Larvicidal activity of Murraya koenigii (L.) Spreng (Rutaceae) hexane leaf extract isolated fractions against Aedes aegypti Linnaeus, Anopheles stephensi Liston and Culex quinquefasciatus Say (Diptera: Culicidae)  

Arivoli S.1 , Raveen R.2 , Samuel T.2
1. Department of Zoology, Thiruvalluvar University, Vellore 632 115, Tamil Nadu, India
2. Department of Zoology, Madras Christian College, Chennai 600 059, Tamil Nadu, India
Author    Correspondence author
Journal of Mosquito Research, 2015, Vol. 5, No. 18   doi: 10.5376/jmr.2015.05.0018
Received: 30 Aug., 2015    Accepted: 02 Sep., 2015    Published: 01 Nov., 2015
© 2015 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Arivoli S., Raveen R. and Samuel T., 2015, Larvicidal activity of Murraya koenigii (L.) Spreng (Rutaceae) hexane leaf extract isolated fractions against Aedes aegypti Linnaeus, Anopheles stephensi Liston and Culex quinquefasciatus Say (Diptera: Culicidae), Journal of Mosquito Research, Vol.5, No.18 1-8(doi: 10.5376/jmr.2015.05.0018)

Abstract

Mosquitoes are significant public health pests and act as a vector of several diseases viz., malaria, filariasis, Japanese encephalitis, dengue fever and chikungunya, which are transmitted by the three genera of mosquitoes, viz., Anopheles, Culex and Aedes. Mosquito control strategies have depended primarily on the use of synthetic chemical insecticides but resulted in rebounding vectorial capacity, environmental and human health concerns. Plants may be a source of alternative agents to replace the synthetic insecticides for mosquito control. In the present study, the isolated fractions of Murraya koenigii hexane leaf extracts were evaluated for larvicidal activity against vector mosquitoes viz., Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus. Six fractions viz., A, B, C, D, E and F were obtained from the residue of hexane extract by column chromatography. Standard WHO protocol with minor modifications was adopted for the larvicidal bioassay. Larvicidal activity was evaluated against the isolated fractions at concentrations of 25, 50, 75 and 100 ppm. Larval mortality was observed 24 hours post exposure. Amongst the isolated fractions tested, fraction ‘D’ showed 100.0, 97.6 and 99.2% mortality against third instar larvae of Aedes aegypti, Culex quinquefasciatus and Anopheles stephensi at 100 ppm, respectively and LC50 values were 35.06, 27.20 and 42.51 ppm respectively. Further investigations are needed to explore the larvicidal activity of the isolated fraction ‘D’ of hexane leaf extract of this plant and also the active principle(s) responsible for larvicidal activity.

Keywords
Murraya koenigii; Larvicidal activity; Aedes aegypti; Anopheles stephensi; Culex quinquefasciatus

1 Introduction
Mosquitoes, referred to as ‘flying syringes’ and ‘public enemy number one’ are the worst enemy of mankind since dawn of time and act as a vector of several diseases (Banerjee et al., 2008; Thomas et al., 2014) viz., malaria, filariasis, Japanese encephalitis, dengue fever and chikungunya, which are transmitted by the three genera of mosquitoes, viz., Anopheles, Culex and Aedes (WHO, 2014). Mosquitoes are significant public health pests due to their predominance as agents of potentially deadly pathogens of human beings and the annoyance of skin reactions caused by their bites (Peng et al., 1998). Since 1950s, mosquito control strategies have depended primarily on the use of synthetic chemical insecticides (Hemingway et al., 2006). However, the unfriendly effect of most of these past advocated synthetic chemical insecticides leads the insect pest managers of the world to comb for alternative ways of countering this disease causing insect (Ileke and Ogunbite, 2015). Also, the long-term stability of many of these chemical insecticides and their tendency to bioaccumulate in non-target organisms have fostered many environmental and human health concerns such as the threats faced due to the development of resistance to chemical insecticides by the mosquitoes, resulting in rebounding vectorial capacity (Senthilkumar et al., 2008). To bridle these problems, safe and effective plant stratagem is in focus against the vectors and vector-borne diseases. Plants may be a source of alternative agents to replace the synthetic insecticides for mosquito control (Bashir and Javid, 2013). Bioactive botanicals are a promising alternative for mosquito control because of lower toxicity to non-target organisms and their innate biodegradation ability (Isman, 2008). In recent years, research from all over the world have documented the effect of plant-borne compounds (essential oils and plant extracts) against a wide range of mosquito species (Sukumar et al., 1991; Arivoli et al., 1999, 2012a,b, 2015a; Shaalan et al., 2005; Sakthivadivel and Daniel, 2008; Ghosh et al., 2012; Samuel et al., 2012a,b; Vargas, 2012; Raveen et al., 2012, 2014, 2015; Han et al., 2013; Benelli et al., 2014; Dias and Moraes, 2014; Samuel and William, 2014; Wachira et al., 2014; Rathy et al., 2015a,b; Tehri and Singh, 2015).

Murraya koenigii (L.) Spreng (Rutaceae) commonly called ‘curry leaf’ in English, ‘karivepu’ or ‘karuveppilai’ in Tamil, ‘karipatta’ in Hindi, ‘girinimba’ in Sanskrit, ‘karibevu’ in Kannada, ‘kariveppu’ in Malayalam, ‘kadhilimb’ in Marathi and ‘karepeku’ in Telugu (Kumar et al., 2015) is an aromatic, deciduous shrub or a small tree found cultivated throughout India (Satyavati et al., 1987). Murraya koenigii is used as a spice for its characteristic flavour and aroma and as a flavouring agent in curries and chutneys (Anonymous, 1998). The plant is used in Indian system of medicine to treat various ailments and also in traditional medicine viz., ayurvedic and unani. Murraya koenigii leaves are used in the ayurvedic system of medicine (Purthi, 1976). Chevalier (1996) reported curry leaf for its medicinal value viz., antiemetic, antidiarrhoeal and as a blood purifier. The oil is applied externally to bruises and eruptions (Anonymous, 1998). The juice of tender leaves is taken orally to stop vomiting (Muthu et al., 2006) and juice of roots is given to relieve pain associated with kidneys (Sharma et al., 2010). The leaves are used for the treatment of piles, headache, stomach ache, influenza, rheumatism, traumatic injury, insect and snake bite, diarrhoea, dysentery (Kong et al., 1986) and to allay heat of the body (Kirtikar and Basu, 1993). The leaves, barks and roots are used intensively in indigenous medicine from ancient time as a tonic for stomach ache, stimulant and carminative (Purthi, 1998). Murraya koenigii is also used in folk remedies and has a broad range of therapeutic effects including analgesic, alexiteric, febrifuge and also in treating leucoderma and blood disorders (Kirtikar and Basu, 1994).

The phytochemical constituents present in Murraya koenigii are tocopherol, β-carotene, lutein, alkaloids (Khanum et al., 2000), volatile oils, glycozoline, xanthotoxin, sesquiterpenes, carbazole alkaloids viz., murrayanine, mahanimbine, girinimbine, murrayacine, isomurrayazoline, mahanine, koenine, koenigine, koenidine, koeinimbine, and murrayazoline (Narasimhan, 1968; Kureel et al., 1970; Bordner et al., 1972). Further, the plant also possess antibacterial (Thomas et al., 1999), antifungal (Kishore et al., 1982), antiprotozoal (Goutam and Purohit, 1974), hypoglycaemic (Arulselvan et al., 2006), antioxidant (Ningappa et al., 2008), hypolipidemic (Khan et al., 1996), antimicrobial (Mathur et al., 2010), hepatoprotective (Pande et al., 2009), anti-inflammatory (Srivastava and Srivastava, 1993), anticancer/antitumor and antimutagenic (Nakahara et al., 2002) properties. Moreover, Murraya koenigii also possess insecticidal properties viz., antifeedant (Kostic et al., 2008). Arivoli and Samuel (2011) have reported the larvicidal activity of the crude hexane leaf extracts of Murraya koenigii against Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus. Kovendan et al. (2012) reported on the larvicidal activity of crude hexane, chloroform and ethyl acetate leaf extracts of Murraya koenigii against Culex quinquefasciatus. Besides, the activity of silver nanoparticles of Murraya koenigii ethanolic leaf extracts were studied against the larvae and pupae of Anopheles stephensi and Aedes aegypti (Suganya et al., 2013). Therefore, the present study was carried out to evaluate the larvicidal property of isolated fractions of Murraya koenigii hexane leaf extracts against the vector mosquitoes viz., Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus.

2 Materials and Methods
2.1 Plant collection and preparation of crude extract

Murraya koenigii leaves were collected in and around Chennai, Tamil Nadu, India (12.9213° N, 80.1220° E). Taxonomical identity of the plant was confirmed at the Department of Plant Biology and Biotechnology, Loyola College, Chennai, Tamil Nadu, India. The leaves were brought to the laboratory, shade dried under room temperature and powdered using an electric blender. Dried and powdered leaves (1 kg) were subjected to extraction using 3 L of hexane for a period of 72 hours to obtain the crude extracts using rotary vacuum evaporator. The hexane crude extract thus obtained was refrigerated at 4ºC.
 
2.2 Isolation and fractionation of crude extracts by column chromatography
The residue from the crude extract of Murraya koenigii (44.786g) was mixed with silica gel (60-120 mesh, 120 g) as admixture, subjected to column chromatography (si gel, 100-200 mesh 400 g) to obtain fractions by increasing polarity of eluents viz., hexane and ethyl acetate in the ratio of 100:0; 80:20; 60:40; 40:60; 20:80 and 0:100 respectively.

2.3 Larvicidal bioassay
Bioassay was carried out against laboratory reared vector mosquitoes free of exposure to insecticides. Standard WHO (2005) protocol with minor modifications was adopted for the study. The tests were conducted in glass beakers. Mosquito immatures particularly third instar larvae were obtained from laboratory colonized mosquitoes of F1 generation. Larvicidal activity at test concentrations of 25, 50, 75 and 100 ppm were assessed. Twenty five healthy larvae were released into each 250 ml glass beaker containing the required test concentration and quantity of test solution. Larval mortality was observed 24 hours post treatment. Larvae were considered dead when they showed no signs of movement when probed on their respiratory siphon with a needle. A total of five trials with three replicates per trial for each concentration were carried out. Distilled water as control was run simultaneously. The larval per cent mortality was calculated and when control mortality ranged from 5-20% it was corrected using Abbott’s formula (Abbott, 1925). SPSS 11.5 version package was used for the determination of LC50 and LC90 values (SPSS, 2007). The percentage data obtained was angular transformed. Data from mortality and effect of concentrations were subjected to two way ANOVA followed by Tukey’s test (P < 0.05) to determine the difference in larval mortality between concentrations.

3 Results
Results revealed that six fractions (A, B, C, D, E and F) were obtained. Amongst them, fraction ‘D’ showed 100.0, 99.2 and 97.6% mortality against third instar larvae of Aedes aegypti, Culex quinquefasciatus and Anopheles stephensi at 100 ppm, respectively. Other fractions showed minimum mortality (Table 1; Figure 1). No mortality was observed in control. The fraction ‘D’ exhibited LC50 values of 27.20, 35.06 and 42.51 ppm against Culex quinquefasciatus, Aedes aegypti and Anopheles stephensi respectively (Table 2).
 



 Table 1 Per cent larvicidal activity of Murraya koenigii hexane leaf extract isolated fractions against vector mosquitoes

 



Table 2 Probit analysis of larvicidal activity of Murraya koenigii hexane leaf extract isolated fractions against vector mosquitoes 

 



Figure 1 Larvicidal activity of Murraya koenigii hexane leaf extract isolated fractions against vector mosquitoes 


4 Discussion
One of the most effective alternative approaches under the biological control programme is to explore the floral biodiversity and enter the field of using safer insecticides of botanical origin as a simple and sustainable method of mosquito control (Ghosh et al., 2012). The results of pesticidal and phytochemical screenings of a number of higher plants based on traditional knowledge strongly indicate that plants are endowed with pesticidal properties that can be harnessed cheaply for use in agriculture and related fields. The need to use plant-based products arises from the fact that the synthetic pesticides are harmful to humans, and the entire ecosystem due to high toxicity and persistence (Okwute, 2012). Several studies have documented the efficacy of plant extracts as the reservoir pool of bioactive toxic agents against mosquito larvae. Mosquitoes in the larval stage are striking targets for pesticides because they rear in water and therefore very easy to handle in this atmosphere (Nandita et al., 2008). Larviciding is more effective since larvae are localized and restricted to a small space before they emerge into adults (Howard et al., 2007).

It has been shown that the extraction of active biochemicals from plants depend upon the polarity of the solvents used. Polar solvents will extract polar molecules and non-polar solvents extract non-polar molecules. This was achieved by using solvent systems ranging from hexane/ petroleum ether, the most non polar (polarity index of 0.1 that mainly extracts essential oil) to that of water, the most polar (polarity index of 10.2) that extracts biochemicals with higher molecular weight viz., proteins, glycans, etc. It has been found that in most of the studies, solvent with minimum polarity have been used viz., hexane or petroleum ether (Ghosh et al., 2012).

Arivoli and Samuel (2011) in their preliminary investigation tested the different solvent extracts (hexane, diethyl ether, dichloromethane and ethyl acetate) of Murraya koenigii leaves against Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus for larvicidal activity and found that the hexane extract was the most active. The results of the present study corroborate with the report of Arivoli and Samuel (2011) by confirming the presence of active substances to be present in the ‘D’ fractionated group of hexane extract, indicated by the lowest LC50 value reported. The findings of the present study are in line with the high potential of non-polar (dichloromethane, chloroform and hexane) extracts demonstrated against mosquito larvae (Krishnappa et al., 2012).

Ghosh et al. (2012) reported that hexane is the most non polar that mainly extracts essential oil. In the present study, hexane fractions were toxic against Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus. This could be due to the presence of essential oil, terpenoids, phenolic compounds and alkaloids within the fraction. It was proven by Mann and Kaufman (2012) that as typical lipophiles, the essential oil passes through the cell wall and cytoplasmic membrane, disrupts the structure of different layers of polysaccharides, fatty acids and phospholipids and permeabilizes them. They also interfere with the basic metabolic, biochemical, physiological and behavioural functions of insects (Tripathi et al., 2009), disruption of the molecular events of morphogenesis, alteration in the behaviour and memory of cholinergic system and inhibition of acetylecholinesterase (AChE). Of these, the most important activity is the inhibition of acetylcholine- esterase activity as it is a key enzyme responsible for terminating the nerve impulse transmission through synaptic pathway (Rattan, 2010). Also, terpenoids are known to possess insecticidal properties (acute toxicity) (Mann and Kaufman, 2012). Phenolic compounds including tannins and flavonoids are known to possess insecticidal properties and act as mitochondrial poisons for insect vectors (Mann and Kaufman, 2012). Alkaloids are nitrogenous compounds that show insecticidal properties at low concentration and the mode of action on insect vectors varies with the structure of their molecules, but many are reported to affect acetylcholinestrase or sodium channels (Rattan, 2010).

Hexane, dichloromethane and acetone fractions of Spondias mombin leaf extracts when tested against the larvae of Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus, it was found that hexane fractions were found to possess more larvicidal activity that the other fractions reported by low LC50 values of 22.54, 92.20 and 326.53 ppm against Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus respectively (Eze et al., 2014). Lame et al. (2015) pointed out that among the four fractions (hexane, chloroform, ethyl acetate and methanol) of Annona senegalensis leaves tested against the larvae of Anopheles gambiae, the hexane fractions were effective, exhibiting LC50 value of 298.8 ppm.

Mudalungu et al. (2013) tested the fractions (C1-C3) of Fagaropsis angolensis chloroform leaf extract against Anopheles gambiae and found fractions C3 and C2 to exhibit high larvicidal activity with LC50 values of 144.4 and 147.6 ppm respectively after 24 hours of exposure. Nyamoita et al. (2013) reported the acetone root bark extract fractions of Vitex payos (F8, F11 and F12) to possess larvicidal activity against the larvae of Anopheles gambiae after 24 hours of exposure and found the fraction F8 to exhibit the highest larvicidal activity whose LC50 value was 7.0 ppm followed by fraction F11 and F12 with 13.4 and 19.6 ppm respectively. Nzelibe and Chintem (2013) tested the Ocimum gratissimum leaf n-hexane fractions (F1-F6) against Culex quinquefasciatus larvae, and found the fraction F1 to be effective with a LC50 value of 1.49 ppm on 24 hours of exposure. Chintem et al. (2014) stated that Datura stramonium leaf methanol extract fractions (DSEE-F1 to DSEE-F7) when tested against the third instar larvae of Culex quinquefasciatus, the highest mortality rate was achieved in DSEE-F1 and its LC50 value was 4.39 ppm 24 hours post exposure. Owino et al. (2014) reported that out of four fractions obtained from the chloroform root bark extract of Turraea abyssinica and Turraea cornucopia, fraction TAF4 elicited the highest larval mortality and its LC50 value was 185.4 ppm while fraction TCF5 of Turraea cornucopia exhibited 56.6 ppm against Anopheles gambiae after exposure of larvae for 24 hours. Arivoli et al. (2015b) reported that the isolated fractions of Citrullus colocynthis dichloromethane whole plant extract when evaluated for larvicidal activity against the vector mosquitoes, the fraction ‘C’ (100 ppm) showed 94.4, 96.0 and 98.4% mortality against third instar larvae of Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus and LC50 values of 18.57, 23.48, 19.26 ppm respectively after 24 hours.

Botanicals have widespread insecticidal properties and identifying plant based insecticides that are efficient as well as suitable and adaptive to local ecological conditions, biodegradable and possessing wide spread mosquitocidal property will obviously work as a new weapon in the arsenal of synthetic insecticides and in future may act as suitable alternative product to fight against mosquito-borne diseases (Ghosh et al., 2012). Identification and isolation of bioactive compounds of plant origin against mosquito menace are imperative for the management of mosquito-borne diseases. Further, Tehri and Singh (2015) stated that the successful results of preliminary studies on mosquitocidal potential of plant extracts encourage further effort to investigate the bioactive compounds in those extracts that might possess good larvicidal properties when isolated in pure form. In addition, novel drug delivery system of plant based active substances is the need of the hour.

Acknowledgement
The first author is thankful to the Department of Science and Technology, Govt. of India, New Delhi, India for financial assistance.

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