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FORUM

Potential Effect of Global Warming onMosquito-Borne Arboviruses

WILLIAM C. REEVES, JAMES L. HARDY, WILLIAM K. REISEN, MARILYN M. MILBY

School of Public Health, University of California, Berkeley, CA

J. Med. Entomol. 31(3): 323-332 (1994)ABSTRACT If global warming in California, daily temperatures in-

by 5C, precipitation patterns will change, and level may rise Studiesdone effect of temperature changes survival of Culex tarsalis Coquillett, the

primary vector of equine encephalomyelitis (WEE) and St. Louis encephalitis(SLE) viruses, in regions where temperatures differed by 5C. Daily mortality ofadultvectors increased by 1% for each 1C increase in temperature. At 25C, only 5% of Cx.tarsalis survived for 8 days, the time required for extrinsic incubation of theseviruses. Extrinsic incubation times for these viruses shortened when temperaturesincreased from 18 25C. WEE virus infection modulated and transmission decreased32C. Iftemperatures in the region increase by 5C, WEE virus may disappear

and SLE virus would persist. In the cooler region, 5C increase would decrease vectorsurvivorship and virus activity in midsummer. In North America, epidemics ofWEE haveprevailed above 21C isotherm and those of SLE below this isotherm. With globalwanning, epidemics of these viruses could extend currently unreceptive northern

WEE virus would disappear from southern regions. Geographic distribution ofvector, human, and animal populations could be altered. North America could become

receptive invasion by tropical vectors and diseases.

KEY WORDS global wanning, mosquito, arbovirus

IN NOVEMBER 1987, the U.S. EnvironmentalProtection Agency convened workshop tosider "The Potential Impact of Climate Changes

Patterns of Infectious Disease in the UnitedStates" (Smith & Tirpak 1989). This meeting pro-vided background meteorological changesexpected to in the twenty-first century. Italso stimulated to reexamine existing data anddevelop research studies to determine how suchenvironmental changes might affect the futureprevalence of arbovirus infections and theirtors in California. We believe it is feasible topredict of the public health consequencesof such events.The majority ofpublications and organizations

concerned with the effects of global warminghave focused their attention economic, indus-trial, general ecological, and demographic inter-

ests and not public health outcomes. A reviewof the rapidly growing literature the effect ofglobal warming during the twenty-first centuryhas provided basis to formulate the followingthree simplified assumptions regarding its futureimpact in California (Smith & Tirpak 1989,Anonymous 1991): (1) daily temperatureswill increase by 3-5C; (2) patterns of precipita-tion will change and alter seasonal and regionalwater availability; (3) coastal levels may rise

much If these three events occur,

believe there could be major changes in theprevalence of endemic arboviruses and in thedistribution oftheir vertebrate hosts and vectors.To simplify this presentation, will focusattention the impact of temperature changes

two mosquito-borne arboviruses, westernequine encephalomyelitis (WEE), alphavirus,and St. Louis encephalitis (SLE), flavivirus,and their primary vector in California, Culex tar-salis Coquillett.

Background

WEE and SLE viruses have been active in

California and recognized important healthproblems since the 1930s. We have considerableknowledge of factors, particularly temperature,that affect the life table of the vector and inter-

relationships of the vector and viruses (Reeves1990). These viruses spend most of their exis-tence in the in the vector, where they

subject to major temperature variations.However, the viruses also dependent uponserial transmission between the poikilothermicvector and homeothermic avian hosts. The trans-mission cycle for WEE virus is representative ofmany arboviruses (Fig. 1). The feral vertebratehosts have viremias that infectious to thevector for only few days (Hardy & Reeves

0022-2585/94/0323-0332$02.00/0 (C) Entomological Society of

324 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 31, 3

rig. 1. Current concept the transmission cycle WEE the Central Valley(from Hardy [1987], with permission of the American Journal of Tropical Medicine and Hygiene).

1990). Therefore, the vector-virus interrelation-ships provide excellent model in which tostudy, the impact of environmental stressesthe survival ofboth the vector and the virus. Cx.tarsalis also is the primary vector of three otherviruses in this region, Turlock (a bunyavirus),Llano Seco (an orbivirus), and Hart Park (a rhab-dovirus). Future studies could be extended toinclude these agents. This would provideunique opportunity to evaluate the impact ofcli-matological changes five widely disparate in-fectious agents in single vector species and itsrange of vertebrate hosts.Our approach has been to initiate studies in

the twentieth century to provide data base thatwill allow to describe probable events thatmay evolve in the twenty-first century. Two ap-proaches have been taken. First, the Imperialand Coachella valleys in southern Californiarently experience the extremes of temperatureanticipated to in the future in thenorthern San Joaquin and Sacramento valleys.We have compared biological and virologicalfindings from these regions to make predictionsand used this information to design further fieldand laboratory studies that will expand the database. The laboratory studies utilized programma-ble environmental chambers to determine the

effects of broad range of temperatures dia-pause, life tables, gonotrophic cycles, and vectorcompetence of Cx. tarsalis. DATAPOD probes(Omnidata International, Logan, UT) that contin-uously record temperatures placed in repre-sentative microhabitats in the Coachella and SanJoaquin valleys where Cx. tarsalis rests duringthe day and in the open spaces where thequitoes after sunset and remain until theyreenter resting sites in the morning (Meyer et al.1990, Reisen et al. 1992a). Thus, realistic tem-perature data obtained that be pro-grammed into the environmental chamberswhere vectors held to study vector compe-tence and survival.

Field Observations

Our primary attention has been concentratedtemperature because it is environmental

factor that be measured and has major in-fluence virus-vector-host interactions, vectorsurvival, and generation time. A summary oferage daily temperatures 30-yr period inthe two regions revealed that there has beenamazingly consistent 5C difference between thesouthern and northern regions throughout theyear (Fig. 2). These differences in temperature

REEVES GLOBAL WARMING ABBOVIRUSESMay 1994

Fig. 2. Average daily temperatures in southern(Indio-Imperial, CoacheIIa-Imperial valleys) andnorthern (Wasco-MarysviIle, San Joaquin-Sacramentovalleys) California.

and accompanying ecological effects have pro-vided with unique natural laboratory inwhich to investigate the potential impact ofglobal warming the transmission of arbovi-

These extremes within 350 km ofeach other.The average monthly abundance patterns of

adult female Cx. tarsalis- in the two regions,based New Jersey light trap collections,consistently different (Fig. 3). In the north, thepopulations very low in winter and earlyspring because the females diapause andgonotrophically inactive in winter (Reisen &Reeves 1990). As result, the annual buildup tohigh populations is delayed until midsummer. Incontrast, high temperatures block the inductionof diapause in southern California (Nelson 1971)and in Texas (Eads 1965). Thus, the vectormains reproductively active, and populations in-

rapidly in the spring. Current studies in-dicate that the southern population is geneticallycompetent to diapause if placed under properlight and temperature conditions. It is fortunatethat daily photoperiods essentially thein the CoacheIIa and southern San Joaquin val-leys, day length is not variable that influ-

diapause differently in the two regions.The absence of diapause and the availability oftemperatures compatible with the extrinsic incu-bation of viruses allows rapid and early buildupofvector populations and increase in theber of virus cycles that be completed inyear in the southern region (Reisen et al. 1986,1993).A second major difference between the north-and southern regions is that vector popula-

tions crash during midsummer in the south whendaily temperatures exceed 30C from June

into September. This population crash repre-sents, in part, decrease in the daily survivor-ship of Cx. tarsalis. Data from field studies inKern County adult female Cx. tarsalis popu-lations indicate that for every 1C increase intemperature, there is 1% decrease indaily survivorship (Fig. 4). The impact of this

I-I 1-I I-1-1-T-r

J F M A M I J A S O N D J

Fig. 3. Adult Cx. tarsalis abundance measured byNew Jersey light trap collections in southern andnorthern California (from Reisen & Reeves [1990],with permission from the California Mosquito and Vec-

Control Association).

decrease successful transmission of WEESLE viruses be very important at higher tem-peratures because the majority ofthe vector pop-ulation will not survive to complete than

gonotrophic cycle, thus horizontal transmis-sion of virus would not because infectedmosquitoes would not refeed (Reisen & Reeves1990).Another factor influencing the abundance of

Cx. tarsalis is autogeny. This is genetic traitthat allows ovarian development without bloodmeal. When larvae from genetically autogenousstrain provided with ample food andter temperature of >22C, they expressed highautogeny rate regardless of the length of photo-period. However, when the temperatureduced to 18C and the daily period of darkincreased from 8 to 14 h, autogeny notpressed (Reisen et al. 1989). Thus, envi-ronmental temperatures probably will increasethe period of the year when autogeny is

326 JOURNAL MEDICAL ENTOMOLOGY Vol. 31, 3

Fig. 4. Environmental temperature effects adultfemale Cx. tarsalis survival. Kern County, 1976-1981.

Fig. 5. Influence of environmental temperaturedaily survivorship ofadult female Cx. tarsalis and theirtransmission of WEE and SLE viruses (adapted fromReisen & Reeves [1990], with permission from theCalifornia Mosquito and Vector Control Association).

pressed. Autogenous females typically olderwhen taking their first blood meal, andpared with anautogenous females, fewer willsurvive to acquire and transmit viruses (Reisen &Reeves 1990). There is evidence that WEESLE viruses transovarially transmitted by Cx.tarsalis (Hardy & Reeves 1990). A high expres-sion of autogeny theoretically could lead to de-velopment oflarge Cx. tarsalis populations with-out efficient virus transmission (Lyness 1970).Regardless of autogeny status, these southernCalifornia populations do not enter diapause for

extended time regardless of photoperiod.To extend this finding further, the effects of30

and 35% daily loss from adult female Cx. tar-salis population illustrated in Fig. 5 (Reisen& Reeves 1990). The 70% survivorshipapproximates data from field studies popu-lation in the northern region exposed to 26Caverage daily temperatures. The 65% survivor-ship takes into account that for every 1C in-

in temperature there is 1% decrease indaily survival and thus models exposure toaverage of31C. This temperature is representa-tive of temperatures during midsummer in thesouthern region. At the higher levels of mortal-ity, population will decrease rapidly if it is notcompensated by elevated recruitment rate,

High mortality in cohort of vectors also in-the risk that extrinsic incubation ofWEE

SLE viruses will not be completed thatcompetentfemales will not refeed. As thein Fig. 5 indicate, at these temperatures it

quires at least 8 dfrom emergence for adult tobecome infected with and complete extrinsic in-cubation for WEE virus, and at least 11 d for SLEvirus (Reisen et al. 1983). By referring to Fig. 5,it be that 5% less of the populationwill survive at those temperatures and completethe extrinsic incubation period for either virus.As further factor in the population crash,

5C increase in temperature from 26 to 31C in

the aquatic environment caused 50% decreasein adult production under controlled laboratoryconditions (Reisen et al. 1984). Maximal larvalsurvival observed at 18C, These studies

done with laboratory colony of Cx. tarsa-lis.We have evidence that heat-stressed Cx.

tarsalis population will develop modified ge-netic capacity for heat tolerance, and this issubject for future study.Data from DATAPODs collected during Au-

gust in the southern and northern environmentsrevealed that major differences in temperature

experienced by adult vectors each day whileresting in refuges during the day and when they

into the open after sundown, at which timethey mate, feed hosts nectar, and oviposit(Meyer et al. 1990). We have selected August

example because it is critical month for virusactivity. Again, the temperatures in the Coa-chella Valley much higher than in KemCounty and will be higher if globaling (Fig. 6). Note that the vertical linemarked "I" is the time of ingress when mosqui-toes enter shelters to spend the daylight periodand the line marked "E" is the time of egress inthe evening. Again, the southern region experi-

much higher temperatures, especially atthe time of egress in the evening, and extremedifferences in daily temperature experiencedby the vector in both in the

Laboratory Observations

We will consider effects of in-creased temperature the vector competenceof Cx. tarsalis for WEE and SLE viruses. Datafrom laboratory studies allow to predict thatincreased ambient temperatures will have bothpositive and negative effects vector compe-tence. As ambient temperatures increase, the

REEVES GLOBAL WARMING ABBOVIBUSESMay 1994 327

Coachella ValleyKern County

45

40

0 35

30

25

20

15

Time of Day

CanopyShelter

"\...6 12 18 24

*’ \

/

/^ N

’

E

6 12 18Time of Day

Fig. 6. Daily temperature in diurnal resting and nocturnal vegetation canopy microhabitats of female Cx.

tarsalis related to extrinsic incubation ofvirnses (adapted, in part, from Meyer al. [1990], with permission of

6\e}ournal of Medical Entomology).

time required for the completion ofthe extrinsic

incubation period of the virus in the vector de-Cohorts of laboratory strain ofCx. tar-

salis females fed WEE SLE virus,then divided into three groups and incubated at

constant temperatures of 18, 25, 32C (Hardy& Reeves 1990). Virus transmission ratesdetermined at various times after infection whenvectors fed individually chickens (Fig.7). Both viruses, and particularly SLE virus,

transmitted efficiently by infected fe-males when incubated at 32C than when held atlower temperatures. The shortening of thetrinsic incubation period in this instance would

compensate, in part, for the increased mortalityof females at the higher temperature, and would

continued virus transmission. However,this would not be the for WEE virus, be-

Cx. tarsalis has enhanced ability totrol modulate WEE virus multiplication andtransmission at higher extrinsic incubationtemperatures (Kramer et al. 1983, Hardy 1988,Reisen et al. 1993).Virus modulation is illustrated by data from

experiment where infection rates deter-mined with WEE-infected Cx. tarsalis heldtime at 18, 25, and 32C (Kramer et al. 1983).Infection rates remained high for 21 d when fe-

Days After Infection

Fig. 7. Effect oftemperature transmission ofWEE and SLE viruses by Cx. tarsalis (SLE data adapted fromHardy & Reeves [1990], with permission from the California Mosquito and Vector Control Association).

328 JOURNAL MEDICAL ENTOMOLOGY Vol. 31, 3

Days After Infection

Fig. 8. Effect of temperature modulation ofWEE virus infection in infected Cx. tarsalis (fromHardy [1988], with permission from CRC Press, BocaRaton, PL).

males incubated at 18 and 25C, however,at 32C infection rates decreased to 75% by day 6after infection and to only 22% by day 12 (Fig. 8).This precipitous decrease in WEE virus infec-tion rates at the higher temperature they growolder may negate the potential enhanced abilityof infected females to transmit WEE virus at thehigher temperature after short periods ofincuba-tion (Fig. 7). Thus, would expectWEE virustransmission cycles to be dampened ambientair temperatures increase to the highest levels,where only small proportion of femalesvives. It surprising to find that WEE virus ismodulated by the vector at 32C because thisvirus experiences temperatures above 40C forperiod of several days during intrinsic incuba-tion in its avian hosts. Subsequent studies dem-

onstrated that WEE virus modulation ge-netically controlled trait of the mosquito (Hardy& Reeves 1990). There is little indicationthat Cx. tarsalis modulate SLE virus multi-plication at any temperature (Hardy & Reeves1990).During period of global warming,

pects temperatures to increase in the aquaticvironments where the preimaginal mosquitoesdevelop. As described above, this could in-

larval mortality and the rate of autogeny.Our data also indicate that increased water tem-perature may affect virus transmission by Cx. tar-salis. For example, demonstrated low levelsof vertical transmission of SLE virus by Cx. tar-salis when the progeny of infected femalesreared at 18C, but when the progenyreared at 27C (Hardy et al. 1984). Thus, highertemperatures for short time may eliminatevertical transmission mechanism for theoverwintering of SLE virus.

Furthermore, 5- to 7-yr period of ob-servation, yearly and intraseasonal changescurred in the susceptibility of isolated popu-lation of Cx. tarsalis to infection with WEE andSLE viruses (Hardy et al. 1990). In this study,late instars and pupae collected monthlyduring the breeding season, transported to thelaboratory, and newly emerged adult females

fed dilution series of virus, held for 14 dat constant temperature of 25C, and thentested for infection (Fig. 9). The mosquito popu-lation highly refractory to infection withWEE virus in 1976 when spring temperatures

unseasonably for long period. Incontrast, this population highly susceptibleto infection during the of 1980 following

unusually cool spring. The short period ofhigh temperature in midsummer in 1980 had

35

30

0

d- 25E

20

M J J A S

Month Month

1976

.-’y^’ ^-

^ \/\’*

**, ***

Temp.--ID 50

6

5!4

5

3

35

30

0

d.25

<-

M J J A S

1980;\/ \

*.*’’ ’’.:

/

"’ ’^’----------~^--

6

-5 !43

3

Fig. 9. Effect ofseasonal temperatures the susceptibility ofCx. tarsalis for WEE virus (ID^ virus dosethat infected 50% of the population (adapted, in part, from Hardy al. [1990], with permission ofthe AmericanJournal of Tropical Medicine and Hygiene).

May 1994 REEVES GLOBAL WARMING ARBOVIRUSES 329

obvious effect susceptibility. A degree-dayanalysis indicated that increases in virus resis-tance correlated significantly with the number ofdays 27 32C accrued from April throughJune. These results indicated that temperaturemay induce changes during preadult develop-ment that affect the susceptibility of adult fe-males to WEE virus (Hardy et al. 1990). How-ever, further analyses indicated that temperaturemost likely acts indirectly unidentified factorsin the aquatic environment that affect the vectorcompetence of emergent adult females. This is

the subject of current studies. Yearly and in-traseasonal changes in vector competence forSLE virus also occurred in the populationof Cx. tarsalis, but these changes did notlate with changes in ambient air temperature(Hardy et al. 1990).No evidence has been found that SLE viruses

isolated from the high- temperature southernCalifornia region have enhanced ability to infect

be transmitted by vectors (Meyer et al. 1983).Similar studies have not been done with WEE

Discussion

The preceding observations, and basicknowledge of the epidemiology of arbovirusesand the biology oftheir vectors, allow to makethe following predictions regarding the probableimpact of global warming these two arbovi-

in California.If temperatures increase further 3-5C inofsouthern California, dramatic changesanticipated. Culex tarsalis will become

less-competent vector for WEE virus in midsum-because it modulates this infection when

temperatures exceed 30C. This may eradicatethe virus from large enzootic The temper-ature change should not affect SLE virus to the

extent, because it is not modulated. In thesouth, Cx. tarsalis may become primarily win-

ter and spring species, happens in the lowerRio Grande Valley of Texas (Eads 1965). If out-door temperatures rise to average of 35Cfor at least 3 mo, vector populations may beforced into estivation if they to survive. Afinding that supported this is that the rate ofovarian maturation after blood ingestion in-creased function of temperature (Fig. 10).However, the rate of oviposition actually de-creased at 30C (Reisen et al. 1992b). Femalescould quiesce gravids at high temperaturesand possibly delay oviposition.We do not know the full effect of increased

temperature the vertical transmission ofarbo-viruses. The study with SLE virus indicated thatthe efficiency ofvertical transmission greaterat 18C than at 27C (Hardy et al. 1984). If thisfinding is generally true, then global warming

0 S 10 16 20 25 30 36TEMPERATURE (C)

Fig. 10. The (inverse of time achievementby 50% of population) of follicle development in Cx.tarsalis Christophers’ Stage V, blood digestion toSella’s Stage 7, and oviposition, plotted function oftemperature (from Reisen al. [1992b], with permis-sion from the Journal of Medical Entomology).

could be detrimental to survival of viruses thatdepend this mechanism for survival.In the northern of California, the peak of

Cx. tarsalis populations could shift from mid-and become biphasic with peaks in the

spring and fall. The periods of WEE and SLEvirus activity should follow the population trend,and of encephalitis should longer peakin midsummer for WEE early fall for SLEthey have for period of >40 yr (Reeves 1990)but may in biphasic pattern, reflectingchanges in the abundance and vector capacity ofCx. tarsalis.

It is tempting to predict what will happen tothe distribution of WEE and SLE viruses in

broader than California. Hess et al. (1963)did interesting evaluation the relationshipofthe 70F (21C) June isotherm to the geograph-ical distribution of WEE and SLE epidemics inthe period 1933 to 1962 (Fig. 11). It is interestingthat the of epidemics in the ensuingperiod, 1963-1992, has followed this pat-tern. If global warming occurs, predictthat epidemics of SLE will northward, andWEE virus may not be able to remain epidemicin of its current southern distributions. Infact, WEE virus could disappear from much ofits

current endemic and becomeinfection in the northern states and Canada.

We do not know what will happen to otheralphaviruses to the receptivity of extensive

of North America to the introduction ofalphaviruses such Venezuelan equinecephalitis, Ross River, and Chikungunya, which

to prevail currently in of the worldwith high temperatures.Three assumptions made originally

garding changes that will result ofglobal warming, and have concentratedstudies temperature. The other assumptions

that there will be major changes in the

330 Vol. 31, 3JOURNAL OF MEDICAL ENTOMOLOGY

194lQ

Fig. II. Distribution ofrecorded human outbreaks of St. Louis and encephalitis in the United Statesin relation the 70F (21C) June isotherm (from Hess al. [1963] with permission ofthe American Journal ofTropical Medicine and Hygiene).

pattern of precipitation and rise in level,

The principal changes in precipitation predictedfor California will be decrease in winterfall and increase in rainfall (Smith & Tirpak1989). An increase in rainfall and tem-perature could make California receptiveto the introduction of exotic vectors suchAedes aegypti (L.) and Aedes albopictus (Skuse)and flaviviruses, such dengue and yellow fe-ver, that they transmit. It may be importantthat major changes will in the availabilityof water for domestic and agricultural purposes.The current system of flood control and waterstorage dams in California developed largelyto redistribute water from snowfall in thetains of northern California to southernneeding additional water for agricultural, domes-tic, and industrial (Kramer 1975, Kahrl 1978).With global warming, snowfall is predicted todecrease and there will be recession ofat least150 in the elevation of the line (Anony-

1991). This recession will have majoreffect water availability, the abundance ofAedes mosquitoes that snow-water pools forbreeding, and the bunyaviruses they transmit(Campbell et al. 1991). The long-term effect thischange will have the geographical relocationof the human population and their exposure toarboviruses has been topic of speculation(Reeves & Milby 1989, Reeves 1991). It is antic-

ipated that extensive change will be made in

agricultural practices result ofdecreasedter availability and that this will decreasequito populations that dependent suchwater usage (Reisen & Reeves 1990).The seasonal patterns of future agricultural

practices and changes in distribution of therent vectors also unknown. We believe thatthere will be substantial changes in the distribu-tion of mosquitoes that currently in Cali-fornia. Species that restricted to the

southern areas, where freezing temper-atures rare, may extend into and become

in the Central Valley and northerncoastal Examples Psorophora colum-biae (Dyar & Knab) and Aedes taeniorhynchus(Wiedemann).Most current coastal salt-marsh habitats will be

inundated by predicted rise ofup to inlevel. This change will decrease eliminate thehabitat of current populations of salt-marshquitoes. Species of birds and mammals thatdependent this habitat, and thatsidered to be endangered, probably will becomeextinct, and viruses that endemic in thisenvironment could disappear (Eldridge et al.1991). At the time, salt-water intrusionswill at great distances inland into currentfreshwater habitats (Smith & Tirpak 1989). Intime, of these may develop into salt

May 1994 REEVES GLOBAL WARMING ARBOVIBUSES 331

marshes that will be populated by salt-marshmosquito species, which be pests and carryviruses.Very few current publications have drawn at-

tention to the national and international impor-tance ofglobal warming with reference to humanhealth problems. A report from the Institute ofMedicine of the National Academy of Sciences(Lederberg et al. 1992) briefly described theproblem and stated, "It is thus disturbing to notethe apparent lack ofinterest in global warmingpossible contributor to public health crises

the part of funding agencies and environmentalgroups." A symposium of the British Society ofParasitology (Hominick & Chapell 1993) coveredwide variety of biological problems associated

with global changes but did not focus attentionthe wide variety of arthropod-borne diseases

that major human health problems in trop-ical regions.

It remains to be if detailed andfocused research of the type describe herewill be forthcoming. We believe that globalwarming and associated ecological changescould result in extreme changes in pathogen dis-tribution. The studies reported here demon-strated that relatively small increases in temper-ature, such expected from global warming,will decreases in vector survival, will altervector competence to transmit pathogens, andcould modify the geographical distribution ofvirus, vector, human, and animal populations.These changes be studied today and deservesuch attention. The concepts and methods devel-oped in the current studies applicable towide variety of vector-borne pathogens that

may emerge health problems in bothtemperate and tropical regions of the world.

Acknowledgments

Substantial contributions this research madeby L. D. Kramer, R. P. Meyer, S. B. Presser, andR. Chiles (University ofCalifornia, Berkeley). Thissearch sponsored in part by grants AI3028,AI26154, and AI32939 from the National Institute ofAllergy and Infectious Diseases, grant M1435 from theCoachella Valley Mosquito Abatement District, annualgrants from the University of California Mosquito Re-search Program, and continuing logistic support fromthe Kern Mosquito and Vector Control District.

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Received for publication 16 August 1993; accepted22 December 1993.