210 JounNar, oF THE An,IpnrcaN Moseurro CoNrRor, AssocrarroN VoL. 7, No. 2

BOTANICAL DERIVATIVES IN MOSQUITO CONTROL: A REVIEW1KUMUDA SUKUMAR,, MICHAEL J. PERICH aNo LEWIS R. BooBAR

U.S. Arrny Biomedical Research and Deuelopment Laboratory, Fort Detrich, Frederich, MD 21702-5010

ABSTRACT' A review on the reported uses of chemicals derived from botanical sources is presented.along with the part of the plant used for extraction, the mosquito species studied and the bioactivityobserved for 344. plant species. Examples of phytochemicals evaluatid against mosquitoes as generaltoxicants, growth and reproduction inhibitors, repellents and ovipositional deterrenls are given. Theeffects of mosquito species and life stage specificity, solvents used for extraction, phototoxic aitivity andthe geographical source from where the plant compounds are derived are discussed.

INTRODUCTION

Phytochemicals derived from various botani-cal sources have provided numerous beneficialuses ranging from pharmaceuticals to insecti-cides. Synthetic organic insecticides, althoughhighly efficacious against target species such asmosquitoes, can be detrimental to a variety ofanimal life including man (Matsumura 1975). Inaddition to adverse environmental effects fromconventional insecticides, most major mosquitodisease vector and pest species have becomephysiologically resistant to many of these com-pounds (Brown 1986). These factors have cre-ated the need for environmentally safe, degrad-able and target-specific insecticides againstmosquitoes. The search for such compounds hasbeen directed extensively to the plant kingdom.

Historically, the commercial development ofbotanical insecticides is credited to a lady ofRagusa, Dalmatia, who noticed dead insects ona discarded bouquet of pyrethrin flowers. Shebegan milling pyrethrum into powder and thusthe pyrethrin industry was born (Hartzell andWilcoxon 1941). Since then, pyrethrins fromchrysanthemum flowers and many synthetic de-rivatives stand prominent as effective pesticides.

One of the earliest reports of the use of plantextracts against mosquito larvae is credited toCampbell et al. (1933) who found that plantalkaloids like nicotine, anabasine, methyl ana-basine and Iupinine extracted from the Russianweed, Anabasis aphylla, killed larvae of Culexpipiens Linn., C.r. territans Walker, and Cr.quinquefosciaifus Say. Haller (1940) noted thatextracts from Amur cork tree ftuit, Phelloden-dron arnurense, yielded a quick-acting mosquito

t The opinions or assertions contained herein arethe private views of the authors and are not to beconstrued as official or as reflecting the views of theDepartment of the Army or the Department of De-fense.

'Indian Institute of Chemical Technology, Councilof Scientific and Industrial Research (CSIR), Hyder-abad-500 007. India.

larvicide. Wilcoxon et al. (1940) reported thatextracts derived from the male fern, Aspidiumfilix-mas, yielded a toxic constituent, filicin, aphloroglucinol propyl ketone, which provedtoxic to Cx. quinquefasciatus.Hartzell and Wil-coxon (1941) evaluated extracts from 150 speciesof plants for their toxicity to mosquitoes andfound several to be very effective. In an exhaus-tive review on insecticides derived from plants,covering a period from 1941 to 1953, Jacobson(1958) reported on several phytochemicalsagainst mosquitoes.

Phytochemicals can be extracted from eitherwhole plants or specific parts of the plant, de-pending on the activity of the derivatives. Someplants accumulate bioactive chemicals differen-tially in the various parts of the plant, such asleaves, fruits, flowers, roots and bark. Investi-gators have found that the effectiveness ofchemicals derived from specific plant parts oftenvaries with the mosquito species. Certain phy-tochemicals have photo-activated toxins thatare reported effective against mosquitoes. Somephytochemicals act as general toxicants to alllife stages of mosquitoes, whereas others inter-fere with growth and reproduction, or act on theolfactory receptors, eliciting responses of attrac-tancy or repellency. In this review, the plantsused for mosquito control, irrespective of theirstatus as higher or lower plants, are arranged byfamilies in alphabetical order. The part of theplant used for extraction, the mosquito speciesstudied and the bioactivity observed have alsobeen listed (Appendix 1).

TOXICITY EFFECTS

Many plant chemicals produce larvicidal, pup-icidal and adulticidal effects, most behaving likegeneral toxicants (Appendix 1). The differentialresponses induced by phytochemicals on variousspecies of mosquitoes were influenced by extrin-sic and intrinsic factors such as the species ofplant, the parts of the plant, the solvents usedfor extractions, the geographical location wherethe plants were grown and the methods em-

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ployed for evaluation. Only a few examples willbe discussed in any detail to illustrate thesefactors.

Extracts from different parts of the same spe-cies of plant can exhibit various degrees of tox-icity to mosquitoes. Marcard et al. (1986) re-ported that among the different plant parts fromAjuga remota and A. reptans, the effectivenessof the derived extracts against Aedes aegypti(Linn.), Ae. togoi (Theobald) and Cr. quinque-fasciatus larvae decreased with roots> Ieaves)shoots> and flowers, respectively. Extracts from325 wild-growing plants of North Dakota andwestern Minnesota were found to have variedeffects on the mortality of Ae. aegypti Iarvae byboth plant species and the plant part of the samespecies (Patterson et al. 1975).

In certain instances, the same phytochemicaltoxin from a single plant species exhibits variousdegrees of toxicity to different mosquito species.Minijas and Sarda (1986) showed that crudeextracts containing saponin from fruit pods ofSwartzia madagascariensis produced highermortality in larvae of Anopheles gambiae Gilesthan in Iarvae of Ae. aegypti and no mortalitywas induced in larvae of Cx. quinquefosciatus.Sujatha et al. (1988) also observed differentialsusceptibilities with petroleum ether extracts ofAcorus calamus, Ageratum conyzoides, Annonasquarnosa, Bambusa arundanasia, Madhuca lnn-gifolia and Citrus medico against larvae of 3species of mosquitoes. Acorus calnmus extract,of the 6 extracts, was most effective against Cr.quinquefasciatus while Bambusa arundanasiawas most toxic against An. stephensi Liston.Citrus medico extracts affected only An. ste-phensi larvae whereas Madhuca longifolia ex-tracts had no effect on this species. Similarly,when extracts of the pond weeds Myriophyllutnand Potamogeton were assayed against larvae ofAn. occidentalrs Dyar and Knab and Cr. pipiens,Cx. pipiens showed more resistance to both ex-tracts (Graham and Schooley 1984). Such a dif-ferential species susceptibility was also noticedby Dhillon et al. (1982) when algal toxins fromRhizoctonium heiroglyphicum a d Chlorella el-lipsoidea were assayed against Ae. aegypti, Cx.quinquefasciatlus and Culiseta inci.dens (Thom-son). Of the 3 species of mosquito larvae tested,Cx. incidens was found to be the most susceptibleand Cr. quinquefasciatusthe least susceptible toRhizocloniurn extracts. The Chlnrella extractsappeared more toxic to Cx. quinqu.efosciatu.s andCx. incidens than to Ae. aegypti. When severalvolatile plant oils were assayed against the lar-vae of An. clauiger (Meigen) and, Ae. cantans(Meigen), the results showed that anophelineswere less sensitive than aedines (Novak 1985).Saxena and Sumithra (1989) found the leaf ex-tract of lpomea carneafistolnso most effective

against An. stephensi when they tested the ex-tract against larvae and pupae ofAn. stephensi,Ae. aegypti and Cr. quinquefasciatus.

At times, certain stages of mosquitoes aremore susceptible to phytochemicals. Osmaniand Sighamony (1980) found that the oil oflemongrass (Cymbopogon citratus), oil of linaloe(Bursera delpechiana) and oil of geranium (Pe-lnrgonium roseum) were poor ovicides and hadno effect on first instar larvae. but did causesignificant growth inhibition and mortality inIater developmental stages of Ae. aegypti. Abr-tanol extract of soapberry pIant, Phytolacca do-decandra, was very toxic to second and thirdinstar larvae of Ae. aegypti, Cx. pipiens fiTolestusForskal (: Cx. pipiens) andAn. quadrimaculatusSay, but eggs and pupae were unaffected andadults died only after ingestion of the concen-trated extract (Spielman and Lemma 1973).Likewise, the ethanolic extracts of Haplophyl-lum tuberculatum did not produce any ovicidaleffect, but killed first instar larvae of Cx. quin-quefasciatus (Mohsen et al. 1989). The latexfrom Calotropis procera showed complete ovici-dal and larvicidal effects on Aedes, AnophelesandCulex but had no effects on adults ofthesegenera.

The extraction of the plant chemicals withspecific solvents exerts a great influence in theresultant bioactivity. It could be possible thatthe active constituent responsible for activity isextracted in greater measures only with certainsolvents. When Macrocystis pyrifera and Arte-nlesid cana were extracted with water and withorganic solvents, the latter extract producedhigher mortality in Cr. quinquefasciatus (Sherifand Hall 1985). This could have been due to thepolarity range of the solvents. Hartzell (1944)tested acetone extracts and water extracts ofcertain plant products against Cx. quinquefascia-fus larvae and found acetone to be a bettersolvent. Extracts of roots of Demis elliptica,when bioassayed against fourth instar larvae ofAe. aegypti, exhibited a response indicating thatamong the liquid extracts, absolute ethyl alcoholwas the most potent, and among the crude resi-dues acetone extract was the most effective(Ameen et al. 1983, 1985). The commercial oilof. Linum usitatissimum had no apparent toxiceffects on Cx. pipiens larvae, but the crude meth-anolic extract showed limitedtoxicity (Banu andNurul-Huda 1983). Dhillon et al. (1982) foundpetroleum ether extracts of Chlorella ellipsoideaand Rhizoctonium heireoglyphicurn eluted withpetroleum ether, benzene or methanol, all in-duced mortality in Ae. aegypti and Cr. quinque-fasciatus, with the methanol fraction being themost active. Bioassay of AIoe puridens rootsextracted with solvents of increasing polarityshowed that the petroleum ether extract pos-

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sessed the maximum insecticidal activity againstAe. aegypti larvae (Confalone et al. 1983). Qur-eshi et al. (1986) assayed alcoholic extracts andpetroleum ether extracts of Eruatamia coronariuagainst fourth instar larvae of Ae. aegypti and,found the alcoholic extracts to be highly toxicwhereas the petroleum ether extract had nolarvicidal activity. But in the case of AcoruscaLan"Lus, when the rhizomes were extracted withdifferent solvents like petroleum ether, ether,chloroform and alcohol, the best results againstCx. quinquefasciatus larvae were obtained withthe petroleum ether extract (Chavan et al. 1979).According to the bioassay results against Ae.aegypti larvae, with different extracts of Litho-spermum aruense, the active principle was con-centrated mainly in the hexane-soluble portion(Madrigal et al. 1979).

Certain plant derivatives showed enhancedaction in the presence of light. As Arnason et al.(1981) observed, light has often been a forgottenor underestimated factor in the study of insects.Until recently, little attention has been paid toits role in plant-insect reactions. The activationofplant secondary substances by light, and theirsubsequent photosensitizing effects on insects,especially mosquito larvae, is an important fac-tor contributing to the enhancement oftoxicity.Polyacetylenes and thiophenes that occur incertain plants of the Asteraceae family show thegreatest potential as photoactive pest controlagents. The common marigold, Tagetes sp.,yielded a highly active polyacetylene alpha-ter-thienyl from its roots, which proved very toxicto Ae. aegypti larvae (Arnason et al. 1981, Kaganet al. 1987). The activity increased with light,indicating a phototoxic action of alpha-ter-thienyl. Berberine, an isoquinoline alkaloidpresent in many different plant families, is alsophotoactivated. Larval, pupal and adult survivalof Ae. atropahus (Coq.) was affected by berber-ine treatment with toxicity of the alkaloid in-creasing after exposure to light. Philogene et al.(1984) speculated that the fluorescent nature ofberberine could be the reason for its photody-namic activity. Rose bengal, a xanthene-deriv-ative, also causes enhanced mortality in mos-quito larvae by photosensitized oxidation reac-tions. Its primary mode of action depends on theabsorption ofvisible light energy, causing photo-oxidative toxicity (Pimprikar et al. 1979).

The geographical distribution of plants maypossibly influence their toxicity. Novak (1985)did not observe any toxicity with acetone andalcohol extracts of garlic, Allium satiuum, inAedes larvae when tested in Czechoslovakia, butAmonkar and Reeves (1970) in the USA re-ported that the extracted oil and crude metha-nolic extract of garlic at very low concentrationscould control larval mosquitoes of 5 species.

Likewise, Jacobson (1958) reported that acetoneextracts of Vetiueria zizanoides roots from theUSA failed to induce larval toxicity, but Murthyand Jamil (1987) found the oil of Vetiueria rootsfrom India very effective against Cx. quinquefas-ciatus Iawae. Although it is not clear in theabove cases whether the geographic origin of theplant material or the difference in solvents usedfor extraction ofthe material is contributing tothe differential toxicity, it suggests that furtherinvestigation is needed.

GROWTH AND REPRODUCTIVEINHIBITION

By and large, plant chemicals act as generaltoxicants. A few, however, show selective inter-ference with growth and reproduction. Preco-cene from Ageratum was noted for its uniqueaction of interfering with growth by transgress-ing certain stages of development. In mosqui-toes, it prevented pupal formation and adultemergence when newly hatched young larvaewere exposed (Cupp et al. 1977). When femaleswere treated with precocene after blood feeding,it inhibited trypsin synthesis, retarding ovarianmaturation, resulting in abnormal oviposition(Kelly and Fuchs 1978). Some other plant chem-icals, such as aristolochic acid from Aristolochiabracteata, inhibited reproduction, inducing ste-rility in mosquitoes (Saxena et al. 1979). Biotinfrom plants, aflatoxin from Aspergillus flauusand pactamycin and porfiromycin from lowerplants have also sterilized mosquitoes (Borkovec1987).

Although numerous plants have shown tend-encies to interfere with growth and reproduc-tion, neem (Azadirachta indica) occupies an im-portant place because of its strong action ininducing toxicity through inhibition of growthand reproduction. Although the exact mode ofaction of azadirachtin and other componentspresent in neem seed kernels is not clearlyunderstood, it seems likely that there is an in-terference in hormonal balance. Zebitz (1984)suggests that azadirachtin acts as an anti-ecdy-steroid or affects the neuroendocrine control ofthe ecdysteroids. The unique mode of action ofazadirachtin, by its controlling effect on hor-mones and its favorable toxicological and selec-tive properties from the ecological perspectives,provides a basis for emergence of a promisingphytochemical in mosquito control.

Patterson et al. (1975) found that extractsfrom several plants of North Dakota exhibitmimics of insect ecdysones and juvenile hor-mone activity at various levels based on theparts of the plant used for extraction. As withtoxicity, growth inhibition from phytochemicalscan also be species specific. Sujatha et al. (1988)

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observed that Acorus calamus extracts inducedmalformations to a greater extent in An. ste'phensi and to a lesser extent in Cx. quinquefas-ciatus and Ae. aegypti, while Madhuca longifoliainduced greater growth inhibition in Cx. quin-quefasciatus.

Growth and reproductive inhibition effectsfrom phytochemicals are also affected by thesolvent used in the extraction process. Only themethanol-eluted fraction of petroleum ether ex-tracts from the filamentous algae Rhizocloniumheiroglyphicune exhibited insect growth inhibi-tory activity and various abnormalities in eclos-ingAe. aegypti, Cx. quinquefasciatus and Culisetaincidens adults (Dhillon et al. 1982).

REPELLENCY AND OVIPOSITIONALDETERRENTS

The use of phytochemicals as repellents, ovi-positional deterrents and antifeedants has beenevaluated against both agricultural pests andmedically important insect species (Jacobson1958). Thorsell et al. (1970) reported that ex-tracts from 3 plant species, Ledunt palustre,Lycopersicon lycopersicon and Myrica gal.e, ex-hibited repellency to Ae. aegypti adults. Theessential oils of certain plants often exhibit re-pellent actions to mosquitoes, as shown with theleaf oil of Ocimum suaue (Chogo and Crank1981).

In addition to repellency, phytochemicals caninfluence the ovipositional behavior of mosqui-toes. Consoli et al. (1989) found ethanolic, hex-anic and lyophilized extracts of 8 plants (Alliumsatiuum, Anacardium occidentale, Bidens sege-tum, C aesalpinia peltophoroide s, J atropha cur -cas, Mihania schenkii, Poinciana regia andSpatodea campanulata) deter oviposition byAe. fluuiatilis (Lutz). Acetone extracts of 4 spe-cies of the Labiatae family are reported ovipo-sitional deterrents to Ae. aegypti (Sharma et al.1981b), with one species, Lauendula gibsonii,having also an ovicidal and general repellenteffect on Ae. aegypti (Sharma et al. 1981a).

The factors of species specificity and the sol-vent used for extraction are components thatcan affect ovipositional deterrence from phyto-chemicals. Aqueous extracts of l*mna minorsignificantly deterred oviposition by Ae. aegypti,but had no effect against Cx. pipiens (Judd ancBorden 1980). The methanolic extract of thesame plant also deterred oviposition in Ae. ae-gypti, but the pentane extract showed no ovi-positional deterrent activity. Judd and Borden(1980) theorized from the results of significantovipositional deterrent activity of the aqueousand methanolic extracts that the active princi-ples are of a polar nature. The need for further

investigation of phytochemicals as repellentsand deterrents against mosquitoes has beenstated by Novak (1985) in his review of non-chemical approaches to mosquito control inCzechoslovakia.

CONCLUSION

Chemicals derived from plants offer promisein future mosquito control programs. In additionto application as general toxicants against var-ious life stages of mosquitoes, phl'tochemicalsalso have potential uses as growth and repro-duction inhibitors, repellents and as oviposi-tional deterrents. Many research opportunitiesexist in the identification and characterizationof new plant compounds, as well as in the eval-uation of their ecological, evolutionary andphysiological significances. Research on the useof phytochemicals against mosquitoes shouldconsider such factors as mosquito species, lifestage specificity to a compound, the plant partsand solvent used for extraction, phototoxic ac-tivity and the geographical origin of a plantcompound.

Phytochemicals offer not only effective mos-quito control agents, but also are biorationalalternatives to organic synthetic pesticides. Thefact these chemicals are from natural sources,with a high degree of biodegradation, makesthem environmentally sound control agents.With an ever increasing public interest andawareness in the environment, in both devel-oped and developing countries, positive publicperception of natural pesticides is an added in-centive for their development and use. In addi-tion, the potential use of phytochemicals frombotanical species in the endangered rainforestregions of the world offers economical and prac-tical reasons for their preservations.

The same public perception can also have anegative effect in the utilization of phy'tochem-icals, due to their often slower and nontoxiccontrol effects on mosquitoes compared withconventional insecticides. People have becomeaccustomed to the immediate toxic effects ofsynthetic insecticides. With phytochemicals'slower modes of action, people believe that theyare not effective and discontinue their use. Ed-ucation of the public is critical if phytochemicalscan be effectively utilized in mosquito controlprograms.

Several botanicals offer great promise assources of ph1'tochemicals for the control ofmosquitoes. Six plant families with several rep-resentative species, Asteracae, Cladophoraceae,Labiatae, Meliaceae, Oocystaceae and Rutaceae,appear to have the greatest potential for provid-ing future mosquito control agents. Some of

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these new compounds with their novel modes ofbioactivity may prove useful in the developmentof safer insecticides for the future.

ACKNOWLEDGMENTS

We acknowledge the able assistance of JoanAuch, Gina M. Pishioneri, Mary A. Hathaway,Melba D. Ashby and Brett W. Collier in manu-script preparation. The efforts of Raj K. Gupta,Robert S. Edgecomb, Bobbie L. Bunner andGunda Reddy in reviewing the manuscript arealso greatly appreciated.

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