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Lavicidal and Pupicidal Activities of Petroselinum Crispum Seed Essential Oil on

Culex Pipiens and Culiseta Longiareolata Mosquitoes

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Transylvanian
Review
Vol XXVII, No. 47, 2020

Transylvanian Review
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Hanane Seghier et al. Transylvanian Review: Vol XXVII, No. 47, March 2020

Lavicidal and Pupicidal Activities of Petroselinum Crispum Seed Essential

Oil on Culex Pipiens and Culiseta Longiareolata Mosquitoes
Hanane Seghier1, Fouzia Tine-Djebbar1,2, Wahida Loucif-Ayad2,3 and Noureddine Soltani2
1
Laboratory of Water and Environment, Department of Nature and Life Sciences, Larbi Tebessa University, Tebessa, 12000- Algeria
2
Laboratory of Applied Animal Biology, Badji Mokhtar University, Annaba, 23000- Algeria
3
Faculty of medicine, Badji Mokhtar University, Annaba, 23000- Algeria

ABSTRACT

Background: The use of synthetic insecticides to control mosquitoes has adverse effects on the environment and also causes increasing
resistance. As a result, other alternatives have been developed, among them the use of plant extracts represented mainly by essential oils, which
exhibit acute toxic effects against insects, including mosquitoes. Materials and Methods: The aim of this study was to determine the chemical
composition of Petroselinum crispum (Umbellifereae) essential oil and to evaluate its impact on mortalities, morphometric measurements (weight,
volume) and the biochemical contents (proteins, carbohydrates and lipids) in larvae and pupae of two most abundant mosquito species in Tebessa
(East Algeria), Culex pipiens and Culiseta longiareolata (Diptera: Culicidae). The essential oil was tested at different concentrations ranging between
5 and 60 ppm on newly molted third-instar larvae, between 10 and 70 ppm on newly molted fourth-instar larvae and between 10 and 150 ppm on
instar pupae of the two species of mosquito under standard laboratory conditions according to the World Health Organization recommendations.
Results: Results of phytochemical screening of P. crispum essential oil revealed the presence of flavonoids, saponins, alkaloids, terpenoids and
steroids and twenty-five compounds have been identified by GC/MS. The major compounds were Pulegone (51.06%) and D-Limonene (18.77%).
Insecticidal tests revealed that this essential oil exhibited larvicidal and pupicidal properties with dose-response relationship. P. crispum essential
oil caused a decrease in the weight, the volume and the energy reserves in treated larvae and pupae of the two tested mosquito species. Conclusion:
Due to its mosquitocidal efficacy, P. Crispum essential oil could be considered as an attractive candidate for further study in monitoring resistance
of mosquito vectors.

Keywords: Petroselinum crispum, Essential oils, Toxicity, Culex pipiens, Culiseta longiareolata.

Introduction 2017; Sarma et al. 2017) that include oviposition deterrence and
repellent actions (Aguiar et al. 2015; Costa et al. 2017).
Mosquitoes are an important vector for transmitting life- Petroselinum crispum (Apiaceae) is native to the
threatening human diseases like dengue, chikungunya, malaria, Mediterranean region (Spain, Italy, Greece, Malta, Algeria,
yellow fever, filariasis, japanese encephalitis and lyme which Tunisia and Morocco) and was introduced in worldwide (Craft
inflict millions of death each year (Nwabor et al. et al. 2019). and Setzer, 2017). In the present study, the essential oil from
As there is no specific treatment, mosquito control remains the dried P. crispum seeds was evaluated for their larvicidal and
most important tool in preventing and controlling transmission pupicidal activities against Cx pipiens and Cs longiareolata, the
of these diseases (Scott, 2016). Management of mosquito most abundant mosquito species in Algeria, particularly in
vectors by applying appropriate chemical compounds such as Tebessa area (Tine-Djebbar et al. 2016). The effects of this
larvicides, adulticides is an essential element to minimize selected essential oil were based on the weight and volume of
disease transmission (Monnerat et al. 2012). However, these larvae and pupae bodies and on their biochemical contents
chemicals caused environmental contamination as well as side (proteins, carbohydrates and lipids).
effects to non-target organisms. Moreover, mosquito control
techniques present serious threats because of the emergence of Materials and Methods
resistance to widely used synthetic insecticides (Naqqash et al.
2016). Therefore, there is an urgent need to develop new Plant materials and phytochemical screening
insecticides in order to reduce and restrain the evolution of The seeds of P. crispum were collected in september 2016
further resistance with biodegradable and environmentally safe in Tebessa (Northeast Algeria) and transported to laboratory.
tools (Pavela, 2015). In this way, the use of biopesticides like On dried plant material (seeds) were used for phytochemical
plant derivative products is encouraged as a promising analysis to detect alkaloids, saponins, quinones, flavonoids,
economic and eco-friendly strategy for fighting the resistance leucoanthocyanins, tannins, terpenoids and steroids according
problem (Chansang et al. 2018). to classical reported procedures (Harborne, 1998).
Plant essential oils with insecticidal activity have been
developed as biopesticides (Alattwani et al. 2016). They are Essential Oil’s extraction
produced as secondary metabolites with different bioactive Dried seeds of the plants (50 g) were swollen with 500
compounds as monoterpenoids (Sarma et al. 2017). Essential ml of distilled water and hydrodistilled in a clevenger type
oils have bioactivities against mosquito species, ranging from apparatus for 3 h according to the method recommended in
toxicity with ovicidal, larvicidal, pupicidal (Andrade-Ochoa et the British Pharmacopoeia (1988). The essential oil was dried
al. 2018) to adulticidal activities (Soonwera and Phasomkusolsil, over anhydrous sodium sulphate until all the water was dried


Corresponding author: [email protected]
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Hanane Seghier et al. Transylvanian Review: Vol XXVII, No. 47, March 2020

and then stored in the dark glass bottle at 4oC prior to GC-MS measurements were performed following the procedure of
analysis. The yield of the oil was calculated based on dried Timmermann and Briegel (1998). The body volume
weight of plant materials. corresponds to cubic value of width. The body weight of
individuals from different instars was also determined.
Gas chromatography-mass spectrometry analysis
Analysis of essential oil’s chemical composition was done Biochemical procedure
via GC-MS analysis using Trace GC ULTRA/Polaris Q (GC-MS, The main biochemical constituents (proteins,
Thermo Electron) previously described by Dris et al. (2017). A carbohydrates and lipids) were extracted following the
VB-5 (5% phenyl/95% dimethyl polysiloxane) column (length procedure of Shibko et al. (1966) and quantified as previously
30 m, internal diameter 0.25 mm, film thickness 0.25 μm). The described by Bouabida et al. (2017). Pooled samples (10
column oven temperature was set at 60oC for 8 min, and then individuals per pool) from each stage were weighed and
increased to 250oC at rate of 2oC/min. The injector and detector extracted in 1 ml of trichloracetic acid (20%). The quantification
temperatures were kept respectively at 250 and 270oC. Carrier of proteins was carried following the Coomassie Brilliant Blue
gas was helium, the flow through the column was1ml/min, and G-250 dye-binding method (Bradford, 1976) with bovine serum
the split ratio was set to 50:1 with injection of 0.2 μl of oil albumin as a standard. The absorbance was measured at 595
sample. The GC-mass spectrometry (MS) analysis was nm. Carbohydrates were determined following the method of
performed with a Quadrupole mass spectrometer that operated Duchateau and Florkin (1959) using glucose as standard and
at 70V. Constituent’s identification was based on comparison anthrone as reagent and the absorbance was measured at 620
of retention times with those of corresponding reference nm. Lipids were estimated according to Goldsworthy et al.
standards using the NIST 02 and WILEY 7N libraries (Jennings (1972) using sunflower oil as standard and vanillin as reagent
and Shibamoto, 1980) and by comparison of the retention index with an absorbance at 530 nm. Each assay was conducted with
relatives to n-alkanes of the components with published data 3 replicates per treatment.
(Adams, 2007). The percentage of the essential oils compounds
were calculated according to the area of the chromatographic Data analysis
peaks. The number of individuals tested in each series is given
with the results. Data are presented as mean ± standard
Mosquito rearing deviation (SD). The significance between different series was
Eggs and larvae of Cx pipiens and Cs longiareolata were tested using one-way analysis of variance (ANOVA) followed
collected from untreated areas located at Tebessa (Northeast by Tukey’s multiple comparaison test. All statistical analyses
Algeria). Larvae specimens were morphologically identified were performed using Prism 7.0 for Windows (GraphPad
according to Brunhes et al. (1999) and reared as previously Software Inc., www.graphpad with a significant level p<0.05).
described by Rehimi and Soltani (1999). Each batch of 25 larvae
were kept in pyrex storage jars containing 150 ml of stored tap Results
water and maintained at 25 ± 2 oC. Larvae were fed daily with
fresh food consisting of a mixture of biscuit Petit Regal-dried Phytochemical screening
yeast (75:25 by weight) and water was replaced every two days. The phytochemical screening revealed the presence of
flavonoids, saponins, alkaloids, terpenoids and steroids (Table
Insecticidal bioactivity 1).
Larval and pupal tests were conducted as previously
described by Boudjelida et al. (2005) to determine the lethaly Table 1: Detection of phytochemical constituents
parameters of P. crispum oil on Cx pipiens and Cs longiareolata in Petroselinum crispum seeds.
under laboratory conditions. Different concentrations (5 - 60 No Secondary metabolites Result
ppm for newly molted third-instar larvae), (10 - 70 ppm for 1 Flavonoids +
fourth-instar larvae) and (10 - 150 ppm for pupae) were applied 2 Leucoanthocyanins -
on Cx pipiens and Cs longiareolata for 24 h according to the 3 Quinones -
World Health Organization standard procedure (Anon, 1983; 4 Saponins +
Who, 2005). Essential oils were dissolved in 1ml ethanol solvent 5 Alkaloids +
and then diluted in 150 ml of filtered tap water to obtain the 6 Catechetical tannins -
desired concentrations. The controls were prepared using 1ml 7 Gallic tannins -
of ethanol in 150 ml of water for positive controls and no 8 Terpenoids +
additive for negative ones. After the exposure time (24 h), 9 Steroids +
larvae and pupae were removed, washed with untreated water +: present, - : absent
and placed in clean water. The test was carried out with four
replicates each containing 25 larvae per concentration. Extraction yield and chemical composition of essential oil
Mortality was registered at 24, 48 and 72 hours following The results of the steam distillation showed that the yield
treatment. The mortality obtained was corrected according to of P. crispum essential oil extraction was 2.12 ± 0.32% (dry
Abbott (1925) and lethal concentrations with their 95% seeds of the plant). The percentages and the retention times of
confidence limits (95% CL) were calculated. the identified compounds of EOs of P. crispum are listed in
table 2 and figure 1. Twenty five compounds, representing the
Morphometric measurements total essential oils, were identified. The two major components
As above, newly moulted third and fourth instar larvae were Pulegone (51.06%) and D-Limonene (18.77%) (Figure 2)
and pupae of Cx pipiens and Cs longiareolata were treated with and other components were present in appreciable contents as
essential oil at its LC25 and LC50. The morphometric trans-Verbenol (5.22%), β-Pinene (3.41%), Kessane (3.28%),

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Hanane Seghier et al. Transylvanian Review: Vol XXVII, No. 47, March 2020

Lavandulol (3.03%), trans-Limonene oxide (1.70%) and α- Dose-response relationship was determined for P.
Amorphene (1.54%). The constituents of the essential oils crispum essential oil applied on newly ecdysed third-instar
mainly belonged to six chemical groups: oxygenated larvae, newly ecdysed fourth-instar larvae and instar pupae of
monoterpenes were the most abundant compound group of Cx pipiens and Cs longiareolata. The mortality was scored at
the oil (62.32%), followed by hydrocarbon monoterpene 24, 48 and 72 hours after treatment. The positive controls
(22.53%); oxygenated sesquiterpene (3.69%) and with a small showed no effect of ethanol against Cx pipiens and Cs
amount of hydrocarbon sesquiterpene (1.94%); Ester (1.19%) longiareolata compared to untreated series. The corrected
and hydrocarbon diterpene (0.09%) (Table 3). mortality calculated showed that the rates were ranged for
newly ecdysed third-instar larvae from 10.00% (10 ppm) to
Larvicidal and pupicidal activities 98.33% (60 ppm) and from 6.66% (5 ppm) to 100.00%.
Abundance

Time (min)
Fig.1 GC-MS chromatogram of P. crispum essential oil.

Table 2: Chemical composition of Petroselinum crispum essential oils analyzed by GC-

MS: Retention time (RT) and concentration (%) of the different constituents.
No Compound RT %
1 Cyclohexene (3,5,5-trimethyl-) 6.96 0.06
2 α-Thujene 10.70 0.13
3 β-Pinene 13.40 3.41
4 Myrcene 14.38 0.16
5 D-Limonene 17.23 18.77
6 Sabinene hydrate (cis-) 20.25 0.55
7 Butanoic acid, 3-methyl, methyl-3-butenyl ester 23.30 0.12
8 cis-Limonene oxide 24.44 0.09
9 trans-Limonene oxide 24.84 1.70
10 trans-Verbenol 25.57 5.22
11 Lavandulol 27.15 3.03
12 Dihydro carveol (iso-) 30.03 0.22
13 Pulegone 32.49 51.06
14 Carvone 32.70 0.09
15 Piperitone 33.10 0.07
16 Furfuryl pentanoate 34.32 0.17
17 Cyclohexanolacetate (cis-2-tert-butyl-) 35.75 1.19
18 Caryophyllene (9-epi-(E)- ) 46.88 0.07
19 Aristolochene (4,5-di-epi-) 47.37 0.19
20 α-Amorphene 48.04 1.54
21 48.88 0.14
α-Selinene
22 50.53 3.28
23 Kessane 57.56 0.03
24 β-Eudesmol 57.87 0.38
25 α-Cadinol 73.66 0.09
Rimuene (tetrahydro-)

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 Hanane Seghier et al. Transylvanian Review: Vol XXVII, No. 47, March 2020

Table 3: Chemical group of Petroselinum the most sensitive species and the third instar larvae the most
crispum seed essential oil constituents. sensitive stage (Table 4). After treatment, intoxicated larvae
Grouped components % and pupae showed a change in their behaviour by sinking to
Oxygenated monoterpene 62.32 the bottom of the jar and remaining immobile until they died.
Hydrocarbon monoterpene 22.53
Oxygenated sesquiterpene 3.69 Effects of P. crispum seed EOs on weight and volume
Hydrocarbon sesquiterpene 1.94 Changes in whole body weight and volume were
Hydrocarbon diterpene 0.09 estimated for the third and fourth larvae and for the pupae
Ester 1.19 stages of Cx pipiens and Cs longiareolata at different times
following the treatment with P. crispum EO (Table 6). Results
(30 ppm), for newly ecdysed fourth-instar larvae from showed that LC25 and LC50 decreased the body weight for the
8.33% (20 ppm) to 98.33% (70 ppm) and from 10.67% (10 three stages and for the two mosquito species. Also, P. crispum
ppm) to 100.00% (40 ppm) and for instar pupae from 1.66% EO significantly reduced the body volume of third; fourth instar
(10 ppm) to 96.67% (150 ppm) and from 21.33% (10 ppm) to larvae and instar pupae at the two concentrations (LC25 and
100.00% (150 ppm) for Cx pipiens and Cs longiareolata, LC50) compared to the controls for the two species.
respectively. Based on the LC values, Cs longiareolata appeared
Table 4: Sublethal and lethal concentrations (ppm, 95 % fudicial limit, FL) of P. crispum seed essential oil against third and fourth instar larvae and instar
pupae of Cx pipiens and Cs longiareolata.
Cx pipiens Cs longiareolata
Time LC25, ppm LC50, ppm LC90, ppm r2 LC25, ppm LC50, ppm LC90, ppm
Instar (hours) r2
(95 % FL) (95 % FL) (95 % FL) (95 % FL) (95 % FL) (95 % FL)
19.69 31.37 79.67 0.95 9.99 13.11 22.60
24 0.99
(12.59-26.77) (25.08-37.65) (55.92-147.6) (9.20-10.81) (12.38-13.88) (20.28-25.52)
19.37 30.06 72.38 0.96 9.38 11.89 19.10
L3 48 0.99
(12.81-25.85) (24.28-35.74) (52.10-123.6) (8.31-10.45) (10.98-12.87) (16.27-22.93)
19.75 28.22 56.45 0.94 9.38 11.89 19.10
72 0.99
(11.06-29.11) (20.52-35.39) (39.44-107.8) (8.31-10.45) (10.98-12.87) (16.27-22.93)
31.35 40.65 68.33 21.18 24.45 32.57
24 0.98 0.94
(26.52-35.94) (36.84-44.40) (58.29-84.01) (12.57-26.05) (19.10-28.28) (26.24-60.95)
31.58 39.78 67.32 19.67 22.04 27.70
L4 48 0.98 0.98
(26.07-34.87) (36.19-43.33) (57.71-81.88) (17.16-21.42) (20.56-23.51) (24.25-32.93)
28.73 38.55 69.45 19.66 22.04 27.70
72 0.97 0.98
(22.54-34.60) (33.54-43.53) (56.17-93.69) (16.56-21.69) (20.28-23.72) (23.66-34.14)
80.79 102.9 167.1 31.29 56.72 186.3
24 0.95 0.95
(38.78-111.0) (74.03-127.9) (119.8-514.3) (10.69-60.74) (32.65-84.74) (95.69-754.1)
64.23 88.91 170.4 14.22 33.04 178.3
Pupae 48 0.96 0.96
(30.41-94.51) (61.50-113.1) (111.0-479.4) (5.00-27.65) (19.08-50.86) (86.23-578.2)
58.59 82.11 161.3 12.02 25.54 115.2
72 0.97 0.95
(31.11-81.90) (58.96-102.6) (106.0-353.4) (3.51-24.50) (13.12-42.48) (48.64-407.6)

Effect of P. crispum EOs on biochemical composition of bodies pipiens with LC50 and of Cs longiareola with LC25 and LC50 at the
The levels of carbohydrates, lipids and proteins have been estimated three times. Concerning the carbohydrate levels, a significant
in the whole body extracts from third, fourth larval and pupal stages reduction was observed in the two larval stages of Cx pipiens and in
of Cx pipiens and Cs longiareolata at different times following the larval and pupal stages of Cs longiareolata with the sublethal
treatment using two sublethal concentrations (LC25 and LC50) of P. concentration LC25 and LC50. Lastly, the lipid content was also
crispum essential oil (Table 7). The comparison of mean values reduced significantly with the two tested concentrations when
shows that the protein content decreased significantly in the third compared to control at 48 and 72 hours in the fourth larval stage of
larval stage of Cx pipiens and Cs longiareolata at 24, 48 and 72 hours Cx pipiens and at the three times in all stages of Cs longiareolata.
with the lethal concentration LC50 and in the pupal stage of Cx

Table 5: Effect of P. crispum essential oil (LC25 and LC50) on the body weight (mg) and the body volume (mm3) at 24, 48 and 72h after treatment in the third and
fourth instar larvae and instar pupae of Cx pipiens and Cs longiareolata (mean ± SD, n= 3 pools each containing 10 individuals).
Time Cx pipiens Cs longiareolata
Instar (hours) Control LC25 LC50 Control LC25 LC50
L3 24 Body weight (mg) 0.96 ± 0.03 a 0.49 ± 0.05 b 0.41 ± 0.00 b 1.57 ± 0.00 a 1.29 ± 0.05 b 0.82 ± 0.05 c
Body volume (mm3) 0.77 ± 0.01 a 0.40 ± 0.04 b 0.37 ± 0.01 b 1.92 ± 0.24 a 1.55 ± 0.10 b 0.71 ± 0.11 c
48 Body weight (mg) 1.13 ± 0.11 a 0.75 ± 0.01 b 0.69 ± 0.07 b 1.85 ± 0.09 a 1.64 ± 0.03 b 1.02 ± 0.03 c
Body volume (mm3) 0.87 ± 0.02 a 0.66 ± 0.04 b 0.61 ± 0.01 b 1.83 ± 0.15 a 1.48 ± 0.17 b 0.56 ± 0.10 c
72 Body weight (mg) 1.30 ± 0.07 a 0.95 ± 0.04 b 0.90 ± 0.10 b 2.10 ± 0.14 a 1.84 ± 0.09 b 1.78 ± 0.07 b
Body volume (mm3) 1.08 ± 0.08 a 0.80 ± 0.11 b 0.79 ± 0.03 b 2.32 ± 0.07 a 1.81 ± 0.18 b 1.80 ± 0.00 b
L4 24 Body weight (mg) 1.75 ± 0.10 a 1.51 ± 0.36 a 1.48 ± 0.05 a 2.29 ± 0.21 a 2.07 ± 0.33 ab 1.78 ± 0.22 b
Body volume (mm3) 1.96 ± 0.39 a 1.82 ± 0.10 ab 1.59 ± 0.06 b 2.69 ± 0.02 a 1.88 ± 0.07 b 1.29 ± 0.20 c

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Hanane Seghier et al. Transylvanian Review: Vol XXVII, No. 47, March 2020

48 Body weight (mg) 2.21 ± 0.40 a 1.56 ± 0.01 b 1.41 ± 0.06 b 2.84 ± 0.24 a 2.08 ± 0.13 b 1.80 ± 0.21 b
Body volume (mm3) 2.90 ± 0.27 a 1.50 ± 0.05 b 1.44 ± 0.04 b 4.46 ± 0.33 a 1.68 ± 0.07 b 1.28 ± 0.10 c
72 Body weight (mg) 2.50 ± 0.16 a 1.64 ± 0.04 b 1.20 ± 0.10 c 4.60 ± 0.22 a 3.01 ± 0.26 b 2.47 ± 0.17 c
3
Body volume (mm ) 3.68 ± 0.14 a 1.48 ± 0.10 b 1.45 ± 0.13 b 5.74 ± 0.12 a 3.51 ± 0.22 b 2.93 ± 0.07 c
Pupa 24 Body weight (mg) 2.84 ± 0.08 a 1.92 ± 0.12 b 1.81 ± 0.14 b 4.84 ± 0.14 a 4.19 ± 0.15 ab 3.74 ± 0.14 b
Body volume (mm3) 4.82 ± 0.17 a 3.86 ± 0.12 b 3.69 ± 0.19 b 17.01 ± 1.73 a 11.17 ± 0.75 b 9.56 ± 0.79 b
48 Body weight (mg) 2.99 ± 0.13 a 1.81 ± 0.12 b 1.58 ± 0.03 c 5.44 ± 0.24 a 4.06 ± 0.50 b 3.41 ± 0.16 b
Body volume (mm3) 4.98 ± 0.17 a 3.54 ± 0.08 b 3.30 ± 0.17 b 17.45 ± 1.15 a 8.29 ± 0.65 b 7.07 ± 0.50 b
72 Body weight (mg) 3.05 ± 0.06 a 1.46 ± 0.11 b 1.32 ± 0.01 b 5.50 ± 0.50 a 3.41 ± 0.52 b 3.11 ± 0.11 b
Body volume (mm3) 5.04 ± 0.18 a 3.29 ± 0.15 b 3.03 ± 0.16 b 18.58 ± 2.01 a 4.98 ± 0.34 b 3.88 ± 0.34 b
Different small letters indicate a significant difference between control and treated individuals (p < 0.05).

Table 6: Effect of P. crispum seed essential oil (LC25 and LC50) on contents of proteins, carbohydrates and lipids (µg/individual) at 24, 48 and 72h after treatment in the
third and fourth instar larvae and instar pupae of Cx pipiens and Cs longiareolata (mean ± SD, n= 3 pools each containing 10 individuals).
Time Culex pipiens Culiseta longiareolata
Instar (hours) Components Control LC25 LC50 Control LC25 LC50
L3 24 Proteins 29.84 ± 1.32 a 29.85 ± 1.91 a 17.71 ± 4.19 b 32.38 ± 1.36 a 29.32 ± 0.87 a 12.10 ± 0.10 b
Carbohydrates 29.35 ± 3.07 a 26.81 ± 0.53 a 21.46 ± 9.56 a 26.40 ± 6.14 a 23.74 ± 0.44 b 15.90 ± 0.33 b
Lipids 50.28 ± 7.73 a 51.59 ± 4.32 a 48.86 ± 7.53 a 44.65 ± 2.38 a 45.79 ± 0.79 a 43.29 ± 4.66 a
48 Proteins 38.23 ± 4.12 a 36.46 ± 5.88 a 28.38 ± 1.91 b 32.45 ± 0.75 a 30.29 ± 0.96 ab 24.75 ± 8.75 b
Carbohydrates 30.84 ± 0.88 a 24.35 ± 6.14 a 14.74 ± 1.33 b 25.93 ± 5.61 a 18.06 ± 4.58 b 13.66 ± 0.75 b
Lipids 56.52 ± 2.13 a 56.55 ± 0.88 a 51.25 ± 9.20 a 52.04 ± 2.27 a 50.37 ± 1.25 a 50.00 ± 0.01 a
72 Proteins 35.87 ± 4.70 a 31.17 ± 1.76 a 22.94 ± 3.52 b 49.31 ± 0.84 a 32.20 ± 2.80 b 27.00 ± 0.30 b
Carbohydrates 26.96 ± 1.95 a 21.47 ± 1.80 a 11.40 ± 1.84 b 19.33 ± 0.77 a 16.48 ± 1.09 ab 10.75 ± 0.40 b
Lipids 53.07 ± 1.93 a 51.82 ± 1.59 a 47.57 ± 2.13 a 44.65 ± 2.84 a 35.90 ± 2.04 b 36.36 ± 1.36 b
L4 24 Proteins 36.32 ± 0.15 a 33.55 ± 1.91 a 29.99 ± 4.11 a 27.20 ± 7.20 a 25.73 ± 1.15 a 19.95 ± 5.25 a
Carbohydrates 62.68 ± 8.04 a 41.89 ± 5.26 b 38.46 ± 1.80 b 46.01 ± 0.44 a 32.77 ± 0.01 b 21.18 ± 0.52 c
Lipids 52.39 ± 4.43 a 50.34 ± 2.07 a 50.33 ± 2.97 a 38.33 ± 8.41 a 26.13 ± 1.13 b 20.66 ± 0.99 b
48 Proteins 28.82 ± 1.47 a 28.66 ± 5.81 a 18.96 ± 4.26 b 28.20 ± 4.70 a 28.51 ± 2.03 a 27.00 ± 5.00 a
Carbohydrates 30.75 ± 5.00 a 21.63 ± 10.61 ab 16.26 ± 4.72 b 39.25 ± 2.45 a 21.10 ± 3.25 b 15.46 ± 1.51 c
Lipids 61.97 ± 9.43 a 51.06 ± 4.43 b 42.78 ± 6.31 b 37.61 ± 7.61 a 27.12 ± 1.65 a 26.58 ± 0.88 a
72 Proteins 32.74 ± 5.31 a 29.55 ± 3.16 a 29.49 ± 2.11 a 33.67 ± 6.25 a 34.25 ± 6.25 a 27.60 ± 7.60 a
Carbohydrates 41.54 ± 4.91 a 28.26 ± 4.78 b 27.92 ± 3.99 b 39.58 ± 0.58 a 26.45 ± 0.01 b 6.73 ± 0.07 c
Lipids 72.75 ± 2.84 a 48.18 ± 0.91 b 55.80 ± 1.47 b 81.63 ± 1.00 a 35.56 ± 7.61 b 38.63 ± 9.54 b
Pupa 24 Proteins 32.17 ± 3.08 a 28.46 ± 5.49 a 19.38 ± 3.00 b 42.64 ± 8.82 a 31.41 ± 1.14 b 29.01 ± 3.70 b
Carbohydrates 20.27 ± 0.94 a 17.91 ± 4.25 a 17.94 ± 4.97 a 26.54 ± 2.54 a 15.58 ± 5.96 b 15.99 ± 1.66 b
Lipids 25.73 ± 0.87 a 25.29 ± 2.04 a 24.40 ± 0.84 a 34.99 ± 8.41 a 16.30 ± 1.16 b 15.60 ± 1.78 b
48 Proteins 25.91 ± 3.59 a 21.10 ± 2.12 a 14.30 ± 1.77 b 34.01 ± 6.72 a 21.60 ± 1.29 b 19.45 ± 0.85 b
Carbohydrates 15.82 ± 0.50 a 14.45 ± 1.92 a 14.66 ± 4.32 a 23.37 ± 0.55 a 16.89 ± 0.61 b 13.00 ± 0.90 b
Lipids 37.99 ± 6.47 a 35.90 ± 0.24 a 34.51 ± 4.55 a 46.48 ± 8.07 a 24.16 ± 0.94 b 23.83 ± 5.17 b
72 Proteins 17.85 ± 2.88 a 16.41 ± 0.85 a 10.11 ± 0.12 b 26.17 ± 1.17 a 17.02 ± 0.24 b 16.05 ± 3.12 b
Carbohydrates 19.59 ± 4.93 a 17.06 ± 4.54 a 16.62 ± 2.94 a 26.37 ± 5.00 a 15.18 ± 2.01 b 13.99 ± 0.87 b
Lipids 49.99 ± 1.53 a 46.45 ± 5.41 a 44.09 ± 1.14 a 61.25 ± 3.30 a 39.27 ± 1.15 b 38.44 ± 3.49 b
Different small letters indicate a significant difference between control and treated individuals (p < 0.05).

Discussion Serbia and 3.44% to 4.45% in China of EOs of dried matter

respectively. Many studies showed that several factors can affect the
Phytochemical screening essential oil contents of parsley yield like water deficit during plant
In the present study, the seeds phytochemical screening growth (Petropoulos et al. 2008; Borges et al. 2016), the lighting
showed a similarity with those obtained by Tadros et al. (2017) who conditions during plant growth (Ascrizzi et al. 2018), irrigation dose
found that parsley seeds from Egypt contain alkaloids, flavonoids, and plant density (El-Zaeddi et al. 2016) or extraction technique
terpenes, tannins, glycosides and saponins. Furthermore, the result (Stankovic et al. 2004; Stankovic et al. 2005; Dong et al. 2017). On
of the phytochemical analysis of the leaves obtained by Al-Hadi et the other hand, the yield of extraction of essential oil seeds of P.
al. (2013) from the samples of the same species in Oman showed the crispum is also higher compared with the yield of EOs of the leaves
presence of phenolic compound and tannins, flavonoids, alkaloids from the same species. In Colombia (Pineda et al. 2018), Estonia
and saponins. Many studies showed that the seeds of P. crispum are (Vokk et al. 2011) and USA (Craft and Setzer, 2017), authors found a
rich in flavonoids and total phenolic (Farzaei et al. 2013; Mert and yield of 0.11%; 0.24%- 0.29% and 0.19% - 0.60% respectively. The
Timur, 2017; Tadros et al. 2017), which confirms their antioxidant relative good performance achieved in our study may be due to the
properties (Chauhan and Aishwarya, 2018) and antimicrobial drought that characterizes the Tebessa region as it is known that the
activities (Tadros et al. 2017). maximum yields are achieved in dry weather.

Extraction yield Chemical composition

The yield of EO isolated by hydrodistillation from P. crispum In comparison with the previous studies about the constituent
seeds (2.12 ± 0.32%) is higher compared to this obtained from the of parsley seed essential oil in other countries, the constituent of
same species in West Algeria (0.14%) in the region of Mascara (Nawel parsley seed oil in Algeria (Tebessa) has the similarities and
et al. 2012) and lower than the EOs extracted from the samples differences. Several studies showed the presence of β-Pinene,
collected in Turkey (2.52%) (Mert and Timur, 2017). Stankovic et al. Limonene, Sabinene, Caryophyllene, α-Thujene, Myrcene, Carvone,
(2004) and Dong et al. (2017) found a yield of 0.87% to 3.12% in Amorphene and Eudesmol (Stankovic et al. 2004; Dong et al. 2017;
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Hanane Seghier et al. Transylvanian Review: Vol XXVII, No. 47, March 2020

Mert and Timur, 2017; Mahmoodi et al. 2014; Louli et al. 2004; Thymus broussonetti and Thymus maroccanus with LC50 of 0.23 and
Farzaei et al. 2013). The literature data suggest that P. crispum is a 0.31 ppm and LC90 of 0.76 and 1.53 ppm against the fourth instar
chemical polymorph species in both the qualitative and/or larvae of Cx pipiens, respectively. Similarly, Vatandoost et al. (2012)
quantitative composition. It has been found that the parsley oils reported that the Kelussia odoratissima Mozaffarian EO exhibited a
seeds from Turkey contain major components, 3-methoxy-γ-asarone toxic effect against the fourth instar larvae of Cx pipiens and An
(21.82-34.19%), Apiol (17.02-27.53%) (Mert and Timur, 2017); from stephensi with an LC50 of 2.69 and 4.88 ppm and an LC90 of 7.90
Serbia, α-Thujene (10.76-54.00%), Apiol (27.59-49.43%) (Stankovic and 9.60 ppm respectively, where the main component was Z-
et al. 2004); from Greece, Myristicin (36.00-42.00%), Apiol (26.70- ligustilide (77.73 %).
34.60%) (Louli et al. 2004); from China, Myristicin (79.58-85.59%) On the other hand, the toxic effect of seven plants EOs was
(Dong et al. 2017) and from Azerbaijan, Myristicin (42.65%), β- examined on third instar larvae and instar pupae of Cx
Phellandrene (21.83%) (Mahmoodi et al. 2014). This variability in the quinquefasciatus and the LC50 was ranged between 4.60 and 49.00
chemical composition of the EO of parsley is also can explained by µg/ml for the third instar larvae and between 51.60 and 236.5 µg/ml
water deficit during plant growth (Petropoulos et al. 2008; Borges for the instar pupae (Andrade-Ochoa et al. 2018). The obtained
et al. 2016), the lighting conditions during plant growth (Ascrizzi et results by Sarma et al. (2017) revealed that the larval stage of Cx
al. 2018), irrigation dose and plant density (El-Zaeddi et al. 2016), quinquefasciatus is more susceptible to the Aegle marmelos essential
seasonal variation (Vokk et al. 2011) and extraction technique oil among all the developmental stages. Also, the study of Soonwera
(Stankovic et al. 2004, Stankovic et al. 2005; Dong et al. 2017). The and Phasomkusolsil (2017) indicate that Z. limonella oil was most
analysis of the phenolic compounds in seeds of the samples of P. effective against immature stages of both Ae aegypti and Cx
crispum from Egypt has led to the identification of 35 components quinquefasciatus.
where the most detected compound was rosmarinic acid followed by
reversetrol, naringin, pyrogallol, salicylic acid, benzoic acid and ellagic Effects on weight and volume of body
acid (Tadros et al. 2017). On the other hand, several differences in The body size is an important trait for mosquitoes because of
the chemical composition of the EO when comparing between seeds its influence on the blood-feeding ability, host attack rate and
and leaves from the same species (Díaz-Maroto et al. 2002; Farzaei fecundity. All of these traits are determinants for their potential to
et al. 2013; Khalil et al. 2015; Maroufpoor et al. 2016; Petropoulos et transmit diseases (Farjana and Tuno, 2013). In this study, a significant
al. 2008; Pineda et al. 2018; Vokk et al. 2011). reduction in the weight and volume of larvae and pupae body was
observed after treatment by P. crispum EO (LC25 and LC50) compared
Insecticidal activity to controls of Cx pipiens and Cs longiareolata. Dris et al. (2017b)
Our results indicate that P. crispum essential oil and their showed that O. basilicum EO (LC50) decreased significantly the
active components (Pulegone and D-Limonene) showed an weight and volume of body of larvae, pupae, male and female adults.
interesting insecticidal activity against mosquito larvae of Cx pipiens Moreover, insecticides were also found to reduce significantly the
and Cs longiareolata for the three stages, where larvae is less body weight, Novaluron in third and fourth larval stage of Cs
sensitive than pupae and Cx pipiens is more resistant than Cs longiareolata (Bouaziz et al. 2011) and Spiromesifen in fourth larval
longiareolata. The insecticidal activity is related to the compounds stage of Cs longiareolata (Bouabida et al. 2017).
present in the essential oil including its quality and quantity
(Suttthanont et al. 2010). Thus, volatile oil from Mentha pulegium Effect on biochemical composition of bodies
showed LC50 values of 38.75 and 28.16 ppm and LC90 values of 85.91 In insects, the hemolymph undergoes metabolic modification
and 53.75 ppm against fourth instar larvae of Cx pipiens and Ae during the developmental stages (Cohen, 2010; Sugumaran, 2010).
caspius respectively, where Pulegone was the main compound of this Energy storage in adult Dipterans is generally in the form of
oil (Guenez et al. 2018). Perumalsamy et al. (2009) demonstrated carbohydrate, which is used for flight metabolism, and lipid, which
that (+)-Limonene had an excellent larvicidal activity against third provides the energy at rest (Gray and Bradley, 2003). The exposure
instar larvae of Cs pipiens, Ae aegypti and Ochlerotatus togoi in 24h of an organism to xenobiotic products can modify the synthesis of
with an LC50 value of 13.26, 24.47, and 19.20 ppm, respectively. Also, some metabolites and disturb its functionality (Rodriguez-Ortega et
Manimaran et al. (2012) have examined the larvicidal activity of the al., 2003). Biochemical analyzes revealed a decrease in the levels of
essential oils extracted from eight plants against third instar larvae proteins, carbohydrates and lipids in whole body of larvae and pupae
of Ae aegypti and the LC50 of these oils ranged between 39.74 and treated by P. crispum essential oil compared to control series.
68.45 ppm for Anopheles stephensi and between 40.40 and 91.23 The carbohydrates is considered as important energy elements
ppm for Cx quinquefasciatus. playing a crucial role in the physiology of the insects, such as the
Guenez et al. (2018) found that the Mentha pulegium essential molt and the reproduction (Kaufmann and Brown, 2008). This
oil exhibits a larvicidal activity against Aedes caspius and C pipiens component was reduced in larvae of Spodoptera littoralis after
larvae; while Dris et al. (2017a, b) showed an insecticidal activity of treatment with essential oil of A. indica and Citrullus colocynthis
Ocimum basilicum and Lavandula dentata essential oils against the methylene chloride extract and was increased with garlic and lemon
fourth instar larvae of Cx pipiens. Also in Bouguerra et al. (2018), essential oils (Ali et al. 2017). This is in accord with the observations
the larvicidal activity of the essential oil extracted from Thymus of Dris et al. (2017b) and Bouguerra et al. (2018) where they found
vulgaris against the same species of mosquito have examined and the a significant reduction in the levels of proteins, carbohydrates and
lethal concentrations showed a variations according to the periods lipids in all stages of development of Cx pipiens treated by O.
after treatment: 24, 48 and 72h (LC50: 72.04; 68.61 and 62.12ppm basilicum essential oil and in the fourth larval stage of Cx pipiens
and LC90: 207.01; 190.54 and 169.82 ppm). Similar variations in the treated by T. vulgaris essential oil.
sensitivities of mosquito species to essential oils were demonstrated, Lipids are also an important source of the acetyl groups needed
and these differences could be attributed to physiological differences to synthesize the enzymes constitutive amino acids (Rivero et al.,
between species (Amer and Mehlhorn, 2006). 2010). A reduction of total lipid in S. littoralis larvae treated with
In other studies, the sublethal and lethal concentrations of garlic and lemon oils was noted (Ali et al. 2017). Dris et al. (2017)
other plant essential oils were lower as compared to our results. and Bouguerra et al. (2018) have reported a decrease in the total
Belaqziz et al. (2010) found a larvicidal activity of the volatile oil of lipid content in Cx pipiens mosquito treated with O. basilicum and
T. vulgaris essential oils respectively. The decline of lipid levels might
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Hanane Seghier et al. Transylvanian Review: Vol XXVII, No. 47, March 2020

be due to the effect of these oils on the mobilization of lipid reserves Adams, R.P., 2007. Identification of essential oil components by gas
for energy production as a result of induced stress (Canavoso et al. chromatograph/mass spectrometry. Carol Stream, USA,
2001). Allured Publishing Corporation.
Protein synthesis is necessary for maintaining body growth and Aguiar, R.W.S., Santos, S.F.D., Morgado, F.D.S., Ascencio, S.D., Lopes,
reproduction. They are involved in various reactions such as the M.D.M., Viana, K.F., Didonet, J., Ribeiro, B.M., 2015. Insecticidal
hormonal regulation and they are integrated in the cell as a and repellent activity of Siparuna guianensis Aubl. (Negramina)
structural element with the carbohydrates and the lipids (Cohen, against Aedes aegypti and Culex quinquefasciatus. PLoS One.
2010; Sugumaran, 2010). Previous observations were reported a 10, 1–14.
reduction in the total proteins content of S. littoralis larvae when Alattwani, R.R.H., Abudaljalil, R.K., Alhashimi, R.A.H., 2016. Chemical
treated with garlic and lemon extracts (Ali et al. 2017). Such decrease composition and antimicrobial and antioxidant activities of
in energetic resources can have drastic consequences for insects Petroselinum crispum (Mill) nym essential oil isolated from
(Rivero et al. 2010). This depletion might be due to their degradation maysan city iraq. Global Journal of Advanced Research. 3, 151–
for metabolic purposes or to an impaired incorporation of amino 156.
acids into polypeptide chains or inhibition of protein synthesis Al-Hadi, AH., Al Rahbi, S.S., Akhtar, M.S., Said, S., Weli, A., Al-Riyami,
(Sharma et al. 2011) or to the breakdown of these proteins into amino Q., 2013. Phytochemical screening, antibacterial and cytotoxic
acids used in the compensatory mechanism as energy source to activities of Petroselinum crispum leaves grown in Oman.
compensate stress (Ali et al. 2014). Iranian Journal of Pharmaceutical Sciences. 9, 61–65.
Ali, A.M., Mohamed, D.S., Shaurub, E.S.H., Elsayed, A.M., 2017.
Conclusion Antifeedant activity and some biochemical effects of garlic and
lemon essential oils on Spodoptera littoralis (Boisduval)
In the present study, it can be concluded that the essential oil (Lepidoptera: Noctuidae). Journal of Entomology and
of P. crispum with Pulegone and D-Limonene as major compounds Zoological Studies. 5(3), 1476–1482.
showed a larvicidal and pupicidal activities against Cx pipiens and Ali, N.S., Ali, S.S., Shakoori, A.R., 2014. Biochemical response of
Cs longiareolata. Moreover, the P. crispum essential oil appeared to malathion-resistant and susceptible adults of Rhyzopertha
be more toxic against Cs longiareolata as compared to Cx pipiens dominica to the sublethal doses of deltamethrin. Pakistan
and more toxic against the larval stage in comparison to the pupal Journal of Zoology. 46, 853–861.
stage. Furthermore, this essential oil disrupt the main biochemical Amer, A., Mehlhorn, H., 2006. Larvicidal effects of various essential
components, induced a decrease in the weight and the volume of oils against Aedes, Anopheles, and Culex larvae (Diptera:
larvae and pupae of the two tested mosquito species. Due to its Culicidae). Parasitology Research. 99, 466–472.
mosquitocidal efficacy, P. Crispum essential oil could be considered Andrade-Ochoa, S., Sánchez-Aldana, D., Chacón-Vargas, K.F., Rivera-
as an attractive candidate for further study in monitoring resistance Chavira, B.E., Sánchez-Torres, L.E., Camacho, A.D., Nogueda-
of mosquito vectors. Torres, B., Nevárez-Moorillón, G.V., 2018. Oviposition deterrent
and larvicidal and pupaecidal activity of seven essential oils and
Acknowledgements their major components against Culex quinquefasciatus Say
(Diptera: Culicidae): Synergism–antagonism Effects. Insects. 9,
1–17
This work was supported by the National Fund for Scientific Anonym., 1983. Informal consultation on insect growth regulators.
Research to Pr. N. SOLTANI (Laboratory of Applied Animal Biology) WHO/VBC/83.
and the Ministry of High Education and Scientific Research of Algeria Ascrizzi, R., Fraternale, D., Flamini, G., 2018. Photochemical response
(CNEPRU Project to Dr. F. TINE-DJEBBAR). of parsley (Petroselinum crispum (Mill.) Fuss) grown under
red light: The effect on the essential oil composition and yield.
Conflict of Interest Journal of Photochemistry and Photobiology, B: Biology. 185,
185-191.
Pr TINE-DJEBBAR F has received research grants from Ministry Belaqziz, R., Harrak, R., Romane, A., Oufdou, K., El Alaoui ElFels,
of High Education and Scientific Research of Algeria (CNEPRU M.A., 2010. Antimicrobial and insecticidal activities of the
project, grant number D01N01UN120120130005). endemic Thymus broussonetti Boiss. and Thymus maroccanus
Pr. SOLTANI N is a headmaster of Laboratory of Applied Ball. Records of Natural Products. 4, 230-237.
Animal Biology, University of Badji mokhtar, Annaba. Borges, I.B., Cardoso, B.K., Silva, E.S., de Oliveira, J.S., da Silva, R.F.,
BOUGUERRA N declares that she has no conflict of interest. de Rezende, C.M., Gonçalves, J.E., Junior, R.P., de Souza, S.G.H.,
Gazim, Z.C., 2016. Evaluation of performance and chemical
Author's Contribution composition of Petroselinum crispum essential oil under
different conditions of water deficit. African Journal of
All authors are equally contributed to this study. Agricultural Research. 11, 480-486.
Seghier Hanane, Tine-Djebbar Fouzia and Soltani Noureddine, Bouabida, H., Tine-djebbar F, Tine, S., Soltani, N., 2017. Activity of a
designed and carried out the experimental study. Tine-Djebbar lipid synthesis inhibitor (spiromesifen) in Culiseta longiareolata
Fouzia analysed data. Tine-Djebbar Fouzia, Seghier Hanane, Loucif (Diptera: Culicidae). Asian Pacific Journal of Tropical
Wahida and Soltani Noureddine wrote the manuscript. All authors Biomedicine. 7, 1120–1124.
approved the manuscript. Bouaziz, A., Boudjelida, H., Soltani, N., 2011. Toxicity and perturbation
of the metabolite contents by a chitin synthesis inhibitor in the
References mosquito larvae of Culiseta longiareolata. Annals of Biological
Research. 2, 134–142.
Boudjelida, H., Bouaziz, A., Soin, T., Smagghe, G., 2005. Effects of
Abbott, W.B., 1925. A method for computing the effectiveness of an
ecdysone agonist halofenozide against Culex pipiens. Pesticide
insecticide. Journal of Economic Entomology. 18, 265–267.
Biochemistry and Physiology. 83, 115–123.

14675
Hanane Seghier et al. Transylvanian Review: Vol XXVII, No. 47, March 2020

Bouguerra, N., Tine-Djebbar, F., Soltani, N., 2018. Effect of Thymus Farzaei, M.H., Abbasabadi, Z., Ardekani, M.R.S., Rahimi, R., Farzaei,
vulgaris L. (Lamiales: Lamiaceae) Essential oil on energy F., 2013. Parsley: a review of ethnopharmacology,
reserves and biomarkers in Culex pipiens L. (Diptera: phytochemistry and biological activities. Journal of Traditional
Culicidae) from Tebessa (Algeria). Essential Oil Bearing Plants Chinese Medicine. 15, 815–826.
Journal. 21, 1082–1095. Goldsworthy, A.C., Mordue, W., Guthkelch, J., 1972. Studies on insect
Bradford, M.M., 1976. A rapid and sensitive method of the adipokinetic hormones. General and Comparative
quantitation microgram quantities of protein utilising the Endocrinology. 18, 306–314.
principale dye binding. analytic. The Biochemistry. 72, 248– Gray, E.M., Bradley, T.J., 2003. Metabolic rate in female Culex tarsalis
254. (Diptera: Culicidae): Age, size, activity, and feeding effects.
British pharmacopoeia. 1988. London: HMSO. 2, A137-A138. Journal of Medical Entomology. 40, 903–911.
Brunhes, J., Rhaim, A., Geoffroy, B., Angel, G., Hervy, J.P., 1999. Les Guenez, R., Tine-Djebbar, F., Tine, S., Soltani, N., 2018. Larvicidal
moustiques de l'Afrique méditerranéen. Logiciel d'identification efficacy of Mentha pulegium essential oil against Culex pipiens
et d'enseignement. IRD edition. L. and Aedes caspius P. larvae. World Journal of Environmental
Canavoso, L.E., Jouni, Z.E., Karnas, K.J., Pennington, J.E., Wells, M.A., Biosciences. 7, 1–7.
2001. Fat metabolism in insects. Annual Review of Nutrition. Kalita, B., Bora, S., Sharma, A.K., 2013. Plant essential oils as mosquito
21, 23–46. repellent. International Journal of Research and Development
Chansang, A., Champakaew, D., Junkum, A., Jitpakdi, A., in Pharmacy and Life Sciences. 3, 741–747.
Amornlerdpison, D., Kongdee Aldred, A., Riyong, D., Wannasan, Khalil, A.F., Elkatry, H.O., Hanaa, F., El Mehairy, H.F., 2015. Protective
A., Intirach, J., Muangmoon, R., and Pitasawat, B., 2018. Synergy effect of peppermint and parsley leaves oils against
in the adulticidal efficacy of essential oils for the improvement hepatotoxicity on experimental rats. Annals of Agricultural
of permethrin toxicity against Aedes aegypti L. (Diptera: Science. 60, 353–359.
Culicidae). Parasites & Vectors. 11, 417. Harborne, J.B., 1998. Phytochemical Methods. London: Chapman and
Chauhan, E. S., Aishwarya, J., 2018. Nutraceuticals potential of Hall.
Petroselinum Crispum: A review. International Journal on Jennings, W., Shibamoto, T., 1980. Qualitative analysis of flavour and
Complementary & Alternative Medicine. 7, 1–6. fragrance volatile by glass capillary gas chromatography. New
Cohen, E., 2010. Advances in Insect Physiology: Insect Integument York: Academic Press.
and Colour (Chap. 2 - Chitin Biochemistry: Synthesis, Kaufmann, C., Brown, M.R., 2008. Regulation of carbohydrate
Hydrolysis and Inhibition). London (UK): Academic Press. p. metabolism and flight performance by a hypertrehalosaemic
5–74. hormone in the mosquito Anopheles gambiae. Journal of Insect
Costa, A.A., Naspi, C.V., Lucia, A., Masuh, H.M., 2017. Repellent and Physiology. 54(2), 367–377.
larvicidal activity of the essential oil from Eucalyptus nitens Louli, V., Folas, G., Voutsas, E., Magoulas, K., 2004. Extraction of
Against Aedes aegypti and Aedes albopictus (Diptera: parsley seed oil by supercritical CO2. Journal of Supercritical
Culicidae). Journal of Medical Entomology. 0, 1–7. Fluids. 30, 163–174.
Craft, J.D., Setzer, W.N., 2017. The volatile components of parsley, Mahmoodi, L., Oroj Valizadegan, O., Mahdavi, V., 2014. Fumigant
Petroselinum crispum (Mill.) Fuss. American Journal of toxicity of Petroselinum crispum L. (Apiaceae) essential oil on
Essential Oils and Natural Products. 5, 27–33. Trialeurodes vaporariorum (Westwood) (Hemiptera:
Díaz-Maroto, M.C., Pérez-Coello, M.S., Cabezudo, M.D., 2002. Effect Aleyrodidae) adults under greenhouse conditions. Journal of
of different drying methods on the volatile components of Plant Protection Research. 54, 294–299.
parsley (Petroselinum crispum L.). European Food Research Manimaran, A., Cruz, M.M.J.J. , Muthu, C., Vincent, S.,
and Technology. 215, 227–230. Ignacimuthu, S., 2012. Larvicidal and knockdown effects of
Dong, X., Jiang, Z.T., Jiang, S., Li, R., 2017. Composition comparison some essential oils against Culex quinquefasciatus Say, Aedes
of essential oils extracted by hydrodistillation and microwave- aegypti (L.) and Anopheles stephensi (Liston). Advances in
assisted hydrodistillation from Petroselinum crispum grown in Bioscience and Biotechnology. 3, 855–862.
China. Essential Oil Bearing Plants Journal. 20, 368–374. Maroufpoor, M., Ebadollahi, A., Vafaee, Y., Badiee, E., 2016. Chemical
Dris, D., Tine-Djebbar, F., Soltani, N., 2017a. Lavandula dentata composition and toxicity of the essential oil of Coriandrum
essential oils: chemical composition and larvicidal activity sativum L. and Petroselinum crispum L. against three stored-
against Culiseta longiareolata and Culex pipiens (Diptera: product insect pests. Essential Oil Bearing Plants Journal. 19,
Culicidae). African Entomology. 25, 387–394. 1993–2002.
Dris, D., Tine-Djebbar, F., Bouabida, H., Soltani, N., 2017. Chemical Mert, A., Timur, M., 2017. Essential oil and fatty acid composition
composition and activity of an Ocimum basilicum essential oil and antioxidant capacity and total phenolic content of parsley
on Culex pipiens larvae: Toxicological, biometrical and seeds (Petroselinum crispum) grown in Hatay region. Indian
biochemical aspects. South African Journal of Botany. 113, 362– Journal of Pharmaceutical Education and Research. 51, 437–
369. 440.
Duchateau, G., Florkin, M., 1959. Sur la tréhalosémie des insectes et Monnerat, R., Dumas, V., Ramos, F., Pimentel, L., Nunes, A., Sujii, E.,
sa signification. Archives of Insect Biochemistry and Physiology. Praca, L., Vilarinhos, P., 2012. Evaluation of different larvicides
67, 306–314. for the control of Aedes aegypti (Linnaeus) (Diptera: Culicidae)
El-Zaeddi, H., Calin-Sanchez, A., Martinez-Tome, J., Noguera-Artiaga, under simulated field conditions. Bioassay. 7, 3.
L., Burlo, F., Carbonell-Barrachina, A.A., 2016. Irrigation dose Naqqash, M.N., Gökçe, A., Bakhsh, A., Salim, M., 2016. Insecticide
and plant density affect the essential oil content and sensory resistance and its molecular basis in urban insect pests.
quality of parsley (Petroselinum sativum). Scientia Parasitology Research. 115, 1363–1373.
Horticulturae. 206, 1–6. Nawel, O., Ahmed, H., Donia zed, E., 2012. Effect of the essential oils
Farjana, T., Tuno, N., 2013. Multiple blood feeding and host-seeking from parsley and fennel seeds on the growth of Lactobacillus
behavior in Aedes aegypti and Aedes albopictus (Diptera: casei Subsp Rhamnosus. Journal of Biotechnology Biomaterials.
Culicidae). Journal of Medical Entomology. 50, 838–846. 2, 1–5.

14676
Hanane Seghier et al. Transylvanian Review: Vol XXVII, No. 47, March 2020

Nwabor O.F., Nnamonu, E.I., Martins, P.E., Odiachi, O., 2019. a single rat liver homogenate or from a subcellular fraction.
Synthetic insecticides, phytochemicals and mosquito resistance. Analytical Biochemistry. 19(3), 514–528.
Academia Journal of Biotechnology. 5(8), 118-125. Soonwera, M., Phasomkusolsil, S., 2017. Adulticidal, larvicidal,
Pavela, R., 2015. Essential oils for the development of eco-friendly pupicidal and oviposition deterrent activities of essential oil
mosquito larvicides: A review. Industrial Crops and Products. from Zanthoxylum limonella Alston (Rutaceae) against Aedes
76, 174-187. aegypti (L.) and Culex quinquefasciatus (Say). Asian Pacific
Perumalsamy, H., Kim, N., Ahn, Y., 2009. Larvicidal activity of Journal of Tropical Biomedicine. 7, 967–978.
compounds isolated from Asarum heterotropoides against Stankovic, M.Z., Nicolic, N., Stanojevic, L., Cakic, M.D., 2004. The
Culex pipiens pallens, Aedes aegypti, and Ochlerotatus togoi effect of hydrodistillation technique on the yield and
(Diptera: Culicidae). Journal of Medical Entomology. 46, 1420– composition of essential oil from the seed of Petroselinum
1423. crispum (Mill.) Nym. ex. A.W. Hill. Chemistry and Industry. 58,
Petropoulos, S.A., Daferera, D., Polissiou, M.G., Passam, H.C., 2008. 409–412.
The effect of water deficit stress on the growth, yield and Stankovic, M.Z., Nicolic, N., Stanojevic, L., Cakic, M.D., 2005. The
composition of essential oils of parsley. Scientia Horticulturae. effect of parsley (Petroselinum crispum (Mill.) Nym. ex. A.W.
115, 393–397. Hill) seeds milling and fermentation conditions on essential oil
Pineda, R., Vizcaíno, S., García, C.M., Gil, J.H., Durango, D., 2018. yield and composition. CI and CEQ. 11, 177–182.
Antifungal activity of extracts, essential oil and constituents Sugumaran, M., 2010. Chemistry of cuticular sclerotization. Advances
from Petroselinum crispum against Colletotrichum acutatum. in Insect Physiology. 39, 151–209.
Revista Facultad Nacional de Agronomía Medellín. 71(3), 8563- Suttthanont, N., Choochote, W., Tuetun, B., Junkum, A., Jitpakdi, A.,
8572. Chaithong, U., 2010. Chemical composition and larvicidal
Rehimi, N., Soltani, N., 1999. Laboratory evaluation of Alsystin, a activity of edible plant-derived essential oils against pyrethroid-
chitin synthesis inhibitor, against Culex pipiens pipiens susceptible and-resistant strains of Aedes aegypti (Diptera:
(Diptera: Culicidae): effects on development and cuticle Culicidae). Journal of Vector Ecology. 35, 106–115.
secretion. Journal of Applied Entomology. 123, 437–441. Tadros, L.K., El-Rafey, H.H., Elfadaly, H.A., Taher, M.A, Elhafny, M.A.,
Rivero, A., Vézilier, J., Weill, M., Read, A.F., Gandon, S., 2010. 2017. Phenolic profile, essential oil composition, purification of
Insecticide control of vector-borne diseases: When is insecticide kaempferol 3- arabinofuranoside and antimicrobial activity of
resistance a problem? PLoS Pathogens. 6, 1–9. parsley cultivated in Dakhalia Governorate. Journal of
Rodriguez-Ortega, M.J., Rodriguez-Ortega, M.J., Grosvik, B.E., Agricultural Chemistry and Biotechnology. Mansoura Univ. 8,
Rodriguez-Ariza, A., Goksoyr, A., Lopez-Barea, J., 2003. 183 – 189.
Changes in protein expression profiles in bivalve molluscs Timmermann, S.E., Briegel, H., 1999. Larval growth and biosynthesis
(Chamaelea gallina) exposed to four model environmental of reserves in mosquitoes. Journal of Insect Physiology. 45,
pollutants. Proteomics. 3, 1535-1543. 461–470.
Sarma, R., Mahanta, S., Khanikor, B., 2017. Insecticidal activities of Tine-Djebbar, F., Bouabida, H., Soltani, N., 2016. Spatio-temporal
the essential oil of Aegle marmelos (Linnaeus, 1800) against distribution of Culicidae in Tebessa area. Germany: European
Aedes aegypti (Linnaeus, 1762) and Culex quinquefasciatus University Press.
(Say, 1823). Universal Journal of Agricultural Research. 5, 304– Vatandoost, H., Dehkordi, A.S., Sadeghi, S.M., Davari, B., Karimian,
311. F., Abai, M.R., Sedaghat, M.M., 2012. Identification of chemical
Scott, L.J., 2016. Tetravalent Dengue Vaccine: A review in the constituents and larvicidal activity of Kelussia odoratissima
prevention of dengue disease. Drugs. 76, 1301–1312. Mozaffarian essential oil against two mosquito vectors
Sharma, P., Mohan, L., Dua, K.K., Srivastava, C.N., 2011. Status of Anopheles stephensi and Culex pipiens (Diptera: Culicidae).
carbohydrate, protein and lipid profile in the mosquito larvae Experimental Parasitology. 132, 470–474.
treated with certain phytoextracts. Asian Pacific Journal of Vokk, R., Lõugas, T., Mets, K., Kravets, M., 2011. Dill ( Anethum
Tropical Medicine. 4(4), 301–304. graveolens L.) and Parsley (Petroselinum crispum (Mill.) Fuss)
Shibko, S., Koivistoinen, P., Tratnyek, C.A., Newhall, A.R., Friedman, from Estonia: Seasonal Differences in Essential Oil
L., 1966. A method for sequential quantitative separation and Composition. Agronomy Research. 9, 515–520.
determination of protein, RNA, DNA, lipid, and glycogen from Who., 2005. Guidelines for laboratory and field-testing of mosquito
larvicides, Ref. WHO/ CDS/WHOPES/GCPP/ 13, 41p.

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