Abstract
Context: Vector control is facing a threat due to the emergence of resistance to synthetic insecticides. In this context, essential oils have received much attention as potentially useful bioactive compounds against insects. Therefore, our present study aimed to evaluate the efficacy of essential oils from the aerial parts of Salvia elegans Vahl, Salvia dorisiana Standl., Salvia splendens Sello ex J.A. Schult Blue Ribbon, and S. splendens Sello ex J.A. Schult Scarlet Sage Red (Lamiaceae) against the fourth instar larvae of Aedes albopictus Skuse (Diptera: Culicidae).
Objective: The mosquito larvicidal activities of the essential oils and chemical composition of four taxa of Salvia are investigated in this article for the first time.
Materials and methods: Chemical compositions of essential oils obtained from four taxa of Salvia were analyzed by gas chromatography-mass spectrometry (GC-MS), GC-FID, and the effects of essential oils on fourth instar larvae of A. albopictus were investigated.
Results: The main components identified from each Salvia essential oils were as follows: spathulenol (38.73%) and caryophyllene (10.32%) from S. elegans; ledol (45.8%) and 4,4'-[(p-phenylene)diisopropylidene]diphenol (17.38%) from S. dorisiana; β-cubebene (22.9%), and caryophyllene (12.99%) from S. splendens Blue Ribbon; phytol (41.46%) and cyclooctasulfur (24.88%) from S. splendens Scarlet Sage Red. The essential oils of S. elegans and S. splendens Blue Ribbon had excellent inhibitory larvicidal effect against A. albopictus larvae, and their LC50 values in 24 h were 46.4 ppm (LC90 = 121.8 ppm) and 59.2 ppm (LC90 = 133.0 ppm), respectively.
Discussion and conclusion: These findings demonstrate that the essential oils of these Salvia species could be considered as the powerful candidates to bring about useful botanicals so as to prevent the resurgence of mosquito vectors.
Introduction
The search for new strategies or natural products to control vectors of diseases is desirable due to the prevalent occurrence of vector resistance to synthetic insecticides and the problem of toxic nonbiodegradable residues contaminating the environment and undesirable effects on nontarget organisms (CitationJantan et al., 2005). Essential oils from plants may be an alternative source of mosquito larval control agents, since they constitute a rich source of bioactive compounds that are biodegradable and potentially suitable for use in integrated management programs. Much effort has, therefore, been focused on the effectiveness of plant essential oils against mosquito larvae because of their broad spectrum of activity against insects, low mammalian toxicity, and ability to degrade rapidly in the environment (CitationJantan et al., 2005; CitationMorais et al., 2007; CitationCheng et al., 2008; CitationSilva et al., 2008).
The genus Salvia (Lamiaceae) is one of the largest genera of flowering plants, with nearly 1000 species (CitationEstilai et al., 1990), largely cultivated for ornamental, aromatic, and culinary usage (CitationClebsh, 2003). The name Salvia derives from the Latin “Salvere,” which means “to heal.” Indeed, this herb is highly regarded for its healing qualities. Many plants of the genus are widely used in the traditional medicine for their medicinal properties such as antidiabetic (CitationBailey & Day, 1989), diuretic (CitationDarias et al., 1989), hemostatic, hypoglycemic (CitationEidi et al., 2005), diaphoretic (CitationLeporatti et al., 1985), anti-inflammatory (CitationBaricevic et al., 2001), antioxidative (CitationWang et al., 1999), cytotoxic, and antibacterial activities (CitationShin et al., 2001). Several species are used to treat cancer, malaria, loss of memory and to disinfect homes after sickness (CitationKamatou et al., 2008). Several kinds of secondary metabolites have been isolated from Salvia species. However, most characteristic secondary metabolite constituents of Salvia species are terpenoids and flavonoids. The essential oil composition of Salvia showed the dominance of monoterpene hydrocarbons, oxygen-containing monoterpenes, and oxygen-containing sesquiterpenes (CitationKamatou et al., 2008).
Aedes albopictus has been the focus of entomologist virologists and public health workers because it is a highly competent vector for several arboviruses, including the four dengue virus serotypes (CitationHawley, 1988; CitationMitchell, 1995). It is a proven vector of dengue viruses and filarial worms in Asia (CitationHawley, 1988; CitationEstrada-Franco & Craig, 1995). Dengue fever is a vector-borne disease that has a major impact on the public health in many tropical areas worldwide. In India, A. albopictus has often been incriminated as a dengue vector in urban environments and also occasionally in rural settings (CitationReuben et al., 1988). It is a competent experimental vector of several other arboviruses, notably chikungunya, Ross river, and Japanese encephalitis viruses (CitationShroyer, 1986; CitationMitchell, 1995; CitationMoutailler, 2009), and can support development of yellow fever virus (CitationJohnson et al., 2002). The bioassays conducted by CitationTantely et al. (2010) on A. albopictus indicated the presence of resistance to insecticides such as organochlorides, organophosphates, and pyrethroids. Chlorpyrifos resistance (CitationLiu et al., 2004) and permethrin resistance (CitationOthman et al., 2008) were also detected in this mosquito species.
In the Lamiaceae family, a wide diversity of active compounds has been found to be effective against a variety of mosquito vectors (CitationIsman et al., 2001; CitationTraboulsi et al., 2002; CitationCetin et al., 2006). However, there have not been any thorough investigations on larvicidal effects of essential oils from Salvia elegans, Salvia dorisiana, Salvia splendens Blue Ribbon, and S. splendens Scarlet Sage Red. In the light of this, the present investigation was designed to identify the constituents of essential oils from the aerial parts of S. elegans, S. dorisiana, S. splendens Blue Ribbon, and S. splendens Scarlet Sage Red and to test their larvicidal efficacy against fourth instar larvae of A. albopictus.
Materials and methods
Plant materials
Fresh aerial parts from S. elegans, S. dorisiana, S. splendens Blue Ribbon, and S. splendens Scarlet Sage Red were collected from Ooty (South India), during the flowering period (April to June 2008). The geographical coordinates of Ooty is 11.35 N, 76.76 E, and 2286 m altitude. Its latitudinal and longitudinal dimensions being 130 km (latitude: 10–38 WP 11–49N) by 185 km (longitude: 76.0 E to 77.15 E). Botanical identity of these samples was confirmed by Dr. A.K. Pradeep (herbarium curator), Department of Botany, Calicut University. The voucher specimens (CALI 123705, CALI 123706, CALI 123708, and CALI 123707) were deposited at the Herbarium (CALI) of Department of Botany, Calicut University.
Essential oil extraction
Aerial parts of S. elegans, S. dorisiana, S. splendens Blue Ribbon, and S. splendens Scarlet Sage Red (50 g each, in triplicate) were air-dried, powdered, and subjected to hydrodistillation using a modified Clevenger-type apparatus for 6 h (CitationCheng et al., 2005). The yield of essential oils obtained were averaged over three experiments and calculated according to dry weight of the plant materials. Essential oils were stored in airtight glass vials in the refrigerator at 4°C until used for the various analyses.
Analysis of essential oils
The gas chromatography/mass spectroscopy (GC/MS) analyses were performed on a Hewlett Packard (HP) 6890 GC interfaced with a Hewlett Packard 5973 Mass Selective Detector (MSD) system operating at 70 eV and 250°C, equipped with a splitless injector. A cross-linked 5% phenyl methyl siloxane column (HP-5), with 320 µm × 30 m and 0.25 µm film thickness, was utilized. Helium was used as the carrier gas at a flow rate of 1.4 mL/min. The temperature program for the HP-5 column was set at 60°C–243°C, at a rate of 3°C/min. Runtime was 61 min. Quantification was performed using percentage peak area calculations and the identification of individual compounds was done using the NIST MS Search, literature (CitationAdams, 2001) and several authentic compounds. The relative concentration of each compound in essential oil was quantified based on the peak area integrated by the analysis program.
The gas chromatography analyses were performed on a Hewlett Packard GC connected with a flame ionization detector (FID) system. Hydrogen was used as the carrier gas. Volatiles were separated using the temperature program 45°C–250°C at a rate of 5°C/min. The temperature of the detector was 250°C. The RT values obtained from the GC-FID analysis was nearly identical to the RT values obtained from the GC-MS analysis. So, we have given the RT values obtained from GC-MS analysis in .
Table 1. Chemical constituents of aerial parts essential oils from S. elegans, S. dorisiana, S. splendens Blue Ribbon, and S. splendens Scarlet Sage Red.
Mosquito larvicidal activity
The larvae of A. albopictus Skuse were identified by the Department of Zoology, University of Calicut and reared at Cell and Molecular Biology Division, Department of Botany, University of Calicut according to the standard method (CitationLatha et al., 1999). Larvae used in the experiments were obtained from the A. albopictus mosquito colony maintained at Cell and Molecular Biology Division, Department of Botany, University of Calicut, Calicut, India. The fourth instar larvae were used to study the larvicidal activity. All bioanalyses were performed according to the method of CitationWHO (1981). No food was given at the time of analyses. The essential oils obtained from the four taxa of Salvia were used to prepare the stock solutions of 10 mg/mL in acetone. The stock solutions were diluted with distilled water to obtain the test solutions of 200, 100, 50, and 25 ppm. Concentrations of the test solutions were determined based on the literature survey (CitationSakthivadivel & Thilagavathy, 2003; CitationCetin et al., 2006; CitationKaushik & Saini, 2008). Two controls were maintained at a time, one consisted of acetone and the other distilled water only. The fourth instar larvae (20 each) were tested at four different test solutions as well as controls in four replicates. The larval mortality was recorded after 24 h. The larvae were considered as dead, if they were not responsive to a gentle prodding with a fine needle. Toxicity and effect were reported as LC50 and LC90, representing the concentrations in ppm with 50% and 90% larvae mortality rate in 24 h, respectively.
Statistical analyses
The mortality percentage was determined and two-way factorial analysis of variance (ANOVA) (CitationFisher, 1970) was conducted to analyze the significant difference among the test essential oils’ larvicidal activity. Results with P < 0.01 were considered to be statistically significant. Mortality data obtained were analyzed by Probit analysis (CitationFinney, 1971) to obtain regression equation, LC50 and LC90, chi-square values, and fiducial limits at 95% confidence limits. Standard errors with means of larval mortalities were also calculated.
Results and discussion
Chemical composition analysis of essential oils
The chemical compositions of the four essential oils are presented in . A wide spectrum of volatile chemical compounds was detected in the essential oils obtained from the aerial parts of four taxa of Salvia. The essential oil yields of S. elegans, S. dorisiana, S. splendens Blue Ribbon, and S. splendens Scarlet Sage Red were found to be 0.23, 0.25, 0.18, and 0.13%, respectively. A total of 54 compounds were identified representing about 92.49%–100% of the oils. The compounds from the four essential oils could be assigned to six different classes: monoterpene hydrocarbons (0.00–4.41%), diterpene hydrocarbons (10.81–41.46%), sesquiterpene hydrocarbons (10.24–76.39%), fatty acid esters (0.00–10.99%), phenols (0.00–17.38%), and others (3.26–8.1%).
Twenty-six compounds were detected from the essential oil of S. elegans corresponding to 94.71% of the total oil. The essential oil contained spathulenol (38.73%), caryophyllene (10.32%), pimara-7, 15-dien-3-one (5.67%), and iso-aromadendrene epoxide (5.39%) as the major components. A previous report on the gas chromatography/mass spectrometry study of S. elegans Vahl in Japan by CitationMakino et al. (1996) showed 28 constituents. Among them, mono- and sesquiterpenoids such as trans-ocimene, linalool, β-caryophyllene, germacrene D, and spathulenol were predominant components. The essential oil of S. dorisiana shows nine compounds accounting for 98.12% of the total oil with ledol (45.8%), 4,4'-[(p-phenylene) diisopropylidene]diphenol (17.38%), phytol (10.81%), ethyl iso-allocholate (6.37%), and caryophyllene (5.32%) as its main constituents. The results differ from that obtained by CitationMaciarello and Tucker (1994) and CitationHalim and Collins (1975). They reported that the main constituents of S. dorisiana were perillyl acetate and methyl perillate. Twenty-eight compounds amounting to 92.49% were identified from the essential oil of S. splendens Blue Ribbon. The main constituents in the S. splendens Blue Ribbon essential oil were β-cubebene (22.9%), caryophyllene (12.99%), phytol (12.27%), aristolene (6.28%), and β-elemene (4.88%). This is the first report on the essential oil constitution of S. splendens Blue Ribbon. S. splendens Scarlet Sage Red essential oil contained six identified compounds, accounting for 100.00% of the essential oil with phytol (41.46%), cyclooctasulfur (24.88%), and 2,2'-methylene-bis[6-(1,1-dimethylethyl)-4-methyl]-phenol (12.42%) as its main constituents. The chemical profiles of S. elegans and S. dorisiana were significantly different from the previously published reports. The discrepancy might have been caused by the differences in the chemotype of these plants or may be due to environmental factors.
The composition analysis of the four Salvia essential oils revealed that sesquiterpenes predominated in S. elegans, S. dorisiana, and S. splendens Blue Ribbon and diterpenes are abundant in S. splendens Scarlet Sage Red. In all the four taxa, diterpenes are present as one of the major components. S. elegans essential oil had low amounts of monoterpene hydrocarbons, whereas S. dorisiana, S. splendens Blue Ribbon, and S. splendens Scarlet Sage Red had no monoterpene contents. Fatty acid esters are present in these species except S. splendens Blue Ribbon. Phenols represented as major compounds in S. dorisiana and S. splendens Scarlet Sage Red.
Effect of essential oils on mosquito larvae
Potential mosquito larvicidal effects were shown by the essential oils of S. elegans, S. dorisiana, S. splendens Blue Ribbon, and S. splendens Scarlet Sage Red against fourth instar larvae of A. albopictus. The essential oils of S. elegans and S. splendens Blue Ribbon induced 100% larval mortality against A. albopictus in 24 h with a dosage of 200 ppm, whereas S. dorisiana essential oil induced 92.5% larval mortality and S. splendens Scarlet Sage Red essential oil induced 75.5% larval mortality. When dosage was decreased to 50 ppm, the larval mortality for the four Salvia species was in the decreasing order of S. elegans (57.5%) > S. splendens Blue Ribbon (45.5%) > S. dorisiana (32.5%) > S. splendens Scarlet Sage Red (27.5%). Among them, the essential oil of S. elegans was found to be the most effective ().
Figure 1. Mosquito larvicidal effects of essential oils from four taxa of Salvia L. against fourth instar larvae of A. albopictus in 24 h (mean ± standard error of mortality%).
The LC50 and LC90 values of essential oils from four different species of Salvia against A. albopictus larvae indicated that the oil from S. elegans has the most effective larvicidal effect against A. albopictus in 24 h (LC50 = 46.4 ppm; LC90 = 121.8 ppm), followed by S. splendens Blue Ribbon (LC50 = 59.2 ppm; LC90 = 133.0 ppm), S. dorisiana (LC50 = 76.7 ppm; LC90 = 187.9 ppm), and S. splendens Scarlet Sage Red (LC50 = 92.7 ppm; LC90 = 257.9 ppm) (). The control treatments (acetone and distilled water) had no effect on the larvae. These results indicated that the essential oils from S. elegans and S. splendens Blue Ribbon exhibited high inhibitory performance against A. albopictus larvae.
Table 2. Efficacy of essential oils from S. elegans, S. dorisiana, S. splendens Blue Ribbon, and S. splendens Scarlet Sage Red against fourth instar larvae of A. albopictus in 24 h treatment.
The analysis of variance (ANOVA) was conducted to analyze the significant difference among the test essential oils’ larvicidal activity. According to F-test (CitationFisher, 1970), the results with P < 0.01 were statistically significant. The LC50 and LC90 values and fiducial limits were calculated by probit analysis and recorded in . The chi-square values 16.025 (S. elegans), 11.921 (S. dorisiana), 4.863 (S. splendens Blue Ribbon), and 24.299 (S. splendens Scarlet Sage Red) were statistically significant at 0.099, 0.29, 0.90, and 0.007 probability levels. The standard errors with means of larval mortalities were recorded in .
In the present study, GC-MS data () reveal that a wide spectrum of sesquiterpenoids, monoterpenoids, diterpenoids, phenols, and other volatile chemical compounds are present in the essential oils of the four species of Salvia studied. According to CitationVieira et al. (2001), terpenoids are the major source of insecticide substances, which perform protection against insects in the plants, demonstrating good insecticide activity in experimental models. A study conducted with essential oil components revealed that the more active compounds against mosquitoes are phenylpropanoids and sesquiterpene alcohols (CitationSimas et al., 2004). According to CitationSantos et al. (2006), the essential oil of Cordia leucomalloides, characterized by high percentage of sesquiterpenes (90.6%), exhibited significant larvicidal activity, which was able to kill 98.7% of the third instar larvae in the concentration of 100 ppm. Another study conducted by CitationPaluch et al. (2009) on the larvicidal and repellent activity against arthropod pests showed that sesquiterpenes possess high larvicidal and repellent activity against a spectrum of arthropod pests.
The literature survey showed that the essential oil components detected in the present investigation possess reputed insecticidal properties. Caryophyllene oxide together with linalool, methyl eugenol, aromadendrene, and caryophyllene might be the probable reason for high mosquito larvicidal activity of S. elegans essential oil. In S. splendens Blue Ribbon also the presence of β-cubebene, caryophyllene oxide, and caryophyllene may cause high mosquito larvicidal activity. Such activity has already been reported on these volatile terpenoids (CitationHarbone & Baxter, 1983; CitationSenthilkumar et al., 2008). Carvacrol and caryophyllene oxide were the main compounds responsible for the potent insecticidal activity of Lippia gracilis and Hyptis pectinata against Aedes aegypti larvae (CitationSilva et al., 2008). These components are relatively low in S. dorisiana essential oil and many of these components are absent in S. splendens Scarlet Sage Red essential oil. This may be the reason for the relatively low larvicidal activity of these species. Overall, the bioactivities of these Salvia essential oils are comparable with many essential oils reported recently as mosquito larvicides.
Conclusion
According to GC-MS analyses, the major constituents of the essential oils were spathulenol, caryophyllene, pimara-7,15-dien-3-one, phytol, and iso-aromadendrene epoxide from S. elegans, ledol, 4,4'-[(p-phenylene)diisopropylidene]diphenol, phytol, ethyl iso-allocholate, and caryophyllene from S. dorisiana, β-cubebene, caryophyllene, phytol, and aristolene from S. splendens Blue Ribbon and phytol, cyclooctasulfur, and 2,2'-methylene-bis[6-(1,1-dimethylethyl)-4-methyl]phenol from S. splendens Scarlet Sage Red. Results obtained from the larvicidal tests, using the essential oils from S. elegans and S. splendens Blue Ribbon showed that they had excellent inhibitory larvicidal effects against A. albopictus larvae. The results indicate that the essential oils of these Salvia species might be considered as potent sources for the production of fine natural mosquito larvicides. However, further investigations for the constituent actions, mode of action, effects on nontarget organisms, and field evaluation are necessary. These results obtained are useful in search of more selective, biodegradable, and naturally produced larvicidal compounds.
Declaration of interest
The authors report no declarations of interest.
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