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Journal of the American Control Association, 10(4):574_5g4,lg94 copyright @ 1994 by the American Mosquito control Association. Inc.

MOSQUITO CONTROL THEN, NOW, AND IN THE FUTUREI

MIR S. MULLA

Department of Entomology, Universityof California, Riverside,CA g2S2l

ABSTRACT. This is a memorial lecture honoring the late Professor Stanley B. Freeborn of the University of California. In the spirit of his life-long academicand researchintereits in mosquitoesand mosquito-bome ,I am presentinghere the evolution ofvector control technology,especially that pertaining to mosquitoesand mosquito-bome diseasesduring the 20th century. controi technology in the first half ofthis century was relatively simple, utilizing sourcereduction, larvivorous fish, petroleum hydrocarbon oils, and some simple synthetic and botanical materials. During the 2nd half of this century, however, various classesof synthetic organic chemicals, improved petroleum oil formulations, insect growth regulators,synthetic pyrethroids, and microbial control agentswere developedand employed in mosquito control and control ofother -vectoringinsects. Among thesegroups ofcontrol agents, petroleum oil formulations have endured to be usedthrough the whole century. It is likely that petroleum oil formulations, insect growth regulators, and microbial control agents will provide the main thrust againstvectors at least during the first quarter ofthe 2lst century. It is also possiblethat effectivetools through the development of vaccinesand molecular entomology techniquesmight become available for the control ofvectors and vector-borne diseasesduring this period ofthe 2lst century.

INTRODUCTION or most of his professionalaccomplishments but instead will focus It is indeed my distinct pleasureto deliver this attention on his contributions to our knowledgeof mosquitoes memorial lecture, honoring the late Professor and their control and his role as teacher researcher. StanleyB. Freeborn,one ofthe distinguisheden- and tomologists and culicidologistswho contributed immensely to our knowledgeof mosquitoes and their control. He not only was a recognizedschol- STANLEY B. FREEBORN ar but also proved to be an effective and dedi- (THE HONOREE) cated teacher, instructing undergraduate and StanleyBarron Freeborn was born in Hudson, graduate students with great enthusiasm. To- Massachusettson DecemberI l, l89l and died ward the end ofhis career,Dr. Freeborn served on July 17, 1960 at Davis, California. He re- with distinction as Provost and then Chancellor ceived the B.Sc. degreefrom MassachusettsAg- of California at Davis. at the University ricultural Collegein l9 I 4 and the Ph.D. in 1924 During my career,I had very little overlap with from Amherst College.The subject of his thesis Upon my arrival as a graduatestudent Freeborn. was the classicalwork, "Mosquitoes of Califor- the of California, Berkeleyin 1952, at University nia." All of his career, with the exception of 2 he had already moved to the Davis campus wartime leaves, was spent at the University of (known as the Farm or Cal Aggiesin those days), California (UC). He started as an instructor in and from there he enteredthe administrative ser- entomology at the University of California, vices. Therefore, whatever biographical infor- Berkeleyin 1914, becamean assistantto Pro- mation I presenthere was gatheredfrom the lit- fessorWilliam B. Herms in 1916,and attained gainedfrom thosewho had professional eratureor the rank of Professorand Entomologistin 1932. and personalcontacts with him (e.g.,Thomas H. Aitken (1939) named Anophelesmaculipennis Aitken, Bruce F. Eldridge, William C. Reeves, G. collected at Davis, California in his and Robert K. Washino). I will attempt to give freeborni honor. This important vector is now a briefbiographical sketch ofhis career,accom- known as An. rl Aitken on the west coast. plishments,and contributions.Because time does freebon From 1924 to 1935,he servedas Chairman of not permit me to presenta complete recognition the Division of Entomology at Davis and then contributions he made in the of all significant becameAssistant to the Dean of the College of research,teaching and service. area ofscientific Agriculture at Berkeley,and 2 years later he be- touch upon his personallife I will not attempt to came Assistant Dean and Assistant Director of the Agricultural Experiment Station. In 1952,he was appointed as the first Provost of the UC Davis Campus,and in 1958 he becameChan- t Memorial l-ecture was presented at the The AMCA scientist, American and California Mosquito and cellor there. To honor this eminent Associations Joint Meeting (AMCA 60th, CMVCA teacher, and administrator, the University of 62nd) held April 9-14, 1994, San Diego, California, California bestowed the honorary degree of USA. L.L.D. upon him and named the Student Center 5't4

JounNlr or rHr Arr.tsRIcANMosqurro Coxrnor AssocrerroN Vol. 10,No.4

Table l. Mosquito speciesincluded in the will not be too different from programs else- publications of L. O. Howard (1902), Freeborn where. It should be remembered that a consid- (1926),and Freebornand Brookman (1943). erableamount ofvector control researchwas also carried out by other universities, the Centersfor DiseaseControl, U.S. Department ofAgriculture mosquitoes recorded laboratories, and others. Freeborn and VECTOR CONTROL DURING THE Brookman EARLY 2OTH CENTURY How- Freeborn (1e43) ard (1926) Pacific Vector control researchand mosquito control (1902) Cali- coast activities in particular beganabout a century ago. Genus USA fornia states In the first quarter of the 20th century, mosquito control activities were basedprimarily on source I l5 23 reduction, the use of petroleum oils (kerosene), J 4 4 and the promotion of guppies and other fish Conchyliastes 2 (Howard 1892, l9O2). These tactics (Table 2), Culex 9 with some modification, continued for 3 or 4 Culiseta I 7 5 decades.Freeborn and Atsatt (1918) provided Mansonia I evidence for mode of action of larviciding oil Megarhinus 3 mixtures. Freeborn also was involved in 1922 in Orthopodomia I the promotion of biological control agents and Psorophora I was overseeingthe first importation and stocking _' Stegomyia 2 of Gambusia in the Chico area of California Theobaldia 4 (Herms 1949).He was the first person involved Toxorhynchites I in the importation, stocking, and evaluation of _ Uranotaenia I I larvivorous fish in mosquito control in Califor- Total 26 32 44 nia.

VECTOR CONTROL DURING THE Association served as its Mosquito Control and 2ND OF THE president 1935.According Nowell's (1983) QUARTER in to 2OTH CENTURY index to the first 50 annual conferencesof the California Mosquito and Vector Control Asso- Vector control technologyemphasizing source ciation (1930-82),there are 23 entriesfor Free- reduction and application of oils and botanical born during this period. Titles of his presenta- preparation (Table 2) continued into the 2nd tions represented diverse areas of research, quarter of the presentcentury. However, a num- administration, program development, and op- ber of other strategiesaimed at larval and adult erational programs for mosquitoes and mosqui- control were added to the arsenalagainst disease to-borne diseases.Some of the topics covered vectors and pests (Table 3). A comprehensive included mosquito control in California and treatment of this technology was reported by abroad, outbreaksof malaria in California, iden- Herms and Gray (1944)in a book that provided tification of mosquitoes, mosquito migrations, a detailed description and analysisofvector con- and other problems pertaining to mosquitoes and trol technologybased on laws leading to the for- mosquito control programs. mation of mosquito abatementagencies. Source From his biographical sketchand scientific ac- reduction and naturalistic and biological control complishments,it is clear that Stanley Freeborn methodologies were promoted as the primary line had keen interest in mosquitoes and that his re- of defense.Oiling and the use of chemical lar- search activity covered both basic and applied vicides and adulticides were considered as an fields. The major thrust of his researchactivities adjunct to the more peffnanent and lasting strat- was directed toward vector control and vector- egiesemployed. Herms and Gray (1944) alluded borne diseases.In the spirit of his interest in to the problem of pest mosquitoes after inter- vector control programs, I now briefly present ruption of disease transmission and recom- the progressionand evolution of vector control mended reduction or elimination of pestiferous technologiesfrom the past into the present and speciesfor the overall comfort and well-being of also project the trends into the near future. Be- the public. The need for the abatement of pes- causeof Freeborn'sinvolvement and association tiferous vectors (speciesserving as diseasevec- with California, I will touch primarily upon vec- tors, as well as those which are pestiferous) is tor control methodologies in California, which even more important today in developed areas, 577 DEcBrvrnEr1994 Mel'roRrAL Lecrunr

I Table 3. Mosquito control technology I .E employed during the 2nd quarter of the 20th -lI century and beYond.t AI oo9 r-l I Types of major mosquito control tactics o O\l C) ()(ll^ manage- lii d q) l. Source reduction, environmental kl ;.E=.E ment fitl tl Drainage and reclamation of freshwaterand EeEgg saltwater marshes >'

o Ethyl hexanediol Adult control J1 .{ Pyrethrin sprays ao o q) o 6 Diversion to farm animals ;: oo Synthetic adulticides 00 o )lY o: I From Hems and Gray (1944). o o v atr 6oci = otr:R )X o o where most vector-borne diseases have been eliminated or abated to an insignificant level. z Es F;S E various is EHE*in P Among the larvicides, reference made o o to kerosene,diesel and stove oils, cresylic acid 9 a 2E3 3,i; q) (high boiling fractions), pyrethrum extracts(aer- o0 osols) and emulsions, Paris green (copper ace-

o toarsinite), DDT (first used in the early 1940s),

v F q phenothiazineor thiodiphenylamine (at the dos- age of 24 E/sO gal. drum), and finally borax () 4 (sodium borate) at the high rate of 1.5 g/liter of water.Among theselarricides, DDT wasthe most :o effective material ever tested up to that time, o 39 o () >i= yielding l00o/okill of mosquito larvae at the con- :ib centrationsof l0-15 parts per billion. evE o ()_ ! o ..i P:H O *rixE VECTOR CONTROL IN THE o h,,'E c 3RD QUARTER OF THE 9 oPiE H F E69HF.; 2OTH CENTURY HHEgeE With the advent of DDT toward the end of E5€9-E the 2nd quarter ofthis century, an unprecedented 578 JounNer or rnp Avrnrcn.l Mosqurro Covrnor AssocrarroN Vor. 10,No.4

Table 4. Relative activity and efficacyof some commonly used synthetic insecticidesagainst mosquito larvae. I"aboratory activity Field efficacy Material LC"o @g/liter) (lb Allacre) DDT 3-10 0.5-1.0 20-50 o.gl.0 Parathion (ethyl, methyl) 24 0.0254.1 Fenthion 3-5 0.054.1 Chlorpyrifos l-3 0.024.05 Temephos 2-5 0.054.10 Diflubenzuron t4 0.0054.05 Pyriproxyfen l-3 0.005-o.025 Methoprenet s-20 0.05-o.25 Petroleum oils 20-50 2.O-5.Ogal ' Ten to 20 times more active against Aedes and Psorophora speciesthan ag inst Culex ^ad Arnpheles sFF,c,,es. flurry ensuedfor finding, synthesizing,and test- .The synthetic pyrethroids are em- ing of novel modes of synthetic compounds dur- ployed primarily for the control of adult mos- ing the early part of the 3rd quarter of this cen- quitoes or as materials of choice for impregna- tury. Thousands of new or modified structures tion of protective clothing and bed nets. were made available for testing againsta variety Compounds used in adult control are allethrins, of injurious pests.The development of lst-gen- tetramethrin, resmethrin, cypermethrin, per- eration, 2nd-generation,and 3rd-generation in- methrin, deltamethrin, lambdacyhalothrin, and secticideswas realizedin the 1950sand 1960s. others. Among the lst-generation insecticides,organo- The decadesofthe 1960sand 1970salso ex- chlorine compounds,well-known and extensive- periencedincreased research on genetic control ly used insecticidessuch as DDT, aldrin, dield- of vectors.Numerous areasofgenetic techniques rin, , and methoxychlor were employed such as translocations, cltoplasmic incompati- in a variety of vector control programs all over bility, meiotic drive, and sterile hybrids were in- the globe. The development of DDT for insect vestigated(Whitten and Foster 1975), but none control provided a potent meansofmalaria erad- of these tactics becameusable. Similarly, much ication or control around the world, and this researchwas conducted on chemosterilants,but material is still used in some countries for this none of thesecompounds becameoperational in and other purposes.The use of DDT and other vector control programs. It is equally important synthetic chemicals has reducedthe risk of ma- to note the voluminous researchon the evalua- Iaria for some one billion people who dwelled in tion and development ofbiological agentssuch endemic areas. Among the 2nd-generation in- as protozoa, fungi, ,and other para- secticides() are materials such sitesand pathogens.Thus far none ofthese agents as dichlorvos, malathion, naled, methyl para- has yielded tangible results as a tool in vector thion, parathion, temephos, chlorpyrifos, fen- control programs. thion, fenitrothion, and others (Table 4). The organophosphateswere followed by organocar- ENVIRONMENTAL CONCERNS AND bamates.which were not used for larval control. DECLINE IN USE OF INSECTICIDES Well known in this group were , car- baryl, bendiocarb, isolan, and others. These In the 1960s,environmental concernswith the compoundswere used primarily for adult control widespreaduse of persistentchemicals and their as aerosolsor residual treatments. bioaccumulationin the biospheresurfaced among In the I 960sand I 970s,chemists began to alter scientistsand the lay public. The publication of and build on the structural features of natural Silent Spring by Rachel Carson in 1962 gave pyrethrins. A whole host of photostable or un- impetus to increasedpublic concernsregarding stable moieties were obtained. This group of in- the use of . These events further ac- pyre- celeratedthe already establishedtrend to reduce secticideswas designatedas the synthetic "hard throids. Thesecompounds have a very high level the use and further development of core" of activity against mosquito larvae, but because pesticides and triggered an eventual decline in of their high toxicity to fish and some other non- the use pattern of many pesticidescharacterized target organisms,none of these compounds has by high mammalian toxicity and posing risks to been developedfor larval control, at least in the nontarget biota and the environment. Com- 579 DncE}vrsER1994 MsuoRrAL LscruRE

PETROLEUMOILS (gals) {

ao o 5 I > 300 F- b z -f: f TOTAL INSECTICIDES a \ ORGANOPHOSPHATES (lbs.) (lbs.) "/

ORGANOCHLORINES t. { (lbs.)

T-

1954 1958 1960 '1962 1965 1968 1970 1975 1978 1981 1984 1985 YEAR Fig.2. Quantities of mosquito larvicides including petroleum hydrocarbon oils used in California mosquito control programs from 1954 to 1985 (from California Mosquito and Vector Control Assoc. Inc., Yearbooks, I 954-85).

pounds perceivedas posing potential risks to the mained constant (350,000400,000 gallons/year) environment and human health came under in- whereasthe useofinsect growth regulators(IGRs) tensive scrutiny and evaluation. As a matter of starting in I 986 beganto increase.It is likely that fact, the decline in the use oforganochlorine in- the quantities of IGRs in the next quarter (lst secticidesin mosquito control in California (Fig. quarter of the 2lst century) will increaseabove 2) had already started before the appearance of the presentlevels. Silent Spring. The amounts of petroleum oils Another important changein the use of mos- usedremained relatively constant between 1954 quito control agentsoccurred in the use of ad- and 1985, while the amounts of organophos- ulticides in 1990. When the use of propoxur was phates, increasing in the 1950s, declined dras- canceledin 1990 (Fig. a), there was an increase tically in the 1980s.The environmental concerns in the usageof malathion, pyrethrins, and syn- further culminated in a rapid decline in the num- thetic pyrethroids. As naled is being withdrawn ber and quantities ofsynthetic organic pesticides from further use, the options for adult control used in the United States,and in California in are becoming very few. In the not too distant particular. The 3rd quarter of this century saw future we will rely on only 2 or 3 chemicalcontrol the emergenceand decline ofsynthetic pest con- agentsfor adult mosquitoes. trol agentson an unprecedentedscale. The quan- The quantitiesofvector control chemicalsused tities oforganophosphatesused in California de- in California are only estimates,because not all clined further, reaching the lowest level in 1990 agenciespracticing vector control submit reports (Fig. 3). Quantities of petroleum oil used re- to the California Mosquito and Vector Control 580 Jounwer or rue Arr,rrnrcet Mosqurro Corgrnor Assocr.crroN Vor. 10,No.4

'e

\ O.P.(lbs. a.i. x 1000fr zF Ers

t6t' IGR(lbs. a.i. x 1000) I

1981 1982 1984 1986 't987 1989 1990 1992 YEAR Fig. 3. Quantities of mosquito larvicides including petroleum hydrocarbon oils used in California mosquito control programs from 1981 to 1992 (from California Mosquito and Vector Control Assoc. Inc., Yearbooks, 1981-92). O.P. : organophosphates,IGR : insect growth regulators.

Association Survey. Therefore, the actual quan- opment in the field of vector control was the tities of materials used are gtreaterfor each cat- isolation and development of spore-forming and egory than reported in the Yearbooks. toxin-producing for vector control. The entomopathogenic bacterium Bacillus thurin- glenslssubsp . israelensis(8. r.i. was registeredin VECTOR CONTROL IN THE ) 1980 for mosquito and blackfly control, and an- 4TH OF THE QUARTER other bacterial agent, B. sphaericus,was regis- 2OTH CENTURY tered in 1992.This latter microbial control agent With the environmental movement in full has been used in operational control programs swingin the 1960sand 1970s,scientists turned abroad but has not yet been made available in their attention to the development of selective the United States.Soon after registrationof B.t.i., biorational pesticidesand integrated pest man- various preparations of this microbial control agement tactics during the 3rd quarter of this agent found their way into vector control pro- century, which became operational in the 4th grams.From 1982onward, the quantitiesof this quarter. As a result of these efforts, the IGRs agent employed in vector control increased, , fenoxycarb, and diflubenzuron were reachinga peak in 1990-91 (Fig. 5). Although developed and registeredduring this period for not all vector control agenciesreported, the data different uses.Additional compounds manifest- are indicative ofthe trend purporting the use of ing developmental regulating properties also were B.t.i. developedand have beenused in other countries. The foregoingis a brief historical treatment of Some of thesecompounds such as pyriproxyfen the development and use ofvector control strat- are being developed now for mosquito control egiesduring the 20th century. As we approach in the United States.Another important devel- the end of this century, few viable options for 581 DEctr"rssn1994 MEMoRIAL Lpcnrnn

another, the biorational pesticidesmethoprene, diflubenzuron, and others (from synthetic en- deavor or plant origins),as well as microbial con- trol agents will continue to be utilized at least during the first quarter of the 2lst century. New and effective environmentally friendly agentswill be developed,but the paceofsuch development the world ex- c, will be unnecessarilyslow unless x periencesepidemics and pandemics of vector- + borne diseases.Even in the absenceof vector- o borne diseaseoutbreaks, we still needto develop I, new control agentsat a more rapid pacethan we F are doing currently. Most hematophagousand z t pestiferousarthropods, asidefrom vectoring dis' o = easeagents, also impair the health and well-being of millions of people. The intensity of this con- stant annoyanceis so great that the populace at large will unequivocally demand control of nox- ious insects in both developed and developing countries regardlessof their involvement in the transmission of pathogenicorganisms. Researchon microbial control agents might 19811982 1984 1986 1987 1989 1990 1992 possibly develop new strains possessinghigh po- YEAR tency and broad-spectrum activity or improve products. Fig.4. Quantitiesof chemicalcompounds used as and broaden the activity of existing adulticidesin Californiamosquito control programs Also, the role of genetic engineeringin cloning from 1981to 1992(from CaliforniaMosquito and toxin-producing genesin other organisms such VectorControl Assoc. Inc., Yearbooks, 1981-92). as Cyanobacteriacould yield a systemthat could be used in mosquito control programs (Berry et al. 199l, Bulla et al. 199l). However,many eco- mosquito and vector control are at our disposal. logical studies on the survival, distribution, and We are still relying heavily on petroleum oil for- persistenceof transgenic organisms are needed mulations, which have been greatly improved before these transformed organisms can be in- over those used in the first half of this century. troduced into the environment. In recent years, Only a few ofthe old synthetic compounds,such concernshave beenexpressed regarding the pos- as resmethrin, malathion, and a few others, are sibility ofdevelopment ofresistanceto the toxins still available for mosquito control. Among the expressedin plants or bacteria that are present new generationofinsect control agents,metho- constantlyin the environment (Stoneet al. l99l). prene and diflubenzuron are used in localized From all indications, repeated applications of situations. The microbial agentsare extensively microbial toxins produced by the parent organ- used now. These agents and other biorational isms might be the most practical and acceptable pesticideswill continue to be used to the end of mode of vector control operations. this century and into the 2lst century. Source Research on vaccines and molecular ento- reduction and elimination of mosquito breeding mology has been given high priority in recent sites in wetland marshes and wildlife habitats years. Progresshas been made in the area of will no longer be an acceptableoption in many vaccinedevelopment, at leastfor targetingsingle areas.Environmental managementtactics have malaria pathogens,and an effective vaccine might to be acceptableand compatible with the diver- be in the realm of possibility during the early sity and abundanceof animal and plant taxa in part of the 2lst century. Ilowever, it should be aquatic habitats. recognizedthat vaccines,at least at the outset, may be aimed at only a singledisease or pathogen or a given strain. Although current advancesin VECTOR CONTROL IN THE vaccine research seem promising, we will still EARLY 21ST CENTURY need many traditional tools to fight and control Having more or lessspanned a whole century, vector-borne diseasesand human pests not tar- I would now like to look into the crystal ball and getedby the development ofsuccessfulvaccines. project future trends in the development ofvec- Notwithstanding these problems, it is quite de- tor control technology. Present indications are sirable to promote vaccinedevelopment and use that petroleum oil formulations of one kind or as a part ofan overall vector control technology. 582 JounNer or rup ArrarruceN Mosquno Cowrnor Assocllrrorl 10,No. 4

U' F z 8c> oi 80 -2F:o >l.L FO =a 60 =o4Z oj 6

1982 1983 1984 1985 1986 1987 1988 1989 1990 1992

Fig. 5. Quantities of subsp. israelensrsused in vector control (mosquito control) programsin California from l982to 1992(from California Mosquito and Vector Control Assoc.Inc., Yearbooks, 1982-92\.

Very recently, attention has been turned to- Aldhous 1993). With genomic knowledge of ward research on molecular entomology. It is mosquitoes and the genetic technology to alter known that a certain proportion ofa given vector mosquitoes and other vectors, it is conceivable population is refractory to infections by parasites that at least some vector-borne diseasesmight and pathogens.The genetic basis for these phe- be controlled through genetic manipulations of notypesand other charactershas been the subject the vectors. However, these approacheswill re- of numerous speculationsand fundamental re- quire detailed field ecologicalstudies to evaluate search.Collins et al. (1986) were successfulin the successof this technology. Likewise, these selectingAnopheles gambiae Giles refractory to approacheswill be speciesspecific and will likely infection by the simian malaria cy- not becomeavailable for practical useduring the nomolgi. They further showed that this refrac- next decadeor so. tory feature,which is geneticallycontrolled, was With theselimitations of biotechnologicalap- also operative againstother malaria parasitesin- proaches,it is still imperative that researchon cluding thoseofhuman malaria. In the refractory developing a diverse cadre of traditional ap- Anopheles,the living ookinetes are fully encap- proachesofvector control is not slighted. Even sulated after passagethrough the midgut wall. ifwe are successfulin controlling a diseasethrough This discovery resulted in a flurry of research alterations of pathogen-vector interactions, we initiatives on geneticmapping of somezl nopheles will still have to control hematophagousand pest mosquitoes, and the future potential of genetic speciesby traditional techniques and methods, engineeringas a tool against mosquito vectors at least over the next quarter of a century or was expressedby severalresearchers (Crampton longer. et al. 1990,Miller andMitchell 1991,James 1992, Among the more practical and less sophisti- 583 DEcerragpn1994 MetvroRrAt,Lecrurs

control Table 5. Examples of single strategyand combination of strategiesin an integrated technologYof mosquito larvae- Single strategies Inundative predators Combination Biocides (e.g., fish alone) biocides * flsh Selective Time lag (weeks) Most efective Provide short-term control Poor control initially Short-term control Provide long-term control Long-term control Weekly or biweekly treatments No reproduction/cold Reduced rates of biocides Not cost effective/large areas No reproduction/short daYlight Cost effective Low potential for recycling Not cost effective/large areas Fewer treatments

catedmethods for the control ofvectors and pest istration ofa new petroleum oil known ,I seea good potential in the development as Rodspray Mosquito Larvicide (RML), which and application ofintegrated vector control strat- was cleared by the Environmental Protection egies.Utilization ofbiological control agentssuch Agency in mid- I 994. This larvicide is a blend of aspredators (invertebrate and vertebrate)in con- petroleum hydrocarbons and essentialfood-fla- junction with safe biorational pesticideswill go voring oils. We first tested this formulation in a long way toward controlling vectors and pests 1992, and field experiments were carried out in (Table 5). This areaoftechnology is an emerging 1993.Because of the simplicity and safetyof the one, and in a few years we should seeits appli- products in the formulation, the registrationpro- cation in some vector control programs. cesswas duly accelerated.There is a ray of light Another areaofresearch that could lead to the in the long tunnel ofthe registration processbe- development of practical solutions is the devel- causeregulatory agenciesmay be looking favor- opment and use of behavior-modifying chemi- ably upon the registration of simpler and safer cals (semiochemicals).Chemical stimuli of host pest control agents.Availability of this new lar- origin facilitating feeding responsesin vectors vicide will provide vector control programswith could be formulated and used in monitoring or additional tools. used directly in vector control programs. An There is indeed a great need for a variety of equally promising area for research on semi- techniquesand methodologiesfor mosquito con- ochemicalsis, for example, the identification of trol. This need is predicatedon the of mosquito oviposition attractants and repellents. diverse groups of mosquitoes breeding and de- We have been able to identify several natural veloping in many types of habitats. No single products (3-methylindole, some phenols, anc tactic will be sufficient to provide a solution in others) that regulate mosquito oviposition be- all situations. Integration of simple traditional havior (Millar et al. 1992').For the first time, confol methods will go a long way toward con- these simple chemicals were tested in the field trolling mosquitoes in a variety of habitats and (Beehleret al. 1994).Oviposition repellentsof situations. some Culexmosquitoeshave beenidentified and In the absenceofan adequatearsenal ofprac- evaluated(Hwang et al. 1980, 1982;Kramer et tical and usable tactics for vector control, it is al. 1980). Some of these repellents(nonamoic imperative that we attack perplexing problems acid and others) were tested under semi-fleld from an ecologicalperspective and integrate the conditions (Schultzet al. 1982).The use of se- few available tools into a practical and cost-ef- miochemicals and host attractants could en- fective vector control technology.In our studies hance our options to control vector and pest on a stagnant water mosquito (Culex tarsalis mosquitoes.These types of chemical agentsmay (Coq.)), we found that natural regulating factors be employed in monitoring adult populations or (such as oviposition cues, predators, etc.) play used in population management. an important role in the natural decline of mos- It should be emphasizedthat techniquesand quito larvae (Mulla 1990).Combining thesenat- methodologiesused in vector control programs ural or biological control agentswith safe bio- should be simple and safe. Sophisticatedmeth- pesticideswill go a long way toward achieving odologieswill not be applicable in all situations satisfactory control of at least some speciesof where financial and technical requisitesare lack- mosquitoesin some habitats. Extending and im- ing. A good example of a simple and readily plementing this integated vector control tech- available technologyis the developmentand reg- nology to other areasor specieswill require im- 584 JounNar or txr Aurnrc.lll Mosqurro CoNrnor AssocrenoN Vor. 10,No.4 plementation of comprehensive applied trol operations.Proc. Pap. Calif. Mosq. Control As- ecological research at the field level. soc.l7:89-93. Herms, W. B. and H. F. Gray. 1944. Mosquito con- trol, practical methods for abatementofdisease vec- ACKNOWLEDGMENTS tors and pests, 2nd ed. Oxford Univ. Press, New York. My students and staffat the University of Cal- Howard, L. O. 1892. An experiment against mos- ifornia, Riverside rendered valuable assistance quitoes.Insect Life 5(1):12-14. preparation in the ofthis paper. Special thanks Howard,L. O. 1902. Mosquitoes.Howtheylive, how are due Harold Axelrod (Staff Research Asso- they carry disease,how they are classified,how they ciate), J. W. Beehler (Postgraduate Research En- may by destroyed.McClure Phillips and Co., New tomologist), and graduate students Jittawadee York. Rodcharoen and Joonhak I-ee for their valuable Hwang,Y.-S., W. L. Kramer and M. S. Mulla. 1980. assistance in preparing this paper. Oviposition attractants and repellents of mosqui- toes. Isolation and identification of oviposition re- pellentsfor Czlex mosquitoes. Chem. Ecol. 6:71- REFERENCES CITED J. 80. Aitken, T. H. G. L939. T}lteAnopheles maculipennis Hwang, Y.-S., G. W. Schultz, H. Axelrod, W. L. Kra- complex ofwestern America. Pan-Pac.Entomol. 15: mer and M. S. Mulla. 1982. Ovipositionalrepel- 191-r92. lency offatty acids and their derivatives egainstCz- Aldhous, P. 1993. Malaria: focus on mosquito genes. lex and Aedes mosqtitoes. Environ. Entomol. ll: Science261:546-548. 223-226. Beehler,J. W., J. G. Millar and M. S. Mulla. 1994. James,A. A. 1992. Mosquito moleculargenetics:the Field evaluation of synthetic compounds mediating hands that feed bite back. Science257:37-38. oviposition in Culex mosquitoes.J. Chem. Ecol. 20: Kramer, W. L., Y.-S. Hwang and M. S. Mulla. 1980. 28t-291. Oviposition repellents of mosquitoes: negative re- Berry, C., J. Hindley and C. Oei. 1991. The Bacillus sponseselicited by lower aliphatic carboxylic acids. sphaericustoxins and their potential for biotech- J. Chem. Ecol. 6:415424. nological development, pp. 3547. fn.' K. Mara- Millar, J. G., J. D. Chaney and M. S. Mulla. 1992. morosch (ed.). Biotechnology for biological control Identification of oviposition attractants for Culex ofpests and vectors. CRC Press,Boca Raton, FL. quinquefasciatwfrom fermented Bermuda grassin- Bulla, L. A., K. C. Raymond and R. M. Faust. 1991. fusions.J. Am. Mosq. Control Assoc.8:11-17. Mosquitocidal toxins of Bdcillus thuringiensrssub- Miller, B. R. and C. J. Mitchell. 1991. Genetic se- speciesisraelensls, pp. 25-34. 1n.'K. Maramorosch lection ofa flavivirus-refractory strain ofthe yellow (ed.). Biotechnology for biological control of pests fever mosquito . Am. J. Trop. Med. and vectors. CRC Press,Boca Raton, FL. Hyg. 45:3994O7. Carson,R. I 962. Silent spring.Houghton Miffiin Co., Mulla, M. S. 1990. Activity, field efficacy,and use of Boston. Baci I lus t huri ngiens i s i sr aeI e ns is againstmosquitoes, Collins, F. H., R. K. Sakai,K. D. Vernick, S. Paskewitz, pp. 134-160.In: H. de Barjacand D. J. Sutherland D. C. Seeley,L. H. Miller, W. E. Collins, C. C. Camp- (eds.).Bacterial control ofmosquitoes and black flies. bell and R. W. Gwadz. 1986. Genetic selectionof Rutgers Univ. Press,New Brunswick, NJ. a plasmodium-refractorystrain of the malaria vector Nowell, W. R. 1983. The Nowell index, contentsand Anophelesgambiae. Science234:6O7 4lO. index for the proceedingsand papersfor the annual Crampton, J., A. Morris, G. Lycett, A. Warren and P. conferencesof the California Mosquito and Vector Eggleton. 1990. Transgenic mosquitoes: a future Control Assoc., Inc. 1930-1982. California Mos- vector control strategy.Parasitol. Today 6:31-36. quito and Vector Control Assoc., Sacramento. Freeborn, S. B. 1926. The mosquitoesof California. Schultz, G. w., Y.-S. Hwang, W. L. Kramer, H. Ax- Univ. of Califomia Agric. Exp. Stn. Tech. Bull. En- elrod and M. S. Mulla. 1982. Field evaluation of tomol. 3:333460. ovipositional repellents against Culex (Diptera: Cu- Freeborn, S. B. and R. F. Atsatt. 1918. The etrects licidae) mosquitoes.Environ. Entomol. I 1:968-971. ofpetroleum oils on mosquito larvae. J. Econ. En- Stone,T. B., R. Sims, S. C. Macintosh,R. L. Fuchs tomol. I l:299-3O7. and P. G. Marrone. 1991. Insect resistanceto -Ba- Freeborn, S. B. and B. Brookman. 1943. Identifica- cillusthuringiensis, pp. 53-63. In: K. Maramorosch tion guide to the mosquitoesof Pacific coast states. (ed.). Biotechnology for biological control of pests U.S. Service,Malaria Control in War and vectors. CRC Press,Boca Raton, FL. Areas, Atlanta, GA. Whitten, M. J. and G. G. Foster. 1975. Genetical Herms, W. B. 1949. Looking back half a century for methods of pest control. Annu. Rev. Entomol. 20: guidancein planning and conducting mosquito con- 461467.