Publish in this journal
Journal Information
Vol. 61. Num. 4.October - December 2017
Pages 271-370
Share
Share
Download PDF
More article options
Visits
829
Vol. 61. Num. 4.October - December 2017
Pages 271-370
Medical and Veterinary Entomology
DOI: 10.1016/j.rbe.2017.08.005
Evaluation of the insecticidal activity of essential oils and their mixtures against Aedes aegypti (Diptera: Culicidae)
Visits
829
Natalia Ríosa, Elena E. Stashenkob, Jonny E. Duquec,
Corresponding author
jonedulu@uis.edu.co

Corresponding author.
a Universidad Industrial de Santander, Escuela de Química, Centro de Investigaciones en Enfermedades Tropicales (CINTROP), Bucaramanga, Colombia
b Universidad Industrial de Santander, Escuela de Química, Centro de Investigación en Biomoléculas – CIBIMOL y Centro Nacional de Investigación para la Agroindustrialización de Plantas Aromáticas y Medicinales Tropicales – CENIVAM, Bucaramanga, Colombia
c Universidad Industrial de Santander, Escuela de Medicina, Departamento de Ciencias Básicas, Centro de Investigaciones en Enfermedades Tropicales (CINTROP), Bucaramanga, Colombia
This item has received
829
Visits
Article information
Abstract
Full Text
Bibliography
Download PDF
Statistics
Tables (4)
Table 1. Essential oil yields collection sites and registration numbers (voucher) of plants studied in this work.
Table 2. Percentages of major components in the essential oils studied.
Table 3. Ae. aegypti larvae mortality rate of each EO concentration tested at 24 and 48h.
Table 4. Larvicidal activity (in mg/mL) of the different EOs against Ae. aegypti larvae at 24 and 48h.
Show moreShow less
Abstract

The search for new insecticides to control dengue fever, chikungunya, and Zika vectors has gained relevance in the past decades. The aim of the present study was to evaluate the larvicidal action of essential oils (EOs) from Thymus vulgaris, Salvia officinalis, Lippia origanoides, Eucalyptus globulus, Cymbopogon nardus, Cymbopogon martinii, Lippia alba, Pelargonium graveolens, Turnera diffusa, and Swinglea glutinosa on Aedes (Stegomyia) aegypti. The EOs were extracted by microwave-assisted hydrodistillation and characterized by gas chromatography/mass spectrometry (GC/MS). The chemical components of the EOs were identified by linear retention indices and mass spectra. Lethal concentrations (LC50 and LC95) were determined by probit analysis using larvae of Ae. aegypti between the third and the fourth instars. All EOs achieved larvicidal activity at LC50 values lower than 115mg/L. The lowest LC50 value (45.73mg/L) corresponded to T. vulgaris EO, whereas C. martinii EO showed the highest LC50 (LC50=114.65mg/L). Some EO mixtures showed lower LC50 than oils used individually, such as the mixtures of L. origanoides+S. glutinosa (LC50=38.40mg/L), T. diffusa+S. glutinosa (LC50=63.71mg/L), and L. alba+S. glutinosa (LC50=48.87mg/L). The main compounds of the EOs with highest larvicidal activity were thymol (42%) and p-cymene (26.4%).

Keywords:
Essential oil
Larvicidal activity
Mosquito control
Full Text
Introduction

Several diseases such as yellow fever, dengue fever, chikungunya, and Zika fever, among several others, can be transmitted by Aedes aegypti (L., 1762) to human beings. Diseases are symptomatic manifestations of infections. Based on its morbidity and rates of mortality, dengue fever is considered the most serious disease from an epidemiological point of view. Approximately 60 million people around the world are estimated to acquire the virus each year resulting in about 10,000 deaths (Bhatt et al., 2013; Stanaway et al., 2016). In the case of Zika fever, global alarms have been activated due to the association of the virus with cases of microcephaly in newborns and Guillain-Barré syndrome reported by health institutions in Brazil and French Polynesian (Abushouk et al., 2016; Plourde and Bloch, 2016).

Due to the lack vaccines against these diseases, prevention strategies are focused on the control of larvae and adult Ae. aegypti populations. The application of synthetic insecticides (organophosphates-OP and pyrethroids-PI) is the most common approach used worldwide (Brandler et al., 2013). On the other hand, Bacillus thuringiensis var israelensis (Bti) is a bacteria widely evaluated in programs for Culicidae control. This mosquito control method is environmentally safe, commercially available and cheaper than synthetic insecticides (OP and PI). However, the principal disadvantage of using Bti in control programs is the low persistence in field conditions (Ritchie et al., 2010; Boyce et al., 2013; Moshi and Matoju, 2017).

Several studies have been conducted to identify new insecticides obtained from secondary metabolites of aromatic and medicinal plants, seeking effective alternatives to combat vector mosquitoes. The aim of such studies is to discover options to replace traditional chemical insecticides and determine natural ingredients to make formulations that can be used in the design of new insecticides (Carreño et al., 2014).

Compared to synthetic products, natural pesticides are less harmful to human health and ecosystems, and so they are widely accepted by the general population. Despite these benefits, commercial insecticides still have more effective lethal concentrations (LC), lethal doses (LD) and lethal times (LT) than natural products (Shaalan et al., 2005; Koul et al., 2008). Therefore, it is important to characterize the insect-killing effectiveness of essential oils (EO) or plant extracts (PE) in their first screening phase in order to determine their promise as insecticides. One of the criteria to guide new larvicide research is that the candidate substances have an LC50<100mg/L (Cheng et al., 2003; Dias and Moraes, 2014). However, this criterion does not include important aspects of the control and protection against mosquito bites, such as repellency, deterrence, and attraction (Castillo et al., 2017).

More studies are needed to compare the insecticidal action of EOs and PEs obtained at different geographical locations (Amer and Mehlhorn, 2006a; Pavela, 2008; Caballero-Gallardo et al., 2012; Manimaran et al., 2012). It is also important to understand that the chemical composition of an EO or PE can determine its insecticidal effect, and that this may vary intra- and interspecifically, according to soil, plant anatomy, edaphic factors, and environmental conditions (Bakkali et al., 2008; Dias and Moraes, 2014). Based on these premises, the aim of the present study was to evaluate the insecticidal activity of essential oils isolated from different aromatic plants, as follows: Salvia officinalis (Lamiaceae), Thymus vulgaris (Labiatae), Eucalyptus globulus (Myrtaceae), Lippia alba (Verbenaceae), Turnera diffusa (Turneraceae), Pelargonium graveolens (Geraniaceae), Cymbopogon nardus, and Cymbopogon martinii (Poaceae), Swinglea glutinosa (Rutaceae), as well as two different chemotypes of Lippia origanoides (phellandrene and thymol).

Material and methods

The experiments were developed using Ae. aegypti insects from the Rockefeller colony. Mosquitoes were kept in 40×40×40cm breeding cages under special conditions of humidity (70±5%), photoperiod (12:12), and temperature (25±5°C). Female mosquitoes were fed with Wistar rat blood (the UIS ethics committee was previously informed, as stated in CEINCI-UIS Minute No. 3, 2013; male mosquitoes were fed with 10% sucrose solution.

Essential oil isolation

The plants were collected from fields located in Santander, Colombia (Table 1). The EOs were extracted by microwave-assisted hydrodistillation (MWHD) as described by Stashenko et al. (2004). In the case of MWHD, plant material and the water were heated using a domestic microwave oven (2.45GHz, 800W), modified with a lateral orifice to connect the flask and the condenser. The microwave oven worked at full power (800W) for 30min (10min×3). The EO was collected in a Dean-Stark, and finally, the condensate was decanted and dried with anhydrous sodium sulfate.

Table 1.

Essential oil yields collection sites and registration numbers (voucher) of plants studied in this work.

Scientific name  Family  Common name  Voucher No.  Site of collection  EO yield, % (p/p) 
Thymus vulgaris  Labiatae  Thyme  555843  Sucre, Santander  0.3 
Salvia officinalis  Lamiaceae  Garden sage  555844  Sucre, Santander  0.4 
Lippia origanoides (Phellandrene)  Verbenaceae  Wild oregano  519798  Cenivam, Bucaramanga  0.4 
Lippia origanoides (thymol)  Verbenaceae  Wild oregano  519799  Cenivam, Bucaramanga  1.6 
Eucalyptus globulus  Myrtaceae  Blue gum  C-470  Cenivam, Bucaramanga  2.0 
Cymbopogon nardus  Poaceae  Citronella grass  578357  Cenivam, Bucaramanga  0.4 
Cymbopogon martinii  Poaceae  Gingergrass  587116  Cenivam, Bucaramanga  0.4 
Lippia alba  Verbenaceae  Quick relief  480750  Cenivam, Bucaramanga  0.5 
Turnera diffusa  Turneraceae  Damiana  516293  Los Santos, Santander  0.7 
Pelargonium graveolens  Geraniaceae  Wildemalva  51718  Cenivam, Bucaramanga  0.2 
Swinglea glutinosa  Rutaceae  African lemon  521530  Cenivam, Bucaramanga  0.2 
Mixture of L. origanoides and S. glutinosa    –  –  –  – 
Mixture of T. diffusa and S. glutinosa    –  –  –  – 
Mixture of S. glutinosa and L. alba    –  –  –  – 

The EOs were characterized by gas chromatography/mass spectrometry (GC/MS), using an Agilent Technologies 6890 (AT, Palo Alto, CA, USA) gas chromatograph with a DB-5MS capillary column (60m×0.25mm id×0.25mm df) using helium (99.995% purity) as carrier gas at a flow rate of 1mL/min and an Agilent Technologies 5973 mass selective detector. Ionization was used electron energy achieved at 70eV. The temperatures of the injector and the transfer line were set at 285 and 250°C, respectively. The initial column temperature was 50°C, which was increased by 3°C/min up to 150°C, and the 250°C temperature was finally reached at 10°C/min. The major components of the EOs were identified using the linear retention indeces and mass spectra, which were compared with those from the NIST, Wiley, and ADAMS databases (Stashenko et al., 2004).

Insecticidal activity

Experiments were initially conducted at exploratory concentrations (EC) of EO with larvae of Ae. aegypti between the third and the fourth instars. Larvae were placed in 100mL plastic cups containing a solution of EO and mineral water. Mortality rates between 2 and 98% have been previously found after exposing larvae to EC of essential oils (Aciole et al., 2011; Vera et al., 2014). The concentrations being tested were initially 30, 300, and 1000mg/L. Each treatment was repeated four times (N=120 larvae), and experiments were replicated three times on different days. The control test used dimethyl sulfoxide (DMSO, 0.5%) and mineral water. Larvae counts were performed at 24 and 48h after initial exposure to each EO concentration. The criteria to consider larvae as dead were that the individuals lacked all movement and failed to reach the water surface (WHO, 1996). Values of LC50, LC95, and mortality rates were determined for five selected EOs. The results of mortality and survival bioassays were subjected to Probit analysis (Finney, 1971).

Results

The EOs obtained by MWHD presented different extraction yields. E. globulus was the plant from which the highest amount of EO was obtained (2.0%, w/w). The major components in the oil were thymol (T. vulgaris), 1,8-cineole (S. officinalis), limonene (L. origanoides chemotype-phellandrene), thymol (L. origanoides, thymol chemotype), 1,8-cineol (E. globulus), citronellal (C. nardus), geraniol (C. martinii), carvone (L. alba), drima-7,9(11)-diene (T. diffusa), and citronellol in the EO of P. graveolens (Table 2).

Table 2.

Percentages of major components in the essential oils studied.

Plant  Major components (%)  Reference 
T. vulgaris  Thymol (42.0), p-cymene (26.4), γ-terpinene (6.3), linalool (2.9), trans-β-caryophyllene (2.6)  Unpublished data 
S. officinalis  1,8-Cineol (26.6), α-thujone (18.1), trans-β-caryophyllene (7.3), α-humulene (5.4)  Unpublished data 
L. origanoides (phellandrene)  Limonene (15.0), p-cymene (14.6), α-phellandrene (10.3), trans-β-caryophyllene (5.8), α-humulene (2.9), α-pinene (2.5), γ-terpinene (2.1)  (Stashenko et al., 2010
L. origanoides (thymol)  Thymol (66.1), p-cymene (7.2), γ-terpinene (4.4), trans-β-caryophyllene (3.6), α-humulene (2.4), methyl thymyl ether (2.3), thymyl acetate (2.0), α-thujone (1.0)  (Stashenko et al., 2010
E. globulus  1,8-Cineol (69.4), α-pinene (4.6), viridiflorol (4.1), α-terpenyl acetate (3.3), limonene (3.0)  Unpublished data 
C. nardus  Citronellal (21.8), citronellol (18.1), geraniol (11.3), germacrene D (4.6), limonene (3.5)  Unpublished data 
C. martini  Geraniol (83.9), geranyl acetate (9.2), linalool (2.3), trans-β-caryophyllene (1.0)  (Rodríguez et al., 2012
L. alba (carvone)  Carvone (35.3), limonene (35.0), bicyclosesquiphellandrene (9.6), piperitenone (3.4), piperitone (1.0)  (Agudelo-Gomez et al., 2010
T. diffusa  Drima-7,9(11)-diene (22.9), β-viridiflorene (6.6), α-silinene (5.9), valencene (5.5), trans-β-caryophyllene (5.2), trans-muurola-4(14),5-diene (5.2), p-cymene (2.1)  Unpublished data 
P. graveolens  Citronellol (14.9), geranial (8.4), geraniol (7.5), guainene (7.4) germacrene D (3.7), iso-menthone (3.7), geranyl formate (3.2)  Unpublished data 
S. glutinosa  trans-Nerolidol (28.4), germacrene D (20.5), α-pinene (9.1), trans-β-caryophyllene (7.5), δ-elemene (3.6), α-cadinol (2.1), γ-elemene (2.6), δ-Cadinene (2.0), espatulenol (1.7), α-humulene (1.5), β-elemene (1.3), geranyl acetate (1.0)  (Stashenko et al., 2015

All EOs displayed insecticidal action against Ae. aegypti larvae at 24 and 48h (Table 3). The relationship between concentration and mortality was most effective with the oil mixture composed of L. origanoides and S. glutinosa (38.40mg/L). T. vulgaris EO showed the lowest LC50 (45.73mg/L). The EOs with highest LC50 were C. martinii and P. graveolens, with 114.65 and 108.96mg/L, respectively, at 24h (Table 4).

Table 3.

Ae. aegypti larvae mortality rate of each EO concentration tested at 24 and 48h.

Essential oil  Concentration, mg/mL  Mortality rate (%±SD)
    2448
T. vulgaris
12  3±1.7  0.0±0.0 
20  4±2.9  8±3.5 
30  16±7.2  18±7.3 
45  37±9.0  43±10 
58  77±4.0  80±4.6 
S. officinalis
20  4±2.1  1.2±0.7 
30  3±2.3  5±1.7 
47  6±4.0  16±8.4 
63  30±17.7  40±20.5 
76  50±24  50±24.7 
L. origanoides (phellandrene)
32  14±7.7  18±9.9 
56  60±18.5  50±11.9 
67  60±13.2  63±7.6 
79  70±18.8  84±10 
93  100±0.0  100±0.0 
L. origanoides (Thymol)
27  3±0.7  58±3.5 
45  27±4.0  59±7.2 
52  40±10.4  64±5.4 
67  60±11.7  76±6.1 
79  50±20.2  92±5.8 
E. globulus
54  11±5.9  13±7.6 
61  4±2.1  4±1.9 
72  11±4.2  13±4.6 
81  20±11.5  20±12.4 
93  30±10.8  30±10.2 
C. nardus
37  16±6.4  19±5.3 
42  13±5.7  14±4.9 
56  34±7.7  43±8.1 
69  31±9.8  39±2.6 
78  50±16.6  60±15.3 
C. martinii
56  7±5.7  18±6.6 
78  16±7.6  31±6.3 
83  19±9.6  30±10.2 
97  20±9.1  41±6.1 
141  70±10.9  70±11.4 
L. alba (Carvone)
30  3±0.6  4±0.6 
59  21±5.5  32±5 .7 
73  50±10.0  75±2.6 
89  80±11.6  90±5.5 
96  95±0.0  96±5.3 
P. graveolens
30  3±0.0  3±0.0 
69  6±1.6  6±1.5 
76  13±2.0  13±2.5 
98  28±3.5  28±1.4 
130  76±6.4  80±4.2 
Mixtures L. origanoides+S. glutinosa
22  9±4.9  9±4.9 
30  12±0.0  12±0.0 
45  17±7.0  21±8.0 
53  40±2.1  44±9.2 
69  60±9.6  60±12.2 
Mixtures T. diffusa+S. glutinosa
22  3±1.1  3±1.53 
30  3±1.4  4±2.36 
45  12±3.7  19±3.3 
49  30±12.7  34±13.4 
53  31±10.2  42±9.8 
69  60±12.8  66±8.4 
Mixtures S. glutinosa+L. alba
30  13±2.3  23±5.0 
42  40±15.3  40±15.6 
57  60±14.7  70±14.8 
69  80±10.1  80±10.4 
78  86±5.7  86±5.7 

SD: Standard deviation.

Table 4.

Larvicidal activity (in mg/mL) of the different EOs against Ae. aegypti larvae at 24 and 48h.

Essential oil or mixture  24h48h
  LC50  LC95  X2  LC50  LC95  X2 
(L. origanoides+S. glutinosa38.40 (35.52–42.37)  94.91 (77.38–128.56)  1.12  34.86 (32.54–37.81)  83.01 (69.64–106.87)  0.39 
T. vulgaris  45.73 (41.29–53.80)  96.25 (75.01–149.01)  5.35  42.33 (40.13–44.73)  76.53 (68.64–89.18)  2.64 
(S. glutinosa+L. alba48.87 (46.17–51.50)  101.76 (92.02–116.32)  0.22  45.93 (42.84–48.84)  109.41 (96.66–129.84)  1.73 
L. origanoides (Phellandrene)  53.79 (50.90–56.69)  116.60 (102.56–140.31)  4.68  53.79 (50.90–56.69)  116.60 (102.56–140.31)  4.68 
L. origanoides (Thymol)  56.18 (53.20–59.89)  124.55 (105.55–160.30)  5.71  38.73 (35.17–41.73)  102.75 (89.36–126.24)  3.46 
(T. diffusa+S. glutinosa63.71 (60.75–67.71)  117.70 (103.39–141.81)  0.31  34.86 (32.54–37.81)  83.01 (69.64–106.87)  0.39 
L. alba (Carvone)  72.34 (69.87–75.05)  110.84 (102.69–123.28)  0.12  63.61 (66.34–66.46)  98.91 (93.58–106.25)  5.38 
S. officinalis  76.43 (71.84–83.79)  123.92 (106.98–136.75)  5.46  77.53 (69.71–91.14)  198.20 (149.17–322.5)  1.37 
C. nardus  75.85 (69.15–86.82)  219.68 (165.93–345.92)  4.22  71.26 (65.60–80.11)  255.42 (182.79–465.99)  5.81 
E. globulus  92.55 (89.37–97.00)  136.82 (124.67–157.14)  2.21  91.29 (88.35–95.30)  133.72 (122.54–152.00)  2.44 
P. graveolens  108.96 (103.62–115.74)  176.61 (157.84–208.81)  2.80  113.16 (106.65–122.15)  198.54 (172.01–248.57)  0.73 
C. martinii  114.65 (107.26–124.94)  251.26 (211.65–321.05)  1.96  114.82 (103.14–141.23)  290.06 (207.20–577.64)  0.99 

LC50 is the lethal concentration causing mortality of 50% of organisms exposed to treatment. LC95 is the lethal concentration causing mortality of 95% of organisms exposed to treatment. The confidence interval is given in parentheses. The statistical analysis was well adjusted to the probit model (Finney, 1947).

Discussion

All of the studied EOs, both individually and as mixtures, presented insecticidal activity against Ae. aegypti larvae. Only C. martinii and P. graveolens presented an LC50>100mg/L, indicating that all EOs evaluated in this study can be utilized as good candidates for the design of new mosquito insecticides against mosquito control (Dias and Moraes, 2014). The mixture of L. origanoides and S. glutinosa was proven to cause the highest insect mortality (LC50=38.40mg/L). As shown by Vera et al. (2014), the mixtures of EOs, in this case L. origanoides (53.37mg/L) and S. glutinosa (65.71mg/L), may enhance the toxic effect of individual oils on Ae. aegypti larvae.

Our results showed T. vulgaris to have the best larvicidal action (LC50 45.73mg/L). This bioactivity reflects a study by Massebo et al. (2009), who studied EO extracted from leaves and seeds of plants from Ethiopia, yet the LC50 was lower (17.3mg/L). Also, T. vulgaris extracts from plants grown in the Czech Republic (LC50=48mg/L) with Culex quinquefasciatus (Pavela, 2008) confirm our present results. Thymol and p-cymene were the major compounds identified in this plant, and the toxicity against mosquitoes was consistent with other reports on these metabolites (Dias and Moraes, 2014).

The L. origanoides EOs of phellandrene and thymol chemotypes, presented similar insecticidal effects (LC50=53.79mg/L and LC50=56.18mg/L, respectively), which matches the LC50 of L. origanoides, obtained by Vera et al. (2014) with Ae. aegypti.

Despite their different major compounds, the larvicidal effect of EOs from L. alba, C. nardus, and S. officinalis showed similar LC50 values (Table 3). In the case of L. alba, the LC50 value (72.34mg/L) was higher than that found by Vera et al. (2014) with Ae. aegypti (LC50=44.26mg/L). This lower activity could be related to a lower amount of carvone in the EO (35.3%) as compared to a previous report (38.3%) by Vera et al. (2014), who found an amount of 38.3%. Besides L. alba insecticidal action, the plant has a record as a repellent with other insects, such as Tribolium castaneum (Olivero-Verbel et al., 2013).

In the present study, the EO of C. nardus presented a much more effective larvicidal activity against Ae. aegypti than that reported by Tennyson et al. (2013) in India (1374.05mg/L). On the other hand, we obtained lower LC50 values than those obtained by Manimaran et al. (2012) for Ae. aegypti (LC50=47.21) and Anopheles stephensi (47.61mg/L); the EOs in that study were obtained from plants cultivated in India.

Pavela (2008) reported a LC50 of 159mg/L with Cx. quinquefasciatus larvae in a study on S. officinalis, a plant of Eurasian origin; when we compared those results with our results on Ae. aegypti, we observed that the LC50 was lower (76.43mg/L), indicating that the EO of this plant had higher insecticidal activity than S. officinalis extract.

The EOs of E. globulus (LC50=92.55mg/L), P. graveolens (LC50=108.96mg/L), and C. martinii (CL50 114.65mg/L) showed less effectiveness. Based on the criterion of plants with CL50<100, only E. globulus EO would be promising as an insecticide (Dias and Moraes, 2014). The EO of this plant had the greatest yield (2.0%, w/w), and mortality rates of 32.92% at 24h and 34.17% at 48h were achieved with a concentration of 93mg/L (Table 3). These results are consistent with those presented by Amer and Mehlhorn (2006b), who reported Aedes larval mortality rates from 16.7% with EO solutions (50mg/L) at 24h of treatment.

L. origanoides and S. glutinosa mixture showed the highest larvicidal activity (LC50=38.40mg/L) of the three mixtures analyzed in this study. It should be highlighted that these EOs, separately, had higher LCs50 than when evaluated as part of mixtures, as has been observed with EOs of L. origanoides (LC50=53.79mg/L) and S. glutinosa (LC50=65.71mg/L) (Vera et al., 2014). These data indicate that the insecticidal effect of EOs can be potentiated by using mixtures of EO, probably due to a synergistic effect (Mansour et al., 2015).

Although there is extensive information on botanical products such as essential oils and plant extracts for mosquito control (larval and adults), it is unusual to find them in formulations of commercial insecticides. Plants such as Azadirachta indica and Melia azedarach (Meliaceae) are among the few that are part of commercial biopesticides. These two species of plants have been studied on at least 103 species of insects and have eco-friendly effects (Mazid, 2011; Thangavel and Sridevi, 2015; Moshi and Matoju, 2017). However, the insecticidal effect on mosquito larvae of these plants is not so effective (LC50>1×10−4 mg/L) as that of essential oils (LC50<50mg/L) (Howard et al., 2009; Kishore et al., 2011; Dias and Moraes, 2014; Vera et al., 2014). This is a good reason to use the plants presented here as source of ingredients for design new insecticides.

Conclusion

All of the EOs evaluated in the present study showed insecticidal activity. The EO of T. vulgaris and the mixture of L. origanoides and S. glutinosa showed highest larvicidal action on Ae. aegypti. The main compounds of the EOs with higher larvicidal activity were thymol (42%) and p-cymene (26.4%).

Conflicts of interest

The authors declare no conflicts of interest.

Acknowledgments

This study was possible thanks to the Patrimonio Autónomo, Fondo Nacional de Financiamiento para la Ciencia, Francisco José de Caldas, contract no. RC-0572-2012-Bio-Red-CENIVAM. Natalia Rios received a COLCIENCIAS scholarship for young researchers in the period of 2014-2015 (617). We would like to thank the Ministerio de Ambiente y Desarrollo Sostenible (MADS), through its Dirección de Bosques, Biodiversidad y Servicios Ecosistémicos for their permission to conduct this research and the access to genetic resources and derived products for the program ran by the Unión Temporal Bio-Red-CO-CENIVAM (Resolution 0812, June 4, 2014).

References
[Abushouk et al., 2016]
A.I. Abushouk,A. Negida,H. Ahmed
An updated review of Zika virus
J. Clin. Virol., 84 (2016), pp. 53-58 http://dx.doi.org/10.1016/j.jcv.2016.09.012
[Aciole et al., 2011]
S.D.G. Aciole,C.F. Piccoli,J.E.L. Duque,E.V. Costa,M.A. Navarro-silva,F.A. Marques,Maia BHLNS,M.L.B. Pinheiro,M. Rebelo
Insecticidal activity of three species of Guatteria (Annonaceae) against Aedes aegypti (Diptera: Culicidae)
Rev. Colomb. Entomol., 37 (2011), pp. 262-268
[Agudelo-Gomez et al., 2010]
L. Agudelo-Gomez,G. Gomez,D. Duran,Stashenko,L. Elena Betancur-Galvis
Artículos Originales Composición química y evaluación de la actividad antiherpética in vitro de aceites
Salud UIS, 42 (2010), pp. 230-239
[Amer and Mehlhorn, 2006a]
A. Amer,H. Mehlhorn
Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae)
Parasitol. Res., 99 (2006), pp. 466-472 http://dx.doi.org/10.1007/s00436-006-0182-3
[Amer and Mehlhorn, 2006b]
A. Amer,H. Mehlhorn
Repellency effect of forty-one essential oils against Aedes, Anopheles, and Culex mosquitoes
Parasitol. Res., 99 (2006), pp. 478-490 http://dx.doi.org/10.1007/s00436-006-0184-1
[Bakkali et al., 2008]
F. Bakkali,S. Averbeck,D. Averbeck,M. Idaomar
Biological effects of essential oils – a review
Food Chem. Toxicol., 46 (2008), pp. 446-475 http://dx.doi.org/10.1016/j.fct.2007.09.106
[Bhatt et al., 2013]
S. Bhatt,P.W. Gething,O.J. Brady,J.P. Messina,A.W. Farlow,C.L. Moyes,J.M. Drake,J.S. Brownstein,A.G. Hoen,M.F. Myers,D.B. George,T. Jaenisch,G.R. William,C.P. Simmons,T.W. Scott,J. Farrar,S.I. Hay
The global distribution and burden of dengue
Nature, 496 (2013), pp. 504-507 http://dx.doi.org/10.1038/nature12060
[Boyce et al., 2013]
R. Boyce,A. Lenhart,A. Kroeger,R. Velayudhan,B. Roberts,O. Horstick
Bacillus thuringiensis israelensis (Bti) for the control of dengue vectors: systematic literature review
Trop. Med. Int. Heal., 18 (2013), pp. 564-577
[Brandler et al., 2013]
S. Brandler,C. Ruffié,C. Combredet,J.B. Brault,V. Najburg,M.C. Prevost,A. Habel,E. Tauber,P. Desprès,F. Tangy
A recombinant measles vaccine expressing chikungunya virus-like particles is strongly immunogenic and protects mice from lethal challenge with chikungunya virus
[Caballero-Gallardo et al., 2012]
K. Caballero-Gallardo,J. Olivero-Verbel,E.E. Stashenko
Repellency and toxicity of essential oils from Cymbopogon martinii, Cymbopogon flexuosus and Lippia origanoides cultivated in Colombia against Tribolium castaneum
J. Stored Prod. Res., 50 (2012), pp. 62-65
[Carreño et al., 2014]
L.O. Carreño,L.Y. Vargas Méndez,J.E.L. Duque,V.V. Kouznetsov
Design, synthesis, acetylcholinesterase inhibition and larvicidal activity of girgensohnine analogs on Aedes aegypti, vector of dengue fever
Eur. J. Med. Chem., 78 (2014), pp. 392-400 http://dx.doi.org/10.1016/j.ejmech.2014.03.067
[Castillo et al., 2017]
R.M. Castillo,E. Stashenko,J.E. Duque
Insecticidal and repellent activity of several plant-derived essential oils against Aedes aegypti
J. Am. Mosq. Control Assoc., 33 (2017), pp. 25-35 http://dx.doi.org/10.2987/16-6585.1
[Cheng et al., 2003]
S.-S. Cheng,H.-T. Chang,S.-T. Chang,K.-H. Tsai,W.-J. Chen
Bioactivity of selected plant essential oils against the yellow fever mosquito Aedes aegypti larvae
Bioresour. Technol., 89 (2003), pp. 99-102
[Dias and Moraes, 2014]
C.N. Dias,D.F.C. Moraes
Essential oils and their compounds as Aedes aegypti L. (Diptera: Culicidae) larvicides: review
Parasitol. Res., 113 (2014), pp. 565-592 http://dx.doi.org/10.1007/s00436-013-3687-6
[Finney, 1947]
D.J. Finney
Probit Analysis: A Statistical Treatment of the Sigmoid, 1971
(1947)
[Finney, 1971]
D.J. Finney
Probit Analysis
Cambridge University Press, (1971)pp. 333
[Howard et al., 2009]
A.F.V. Howard,E.A. Adongo,A. Hassanali,F.X. Omlin,A. Wanjoya,G. Zhou,J. Vulule
Laboratory evaluation of the aqueous extract of Azadirachta indica (neem) wood chippings on Anopheles gambiae s.s. (Diptera: Culicidae) mosquitoes
J. Med. Entomol., 46 (2009), pp. 107-114
[Kishore et al., 2011]
N. Kishore,B.B. Mishra,V.K. Tiwari,V. Tripathi
A review on natural products with mosquitosidal potentials
Research Signpost, (2011)
[Koul et al., 2008]
O. Koul,S. Walia,G. Dhaliawal
Essential Oils as Green Pesticides: Potential and Constraints
Biopestic. Int., 4 (2008), pp. 63-84
[Manimaran et al., 2012]
A. Manimaran,J. Cruz,C. Muthu,S. Vincent,S. Ignacimuthu
Larvicidal and knockdown effects of some essential oils against Culex quinquefasciatus Say, Aedes aegypti (L.) and Anopheles stephensi (Liston)
Adv. Biosci. Biotechnol., 3 (2012), pp. 855-862
[Mansour et al., 2015]
S.A. Mansour,A.Z. El-Sharkawy,N.A. Abdel-Hamid
Toxicity of essential plant oils, in comparison with conventional insecticides, against the desert locust, Schistocerca gregaria (Forskål)
Ind. Crops Prod., 63 (2015), pp. 92-99
[Massebo et al., 2009]
F. Massebo,M. Tadesse,T. Bekele,M. Balkew,T. Gebre-michael
Evaluation on larvicidal effects of essential oils of some local plants against Anopheles arabiensis Patton and Aedes aegypti Linnaeus (Diptera, Culicidae) in Ethiopia
African J. Biotechnol., 8 (2009), pp. 4183-4188
[Mazid, 2011]
S. Mazid
A review on the use of biopesticides in insect pest management
Int. J. Sci. Adv. Technol., 1 (2011), pp. 169-178
[Moshi and Matoju, 2017]
A.P. Moshi,I. Matoju
The status of research on and application of biopesticides in Tanzania
Rev. Crop Prot., 92 (2017), pp. 16-28
[Olivero-Verbel et al., 2013]
J. Olivero-Verbel,I. Tirado-Ballestas,K. Caballero-Gallardo,E.E. Stashenko
Essential oils applied to the food act as repellents toward Tribolium castaneum
J. Stored Prod. Res., 55 (2013), pp. 145-147
[Pavela, 2008]
R. Pavela
Larvicidal effects of various Euro-Asiatic plants against Culex quinquefasciatus Say larvae (Diptera: Culicidae)
Parasitol. Res., 102 (2008), pp. 555-559 http://dx.doi.org/10.1007/s00436-007-0821-3
[Plourde and Bloch, 2016]
A.R. Plourde,E.M. Bloch
Literature Review of Zika Virus
Emerg. Infect. Dis., 22 (2016), pp. 1185-1192 http://dx.doi.org/10.3201/eid2207.151990
[Ritchie et al., 2010]
S.A. Ritchie,L.P. Rapley,S. Benjamin
Bacillus thuringiensis var. israelensis (Bti) provides residual control of Aedes aegypti in small containers
Am. J. Trop. Med. Hyg., 82 (2010), pp. 1053-1059 http://dx.doi.org/10.4269/ajtmh.2010.09-0603
[Rodríguez et al., 2012]
R. Rodríguez,R. Carlos,G. Arias,H. Castro,J. Martínez,E. Stashenko
Estudio comparativo de la composición de los aceites esenciales de cuatro especies del género Cymbopogon (Poaceae) cultivadas en Colombia
Bol. Lat. Caribe Planta. Med. Aromát., 11 (2012), pp. 77-85
[Shaalan et al., 2005]
E.A.-S. Shaalan,D. Canyon,M.W.F. Younes,H. Abdel-Wahab,A.-H. Mansour
A review of botanical phytochemicals with mosquitocidal potential
Environ. Int., 31 (2005), pp. 1149-1166 http://dx.doi.org/10.1016/j.envint.2005.03.003
[Stanaway et al., 2016]
J.D. Stanaway,D.S. Shepard,E.A. Undurraga,Y.A. Halasa,L.E. Coffeng,O.J. Brady,S.I. Hay,N. Bedi,I.M. Bensenor,C.A. Castañeda-Orjuela,T.W. Chuang,K.B. Gibney,Z.A. Memish,A. Rafay,K.N. Ukwaja,N. Yonemoto,C.J.L. Murray
The global burden of dengue: an analysis from the Global Burden of Disease Study 2013
Lancet Infect. Dis., 16 (2016), pp. 712-723 http://dx.doi.org/10.1016/S1473-3099(16)00026-8
[Stashenko et al., 2015]
E. Stashenko,J.R. Martínez,J.D. Medina,D.C. Durán
Analysis of essential oils isolated by steam distillation from Swinglea glutinosa fruits and leaves
J. Essent. Oil Res., 27 (2015), pp. 276-282
[Stashenko et al., 2004]
E.E. Stashenko,B.E. Jaramillo,J.R. Martı??nez
Comparison of different extraction methods for the analysis of volatile secondary metabolites of Lippia alba (Mill.) N.E. Brown, grown in Colombia, and evaluation of its in vitro antioxidant activity
J. Chromatogr. A, 1025 (2004), pp. 93-103
[Stashenko et al., 2010]
E.E. Stashenko,J.R. Martínez,C.A. Ruíz,G. Arias,C. Durán,W. Salgar,M. Cala
Lippia origanoides chemotype differentiation based on essential oil GC-MS and principal component analysis
J. Sep. Sci., 33 (2010), pp. 93-103 http://dx.doi.org/10.1002/jssc.200900452
[Tennyson et al., 2013]
S. Tennyson,D.A. Samraj,D. Jeyasundar,K. Chalieu
Larvicidal efficacy of plant oils against the dengue vector Aedes aegypti (L.) (Diptera: Culicidae)
Middle-East J. Sci. Res., 13 (2013), pp. 64-68
[Thangavel and Sridevi, 2015]
P. Thangavel,G. Sridevi
Environmental sustainability: role of green technologies
Environ. Sustain. Role Green Technol., (2015), pp. 1-324
[Vera et al., 2014]
S. Vera,D. Zambrano,S. Méndez-Sánchez,F. Rodríguez-Sanabria,E.E. Stashenko,J.E.L. Duque
Essential oils with insecticidal activity against larvae of Aedes aegypti (Diptera: Culicidae)
Parasitol. Res., 113 (2014), pp. 2647-2654 http://dx.doi.org/10.1007/s00436-014-3917-6
[WHO, 1996]
WHO
Report of the WHO informal consultation on the evaluation and testing of insecticides
(1996)
Copyright © 2017. Sociedade Brasileira de Entomologia
Idiomas
Revista Brasileira de Entomologia

Subscribe to our Newsletter

Article options
Tools
Cookies policy
To improve our services and products, we use cookies (own or third parties authorized) to show advertising related to client preferences through the analyses of navigation customer behavior. Continuing navigation will be considered as acceptance of this use. You can change the settings or obtain more information by clicking here.