Bull. Org. mond. Santet 1974, 50, 427-440Bull. Wld Hlth Org. J

Review of the ecology of malaria vectorsin the WHO Eastern Mediterranean RegionA. R. ZAHAR 1

On the basis ofpublished records and unpublished reports to WHO, the author reviewsthe information available on the ecology of 15 anopheline malaria vectors occurring in areasof the WHO Eastern Mediterranean Region where attack measures are being applied. Theinformation, which is still incomplete, relates chiefly to the period since 1956, the year whenthe malaria eradication programme in the Region was launched. An attempt is made toevaluate the control measures undertaken so far, and to provide data on the sensitivity toinsecticides, behaviour, and mortality of vector populations.

This paper reviews recent information on theecology of malaria vectors in the area designated bythe World Health Organization as the EasternMediterranean Region,a with special reference totechnical problems. Earlier information can be foundin older literature (11, 15, 19). The review mainlycovers the principal and some additional malariavectors on which information is available in pub-lished and unpublished reports from countries with amalaria eradication or control programme underway. Vectors in countries with programmes in themaintenance phase (Israel and Lebanon) or wheremalaria has been eradicated (Cyprus) are not in-cluded, since the potential of former vectors in suchareas is outside the scope of this paper.The area under discussion contains fauna of

three zoogeographical regions-the Ethiopian, thePalaearctic and the Oriental regions. As far aspossible the review follows this sequence, startingwith vectors occurring in the southernmost part ofthe area and then discussing those of the north andnorth-east.

Anopheles gambiae Giles

This is the most important malaria vector of theEthiopian zoogeographical region. In Democratic

1 Entomologist, Division of Malaria and other ParasiticDiseases, World Health Organization, Geneva, Switzerland.

a The WHO Eastern Mediterranean Region comprisesthe following countries: Afghanistan, Bahrain, Cyprus,Democratic Yemen, Egypt, Ethiopia, Iran, Iraq, Israel,Jordan, Kuwait, Lebanon, Libyan Arab Republic, Oman,Pakistan, Qatar, Saudi Arabia, Somalia, Sudan, Syrian ArabRepublic, Tunisia, United Arab Emirates, and Yemen.

Yemen, Ethiopia, Saudi Arabia, Somalia, Sudan, andYemen, A. gambiae can be found throughout theyear in riverine areas or areas with permanentsources of water, though at much reduced densitiesduring the dry season. Even in areas with limitedsources of water, as in Saudi Arabia, Somalia, andSudan, A. gambiae can persist throughout the dryseason at a very low density, breeding in theecologically most suitable sites. These may be termed" mother foci ", from which A. gambiae spreadsduring the rainy season to the surrounding areas thatare dry during the arid season. According toDavidson,b species B is the only member of theA. gambiae complex that has so far been identifiedfrom Saudi Arabia, Democratic Yemen, Sudan, andEthiopia, although there is a single record ofspecies C from Ethiopia (G. Davidson and G. B.White, personal communications, 1973). In climati-cally favourable years, severe malaria epidemics maydevelop, as happened in 1950/51 and 1957/58 inSaudi Arabia.

Fontaine et al. (4) reported an epidemic inEthiopia in 1958 that struck areas at altitudes of1600-2150 m and concluded that A. gambiae was theonly vector involved. The main precipitating causewas the unusual weather in that year; rainfallexceeded all previous records while temperature andhumidity were abnormally high. Working nearNazareth at an altitude of 1600-1800 m in 1964/65,in an unsprayed area where the parasite rate ranged

b DAVIDSON, G. Distribution records of member speciesof the Anopheles gambiae complex (identification up toMay 1966). Geneva, WHO, 1966 (mimeographed documentWHO/MAL/66.570).

3208 - 427

428 A. R. ZAHAR

between 2.8% and 31.9%, Rishikesh a reportedsporozoite rates as low as 0.11-0.31% in 4513A. gambiae females dissected. A review of anophe-line mosquitos in Ethiopia by O'Connor (21) quotesmany negative results of dissections of A. gambiaecarried out by several workers in different parts ofthe country; an exception was one record of highergland infection, found in 3 out of 100 A. gambiaedissected in Welo Province by Rice in 1955/56.Krafsur (13), working in a savannah area extendingalong the River Baro at Gambela, recorded anaverage sporozoite rate of 2.89% in the wet seasonand 0.37% in the dry season. Using the parous rateand the immediate and delayed sporozoite rate tocalculate the theoretical daily survival for A. gambiaeand A. funestus, he arrived at estimated values of0.89 for the wet season and 0.79 for the dry season.

In the area under the attack phase of the malariaeradication programme in Ethiopia, where opera-tions began in 1966/67, A. gambiae house-resting andbiting densities have been much reduced, except ininstances when operational defects, mainly related tohuman ecology, were involved. Jolivet (unpublishedreport to WHO, 1959) reported that some A. gam-biae were found resting in a sugar-cane plantationnear breeding places during the day, but no detailson the density and the abdominal stages were given.From observations made in Nazareth, Rishikesh aconcluded that the species is highly endophilic. Hisdata on the blood digestion stages of house-restingpopulations suggest, though, that a proportion offemales leaves the indoor resting shelter before thecompletion of the gonotrophic cycle. However, boxshelters used for sampling outside resting popula-tions did not yield a significant number of A.gambiae.

Outdoor resting of species B was observed byHaridi (9) in July-October 1967 in the Khashm ElGirba area, Kassala Province, Sudan. The area of ob-servation had been under DDT house spraying since1964 and a high incidence of malaria was recordedduring the period of study. Of 432 females collectedfrom outside natural shelters in September andOctober, 57 % were bloodfed and the fed/gravid ratiowas 2:1. Of 125 females caught at these shelters thathad taken bloodmeals, 26% contained human blood,70% cattle blood and the remainder blood of othervertebrates. It is not known whether the femalesfound positive for human blood had escaped from

a RISHIKESH, N. Observations on anopheline vectors ofmalaria in an upland valley in Ethiopia. Geneva, WHO,1966 (mimeographed document WHO/MAL/66.554).

human habitations or had fed on people sleepingoutside with their cattle. Two individuals positive forsporozoites were detected among 56 females collect-ed from outside shelters. At the same time, theparous rate among 54 females collected from outsideshelters was 57 %, giving a probability of dailysurvival of 0.758 assuming that the gonotrophic cycleof the outside resting population was 2 days. Theoutside resting of A. gambiae coincided with a largeexodus from sprayed houses, as demonstrated bywindow trap observations, with a survival rate of88-94%. The species was found to be susceptible toDDT. The indoor density also markedly increasedduring September and October; a fed/gravid ratio of3.5:1 was found and one sporozoite-positive femalewas detected among 11 parous females dissected.Haridi suggested that the exodus of mosquitos fromsprayed houses and the high survival rate may havebeen partly attributable to a natural behaviour patternof A. gambiae species B in this part of Sudan, or aresult of the irritant effect of DDT. The high survivalrate could also be explained by the ageing of DDTdeposits or by inadequate spraying and the presenceof unsprayable objects, suggesting that in view of thepartial exophily of A. gambiae and irritant effects ofDDT, only active deposits of the insecticide would beeffective in producing a high mortality. Haridiconcluded that the epidemiological significance ofoutdoor resting populations should not be over-looked and further observations should be made toidentify the ecological conditions favoured by suchpopulations in different parts of Sudan.The dry season biology of a member of the

A. gambiae complex (probably species B) and itsresurgence in seasonally waterless areas has beeninvestigated in Sudan (21). In the White Nile valley,the species was found to maintain itself by low-levelbreeding; larvae, male mosquitos, and parousfemales were found throughout the dry seasons of1966 and 1967. In contrast, in scattered villages ofthe arid area of Fattasha situated more than 20 kmfrom the Nile Valley, regular sampling through thecool dry and hot dry months of the year failed todetect any A. gambiae except nulliparous females ininhabited and vacant huts, dry wells, and animalburrows. In the females collected from November toApril, the ovaries did not develop beyond Christoph-ers' stages II and III and the stomachs containedsmall amounts of fresh or old blood. Normaldevelopment of the ovaries was observed during thefavourable season. Evidently the female A. gambiaepopulation can adapt to the severe drought and heat

MALARIA VECTORS IN THE EASTERN MEDITERRANEAN 429

of the arid zone in Sudan by continuing to feed, butovarian development is extremely retarded.The first confirmed record of DDT resistance in

A. gambiae in East Africa came from El Guneidsugar estate, Sudan, in January and March 1970, andthe mode of inheritance of the resistance was studiedby Haridi (10). The same mosquito population alsoshowed a pronounced resistance to dieldrin. Pre-viously, HCH had been sprayed in this locality, beingreplaced by DDT in 1969. It seems that highselection pressure had been created by pesticidesused on cotton crops before the sugar-cane wasplanted and in cotton plantations still surroundingthe estate. The area was carefully sprayed with DDTin August 1970 in an attempt to determine thepractical implications of DDT resistance in thispopulation. With 4 hours' exposure to 4% DDT inSeptember 1970, the lowest mortality was 76 %,while trap mortality was about 24 %, gravid femalesforming a large proportion of exit trap collections.The man-biting density was as high as 27 per man pernight, and the indoor resting density was estimatedto be about 60 per man-hour of searching. Furtherinstances of DDT resistance in A. gambiae in otherparts of Sudan were reported to WHO in 1971and 1972.

Anopheles funestus GilesNext to A. gambiae, this is the second most

important malaria vector in the Ethiopian zoogeo-graphical region. It occurs in Ethiopia, Somalia andSudan, though information from these countries onits ecology and behaviour is fragmentary. In Ethio-pia, although it is present in most areas occupied byA. gambiae, its density is usually much lower, exceptin certain areas where favourable breeding condi-tions prevail (20). From observations in Ethiopia,Rishikesh a concluded that A. funestus, like A. gam-biae, is highly endophilic and acts as an additionalvector. No gland infection was found in 339 femalesdissected. The species responds to residual housespraying with DDT. Limited susceptibility testsrecently carried out in Ethiopia showed that it issusceptible to DDT but a low level of resistance todieldrin was encountered. Krafsur (14), reviewing hisinvestigations in the Gambela area, determined thevectorial status of A. gambiae, A. funestus and A. nilion a seasonal basis by multiplying estimates of theirman-biting rates by their seasonal sporozoite rate.A. funestus was the predominant vector, followed byA. nili and A. gambiae.

a RISHIKESH, N., op. cit.

Anopheles pharoensis Theobald

A. pharoensis is widely distributed in Ethiopia,Somalia and Sudan and also extends into Egypt.Jolivet (unpublished report to WHO, 1959) mentionsthat one infected specimen was found in Ethiopiaby Ovassa. Rishikesh b could not detect any glandinfection in 2 577 females of this species dissected inEthiopia, and he considers that it is less endophilicthan A. gambiae. In Sudan, where it has not beenincriminated as a vector so far, it was found restingindoors and outdoors, and was often encounteredon shaded vegetation around houses.

In Egypt, A. pharoensis was first reported as avector by Barber & Rice (2), who found a sporozoiterate of 0.33 % in 1 513 specimens dissected during amalaria outbreak. The species was further studiedfrom 1959 to 1962 in the southern part of the NileDelta by Zahar et al.c Baseline observations showedthat it bites man and animal indiscriminately bothindoors and outdoors. A human blood index of32.1 % was recorded in an area with a man/animalratio of 1: 7. The partial exophily of this species wasdemonstrated by using outlet window traps and bythe collection from rice plants of blood-fed femaleswith a human blood index of 19.4%. In a study ofthe age grouping of this vector by Polovodova'stechnique in samples collected in window traps in anunsprayed area, the highest numbers of dilatationsobserved were 3 and 4, each occurring in 0.05% of1 980 females dissected during 1960-1962. Dry cli-matic conditions in June do not favour the species'survival.

Longevity markedly increases with the increase ofthe relative humidity from July to September. AfterSeptember, a decline in vector output and densityoccurs as the rice fields dry up, leading to atemporary imbalance in the proportions of nulli-parous and parous mosquitos.The paucity of aged individuals shows that though

A. pharoensis attains very high biting densities duringthe favourable season, females of epidemiologicallydangerous age are still scarce in the population. Thismay explain the low infectivity and the low degree ofmalaria transmission effected by this species. Theintensity of transmission may vary from place toplace and from year to year depending on the relativehumidity and the size of the reservoir of infective

b RISHIKESH, N., op. Cit.C ZAHAR, A. R. ET AL. Epidemiological evaluation of

DDT spraying with studies on behaviour of Anophelespharoensis Theobald in Egypt, UAR. Geneva, WHO, 1966(mimeographed document WHO/MAL/66.566).

430 A. R. ZAHAR

cases. Rice cultivation is a very important factor inproducing an increase of breeding of A. pharoensisand in raising relative humidity, thus favouring theadults' survival.

A. pharoensis was reported to be susceptible toDDT before 1959 by Zahar (30), and was later foundto be resistant to both dieldrin and DDT. a, bDouble resistance also appeared in A. pharoensisfrom unsprayed areas; it was probably related tothe extensive use of chlorinated hydrocarbon insecti-cides for control of cotton pests.

Starting the first cycle in June 1960, a limited scalefield trial was carried out in Egypt in order toevaluate the impact of DDT spraying on malariatransmission when applied at a dose of 2 g oftechnical DDT per m2 once a year for a period of3 years. Under the influence of insecticidal attack,the overall parasite rate dropped in 1960 to 20% ofthat of 1959. This indicated an adequate regressionduring the first year which, if maintained, wouldultimately have resulted in a diminution of malariato a very low level (17). There was evidence that theinsecticide was starting to wear off in September1960, when 4 infants born after spraying becamepositive. Except for that temporary reversal, reflect-ing operational defects, the overall picture of the yearwas generally satisfactory. The control of vectorlongevity was satisfactory when the average trapmortality was 70% or more; it became unsatisfactorywhen the average was below about 54 %. In terms ofprobability of survival through one day (16), resultswere adequate as long as this index was kept below0.5. Taking the data on satisfactory response in 1960as a basis for assessment, the appropriate criticalvalue for survival through the extrinsic cycle mightbe approximately 0.002.

In 1961, the second year of the trial, the crudeparasite rate showed a much smaller decline, indicat-ing a less favourable response. It fell only from2.37% to 1.87%, the latter level being equal to 16%of the baseline level, instead of the 4% that wouldhave been expected after 2 years of attack had theinitial rate of decrease been maintained. Trapmortality was only slightly over half the 70% levelrequired for satisfactory control. Vector probability

a ZAHAR, A. R. & THYMAKIS, K. Investigation on thesusceptibility of Anopheles pharoensis to insecticides inEgypt, UAR. Geneva, WHO, 1962 (mimeographed docu-ment WHO/MAL/341).

b ZAHAR, A. R. ET AL. Studies on the susceptibility ofAnopheles pharoensis to DDT in the Nile Delta, UAR.Geneva, WHO, 1965 (mimeographed document WHO/MAL/482.65).

of survival through one day increased to 0.62 andthrough the extrinsic cycle to 0.013, i.e., over sixtimes the critical value of 0.002 suggested on thebasis of the data of satisfactory response. In 1962, thethird year of attack, the general parasite rate fell to4.5% of the original 1959 level, compared with thelevel of 0.4% expected had satisfactory control beencontinuously maintained. That rate of decline im-plied further low-grade transmission in the sprayedarea in the third year of attack. The critical levels forthe probability of vector survival through one daythrough the extrinsic cycle were exceeded. The trapmortality was only 41.8 %, again much inferior to the70% level required for satisfactory control. Thisunsatisfactory control coincided with a deteriorationin the susceptibility of A. pharoensis to DDT, whichwas determined periodically throughout the study.Further observations c confirmed the ineffectivenessof two rounds of DDT spraying, each at 2 g/m2, inthe same trial area in 1963. However, it was notcertain whether this was the main factor responsiblefor continued transmission, or if outdoor biting andoutdoor resting of the vector population had playeda role.

Anopheles sergenti Theobald and A. multicolor Cam-bouliuA. sergenti is an important vector of malaria in the

oases and in Fayoum Province in Egypt, and inthe Libyan Arab Republic. In the eastern part of theRegion, it is recorded from Iran, Iraq, Jordan, SaudiArabia, and some pockets in the Syrian ArabRepublic. Eradication was attempted at the Khargaand Dakhla oases, Egypt, by an intensive larvicidingcampaign from 1946 to 1948, which resulted in a fallin the parasite rate from 13.5% to 0.3%. The returnof this species to 3 oases was observed in 1951 (8),indicating that eradication had not been achieved.There has been little investigation of the bionomics

and behaviour of A. sergenti in the Libyan ArabRepublic and Tunisia. It is quite likely that it was thevector responsible for the malaria outbreaks of 1964and 1965 observed in Ghat and Barakat, on theLibyan southern border. It was recently found to beresponsible for malaria transmission in the southernpart of Tunisia (Wernsdorfer and Iyengar, unpub-lished reports to WHO, 1969-1971). The role ofA. multicolor, where it exists with A. sergenti or alone

C SHAWARBY, A. ET AL. Entomological evaluation -ofDDT, HCH and malathion in a field trial against Anophelespharoensis in the Nile Delta, 1963. Geneva, WHO, 1965(mimeographed document WHO/MAL/493.65; WHO/VectorControl/I 15.65).

MALARIA VECTORS IN THE EASTERN MEDITERRANEAN 431

in these oases, remains unknown. A. multicolor hasnot been incriminated in nature, but is suspected tobe a vector on epidemiological grounds as it has beenfound alone in some oases where malaria is transmit-ted.

Farid (3) reviewed the situation of A. sergenti inrelation to malaria in Western Asia. His observationsin the Jordan valley during 1949-1952 showed thatdespite 2 cycles of DDT and HCH residual sprayingin 1951, malaria transmission continued in 4 out of12 villages. A malaria outbreak was observed in 1952at El-Gurm, where a 55.3 % overall parasite rate anda 38% infant parasite rate were recorded. No adultA. sergenti were found in sprayed premises but theywere abundant in caves and fissures in the neigh-bouring hills. One sporozoite-positive specimen wasdetected in a sample from the caves. Antilarvalmeasures were then introduced to supplement resid-ual house spraying. Dieldrin was used as a larvicideuntil resistance to it was discovered in the JordanValley (Garrett-Jones, unpublished WHO docu-ment, 1958), when it was replaced by DDT. Singh &Gad (27) reported some tolerance to DDT inA. sergenti larvae, which was attributed to lowtemperatures during the cold season. Davidson(unpublished report to WHO, 1967) succeeded inraising a self-perpetuating colony of A. sergenti fromegg batches sent from Fashkha in the Jordan Valleyin May 1967. Tests made with samples from thiscolony indicated that the species was still resistant todieldrin, while tolerant to DDT. This was probablyslightly enhanced tolerance to DDT in the dieldrin-resistant strain selected to near homozygosity. Ac-cording to reports to WHO, DDT house sprayingsupplemented by larviciding with DDT/diesel oil andlater with temephos a have given satisfactory controlof A. sergenti and consequently no malaria transmis-sion has taken place.

In Saudi Arabia, larviciding of all potentialbreeding places of A. sergenti using Paris green insuspension at a dosage of 0.15 g of Paris green per m2did not give satisfactory control during 3 years'operations in Khaiber oasis. The output of adultsremained high and malaria transmission continued(Zahar, unpublished report to WHO, 1967).

Anopheles labranchiae FalleroniThis is a palaearctic species with a limited

distribution along the North African littoral. It hasbeen reported from the north-western part of the

a Proposed to the ISO as the common name for 0,0,0',O'-tetramethyl O,O'-thiodi-4,1-phenylene phosphorothioate.

Libyan Arab Republic, which represents the easternlimit of its distribution in northern Africa. In Tunisiait is the principal malaria vector in a large part of thecountry, particularly in the northern governorates.Since the initiation of Tunisia's malaria eradicationprogramme A. labranchiae has succumbed to DDThouse spraying, as shown by its virtually completeabsence from hand spray captures and bait capturesin properly sprayed areas. In susceptibility testscarried out by Iyengar in 1971 (unpublished reportsto WHO), about 12% survival was observed withexposure to 4% DDT for 1 hour, but an almostcomplete kill was obtained with 2 hours' exposure tothis concentration. Residual spraying together withcase detection has succeeded in interrupting malariatransmission in large areas of Tunisia, which haveadvanced to the consolidation phase.

Anopheles claviger MeigenA. claviger is widely distributed in the Middle East.

In 1956, when Gramiccia (7) reviewed its position inthe area as a vector of malaria on an epidemiologicalbasis, no records of its incrimination in nature in theEastern Mediterranean Region were available exceptfrom Cyprus. In October 1970 an outbreak ofmalaria occurred in a small village on the outskirts ofAleppo, Syrian Arab Republic, where 58 indigenouscases of P. vivax were detected. A. claviger was theonly anopheline found in this area and dissection of20 specimens showed 2 females with sporozoiteinfection.b Oil larviciding in wells where it breedscould bring about control of malaria transmission.

Anopheles pulcherrimus Theobald and Anopheleshyrcanus PallasA. pulcherrimus occurs in the north-eastern part of

the Eastern Mediterranean Region, including easternSaudi Arabia, the Syiian Arab Republic, Iraq, andAfghanistan. In Saudi Arabia and the Syrian ArabRepublic there has been no suspicion that it isresponsible for malaria transmission, but in Iraqsome epidemiological evidence was found that anoutbreak of malaria in a small area was associatedwith the presence of this species alone (26). However,no dissections were made to provide evidence of itsincrimination in nature nor have the observationsbeen followed up.

In the Kunduz area of northern Afghanistan,which has been under the attack phase for a long

b MUIR, D. A. & KEILANY, M. Anopheles claviger Meigenas a malaria vector in Syria. Geneva, WHO, 1972 (mimeo-graphed document WHO/MAL/72.757).

432 A. R. ZAHAR

time, A. superpictus has not been reported for some15 years, but A. pulcherrimus and A. hyrcanus weresuspected to be vectors. After 1966 a steady increasewas noted in the number of malaria cases in theKunduz area and attempts were made to detect thevector responsible. Badawy (unpublished reports toWHO, 1969) demonstrated gland infections amongwild-caught females of A. pulcherrimus and A. hyrca-nus dissected within 1 day of capture. Entomologicalinvestigations indicated that both species had existedin areas sprayed with DDT, biting man and animalsin high densities outdoors, particularly during theseason when people slept outside. Both species wereencountered resting in natural shelters, but A. pul-cherrimus also uses unsprayed indoor shelters, e.g.,those missed during spraying. Susceptibility testsshowed that A. pulcherrimus remained susceptible toDDT whereas A. hyrcanus exhibited marked resis-tance to this insecticide. Both species showed normalsusceptibility to dieldrin. This is in contrast toPeffly's finding (23) that A. pulcherrimus showedpronounced dieldrin resistance in the Eastern Pro-vince of Saudi Arabia. In investigations by Zahar(unpublished report to WHO, 1970) in Afghanistan,A. hyrcanus appeared to play an important role inmalaria transmission during May and part of June,after which A. pulcherrimus took over despite DDTspraying. Transmission continued throughout Julyand August, though at a slower pace during the lattermonth. Age grouping dissections carried out onoutside resting populations of A. pulcherrimus inAugust 1970 indicated a high parous rate andconsequently a high probability of daily survival.Specimens with 1-6 dilatations were also encoun-tered. This provides evidence that A. pulcherrimuscould withstand adverse conditions in the outsidenatural resting shelters. A high biting density on manwas recorded during the same investigation. In allfoci of transmission studied, there were obviousoperational deficiencies of DDT coverage in timeand space; thus it was difficult to determine whetherpersistence of transmission was attributable to theexophilic tendency of A. pulcherrimus or to opera-tional defects alone. No valid basis has been foundfor identifying the form of A. hyrcanus that occurs inthe Kunduz area as A.h. pseudopictus; the form hasrecently been confirmed to be typical A. hyrcanusPallas (29).

Anopheles superpictus Grassi

This important palaearctic vector is commonlyfound in association with A. sergenti in Jordan

and in north-western Saudi Arabia. In these areas,it has apparently responded to attack measures. Itextends further north in the Region, occurring in theSyrian Arab Republic, Iraq, Iran, and Pakistan,where it has been recorded in Baluchistan and southWaziristan. The species has also been recorded inTunisia.

In the Syrian Arab Republic transmission stillpersisted in 1965-1966 in the Armala area, IdlebProvince, in the north-western part of the countrywhere A. superpictus is the principal vector, breedingin hill streams. A household survey by de Zulueta(unpublished report to WHO, 1966) indicated thatsleeping outdoors was rare even during summermonths. On the other hand, spraying of temporaryfarm huts built between the 2 spraying rounds in1966 had been overlooked and these were found toshelter A. superpictus. In addition, houses had beenplastered after DDT spraying. When total coveragewas achieved in house spraying with DDT, A. super-pictus was brought under control and malariatransmission was interrupted.

In Iran, A. superpictus is widely distributed exceptin the coastal area of Shatt el Arab. In the region ofthe Caspian Sea, however, its distribution is veryrestricted. In 1965, it was reported a that A. superpic-tus had a similar pattern of seasonal prevalence toA. fluviatilis, their density peaks occurring in thespring and autumn. The human blood index forA. superpictus was 22.4%. Applying Polovodova'stechnique, it was found that the proportion ofpotentially dangerous females in the A. superpictuspopulation, i.e., females having more than 3 dilata-tions, was 1.5 %. This species, together with A. fluvia-tilis, has proved refractory to attack measures.Mesghali (unpublished observations, 1968) pointedout that in some parts of Iran, particularly inKermanshah and in Kashaf-rud, Khurasan, despitethe campaign against malaria, transmission byA. superpictus had not been interrupted. The specieswas almost absent from sprayed dwellings butpresent in caves and other natural shelters. Offemales taken from caves, 4.1 % had human bloodand 0.9% were sporozoite-positive. A. superpictuswas reported to be susceptible to dieldrin and DDTdespite repeated spraying; it was likewise susceptibleto malathion.

a INSTITUTE OF PUBLIC HEALTH RESEARCH, TEHERAN.Progress report on investigations and research on malariaepidemiology and malaria education in Iran. Teheran, 1965(Publ. Inst. Pub. Hlth Res., Teheran, No. 1463).

MALARIA VECTORS IN THE EASTERN MEDITERRANEAN 433

Anopheles fluviatilis JamesThe vector A. fluviatilis also has a wide distribu-

tion in the Region. It exists in the central northernpart and in the Eastern Province of Saudi Arabia, inIraq, and in Iran where it occupies the southernslopes and foothills of the Zagros mountains to-gether with A. stephensi and A. superpictus. Its dis-tribution extends to Pakistan.The behaviour of A. fluviatilis has been studied in

some detail in Iran. Age determinations showed thatonly 1-2.5% of the population of this species couldreach a potentially dangerous age, i.e., over 3 dilata-tions.a The data reported included a sporozoite rateof 0.980% and a human blood index of 10%, whichappears to be an underestimate. Like A. superpictus,A. fluviatilis exhibited exophilic behaviour. Mesghali(unpublished observations, 1968) reported that inJirfot, southern Iran, when the inhabitants weresleeping indoors, 82.6% of the specimens of A. fluvia-tilis caught in outside shelters were found to have fedon man, indicating that they bite indoors and restoutdoors. In the Bandar Abbas area, observationsindicated that the species feeds indoors and out-doors, resting both in houses and in outside shelters.Mesghali noted that in view of the absence ofbaseline information on the behaviour of A. fluvia-tilis and A. superpictus, it is difficult to judge whethernatural exophily played a role in the pattern ofbehaviour encountered after spraying. A. fluviatilistoo is susceptible to DDT, dieldrin and malathion. InSaudi Arabia this species, which has not beenincriminated as a vector, was found to be susceptibleto DDT (23), but resistant to dieldrin.b

In Pakistan, A. fluviatilis is found in the foothillregions of the mountainous tracts. Its role in malariatransmission is not clear although it is known to be avector in the neighbouring countries of Iran andIndia. Bloodmeal smears collected from partiallysprayed human and animal shelters in the Sind plaingave a human blood index of 5.4%. In unsprayedmountainous areas the index was 11.5 % (Akiyama,unpublished reports to WHO, 1968). Malaria wasreported to be hypoendemic in the area dominatedby this species. The classification of abdominal stagesof A. fluviatilis caught by spray capture indicatedthat it is highly endophilic in the mountainous areas.Dissection of 434 females of A. fluviatilis yielded no

a INSTITUTE OF PUBLIC HEALTH RESEARCH, TEHERAN,op. cit.

b PEFFLY, R. L. Dieldrin-resistant Anopheles fluviatilis ineastern Saudi Arabia. Geneva, WHO, 1959 (mimeographeddocument WHO/MAL/239).

sporozoite-positive specimens. In Pakistan the spe-cies was found to be susceptible to DDT.

Anopheles d'thali Patton

This species is widespread in semi-arid parts of theRegion, but was not considered to be a vector ofmalaria until gland infections were recently reported.

In Somalia, Rishikeshc found 1 specimen withsporozoite-positive glands among 14 females of thisspecies dissected. It is not understood why none ofthe A. gambiae females dissected at the same timeshowed any gland infection. Of the 14 femaleA. d'thali, the ovaries of 9 were dissected and 8 werefound to be parous. The parasite rate in the localhuman population was about 20 %. However, preci-pitin tests of 11 bloodmeal smears showed nopositive reaction to human blood. Observationsusing baited nets showed that A. d'thali mainly bitesoutdoors. Its incrimination as a malaria vector hasnot been further confirmed in Somalia.

In Iran, the species is found in association withA. fluviatilis, A. stephensi, and A. superpictus. Glandinfection in A. d'thali was reported by Mesghali(unpublished report to WHO, 1967) and this wasconfirmed by Manoochehri et al. (18). The specieswas repeatedly found infected during 1965-1967. Thesporozoite rates ranged between 1 % and 2.1 %, whilethe human blood index ranged from 1% to 250%depending on the area. A high man-biting densitywas recorded. Age composition showed a parous rateof 11%43 %. A. d'thali was found to rest in bothindoor and outdoor shelters. While it is quitesusceptible to DDT, it showed some resistance todieldrin.

Anopheles sacharovi Favre

The palaearctic species A. sacharovi is a majorvector in the Syrian Arab Republic and in northernIraq, but in Iran it has a more localized distributionin the central, north-western and south-westernareas. At the junction of the Khabur and Tigris riverson the borders of Iraq, the Syrian Arab Republic andTurkey, swampy areas provide A. sacharovi withsuitable breeding places. The biting of peoplesleeping outside during the summer months and thesuspected outdoor resting of A. sacharovi are thoughtto be responsible for the persistence of malariatransmission in this ecologically homogeneous border

C RISHIKESH, N. Anopheles d'thali Patton as a possiblesecondary vector of malaria in the northern region of SomaliRepublic. Geneva, WHO, 1961 (mimeographed documentWHO/MAL/308).

A. R. ZAHAR

area (de Zulueta, unpublished report to WHO, 1967).Larval tests made at Darik, El Haseke Province,Syrian Arab Republic, in the first week of October1965 (Cullen, unpublished report to WHO, 1965),indicated that the species was susceptible to DDT.

Soliman (28) reported that in the Syrian ArabRepublic A. sacharovi was susceptible to DDT anddieldrin in 1958 in unsprayed areas in El HasekeProvince and the Rouge valley, Aleppo Province, inwhich some agricultural pesticides had been appliedin 1952, and house spraying with DDT had com-menced under the malaria eradication programme in1956. In June 1960, tests at Haret el Khaleb, LatakiaProvince, also showed that A. sacharovi was suscep-tible to DDT and dieldrin (Keilany, unpublishedreport to WHO, 1960). Tests by Thymakis (unpub-lished report to WHO, 1963) indicated an increasedtolerance to DDT; mortality after 1 hour's exposureto 4% DDT was 84.6% (26 exposed) at Ras el Ain,El Haseke Province, and 87% (23 exposed) at onelocality in the Ghab area, Orontes valley, HamaProvince. In the latter area, exposure to 4% DDT for2 hours gave complete mortality.

Focal DDT spraying began in the Ghab area in1964 and in 1967 this was replaced by total-coveragespraying. Following a marked increase in malariatransmission in that year, A. sacharovi was collectedin large densities during October in both unsprayedand sprayed premises. Tests made from 3 to29 October (Oddo, de Zulueta, & Keilany, unpub-lished report to WHO, 1967) showed 10.5% mortali-ty with 4% DDT after 1 hour, 0-85 % after 2 hours,and 28.6% after 4 hours. One-hour exposure to 0.4%dieldrin gave 60-78 % mortality and to 0.8% dieldringave 76.4-96% mortality. As the temperature duringOctober 1967 was above 20°C, it was assumed thatprehibernation adaptation was induced rather byphotoperiodic reaction than by temperature, result-ing in high tolerance to insecticides in late October.

Observations were repeated in July and August1968, just before the second round of DDT spraying(Onori & Zahar, unpublished data, 1968). Theaverage mortality obtained with exposure to 4%DDT for 1 hour was 19.1 %, for 2 hours 27.1 %, andfor 4 hours 62.7%. At the time of susceptibilitytesting, sprayed surfaces showed extensive distur-bance from replastering or whitewashing. A. sacharo-vi was found in disturbed and apparently sprayedpremises in fair densities and at different stages of thegonotrophic cycle, mostly on unsprayable surfaces,though a few were collected from sprayed walls. Thenumber of indigenous malaria cases increased pro-

gressively after the first DDT spraying round of1968. Window trap observations in apparentlysprayed and disturbed premises showed that A. sa-charovi leaves the house mainly in the empty andgravid states. The average trap mortality was 18%,while the average biting density per man per nightwas 8 indoors by direct capture and 15 by baited netsoutdoors. The average house resting density variedfrom 6 to 12 individuals per room. Most people inthe Ghab sleep outdoors in summer and A. sacharovienters houses during the early hours of the morningafter feeding outdoors. Thus, A. sacharovi seems tobe largely endophilic in that area.

It was difficult to determine to what extent DDTresistance was responsible for persistence of trans-mission, since large-scale disturbance of sprayedsurfaces occurred after the first spraying round.Observations continued after the second DDT spray-ing round, which was applied in August/September1968. The results of susceptibility tests carried out inSeptember and October did not vary much fromthose obtained before the second round of spray-ing. Spray capture and window trap data indi-cated that an appreciable proportion of gravidA. sacharovi females could still be found in sprayedpremises; they constituted 59-82% of the trapcollection made during the month following thesecond spraying round, with an average trap mortali-ty of about 28 %. House resting and biting densitiestended to increase after a brief reduction followingthe second round. The presence of such densities,with high survival in window trap catches, showsthat the response to the second DDT round wasunsatisfactory. Supporting epidemiological evidenceindicated that transmission persisted in the area afterthe second round despite a sharp reduction in thenumber of cases brought about by mass drugadministration (22). When susceptibility to 0.8%dieldrin was tested in August 1968, complete mortali-ty was obtained after 1 hour's exposure, but tests inSeptember and October showed a few survivors atthis exposure (Chang & Keilany, unpublished reportsto WHO, 1968). This small survival was attributed toprehibernation tolerance. On the basis of the aboveinvestigations it was decided to replace DDT withdieldrin, and commencing in 1969 the areas of DDTresistance received 2 spraying rounds of dieldrin peryear.

This regime drastically reduced the density ofA. sacharovi, as measured by different methods ofcapture following dieldrin spraying, and tests with0.80% dieldrin on small insect samples resulted in

434

MALARIA VECTORS IN THE EASTERN MEDITERRANEAN 435

either complete mortality or only an occasionalsurvivor. With a small batch of A. sacharovi tested inSeptember 1971 there was, for the first time, 25%survival after 1 hour's exposure to 0.8% dieldrin.Tests during July and August 1972 (Keilany, unpub-lished reports to WHO, 1972) demonstrated withoutdoubt a pronounced dieldrin resistance in A. sa-charovi. The mortality after 1 hour's exposure to 4%dieldrin was below 10% and there was little differ-ence between the mortalities obtained with dieldrinconcentrations ranging from 0.8% to 4%.

Anopheles stephensi Liston

The oriental malaria vector A. stephensi is presentover a fairly large area in the northern and easternparts of the Region. A. stephensi mysorensis has beenidentified in the Eastern Province of Saudi Arabia(23) and in southern Iran.a

In Iran, Iraq, and Saudi Arabia A. stephensi isresistant to DDT and dieldrin. The status ofresistance in this vector and its operational signifi-cance were reviewed by Chang & Ungureanu.b AsDDT residual house spraying proved still able tocurtail the severe malaria epidemic that occurred inIraq and Iran in 1962-1963, DDT residual sprayingwas reinstituted in the A. stephensi area of southernIran and Iraq in combination with other measuressuch as surveillance and larviciding operations, in aneffort to interrupt malaria transmission. The suscep-tibility level of A. stephensi to DDT was checkedperiodically and routine estimation of house restingdensity by spray capture continued. The results fromsouthern Iraq were reported by de Zulueta et al.(31). Susceptibility tests carried out in 1965 and early1966 indicated no further increase of the resistancelevel of A. stephensi. It was only in November 1966that an extremely low kill was recorded. The aver-age mortality obtained after 1 hour's exposure to4% DDT was 1% and 10.2% respectively in the Faoand Shatt al Arab areas of southern Iraq. Evenexposure to 4% DDT for 4 hours in Fao Mamlahadid not give more than 2.5% mortality. This localityhad received 3 rounds of DDT spraying with

a MOFIDI, M. H. Resistance of Anopheles stephensi toinsecticides in Iran. Teheran, Institute of Parasitology andMalariology, 1962 (mimeographed document Teheran IPM978.6.1962).

b CHANG, T. L. & UNGUREANU, E. M. Insecticide resist-ance in Anopheles stephensi and its operational importance.In: UNGUREANU, E. M. & HAWORTH, J., ed. Insecticideresistance in major vectors of malaria and its operationalimportance in malaria eradication programmes. Geneva,WHO, 1965 (mimeographed document WHO/MAL/482.65).

excellent coverage. The great increase in the resis-tance level coincided with a marked increase ofA. stephensi densities in Basra Liwa. Room densitiesduring August, September and November 1966 weresome 10-29 times those recorded during the corre-sponding months in 1965. The species spread beyondits normal limits of distribution in the country andwas found as far away as Kurkuk Liwa in the northof Iraq.The possibility that several forms of A. stephensi

existed in southern Iraq and Iran, having a differentpotential for malaria transmission, was consideredby de Zulueta et al. It was noted that in the Fao areatransmission had persisted since the reintroductionof DDT house spraying in 1964, whereas in otherareas the species existed but transmission had beeninterrupted or had continued at a very low rate.Laboratory investigations carried out at the RossInstitute of Tropical Hygiene, London, using dif-ferent strains of A. stephensi, produced no evidenceof hybrid sterility among 5 populations originatingfrom India (Delhi), Iraq (Fao Mamlaha, Gezira andBaghdad) and Iran (Kazeroun). It was also suspectedthat more than one type of DDT resistance mightexist in A. stephensi populations in southern Iraq.Crosses made at the Ross Institute indicated thatresistance in colonies from Gezira and Fao Mamlahawas genetically identical. From selection studies, theauthors considered that the changes in the pattern ofresistance of this species to DDT in southern Iraqmight be explained by the existence of genes ancillaryto the oligogene common to all populations studied.Absolute homozygosity for all genes does not appearto have been reached, as indicated by the increasedmortalities recorded in the same areas of southernIraq in 1967, which continued to be sprayed withDDT.

Assessment of the malaria situation in southernIraq indicated an almost equal parasite incidencethroughout 1965-1967, during which period thehouse-resting density of A. stephensi was generallylow except in 1966. DDT spraying continued during1968 with no appreciable reduction of malariatransmission. In fact, in that year a malaria outbreakoccurred in a group of villages in Basra Liwa. Anentomological investigation was carried out duringOctober 1968 in villages where indigenous cases hadrecently been recorded (Zahar, unpublished report toWHO, 1969). The spraying coverage in the area wasestimated during the investigation to be about 84%.In sprayed rooms, A. stephensi was captured fromunsprayed surfaces but some were found resting on

436 A. R. ZAHAR

sprayed surfaces. The average densities of A. ste-phensi were 5.2 per sprayed room and 6.7 perunsprayed room. Susceptibility tests showed 26.5 %mortality with 4 hours' exposure to 4% DDT amongspecimens collected from unsprayed shelters. Twonights of window trap collections showed that themaximum exodus of A. stephensi from sprayedhouses took place 2-3 hours after sunset. Gravidfemales constituted a large proportion of trapcollections, indicating that the mosquitos werecompleting their gonotrophic cycle in the sprayedpremises. The average density per trap per night was10 A. stephensi. Mortality after a 24-hour holdingperiod in unfed and fed females was 30% and 14%respectively. At the same time, the parous raterecorded in samples collected from sprayed premiseswas 53 %. Assuming that the gonotrophic cycle was2 days, the probability of daily survival was about0.726. During dissections, a number of females werefound to have 3-6 dilatations, confirming thatA. stephensi had a high survival rate within sprayedpremises. For comparison, a parous rate of 600%,giving a probability of daily survival of 0.775, wasrecorded in an unsprayed urban area in central Iraqwhere transmission had recurred. This figure is veryclose to that estimated for the DDT sprayed area.

In view of the above results, it was decided toreplace DDT with malathion in Basra Liwa.Observations throughout 1969-1972 showed a goodresponse under malathion spraying, and A. stephensihas become very scarce except where refusals weremet with or operational defects occurred. Thesupporting epidemiological evidence reported toWHO indicated that transmission has been almostinterrupted. In 1968, a small area comprising 2 vil-lages was sprayed with propoxur. Indigenous casesstarted to appear shortly after the second sprayinground, giving the impression that transmissioncontinued even though A. stephensi could not befound by daytime capture, bait capture, or larvalsearches. However, observations throughout 1969confirmed that these cases were relapses that possiblyhad not received radical treatment previously andthat transmission in the area had in fact beeninterrupted by propoxur spraying.

In Iran, data collected by Kazeroun ResearchStation before spraying in Kazeroun area a showedthat the average density of A. stephensi per room was200 and that from June to October the density was

a INSTITUTE OF PUBLIC HEALTH RESEARCH, TEHERAN,op. cit.

higher in human habitations than in stables. Thespecies was observed resting on clothes and strawmaterial and occasionally on walls. From October toDecember, mosquitos were often found in stables.They were occasionally collected from pit shelters.However, A. stephensi is known to be largelyendophilic. In longevity studies, 4.4% of A. stephensidissected were found to have at least 3 dilatationsand therefore to be at a potentially dangerous age.The sporozoite rate recorded was 0.51 %. Precipitintests showed a human blood index of 24%. When2 humans and 1 animal were used in a magoon trap,A. stephensi showed a maximum human bloodpreference of 47% and a minimum of 5 %.

Continual evaluation of DDT spraying in 1965-1967 showed that the resistance of A. stephensi toDDT was increasing, and that transmission persistedin southern Iran as in southern Iraq. Malathion wastherefore tried in Iran, first of all on a village scale. In1967, it was decided in the littoral and plain areas tospray DDT in one round in the spring and malathionin a second round later in the year. According to aprogress report from the Institute of Public HealthResearch, Teheran,b A. stephensi density in thecoastal area, despite the DDT spraying in the spring,showed a steady increase from June until September.Persistence of transmission was observed in a villagein the coastal area, where the density of A. stephensiwas 15.2 per room and the proportion of dangerousfemales had reached a maximum in September 1967.Dissection of 136 A. stephensi females gave asporozoite rate of 1.47 %. At the same time, 10 casesof Plasmodium vivax infection were detected in thevillage. In October, after applying malathion, amarked reduction in house-resting density wasobserved. However, since seasonal changes inter-vened, it was difficult to draw a firm conclusion onthe success of the application of malathion inSeptember and October.

In 1968, the regimen of spring DDT and autumnmalathion spraying rounds was repeated, though thelatter spraying was advanced to start in mid-August.Through the period 1965-1968, susceptibility tests onA. stephensi showed a steady deterioration, mortalityfalling in 1968 to 15.7% after 1 hour's exposure to4% DDT. High parous rates were recorded duringAugust (68.8 %) and September (79.3 %) in 1967,with a probability of daily survival of 0.83 and 0.89

b INSTITUTE OF PUBLIC HEALTH RESEARCH, TEHERAN.Progress report on investigations and research on malariaepidemiology and malaria education in Iran. Teheran, 1967(Publ. Inst. Pub. Hlth Res., Teheran, No. 1604).

MALARIA VECTORS IN THE EASTERN MEDITERRANEAN

respectively before malathion was applied in October1967. At the same time, the mortality in window trapcollections was not more than 7 %. The parous ratesof 55% and 58% recorded in July and August 1968during the period following DDT spraying werelower than before. There was a slowly rising trend inthe monthly parasite incidence, but at a lower levelthan in the years when only DDT was applied. Spraycatches indicated that the density of vectors in houseswas generally low; no mosquitos were captured innight catches or by window traps. It was concludedthat under the regimen of 2 annual DDT sprayingrounds, there was always a marked building up of thedensity of A. stephensi combined with increasinglongevity, which led to persistence of transmission ata fairly high rate. Under the DDT and malathionregimen, there was a definite shortening in the periodof vector activity and high mosquito density, result-ing in a much lower rate of transmission. Malathionreduced the A. stephensi population drastically and itwas suggested that in view of the increase in the levelof DDT resistance, it would be better to replaceDDT entirely with malathion (Zahar, unpublishedreport to WHO, 1969). According to recent reportsfrom Iraq and Iran, A. stephensi remains susceptibleto malathion in areas where spraying with thisinsecticide is in progress.

Quraishi et al. (24) made observations on flightrange in Iran by releasing P32-labelled A. stephensi.Since the number of recaptures was very small andvariations were numerous, catches could be takenonly as indicating a rough trend. The number ofmosquitos recaptured was markedly lower at 3-5 kmfrom the point of release than at 1-3 km. Both malesand females were able to fly 1.8 km overnight. Onefemale was caught in a village 2.8 km from the pointof release within 16 hours of release. In the course ofthe observations, an attempt was made to determinethe daily mortality. This could only be done for thefirst 6 days because too few marked mosquitos wererecaptured thereafter. An attempt was also made tostudy the duration of the gonotrophic cycle.

In Pakistan, A. stephensi occurs in varying den-sities in association with A. culicifacies. In the urbanarea of Karachi, Husain & Talibi (12) reportedmonthly dissections carried out from 1947 to 1951,during which a total of 23 223 A. stephensi weredissected for gland infection and 9 617 of these werealso examined for gut infection, in both cases withnegative results. Afridi et al. (1) showed thatA. stephensi mysorensis occurs in the Karachi,Sukkur and Hyderabad zones, though the type form

was either absent or, if present, occurred in suchsmall numbers that it could not be detected.Rahman & Muttalib (25), investigating the malaria

situation in Karachi city, reported a spleen rate of upto 34.3 % and a parasite rate of 15.5%. A. stephensiand A. subpictus were the only anophelines theyencountered either as adults or larvae in the differentparts of the city surveyed. They found 1 femaleA. stephensi with sporozoites among 204 dissectedduring July-August 1966 in Karachi. Further dis-sections made by Muttalib and Akiyama (unpub-lished reports to WHO, 1966 and 1967) of 505A. stephensi and 2 015 A. subpictus collected from thecity revealed 6 gland infections (1.18%) in A. ste-phensi and none in A. subpictus. In April 1967,1 gland infection was recorded from 328 dissectionsof A. stephensi.

Susceptibility tests carried out with A. stephensi inKarachi city in 1967-1968 indicated resistance toDDT, but at a much lower level than in Iran andIraq. The mortality recorded on exposure to 4%DDT for 1 hour ranged from 32.5 % to 80% and for2 hours from 76% to 92%.

Information on A. stephensi in rural areas ofPakistan is given in the section on A. culicifaciesbelow.A species found at Ras Gharib on the Gulf of

Suez, Egypt, was identified as A. stephensi by Gad(5). The identification was checked by Dr P. F.Mattingly of the Department of Entomology, BritishMuseum (Natural History), London, who found itresembling A. dancalicus Corradetti, although he wasinclined to consider it as being slightly aberrantA. stephensi. Breeding sites and the ecologicalconditions in the locality where the species was foundwere described by this author. The susceptibility ofits larvae to DDT, dieldrin, lindane, and malathionwas noted by Gad & Kamel (6). There has been noevidence of malaria transmission in the area. How-ever, control of breeding places by oil larviciding wasintroduced and no material could be obtained forcrossing experiments with known strains of A. ste-phensi to confirm the mosquito's identity. A. ste-phensi has also been recorded in the northern part ofthe United Arab Emirates (see under A. culicifacies).

Anopheles culicifacies Giles

The oriental species A. culicifacies is the principalmalaria vector in Pakistan, where it is widelydistributed. It has been connected with the unstabletype of malaria. Throughout the rural areas of

437

438 A. R. ZAHAR

central and southern Pakistan, it is commonlyassociated with A. stephensi. Prespraying observa-tions showed that the 2 species are found throughoutthe year. A. culicifacies appears in high density inApril, declines in May-June, but increases againfrom July-August to reach a peak in September-October. A. stephensi density declines in July butincreases again in August, reaching a peak inSeptember. The lowest densities of the 2 vectors areusually encountered during December-February.When the malaria eradication programme began in1961, DDT residual house spraying was successful indrastically affecting the densities of both vectors. Theepidemiological results were satisfactory, so thatmany zones were switched to the consolidationphase. The 2 species, which are endophilic, werefound to be absent or scarce in properly sprayedhouses after the application of DDT. However,reports to WHO showed that high densities of bothspecies were encountered wherever there were opera-tional defects, necessitating the continuation ofDDTspraying in some areas. Records of susceptibilitytests carried out in 1962 indicated that A. culicifacieswas susceptible to DDT. However, resistance startedto appear from 1964 onwards in both species indifferent zones, and throughout 1967-1972 morerecords ofDDT resistance in both A. culicifacies andA. stephensi were obtained. This resistance reached ahigh level in most zones although the generally smallsample size in the tests of some 50-60 mosquitos oreven less has not permitted conclusions to be drawn

on the resistance level in the mosquito population asa whole (unpublished reports to WHO). No specialinvestigations have been carried out to determine thepractical implications of this resistance. However,the epidemiological situation has been studied inareas where malaria transmission has recently flaredup. Because of the high level of DDT resistance inboth vectors in many areas, HCH has been triedextensively in the North-West Frontier Provincein 1972-1974. Recent susceptibility tests with dieldrinhave indicated that resistance to cyclodiene insecti-cides has appeared, and a suitable alternative insecti-cide is being sought.

In 1968, a survey was carried out in the northernpart of the United Arab Emirates, previously knownas the Northern Trucial States (Zahar, unpublishedreport to WHO, 1969). A. culicifacies s.l.a inassociation with A. stephensi was found in highdensities, and was connected with a high endemicityof malaria, the crude parasite rates ranging from15% to 49%. The parasite formula showed 68.5%Plasmodium fakciparum, 22.4% P. vivax and 9.1 %P. malariae. A. culicifacies and A. stephensi werefound breeding in wells-the only source of water-and cement basins used for water storage in therural areas.

a The identification of this species was checked byDr M. T. Gillies, who reported that the form appears to beintermediate between the nominate subspecies and thesubspecies adenensis but suggested that for the time being itshould be referred to simply as A. culicifacies s.l

ACKNOWLEDGEMENTS

The author thanks all those national and internationalworkers whose valuable contributions in unpublishedreports to WHO have added to our knowledge of theecology of malaria vectors in the Eastern MediterraneanRegion.He also thanks: Mr J. Hamon and Dr B. de Meillon,

the organizers of Section B2 of the Eighth InternationalCongresses on Tropical Medicine and Malaria, Teheran,Iran, 7-15 September 1968, for their comments on the

paper, which was originally prepared in somewhat differ-ent form for that meeting; Dr M. T. Gillies, for checkingthe identification of samples of anophelines collected inthe area previously known as the Northern Trucial States;and Dr S. C. Edwards, Public Health Administrator(Malaria), WHO Regional Office for the Eastern Mediter-ranean Region, Alexandria, Egypt, for his helpful sugges-tions.

RIESUMtL'ECOLOGIE DES VECTEURS DU PALUDISME DANS LA REGION OMS

DE LA MEDITERRANEE ORIENTALE: REVUE DE LA QUESTION

L'auteur passe en revue la documentation disponiblesur 1'ecologie de 15 vecteurs du paludisme de la RegionOMS de la Mediterranee orientale.

Les renseignements presentes se rapportent surtout a laperiode &oulee depuis 1956, date du lancement du pro-gramme de lutte ou d'eradication dans cette Region.

MALARIA VECTORS IN THE EASTERN MEDITERRANEAN 439

Les donn&es concernant l'etude epidemiologique de lasituation du paludisme et l'evaluation des mesures d'at-taque du point de vue entomologique sont tirees destravaux publi6s a ce sujet ou de rapports non publiesadresses a l'OMS. Des indications sur le degre de sensi-bilite aux insecticides des vecteurs du paludisme, et surle comportement et la mortalite des populations de vec-teurs ayant fait l'objet de mesures d'attaque, sont egale-ment fournies dans cette analyse qui renseigne en outre

sur l'indice d'anthropophilie, la preference trophique etla longevite des vecteurs. Les informations relatives achaque espece sont plus ou moins completes, selonl'importance des recherches entomologiques effectueesdans les diverses zones, mais l'article a le merite de faireapparaitre les lacunes de nos connaissances sur l'ecologiedes vecteurs, ce qui devrait inciter les chercheurs a pour-suivre leurs observations ou a entreprendre de nouvellesinvestigations.

REFERENCES

1. AFRIDI, M. K. ET AL. Identification of the races ofA. stephensi in the Federal Karachi area by measure-ment of the ova. Pak. J. Hlth, 8: 71-76 (1958).

2. BARBER, M. A. & RICE, J. B. A survey of malaria inEgypt. Amer. J. trop. Med., 17: 413 (1937).

3. FARMI, M. A. The implications of Anopheles sergentifor malaria eradication programmes east of theMediterranean. Bull. Wid Hlth Org., 15: 821-828(1956).

4. FONTAINE, R. E. ET AL. The 1958 malaria epidemic inEthiopia. Amer. J. trop. Med. Hyg., 20: 795 (1961).

5. GAD, A. M. Anopheles stephensi Liston in Egypt,UAR. Mosquito News, 27 (2): 171 (1967).

6. GAD, A. M. & KAMEL, 0. M. (1967) Further notes onA. stephensi in Egypt, UAR. J. Egypt. publ. HlthAss., 42: 249-252 (1967).

7. GRAMICCIA, G. Anopheles claviger in the MiddleEast. Bull. Wld Hith Org., 15: 816-821 (1956).

8. HALAWANI, A. A. & SHAWARBY, A. A. Malaria inEgypt. J. Egypt. med. Ass., 40 (11): 753-792 (1957).

9. HARIDI, A. Partial exophily of Anopheles gambiaespecies B in Kashm Elgirba area in eastern Sudan.Bull. Wld Hlth Org., 46: 39-46 (1972).

10. HARIDI, A. Inheritance of DDT resistance in spe-cies A and species B of the Anopheles gambiaecomplex. Bull. Wld Hlth Org., 47: 619-626 (1972).

11. HORSFALL, W. R. Mosquitos. London, Constable,1955.

12. HUSAIN, M. Z. Y. & TALIBI, S. A. Incrimination of thevector of malaria in Federal Karachi area (Pakistan).Pak. J. Hlth, 6: 65 (1956).

13. KRAFSUR, E. S. Estimation of the theoretical dailysurvival rate in some malaria vectors in a lowlandregion of Ethiopia. Parassitologia, 12: 47 (1970).

14. KRAFSUR, E. S. Malaria transmission in Gambela,Illubabor province. Ethiop. med. J., 9: 75 (1971).

15. London School of Hygiene and Tropical Medicine.Anopheles and malaria in the Near East. London,Lewis, 1950 (Memoir No. 7).

16. MAcDONALD, G. The epidemiology and control ofmalaria. London, Oxford University Press, 1957.

17. MACDONALD, G. & GOECKEL, G. W. The malariaparasite rate and interruption of transmission. Bull.Wld Hith Org., 31: 365 (1964).

18. MANOOCHEHRI, A. ET AL. Anopheles dthali Patton,1905, a new secondary vector in southern Iran. Ann.trop. Med. Parasit., 66: 537 (1972).

19. MATrINGLY, P. F. & KNIGHT, K. L. The Mosquitosof Arabia. I. Bull. Brit. Mus. (Nat. Hist.) Ent.,4 (3): 89 (1956).

20. O'CONNOR, C. T. The distribution of anophelinemosquitos in Ethiopia. Mosquito News, 27 (1): 42(1967).

21. OMER, S. M. & CLOUDSLEY-THOMPSON, J. L. Survivalof female Anopheles gambiae Giles through a nine-month dry season in Sudan. Bull. Wld Hlth Org., 42:319-330 (1970).

22. ONORI, E. Experience with mass drug administrationas a supplementary attack measure in areas of vivaxmalaria. Bull. Wld Hlth Org., 47: 543-548 (1972).

23. PEFFLY, R. L. I,nsecticide resistance in anophelines inEastern Saudi Arabia. Bull. Wld Hlth Org., 20: 757-776 (1959).

24. QURAISHI, M. ET AL. Flight range, lengths of gono-trophic cycles, and longevity of P32-labelled Ano-pheles stephensi mysorensis. J. econ. Ent., 59 (1): 50-55 (1966).

25. RAHMAN, M. & MUrrALIB, A. Determination ofmalaria transmission in central part of Karachi cityand incrimination of A. stephensi as the vector. Pak. J.Hlth, 17: 73-84 (1967).

26. RIsHIKESH, N. Anopheles pulcherrimus Theobald(1902) as probable vector of malaria in Iraq. Bull.Endem. Dis., 13: 7-13 (1972).

27. SINGH, P. & GAD, A. M. Susceptibility to DDT ofmalaria vectors, Jordan. Bull. endem. Dis., 3: 182(1959).

440 A. R. ZAHAR

28. SOLIMAN, A. A. Determination of the insecticidesusceptibility level for A. sacharovi of Syria, UAR.In: Proceedings of the Fourth Arab Science Con-gress, Cairo, UAR, February 1961. Cairo, 1961,pp. 531-540.

29. WARD, R. A. Mosquitoes of Afghanistan-Anannotated checklist. Mosquito Systematics, 4: 93-97(1972).

30. ZAHAR, A. R. Review of status of anopheline

resistance to residual insecticides in the EasternMediterranean Region. In: Proceedings of the Re-gional Symposium on Insect Resistance to Insecti-cides, 11-13 May 1959, Cairo, UAR. Cairo, UNESCOMiddle East Science Cooperation Office, 1960,pp. 19-46.

31. ZULUETA, J. DE ET AL. Recent observations oninsecticide resistance in Anopheles stephensi in Iraq.Mosquito News, 28: 499-503 (1968).