a

30.6622.18
49.9233.81
54.1216.28
71.0714.85
82.1610.26
1000 a

hijk
efgh
fgh
cdef
bc

5.137.18 kl
6.5912.85 jkl
10.567.59 jkl
62.9719.03 defgh
65.9010.53 cdefg
98.551.30 a

120
90
75
60
45
30
15
0

Time post-application of repellent (min)

Dosage (L/cm2 of skin)

Table 3 Efficacy protection of different dosages of essential oil from C. sativum fruits against A. albopictus during 120 min of observations. Each datum represents the mean of five replicates. Each
mean was followed by a standard deviation. Means followed by different letters are significantly different (P<0.05, GLM, TukeyKramer HSD test)

Parasitol Res (2013) 112:11551161

well known that the chemical composition of an EO may be

affected by geographical origin, growing conditions, and collecting period (Noudjou et al. 2007).
Results from the repellence experiments highlighted that C.
sativum essential oil was also a good repellent against A.
albopictus, even at the lower dosages. The RD 50 was
0.0001565 L/cm2 of skin (95 % confidence interval:
0.00013060.0001876 L/cm2 of skin; regression equation:
y=8742.3x+44.267), while RD90 was 0.002004 L/cm2
(95 % confidence interval: 0.00075270.005333 L/cm2 of
skin). Significant differences in repellence rates were detected
as a function of dosage (F=85.11; df=5; P<0.0001), time (F=
281.89; df=7; P<0.0001) and their interaction (F=6.02; df=
35; P<0.0001). At the highest dosage (0.2 L/cm2 of skin), C.
sativum essential oil can repel more than the 50 % of mosquitoes for at least 75 min (Table 3). At the medium concentration
(0.04 L/cm2 of skin) more than the 60 % of A. albopictus
females were repelled for at least 45 min. Furthermore, at the
maximum dosage the full protection time achieved with C.
sativum essential oil was 60 min, while at the lower concentration (0.08 L/cm2 of skin) the protection did not last more
than 16 min (Table 4). We hypothesize that the repellent
activity of C. sativum EO could be mainly due to the presence
of linalool as major constituent, since this molecule is already
known as an effective repellent against other mosquito species
(Hwang et al. 1985). However, it cannot be neglected the
possible contribution of other volatiles. In agreement with
our results, it was recently reported that methanol and ethyl
acetate extracts of coriander fruits were able to repel adults of
A. stephensi and C. quinquefasciatus for at least 50 min (tested
dose, 500 ppm; Kamaraj et al. 2011). By contrast, Kang et al.
(2009) observed that coriander EO (JinArome, USA) showed
low repellence rates, since a dosage of 0.005 mg/cm2 of skin
gave less than 40 % of repellence after 10 min.
Overall, this study adds knowledge about the composition and the bioactivity of the essential oil extracted from C.
sativum fruits. Coriander essential oil resulted mainly composed by the oxygenated monoterpene linalool. Larvicidal
assays clearly demonstrated the toxicity C. sativum essential
Table 4 Protection time given by the essential oil extracted from C.
sativum fruits. Each datum represents the mean of five replicates. Each
mean was followed by a standard deviation. Means followed by
different letters are significantly different (P<0.05, GLM, Tukey
Kramer HSD test)
Dosage (L/cm2 of skin)
0.004
0.012
0.024
0.04
0.08
0.2

Protection time (min)

0.550.26 a
2.000.33 b
15.441.43 b
18.041.35 b
16.431.40 c
60.264.09 c

1160

oil against A. albopictus, even at low dosages. Furthermore,

the coriander essential oil was able to exert noticeable
repellency against the Asian tiger mosquito. On this basis,
we believe that our findings could be used for the development of new and safer products against A. albopictus.
Acknowledgments We would like to thank Dr. Angelo Canale (University of Pisa) for his insightful critical comments on an earlier
version of the manuscript, Prof. Mario Macchia (University of Pisa)
for providing the C. sativum fruits; Dr. Helen Romito (SantAnna
School of Advanced Studies, Pisa) for proofreading the article; Giulia
Giunti, Raffaele Profeti, and Paolo Giannotti (University of Pisa) for
their kind assistance during experiments and the ten patient volunteers.

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