Int.J.Curr.Microbiol.App.Sci (2013) 2(4): 172-182

International Journal of Current Microbiology and Applied Sciences ISSN: 2319-7706 Volume 2 Number 4 (2013) pp. 172-182 http://www.ijcmas.com

Original Research Article

A Study on the Predatory Potency of , geminata Nymphs over the Immature Stages of the Filarial Vector, Culex quinquefasciatus Say

Amitabh Shad* and J. Andrew

Department of Zoology and School of Entomology, St. John’s College, Agra-282002, Uttar Pradesh, India *Corresponding author

ABSTRACT

Pressure of urbanization, improper management of the domestic, polluted and other neglected water collections has led to the formation of enormous mosquito breeding

sites resulting in the spread of various mosquito borne diseases such as Japanese encephalitis, chickungunya, dengue, filariasis etc. Since many decades chemical K e yw or ds insecticides are widely used to control mosquitoes. Residues of these insecticides are

found in the air, water, soil and even within the body of organisms. The use of Culex chemical insecticide is now no more the concrete solution to suppress the vector quinquefasciatus , population. Mosquitoes have many natural enemies, both as predators and parasites. Dragonfly Certain species of fishes, birds, bats, and prey upon them. are one nymphs, among these predatory insects belonging to the order . In the present study an Bradinopyga attempt has been made to understand the predatory potency of the locally available geminata , dragonfly, nymphs over the immature stages of the Predation mosquito,Cx. quinquefasciatus, with the aim to develop an eco-friendly, economical

and safe alternative in mosquito control. Results indicate that the maximum predation was on the first instar larvae while the minimum predation was of the pupal stage by

different sizes of nymphs. The present study reveals voracious, intense and active predation of dragonfly nymphs over the Cx. quinquefasciatus immature larval and pupal stages.

Introduction.

Mosquitoes pose a major threat to human is a major problem of the tropics and health as they play a predominant role in subtropics. Accordingto the expert the transmission of Japanese encephalitis, committee on filariasis, 905 million people filariasis, chikungunya, malaria, dengue were at risk of filariasis with 90.2 million and other such vector borne communicable of victims worldwide in 1984 and the diseases (Jang et al., 2002).Among these figures were 751.4 million and 78.6 communicable diseases, Lymphatic million in 1992 respectively (Ottesan et filariasis caused by Wuchereria bancrofti al., 1997). At present, 1.3 billion people

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Int.J.Curr.Microbiol.App.Sci (2013) 2(4): 172-182 are at risk of lymphatic filariasis infection diazinon, bensolid and fenthion and and about 120 million people are affected carbamates like adizarb, carbofuran and in 83 countries amongst them about 45.5 carboxyl. Residues of many such million people are from Indian insecticides were found in the air, water, subcontinent (WHO, 2006). It is an soil and even within the body of alarming situation to limit filarial organisms. Some of theseget incorporated transmission through different means by within the human bodies as persistent reducing vector population by larvicides, deposits in fatty tissues and sometimes adulticides and introduction of natural even found being secreted in the mother’s predators of mosquitoes in ecosystem. milk.The use of chemical insecticide is Japanese encephalitis is another major now no more the concrete solution to mosquito borne disease endemic in at least suppress the vector population. Biological 21 countries with nearly 30,000-50,000 control methods particularly the cases annually from Asia (Solomon, application of the predators like 2006). In India, as estimated 378 million indigenous larvivorous fishes, dragonfly people are living at the risk of Japanese nymph, bugs, and parasites like bacteria, encephalitis in 12 states including Uttar fungi, nematodes etc., provide an Pradesh (Okuno,1978; Bharadwaj, 1981). alternative means of mosquito control. The The chronic forms of these diseases are distinct advantage with these biocontrol assumed to be debilitating, leading to the agents are their ability to kill target species restriction in the economic productivity at low doses, safety to non-target (Evans et al., 1993). organisms, easy application in the field, inexpensive production, lack of infectivity The mosquito Culex quinquefasciatus Say, and no pathogenicity in mammals is the major vector of Filariasis, Japanese including man. encephalitis and other plagues throughout the world, especially in the tropical and Mosquitoes have many natural enemies, the subtropical countries (WHO, 2006). It both as predators and parasites. Certain is found throughout all the warmer parts of species of birds, bats, and insects prey the world breeding in association with upon them. Many species of fish feed on human habitation, preferring polluted their larvae and certain top feeding waters such as sewage and silage water minnows, particularly of the collections, including cesspools, cesspits, Gambusia, have been extensively drains, septic tanks and the places employed in many parts of the world in provided with a sufficient degree of mosquito control (Das and Prasad, 1991). organic pollution. It is claimed that the Invertebrate predators have been shown to careful and prolonged control of the be responsible for the drastic reduction in mosquito, Culex quinquefasciatus can the larval population of mosquitoes. eradicate filariasis, Japanese encephalitis Important group of insects predators in the and other such mosquito borne diseases. rice field includes Coleopterans specially Dysticidae and Hydrophillidae, For many decades chemical insecticides Hempiptera particularly Notonectidae and are widely used to control mosquitoes. Odonata mainly Anisopterans. Predators They are generally chlorinated usually have a limited breeding season and hydrocarbons like DDT, Dieldrin, longer generation time than that of endosulphan; organophosphates like mosquitoes and hence they play a vital

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Int.J.Curr.Microbiol.App.Sci (2013) 2(4): 172-182 role in control of mosquito larvae. Among Materials and Methods these biological agents of mosquito control the Odonates are one of the best predators. Collection of Culex quinquefasciatus The importance of Dragonflies (Odonata) Say: The larvae and adults of the as consumers of mosquitoes has been mosquito, Culex quinquefasciatus were known for a long time ago (Corbet, 1980). collected from various mosquitogenic regions of Agra city (26° 44’ N to 27° 25’ Odonates were one of the first N latitude; 77° 26’ E to 78° 32’ E to be examined as biological agents to longitude). Sampling of larvae and pupae control mosquitoes. They are voracious were done using aquatic handdipnet and important predators of mosquito having sieve with fine pores and a larvae in the fresh water ecosystems. They diameter of 4 inch. The larvae and pupae detect their prey by compound eyes and were identified, numbered and carried to mechanical receptors and capture them laboratory along with water samples in with their labium. Both the nymph as well specimen bags made of polythene, keeping as the adults catches mosquitoes (Corbet, half of the space in the bag empty for 1980). aeration. Sometimes pipette and ladles were also used for collection. Egg rafts, if In feeding experiments, Anisopteran any, were collected in the filter paper and nymphs proved to be extremely voracious. kept in the specimen box. The samples Nymphs of Aeshnacyanea consumed up to were marked carefully recording the date, 100 mosquitoes larvae each day and location, type of site and other physical approximately around 2110-2120 during parameters. Identification of species was its life time (Becker et al., 2003). Such done following standard key (Barraud, research finding indicates that the 1934).Fourth instar larvae were taken for development, survival and abundance of categorization and reared until adult larval mosquito populations in the field are emergence for further confirmation of the limited by predaceous insects which are species. Both the larvae and adults were primarily responsible for mortality in identified and preserved. immature stages of mosquitoes. Collection of dragonfly nymph This effect has been reported in many different aquatic habitats and is Dragonfly nymphs were collected from the responsible for restraining the density of various region of Agra city. Nymphs were such prey populations below the critical collected with the help of the dipper and threshold where transmission of diseases strainer from the ponds, ditches, cemented could not occur (Das et al., 2006). tanks and other water bodies. The collection was done from the water bodies Today, environmental safety is considered by sweeping the aquatic handdipnet from a to be of paramount importance. Therefore depth of one to two feet inside the water in the present study was undertaken to study the downward to upwards direction. the predatory potencyof the locally Nymphs were numbered, recorded and available nymphsof dragonfly, then transferred to the sampling jars along Bradinopyga geminate over the immature with the leaf litter, water weeds, with very stages of the mosquito, Culex little free water. These sampling jars were quinquefasciatus Say. then kept in the sampling bags and

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Int.J.Curr.Microbiol.App.Sci (2013) 2(4): 172-182 transported carefully to the laboratory. processed again to yield adults as These nymphs were identified at School of described above. Deposited egg rafts were Entomology, Department of Zoology, St. collected daily, numbered, marked and John’s College, Agra using standard keys incubated for experimental usage. (Fraser, 1934). “Rekha”, a chemical repellent was used to Laboratory rearing of Culex mark the boundary of the rearing cages so quinquefasciatus Say as to check the entry of ants, spiders and other such insects which may damage the The colony was maintained from the egg mosquito colony. rafts. The egg rafts were kept in white enamelled breeding bowls 10 inches in Laboratory rearing of dragonfly diameter, 5 inches deep and half filled nymphs with de-chlorinated tap water. The water in the breeding bowls, on the onset of the The collected nymphs of the dragonfly, first instars larvae, was supplemented with Bradinopyga geminata, were released in yeast at an interval of every twenty four the aquarium with dimension of 60 × 30 × hour, till the larvae transformed into 35cm and the water was filled up to 10 cm pupae. Each bowl contained about 150- for maintaining them alive. This water 200 larvae. The amount of food added contained both protozoan and planktonic daily was increased with larval stage. The algae, which are a natural source of food scum, if formed, was removed using a for dragonfly. Once they are measured, glass rod. The duration of larval stage was each dragonfly nymphs were given their seven to eight days at 28±1°C and about own containers and fed with bloodworms 65 – 80 percent of relative humidity. or mosquito larvae. The nymphs were fed Pupae were collected daily and transferred twice or thrice a week during winters and in groups of fifty pupae at a time into several times a week in summers. When beakers; half filled with clean water and the nymphs were about to emerge as adults placed in empty 18″×18″×18″ mosquito or imago, they were transferred into breeding cages. The metamorphosed emergence cages, allowed to emerge, and adults were fed with 10 % sugar solution then released back to the environment. A or honey soaked in a piece of cotton for few adult specimens were kept in glassine three to four days. Each cage contained envelope after killing and preserving using about 200♀ and 100♂ adults which were acetone in School of Entomology, allowed to mate. Department of Zoology, St. John’s College, Agra for further reference. The females were given blood meals from a healthy but immobilized pigeon which Predation experiment was placed inside the rearing cages during nights on alternate days. For egg laying To determine the predatory potency of the suitable containers half filled with water locally available dragonfly, Bradinopyga were introduced inside the breeding cages geminatanymphs the method followed by which contained fertilized females. Each Singh and Dhiman (2003) was used with container was lined with filter paper to slight modifications. The dragonfly prevent the egg rafts from adhering to the nymphs, of different sizes were brought containers walls. The egg rafts were from the field and maintained in the

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Int.J.Curr.Microbiol.App.Sci (2013) 2(4): 172-182 aquarium. Three stages of dragonfly quinquefasciatus without showing any nymphs of different size i.e. small (5mm), preference for first or fourth instar larvae medium (10 mm) and large (15mm), were while smaller nymphs preferably predated measured lengthwise and used in predation over initial stages of the Cx. experiments. All three nymphal stages of quinquefasciatus. The results also B.geminata were provided with Cx. indicates that among the different nymphal quinquefasciatus larvae as supplementary size (small, medium and large) the small food, obtained through laboratory rearing. sized nymphs (5mm) highly predated over A series of experiments were conducted in the third instar larvae 39.1, 52.3 and 68.4 the laboratory within the troughs of 500 ml after 12 hours, 24 hours and 36 hours capacity containing 300 ml of water with respectively (Table: 1, 2 and 3 ). There larval food. One hundred larvae of each was no marked difference in the predation instars and pupae were provided to each by medium (10 mm) and large (5 mm) size of dragonfly nymphs i.e. small, nymphal size of dragonfly. However, both medium and large, in five replicates along large and medium size of dragonfly with control. Thus each size of dragonfly nymphs preferred early stages of Cx. nymph was studied with five replicates quinquefasciatus larvae (Figure: 1, 2 and each, separately for predation against 3). Pre-moulting time of nymphal stage every immature stages of the mosquito, also decreased the feeding rate. Cx. quinquefasciatus. Observations on prey mortality were made by counting and Introduction of dragonfly nymphs as recording of live mosquito larvae and predators over mosquito larvae in water pupae present in the trough at an interval reservoirs has resulted in reduction of of 12 hours, 24 hours and 36 hours. mosquito larvae and even their complete elimination in the water bodies (Sebastian Results and Discussion et al., 1980; Sebastian et al., 1990; Garcia et al., 1996). The present study reveals Results of the feeding rate of dragonfly voracious, intense and active predation of nymph on the immature stages of the dragonfly nymphs over the Cx. mosquito, Culex quinquefasciatus quinquefasciatus immature larval and indicates that the maximum predation was pupal stages. From the results it is clear on the first instar larvae while the that the mosquito larvae are the very minimum predation was of the pupal stage apparent food of dragonfly nymphs. The by different sizes of nymphs (small, results indicate that dragonfly nymphs medium and large) Table 1, 2 &3. Increase preferred mostly the first instar larvae in immature stages of Cx. quinquifasciatus (Figure 1,2 and 3). Results of feeding rates resulted in the decreased feeding rate of of dragonfly nymph, B. contaminate over nymphs. As the size of the nymphs the aquatic stages of Anopheles stephensi, increased, there was increase in predation and also indicated that the rate also. It is shown in the experiment that maximum predation was of first instar the nymphal stages (small, medium & larvae (127.8 and 112.5respectively) large) seemed to prefer early larval stages while the minimum was of pupal stage of mosquito (Figure 1, 2 & 3). Pupae were (Singh and Dhiman, 2003). The dragonfly least preferred by all nymphal size (Table nymphs belonging to the Labellula spp. in 1,2& 3). It was also observed that the large an experiment over the predation of Aedes sized nymphs predated more larvae of Cx. aegypti larval and pupal stages also

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Int.J.Curr.Microbiol.App.Sci (2013) 2(4): 172-182 reported that the dragonfly consumed both age and when they are advanced in age the stages with preference towards the they are particularly addicted to the smaller onceover the pupae (Alahmed et Culicidae larvae. The results of the present al., 2009). Rashed et al., (2005) also study also indicates that among the reported that the dragonfly preferred small different nymphal size i.e. small, medium prey over large prey in his experiments and large, the small sized nymph (5mm) first using small H. rapax and large mostly predated over the third instar Sarcophaga spp. The size of prey in larvae of Cx. quinquefasciatus, 39.1, 52.3 relation to the predator is important factor and 68.4 after 12 hours, 24 hours and 36 influencing the predation rate by nymph. hours respectively ( Table. 1, 2 and 3). The reason of decreasing predation with increase in size of immature stages of Cx. Mandalet.al. (2008),in his experiment quinquefasciatus is due to increase in size related to the predation of dragonfly of prey, which provides more quantity of nymph over Cx. quinquefasciatus, food intake resulting in reduction in reported that the feeding rate varied number of prey to be preyed. However, significantly between dark and light pupae were preferred least over all conditions and concluded that darkness nymphal stages. Lee (1967),found that the had negative influence on the predatory mosquito larvae are consumed more than potency of dragonfly nymph. Odonata pupae by predator due to inclination of nymphs belonging to Tramea spp. pupae to exhibit rapid tumbling action consumed more larvae in darkness than in when startled. normal illumination and it was noticed that darkness did not affect the predatory The present study also suggests that the activity of the nymph (Lee, 1967). rate of predation increases along with the size of dragonfly nymphs and the decrease In the present study also, there was no in feeding rate with increase in larval marked differences in predation by stages of mosquito (Fig. 1, 2, and 3; Table. different size of dragonfly nymph in 12, 1, 2 and 3). 24 and 36 hours, however both the medium and large sized nymphs seems to In a study of predation by dragonfly be predating more over the first and nymph, Orthemis spp. over the mosquito second instar larvae of Cx. larvae, it was revealed that the large quinquefasciatus. nymphs ate more mosquito larvae without showing any preference for the immature The other factors that determine the stages of mosquito (Lee, 1967; Cordoba predatory potency of dragonfly nymphs is and Lee, 1995). During a study on the role the predator or prey density. It was of dragonfly nymph Brachytronpratense, believed that the prey consumption was as a bio control agent of mosquito larvae, inversely related with the space. The it was noted that the small sized nymphs predation of dragonfly nymph, Enallagma were not interested to prey upon fourth civile over Cx. tarsalis showed that when instar stage of mosquito larvae in the density of prey and predators were laboratory; however on starvation they varied more prey were consumed as prey consumed early instar larvae of mosquito density increased however prey were (Chatterjee et al., 2007). The food habitats consumed at higher predator densities of nymphs change with advancement of (Miura and Takahashi, 1988).

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Table.1 Predatory potency of Bradinopyga geminata nymphs over the mosquito larvae and pupae of Culex quinquefasciatus Say. in 12 hours

Nymphal Larval instars and Pupal stage Size I II III IV P SD SD SD SD SD Small 24.1±3.8 30±5.2 39.1±4.1 11.7±2.2 5.3±2.1 (5mm) Medium 51.6±4.7 41.2±4.9 32.7±3.7 21.3±4.0 20.1±1.8 (10mm) Large 49.3±2.8 47.1±3.9 44.8±5.3 41.5±3.4 22.3±2.7 (15mm)

Table.2 Predatory potency of Bradinopyga geminata nymphs over the mosquito larvae and pupae of Culex quinquefasciatus Say. in 24 hours

Nymphal Larval instars and Pupal stage Size I II III IV P SD SD SD SD SD Small 33±4.35 48.6±3.0 52.3±6.11 16±3.6 8±1 (5mm) Medium 72±2.64 52±2.6 41±3.6 29±6.55 27±3 (10mm) Large 79.6±6.65 65.6±3.78 68±3 57±5 31.3±2.5 (15mm)

Table.3 Predatory potency of Bradinopyga geminata nymphs over the mosquito larvae and pupae of Culex quinquefasciatus Say. in 36 hours

Nymphal Larval instars and Pupal stage Size I II III IV P SD SD SD SD SD Small 51.9±3.9 60.7±4.6 68.41±5.1 29.8±5.8 19.6±3.5 (5mm) Medium 93.8±3.2 86.4±5.0 77.4±4.8 69.5±6.3 33.1±4.9 (10mm) Large 92.21±3.8 90.3±3.7 91.7±3.8 73.0±6.1 39.8±4.7 (15mm)

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Figure.1 Predatory potency of Bradinopyga geminata nymphs over the mosquito larvae and pupae of Culex quinquefasciatus Say. in 12 hours

Figure.2 Predatory potency of Bradinopyga geminata nymphs over the mosquito larvae and pupae of Culex quinquefasciatus Say. in 24 hours

Figure.3 Predatory potency of Bradinopyga geminata nymphs over the mosquito larvae and pupae of Culex quinquefasciatus Say. in 36 hours

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Nymphs of five Odonate species Aeshna compatible a manner as possible (Axtell, flavifrons, Coenagrion kashmirum, 1979). Sometimes cultural or physical Ischnura forcipata, Rhinocypha control methods have been included. signipennis and Sympetrum durum in Predaceous insects are closely associated semi-field conditions in West Bengal, with mosquito immature as they co-inhabit India, significantly lowered the mosquito in a wide variety of aquatic habitats such larval density in dipper samples after 15 as rice fields, tree holes, man-made ponds, days from the introduction, followed by a snowmelt pools, temporary lagoons, significant increase of larval mosquito floodwaters and rain pools. These density after 15 days from the withdrawal predators significantly affect the survival, of the larvae (Mandal et al., 2008). These development and recruitment levels of results are suggestive of the use of mosquitoes which most likely has an Odonata larvae as potential biological influence on vector-borne disease agent in regulating the larval population of transmission rates. Biological and physical mosquito vectors. Mosquito ecologists conditions were found to influence have increasingly taken the approach that capacity of such predators. Biological understanding how a predator, directly and conditions divided into predator and prey indirectly, affects community structure is factors. Species, competence and predator also important for understanding under prey density were the most common what set of environmental conditions a predator factors while species, stage and predator will be effective in reducing prey density were more likely prey factors. mosquito populations. Stavet al. (1999) Illumination, temperature, container size reported that the predaceous dragonfly and foraging area were the physical larvae of Anaximperator produced 52% conditions that have been searched. Also reduction in Culiset alongiareolata field studies and implementation of oviposition in outdoor artificial pools. The predaceous aquatic insects in integrated reduced number of Cs. longiareolata egg vector control were documented in some rafts found in the presence of A. circumstances. Dragonfly nymphs capture imperatorwas largely due to oviposition mosquito larvae by the modified labium, habitat selection by Cs. longiareolata which is drawn out into a prehensile organ females. Stavet al. (2000) found that the called the mask. While catching the prey, egg rafts of the mosquito Cs. longiareolata the mask is thrown forward and extended deposited in the free Anax treatment were with incredible swiftness and the prey less than deposited in caged Anaxand transfixed with the hook is drawn into the control treatments. There was statistically mouth cavity. significant difference in the number of egg rafts between control and caged Anaxpools As can be expected, further studies are which means that, while Culiseta females needed to ensure successful and oviposit less egg rafts in the presence of satisfactory mosquito control with Anax, they did not respond to predation predaceous insects. Another important risk from the caged Anax. advantage of predators is their released kairomones that have the potency to repel The concept of integrated control is a ovipositing female mosquitoes for over a fairly specific one, which historically has week. If these kairomones were meant the use of a combination of commercially produced, they may provide chemical and biological agents in as eco-friendly and effective mosquito

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Int.J.Curr.Microbiol.App.Sci (2013) 2(4): 172-182 control, but more research is necessary to G. 2007. Eco-friendly control of determine their total impact. Thus, mosquito larvae by understanding the interaction between Brachytronpratenselarvae.Journ.of mosquito vectors and their aquatic Env. Health .69:44-49. predaceous insects is imperative for Corbet, P.S.,1980. Biology of Odonata. developing and implementing successful Ann. Rev. Entomol. 25: 189-217. biological or integrated control measures Cordoba, A.A. and Lee, M. 1995. Prey that include the use of predators to control size selection by the vector population. Orthemisferruginea(Fabricius) larvae (Odonata: ) Acknowledgements over mosquito instar. Folia.Ent. Mexi.91: 23-30. The authors are grateful to the University Das, M.K. and Prasad, R.N. Grant Commission, New Delhi for 1991.Evaluation of mosquito fish providing the financial assistance through Gambusiaaffinis in the control of the Project F. No. 34-481/2008 (SR). mosquito breeding in rice fields. Indian J. Med. Res.72: 214-7. References Das, P.K., Sivagnaname, N. and Amalraj,D.D. 2006.Populations Alahmed, A.M., Alamr, S.A., and Kheir, interactions between Culex S.M. 2009.Seasonal activity and vishnuimosquitoes and their natural predatory efficacy of the water bug enemies in Pondicherry, India. Siagrahog garica Poisson Jour. of Vect.Eco.31(1):84-88. (Hemiptera: Corixidae) against the Evans, D.B., Gelband, H. andVlassoff, C. mosquito larvae Culex 1993. Social and economic factors quinquefasciatus (Diptera: and the control of Lymphatic Culicidae) in Riyadh city, Saudi filariasis: A review. Act. Trop. Arabia. Jour. of Entomol.6(2): 90- 53:1–26. 95. Fraser, F.C.1934. The Fauna of British- Axtell, R.C.,1979. Principles of integrated India including Ceylon and Burma, pest management (IPM) in relation Odonata. Vol. II. Taylor and to mosquito control. Mosq. News Francis Ltd. London. 39(4): 709-718. Garcia, A.I., Vivar, G.R., Quezada, M.J. Barraud, P.J.,1934The fauna of British and Huaman, M.P.1996. Aquatic India: Diptera. Vol. V, Taylor and insects that are bioregulators of Francis London. mosquito larvae present in Becker, N., Zgomba, M., Petric, D., Dahl, Pantanos de Villa, Lima, Peru. C., Boase, C. and Lane, J. Rev. Cub. de Med. Trop. 48: 227- 2003.Mosquitoes and their 228. control.Kluwer Academics/ Jang, Y.S., Kim, M.K., Ahn, Y.S. and Lee, Plenum Publishers, New York.356. H.S. 2002.Larvicidal activity of Bharadwaj, M., 1981. Serological study of Brazilian plant against Aedes Japanese encephalitis in Deoria aegypti and Culex pipiens.Agri. district of Uttar Pradesh. J. Chem. Biot. 4:131-134. Commun. Dis. 13:96-101. Lee, F.C., 1967. Laboratory observations Chatterjee, S.N., Ghosh, A. and Chandra, on certain mosquito larval

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