i IitsecL Sci. Applicofion, Vol. 1, No. 4, pp. 319-338, 1981. 0191-9040/8 1/040319-20E02.00/0 , \ 2 Printed in Great Britain. Pergamon Press Ltd.

BIOLOGY AND CONTROL OF CULEX PIPIENS Q UlNQUEFASCIATUS" SAY, 1823 (DIPTERA, CULICIDAE) WITH SPECIAL REFERENCE TO AFRICA

R. SUBRA International Centre of Insect Physiology and Ecology (ICIPE), Coastal Field Station, P.O. Box 80804, Mombasa, Kenya

(Received 20 October 1980)

Abstract-This paper is an attempt to synthesize information available on C. p. quinquefasciatus in Africa. The latter is presently found in most urban areas of the African continent and in rural settlements which show some trends towards urbanization. In East Africa, and the islands of the Indian Ocean, C. p. quiriquefasciatus is one of the major natural vectors of Wuchereria bancroftti. In addition it can also transmit, under laboratory conditions, some other pathogenic agents. Preimaginal forms develop in different kinds of man-made breeding-places, especially those containing polluted water. The situation in each African region is reviewed in detail. Female behaviour during the different phases of the gonotrophic cycle is analysed, together with population dynamics. Control methods by synthetic insecticides are discussed in relation to resistance problems and the characteristics of the breeding sites. Other control methods based on the use of growth regulators, genetic manipulation, biological agents (parasites and predators) and environmental management have been investigated as well. Most of them cannot be easily applied or are not yet applicable for control operations.

Key Words: Culex pipiens qui~iquefasciatus,Africa, distribution, role in public health, preimaginal stages, adult mosquitoes, chemical control, insecticide resistance, alternative control methods

RésumLCet article est un essai de synthèse des informations concernant C. p. quiilquefasciatus en Afrique. Ce moustique se rencontre actuellement dans la plupart des zones urbaines du continent Africain et également dans de nombreuses zones rurales presentant certains caractères d'urbanisation. En Afrique de l'Est et dans les îles de l'Océan Indien, C. p. quinquefasciatus est l'un des vecteurs majeurs de la filariose de Bancroft. En laboratoire il peut également transmettre d'autres maladies. Ses formes préimaginales se développent surtout dans des gîtes à eaux polluées; d'origine anthropique. Les situations propres à chacune des grandes régions Africaines sont passées en revue. Le comportement des femelles au cours des différentes phases du cycle gonotrophique et la dynamique des populations sont analysés en détail. Les moyens de lutte par l'emploi d'insecticides de synthèse sont examinés en relation avec les pro- blèmes de résistance et la nature des gites larvaires. I1 existe d'autres possibilités de lutte, basées sur l'utilisation de régulateurs de croissance, de méthodes génétiques, d'agents biologiques (parasites et prédateurs) et sur l'aménagement de l'environnement. Cependant la plupart d'entr'elles sont difficilement applicables ou non encore opérationnelles.

Mots Clés: Culex pipiens qiJiHqUefaSCiatUS, Afrique, répartition, rôle en santé publique, formes pré- imagínales, adultes, lutte chimique, résistance aux insecticides, lutte non chimique

INTRODUCTION The sanitation problems inherent in the rapid urbanization taking place in some of these regions for scientific and the efforts Of the health services it has not yet become possible to effec- the last few decades have been only partially over- tively control certain tropical diseases whose causal come by the responsible departments. This applies agents are transmitted by one or more arthropod especially to the disposal of waste-water in open drains, species. In the case of some of these diseases, the situ- which constitutes an ideal breeding place for Culex ation has even become (GRATZ,1974a). This pipiells quinquefasciatus~One Of the main vectors Of applies to bancroftian filariasis, whose incidence is bancroftian filariasis. For this and other reasons that increasing every year. The prospects in regard to this will be considered later, this mosquito is present in disease are not encouraging, particularly in Asia and vast numbers in most tropical cities, creating a vector or pest control problem everywhere. Africa, its Africa (MATTINGLY' 1974b; In 1974). prevalence may well extend filariasis transmission to all the cities south of the Sahara (HAMONet al., 1967), thus creating throughout the whole continent a situ- *~~~~~~l~culex IRIVANA- ation similar to that now present in the coastal areas KARN and WHITE,1978) of East Africa and in certain towns south-west of the 0. R. S. T. Q. M. Foads Bircumentaire 319

Este : 320 R. SUBRA

Indian Ocean. In addition to rural filariasis (trans- represented only a small percentage of the culicid mitted most often by Anopheles spp. or sometimes by fauna, though in Accra (Ghana) MACFIEand INGRAM both Anopheles spp. and C. p. quinquefasciatus), urban (1916) found this subspecies in 14.86% of all positive filariasis transmitted by C. p. quinquefasciatus could larval collections in domestic water containers. After become established throughout the continent. C. p. the Second World War, the number of places where it quinquefasciatus seems capable of invading the whole became the prevalent species increased considerably. environment in town or country as a result of changes This phenomenon seems to have accelerated during caused by the habits of the population and various the last 20 years, and today C. p. quinquefasciatus is aspects of modern life (CHINERY,1968; SUBRA,1975). the dominant if not the sole species of mosquito in For that reason, all aspects of the study of this mos- most of the urban areas in West Africa. It is found quito are of primary importance in order to better only very sporadically in rural environments. In Cen- understand how to control it most effectively. The tral Africa, C. p. quinquefasciatus was known in some present review is an analysis of information available localities at the beginning of the century and became on this subject as a whole. common before 1940, particularly along the Congo River. In subsequent years it spread widely, becoming prevalent in a large number of urban areas and also GENERAL CONSIDERATIONS in certain large villages in the Cameroons, though this does not seem to be the general rule as yet; recent Distribution surveys in the Central African Republic showed that Geographical distribution. C. p. quinquefasciatus is it was still only present in the big towns, a situation widely distributed in the tropical and subtropical similar to that found in West Africa. The situation in areas of the world; it has been found in the southern East Africa is quite different, particularly in the coas- United States (in the Nearctic Region) and in the tal areas and in certain islands of the Indian Ocean. southern part of Japan (in the Palearctic Region). The first authors to study the insect fauna of this area In the case of Africa, Culex pipiens pipiens and C. p. at the beginning of the century remarked upon the quinquefasciatus are both present. While C. p. pipiens rapid expansion of this species in the Mascarenes has a limited distribution, usually in mountainous (D’EMMEREZDE CHARMOY,1908-1909) and Zanzibar areas, more rarely at low altitudes (Mauritania and (ADERS,1917). Since that time, C. p. quinquefasciatus Cameroon) (HAMONet al., 1967), C. p. quinquefasciatus has become even more widespread in these regions. is now a very common mosquito over most of the Here its distribution is not restricted to urban areas African continent, although its presence in the north as it is also very abundant in a number of rural locali- of Africa seems to be debatable. KNIGHTand MALEK ties. Usually this occurs in large villages which are (1951) did not encounter it during a study of the constructed on a town-like pattern, several hundred Culex pipiens complex in the Cairo region, nor did houses built along streets and lanes, and where a cer- VERMEIL(1955) in Tunisia. However GAABOUBet al. tain percentage of the population is no longer (1971) tested the susceptibility to insecticides of larvae engaged in traditional activities, such as farming and of the C. pipiens collected 20 miles (32 km) from Alex- fishing. As in most tropical towns, space is limited in andria and assigned them to the C. p. quinqziefasciatus the centre of these localities; thus people have tio dig subspecies. On the other hand, C. p. quinquefasciatus pit latrines and cesspools to eliminate waste and used is widespread in the Ethiopian region, i.e. on the Afri- water. In small villages of around 10 or so scattered can continent south of the Sahara (HAMONet al., houses, there is little problem of waste elimination, 1967) and in the neighbouring islands: Madagascar, and C. p. quinquefasciatus remains rare or completely the Mascarenes and the Comoro Archipelago absent, finding no breeding places to support it. (BRUNHES,1975), the Seychelles and the Chagos The case of the Seychelles deserves special atten- Archipelago in the Indian Ocean (LAMBRECHT,1971), tion. In these islands, C. p. quinquefasciatus was rela- Sa0 Tome and Fernando-Po in the Gulf of Guinea, tively uncommon even as recently as 25 years ago, and the Cape Verde islands in the Atlantic (HAMONet and was concentrated round Port Victoria, the capital al., 1967). (MATTINGLYand BROWN,1955). Some 15 years later, C. p. quinquefasciatus occurs in all climatic zones, LAMBRECHT(1971) found it was abundant throughout ranging from forest to semi-desert. Altitude does not the Archipelago, where it had colonized not only its seem to limit its distribution, since it has been found classical larval habitats but other less suitable types as as high as 2770 m in India (BHAT,1975) and at 2130 m well. Thus C. p. quinquefasciatus was successful in in Sri Lanka (ABDULCADERet al., 1965). However, it is adapting to an environment where only a short time not generally found at such a high altitude and the before it occupied only a relatively restricted habitat. upper limit of its altitudinal distribution in other In East Africa, as in West Africa, C. p. quinquefas- regions is said to be at about 1600m, e.g. 1680m in ciatus densities do not seem to have stabilized. In an the South Pacific (DOBROTWORSKY,1967) and 1600 m analysis of data from 1954 to 1971 in Dar es Salaam, in Réunion (HAMONet al., 1967). for example, they have been shown to be increasing The distribution of C. p. quinquefasciatus in conti- more or less steadily each year as observed by BANG nental Africa deserves special attention since it has et al. (1973b). changed considerably during the last few decades. Relationship to human environment. The distribution Only a summary will be given here, since this has and density of C. p. quinquefasciatus in tropical Africa been the subject of reviews by HAMONet al. (1967) are therefore two constantly evolving phenomena for and SUBRA(1975). In West Africa, before the Second which different explanations have been suggested. World War, C. p. quinquefasciatus was known only in Here again reference is made to the reviews an the a few seattered localities, mainly on the coast where it subject by SERVICE(1966), HAMONet al. (1967) and Biology and control of Culex pipiens quinquefasciatus 321

SUBRA(1975). Apart from the development of rapid Australian region, where the periodic form of Wucher- modes of transportation which promote the dispersal eria bancrofi is encountered (CHOW,1973). of C. p. quiilquefasciatus (HIGHTONand VANSOMEREN, So far as Africa soutkof the Sahara is concerned, 1970) though not its establishment, there are two the vector role of C. p. quiiiquefasciatus has been essential reasons which lead to the rapid multipli- demonstrated in East Africa by NELSONet al. (1962) cation of this mosquito: the utilization of insecticides and WHITE(1971a). Similar observations have been and rapid urbanization. The excellent results obtained made in the islands of the south-west Indian Ocean with organochlorine insecticides for the control of by BRUNHES(1975) and in the Seychelles by LAM- medically important insects led to their use in many BRECHT (1971). The situation in Central Africa is not tropical areas. Unfortunately, however, C. p. quinque- clear, since there has not been any adequate recent fasciatus, which is less susceptible to these compounds work. However, in 1964 COSTAMOURAO discovered than many other species, soon became highly resistant in C. p. quiiiquefasciatus females on Sao Tome the to them. In as much as species like Culex iiebulosus sausage-shaped forms of filariae, suggesting that the and Culex cinereus with which it was formerly in risks of transmission in nature in this area are quite competition for larval breeding places had been elim- serious. In West Africa, where the spread of this inated by the insecticides, C. p. quinquefasciatus was mosquito is comparatively recent (after the end of able to make use of the newly available sites (SERVICE, the Second World War), a considerable amount of 1966). Furthermore, the number of such breeding research has failed to demonstrate that this species places has considerably increased with the growth of plays any role at all in the transmission of filariasis towns and poor sanitation. In Africa, the natural (SUBRA,1973 ; BRENGUES,1975). Various laboratory population increases and subsequent growth in size of observations on the other hand demonstrated that towns has often been compounded by large migratory microfilariae could develop up to the infective stage in movements of people to the cities, which has led to Upper Volta (SUBRA,1965) and in Nigeria (OGUNBA, the overcrowding of numerous quarters. The sanita- 1971), but with low infection rates. In Liberia the sus- tion services in most cases have been unable to deal ceptibility of C.p. quinquefasciatus to Wuchereria ban- adequately with this influx of people. The disposal of crofti has been found to be only 28% as high as that the various types of waste has been left partly to the of the anophelines (MAASCH,1973). This could explain initiative of the inhabitants themselves, who have why C. p. quinquefasciatus is not yet a natural vector often dug poorly constructed, insanitary latrines or in this area (BRENGUES,1975; KUHLOW,1976). The soakage pits. C. p. quinquefasciatus has therefore been susceptibility of this mosquito to W. bancrofti seems able to colonize easily all those breeding places which to be under the control of at least two genetic factors insecticides had previously cleared of possible (ZIELKEand KUHLOW,1977). In addition, BRENGUES competitors. (1975) found a different intensity of infection between Urbanization is often accompanied by an abandon- strains which can be differentiated by cytoplasmic ment of the traditional way of life in favour of differ- incompatibility. ent habits and the amenities provided by the modern In addition to bancroftian filariasis, C. p. quinque- world. Thus detergents are now used on a large scale fasciatus was found to be infected with Chikungunya by numerous African housewives. Such products in virus during an epidemic that occurred in 1953 in waste-water could also well play a part in eliminating southern Tanzania (quoted in WHITE,1971b). More species in competition with C. p. quinquefasciatus, recently in Senegal, WILLSet al. (1976) demonstrated which itself tolerates high levels of pollution and the presence of hepatitis B virus on the mouthparts of seems to adapt easily to these new type of habitat. these mosquitoes. Reovirus type 3 can be picked up This would partly explain the recent expansion of by C. p. quiiiquefasciatus larvae and it is maintained breeding of this mosquito in those urban areas where through the pupal stage to the first days of adult life. there has never been any insecticide spraying and It could also be an important vector of Rift Valley where it has remained susceptible to organochlorine fever virus: in Egypt this virus has been isolated from insecticides (SUBRA,1973). mosquito specimens collected in the home of a RVF patient (WHO, 1978). In India, C. p. quinquefasciatus can be one of the Public health importance of C. p. quinquefasciatus as a vectors of West Nile virus (RAo, 1975), and in the disease vector Americas it can transmit St. Louis encephalitis virus A distinction will be drawn under this heading (GILLET,1972). It also is of importance in veterinary between diseases which C. p. quinquefasciatus is medicine, since in Australia it is the main vector of known or presumed to carry, and diseases whose cau- fowl pox virus (LEEet al., 1958). sal agent may be maintained or may develop in this In the laboratory. In Madagascar, BRYGOOand mosquito, but only in the laboratory. SUREAU(1962) found that poliomyelitis virus persists In nature. C. p. quinquefasciatus plays a major role for 24 hr without losing its virulence in C. p. quinque- in the transmission of bancroftian filariasis. It has a fasciatus hatched from larvae raised in aquaria con- more restricted role as a vector of viral diseases of taining the virus. In 1946 the species was suspected by man and animals. GALVEZGOMEZ (1947) of being responsible for the In most tropical areas where C. p. quinquefasciatus transmission of poliomyelitis virus in Havana. Its role became established several decades ago, it transmits as a vector of this virus had not been directly demon- filaria in the towns and in areas where urban life has strated, the author basing his hypothesis merely on led to the creation of its favourite larval breeding the fact that the number of cases were localized near places. This is also the case in the neotropical and C. p. quinquefasciatus breeding places and the number oriental regions (HAWKING,1973) and in part of the decreased after those breeding places had been elimin-

I.$ A. 1/44 322 R. SUBRA ated. This mosquito can also transmit the yellow fever female larvae hatch out simultaneously. However, the virus in the laboratory as was demonstrated by Mus- duration of the larval stages in the males (about PRATT (1956) in South Africa. Nevertheless, C. p. quin- 118 hr) is shorter than that in the females (about quefasciatus does not seem to play a role either in the 135 hr) while the reverse is true for the pupal stage. In natural transmission of yellow fever as stated by this Africa, field studies by SUBRA(1973) at Bobo Diou- author or in the epidemiology of Burkitt's tumour lasso showed that the average time elapsing between (MCCRAEet al., 1968). oviposition and hatching ranged from 24 to 36 hr. Laboratory work in other regions of the world has The larval stage lasted between 6 and 8 days and shown that C. p. quinquefasciatus was also mechani- pupal stage about 40 hr. The wide range of the incu- cally able to transmit smallpox virus, which it could bation and larval periods observed by SUBRA(1973) harbour for about 72 hr (SARKARet al., 1973). In the may be due to temperature differences of the larval same way, it can transmit Wesselbron virus (SIMA- breeding places in various types of soakage pits: a SATHIEN and OLSON,1973) and Venezuelan equine en- difference of several degrees was observed between cephalitis virus (KRAMERand SCHERER,1976). On the surface water at ground level and that deep down in other hand, multiplication of rubella virus (TESHand the pits. ROSEN,1975) or the trans-ovarial transmission of La C. p. quinquefasciatus develops mainly in habitats Crosse virus (TESHand GUBLER,1975) does not occur. containing highly polluted water rich in organic Nuisance role. In addition to its role as a vector of matter that the larvae can use for nourishment. Thus pathogenic agents, C. p. quinquefasciatus frequently food supply is a factor which can be disregarded in causes considerable annoyance to people exposed to most cases, since food is usually available in excess in its constant biting, particularly when they cannot their numerous breeding places. A shortage of food afford to buy mosquito nets. Thus in Bamako (Mali) obviously leads to a low production of pupae in the SUBRAet al. (1965) observed several hundred bites per breeding places concerned. SUBRA(1973) reported on man per night indoors by this species. This situation one such breeding place where daily pupal production is common in most large African towns. Its effects are was only 20 or so pupae, even though the daily aver- difficult to measure, but there is no doubt that the age of stage I larvae which hatched was something loss of sleep involved reduces the productivity of like 35,000. The effects of the amount of nourishment numerous workers. In this way, therefore, it has available in the breeding places are reflected not only economic repercussions. in the number and size of the pre-imaginal forms but also in the size of the adults, which are larger when a greater amount of nourishment is available (KURI- BIOLOGY HARA, 1963; SUBRA,1971a, b). Types of larval breeding places. While the pre- Eggs imaginal stages of C. p. quinquefasciatus develop C. p. quinquefasciatus eggs are laid in the form of mainly in polluted water, a study of the literature rafts which can float on the surface of the water. At on this mosquito throughout the world shows that the time of laying, they are whitish but they darken though waste-water represents the main breeding within a few hours. An average of 155 eggs per raft sources, the larvae can develop in virtually any type was observed by SUBRA(personal observation) in East of breeding place found in the human environment. Africa, but there may be very important variations Most breeding sites are of medium size (a few cubic from one female to another. Generally, females that metres) or small (a few litres), and the species can have fed on birds lay a greater number of eggs than develop in either sunny or shady places. The classifi- those that have fed on man (KRISHNAMURTIand PAL, cation adopted here for these larval breeding sites is 1958). based on their location in relation to human dwell- In tropical countries, hatching usually occurs one ings. There are two main categories: man-made and day after egg-laying. Nevertheless, in some cases, the naturally occurring breeding places which cover all crossing of two different strains gives no offspring the tropical areas of the world where C. p. quinquefas- because of cytoplasmic incompatibility which results ciatus has been found. The situation in Africa will be in the death of the embryo in the egg. It is usually discussed in more detail below. uni-directional : crosses between two strains are fertile (a) Man-made or nian-modijied larval breeding in one direction but sterile in the other. In some cases places. These are by far the most important and (less common) it may be both ways, crosses being depend on man for their establishment. sterile in both directions. Breeding places in highly polluted water. In this group latrines are the most widespread type of breed- Larvae ing place in most countries. In flat areas, they may Larval development. The two main factors that often be excavated down to the underground water- regulate mosquito larval growth are nutrition and the table, particularly in high-rainfall regions where the temperature of the water in the breeding places table is very close tco the surface. The water mixed (CLEMENTS,1963). In the southern United States dur- with excreta therefore constitutes a highly polluted ing the coldest months, pre-adult life lasts 48 days on environment perfectly suited to C. p. quinquefasciatus the average (HAYES,1975). In the tropics, it is much larvae. Furthermore, since latrines are usually pro- shorter. In Rangoon, where the mean temperature tected against heavy rainfall, which may flood other varies little throughout the year, DE MEILLONet al. breeding places, their production of larvae during the (196713) studied the duration of the different stages. rainy season continues practically uninterrupted. At a temperature around 28"C, the egg incubation Relatively slight fluctuation in the water table usually period is approximately 27hr, and the male and gives them a great stability; in regions with a marked Biology and control of Culex pipieiis quiilquefasciatus 323 dry season the level of the underground water-table rainy season and act as mosquito breeding places dur- may fall below that of the latrines, which then cease ing that time of the year. In towns, old tyres, which to be favourable breeding places for C. p. quinquefas- often accumulate in large numbers, constitute impor- ciatus. tant breeding places for Ae. aegypti and C. p. quinque- Soakage pits are designed to collect waste washing fasciatus. In seaside communities, abandoned canoes and cooking water. These consist of holes dug in the fill with rainwater, and sometimes provide breeding ground to varying depths, sometimes filled with places for both these species. pebbles. Most are accessible from the outside, as the (c) hidustrial and agricultural breeding places. covered top is rarely completely sealed or mosquito- Waste-discharge channels at sugar or sisal-processing proofed. Heavy rain may cause the pits to overflow, factories may enable the development of large providing less stable breeding places than latrines. numbers of the aquatic forms of C. p. quinquefasciatus. Unlike latrines, however, they contain water through- The organic pollution usually found in the breeding out most of the year and represent actual or potential places of this species is supplemented here by a breeding places over a longer period. In quarters chemical pollution to which the larvae seem well where housing is modern and of good quality, septic adapted. tanks form the main breeding places. They maintain C. p. quiriquefasciatus larvae may sometimes de- high culicid densities almost uninterruptedly through- velop in irrigation channels but these are of secondary out the year. importance. Breeding places in unpolluted or slightly polluted (d) Natural larval habitats. Natural sites are usually water. These sites allow mosquito breeding during small and C. p. quinquefasciatus is often found breed- most or all of the year. A distinction will be drawn ing with other species. By themselves, they doubtless between fixed receptacles (usually very large) and contribute quite small adult numbers; but they can- smaller (usually domestic) containers. not be disregarded in campaigns designed to interrupt In the absence of polluted water for breeding, C. p. disease transmission. Three categories of breeding quinquefasciatus can utilize sites containing limpid place have been observed which differ greatly from water used for domestic needs of the population. In each other in origin and structure: tree-holes, crab the Maldives, the 20,000 existing wells represent the burrows, and coral rock-holes. most important C. p. quinquefasciatus larval habitats Some authors have collected C. p. quinquefasciatus (IYENGAR,1952; VELIMIROVICand CLARKE,1975). In larvae from brooks, but if these watercourses have the Indian subcontinent, C. p. quinquefasciatus is been polluted from man-made sources, they should be present in rural areas where it develops in wells used placed in the previous category. for irrigation (YASUNOet al., 1975). The case of tanks The situatimi in Africa. Madagascar. At Tananarive and cisterns in Grand Comoro, in which C. p. quin- in the uplands, C. p. quinquefasciatus is very abundant quefasciatus larvae are also encountered, will be dealt in polluted water (CHAUVETand RASOLONIANINA, with later. 1966, 1968), particularly in the lower part of the town Small receptacles or containers represent a very where the water-table rises to ground level during the widespread type of breeding place in all tropical areas rainy season. Larvae have been gathered from latrines of the world. In regions where the inhabitants still and from pools with water contaminated by various pursue a traditional way of life, water for domestic types of rubbish, particularly excreta from pigs use is stored mainly in earthenware jars which may (SUBRA,personal observation). They are also found in hold up to several dozen litres. In more modern numerous containers used for storing domestic water environments, these easily breakable jars are often re- and in various peridomestic breeding places, often in placed by metal containers with a capacity of as much company with Aedes dbopictus Skuse, 1894. The same as 200 1. When the water is changed irregularly, or at situation applies in coastal towns. However, on the too great intervals (several weeks), mosquito larvae west coast of Madagascar, C. p. quinquefasciatus is can develop therein. C. p. quinquefasciatus and Aedes associated with Ae. aegypti instead of with Ae. albo- aegypti can be found in such containers. pictus. C. p. quiiiquefasciatus has also been collected (b) Peridoniestic breeding places. Ditches and from tree-holes by BRUNHES(personal communi- gutters designed to take away rain-water in towns cation) in Tananarive and by SUBRA(personal obser- frequently become breeding places for C. p. quinque- vation) in the southern part of the island. During fasciatus if not properly cleaned. The organic detritus surveys throughout the country, only a few soakage that accumulates pollutes the water often to a very pits were seen in Majunga. Such pits do not, there- high degree, and furthermore prevents the normal fore, seem to be important breeding places for C. p. flow, thus providing excellent conditions for larval de- quinquefasciatus in Madagascar as a whole. velopment. In some regions, brooks and ponds are The species is absent from those rural areas with used as municipal tips where human and animal low human densities where people are still living excreta are also discharged. When pollution reaches according to old traditions and do not have any prob- its peak, these ponds favour intense breeding of C. p. lem of water or waste disposal. In the south of Mada- quinquefasciatus (COLLESS,1957). gascar, which suffers from serious water supply prob- Also in this category are breeding places in which lems, C. p. quinquefasciatus is found in various water- water is not highly polluted. They consist of various storage containers and other peridomestic breeding used containers thrown away through negligence or places. Investigations carried out by the author in rice lack of sanitary education of the inhabitants. They fields near the big tovns did not reveal any C. p. may be the remains of jars, empty tins, bottles, broken quinquefasciatus. metal cans, broken coconut husks, bamboo stalks, The Mascarenes and the Seychelles. In the case of -and shells. These containers fill up with water in the the Mascarenes, it is difficult to make a distinction 324 R. SUBRA between urban and rural environment. In places can also be colonized by C. p. quinquefasciatus Réunion, C. p. quinquefasciatus has long been found in (HARRIS,1942; VANSOMEREN et al., 1955). The species . all the inhabited zones, and it can be collected from even develops in rice fields in the interior: SURTEES most types of breeding places including crab burrows (1970) gathered specimens in rice-growing areas in (HAMONet al., 1967). In 1950, it was particularly greater numbers than in unmodified ecosystems. abundant in the waste-water from sugar factories CHANDLERand HIGHTON(1975), when sampling (HAMON,1953a). newly hatched adult mosquitoes in the rice fields, In the Seychelles, C. p. qzrinqzrefasciatus is found in found among them males and females of this species. all types of domestic and peridomestic breeding Finally, in East Africa, C. p. quinquefasciatus larvae places already described; and also in tree-holes, rock- can develop in certain natural habitats such as holes, cut bamboo, pools next to rice fields, and leaf banana leaf axils (TEESDALE,1941) or tree-holes (VAN axils (LAMBRECHT,1971). SOMERENet al., 1955). Although Ae. aegypti and Ae. Comoro Archipelago. In Grand Comoro, a volcanic simpsoni larvae were found breeding in coral rock- island of recent origin, polluted water and surface holes, C. p. quinquefasciatus was not found in that water are almost non-existent because of the high per- type of site either in Tanzania (TRPISet al., 1971) or in meability of the soil. C. p. quinquefasciatus develops in Kenya (TRPIS,unpublished report). all the containers used for storing water (cisterns, Central Africa. In the urban environment, metal cylinders and wash bowls) as well as in peri- numerous C. p. quinquefasciatus have been collected domestic breeding places. It has also been found in in the classical polluted-water breeding places in the hollows of trees (BRUNHES,1975). Zaire (HENRARDet al., 1946), in southern Cameroon In Mayotte, on the other hand, waste-water is (MOUCHETet al., 1960), in Angola (RIBEIROand generally common in the human environment and MEXIA,1966) and in the People’s Republic of the soakage pits are constructed for its disposal. Further- Congo (HAMONet al., 1967). more, during the rainy season the water-table rises In Central Africa, breeding sites with only slightly sufficiently to reach the latrines. There are therefore polluted water or natural sites are usually not colo- two types of highly productive C. p. quinqzrefasciatus nized. In Angola, RIBEIROand MEXIA(1966) only very breeding places. Their distribution is not uniform, but rarely found C. p. quinquefasciatus in artificial or depends on the ethnic origin of the people concerned natural breeding places. On the other hand, in Sa0 (SUBRAand HEBRARD,1975). The nature of the village Tome it is frequent in various containers and is also site also affects the productivity of the breeding places found in the hollows of trees or the axils of certain (BRUNHESand DANDOY,1973). To these purely man- leaves (COSTAMOURAO, 1964). In Zaire, it was present made breeding sites, must be added the mouth of 40 years ago breeding in crab-burrows (WANSON, coastal streams, which are often used as public tips. 1935). At certain times of the year, the mouths are West Africa. In urban areas of the savanna zones, obstructed by sand bars and represent excellent C. p. the main larval breeding places of C. p. quinquefas- quinquefasciatus breeding sites. Other breeding places ciatus at the end of the rainy season are soakage pits, for this species have been described by SUBRAand ditches filled with polluted water and gutters (SER- HEBRARD(1975) and BRUNHES(1975). Water jars VICE,1966; CHINERY,1969, 1970; SUBRA,1971a, 1973). inside dwellings do not contain mosquito larvae, since In Bobo Dioulasso, the present author found that the water is changed daily. latrines seemed to play an insignificant role, even at In the other islands, Moheli and .Anjouan, the situ- the end of the rainy season. In more humid climatic ation is similar to that of Mayotte except that in zones (lower Guinea), C. p. quinquefasciatus was found Anjouan, coastal streams are less common than in in septic tanks (TOUMANOFFet al., 1956). In Accra, Mayotte. septic tanks and concrete water tanks constituted im- East Africa. In the coastal regions of East Africa, portant perennial breeding places (CHINERY,1970). In and in Zanzibar, the same types of breeding place are eastern Nigeria, pots and drums used for cassava found both in the towns and big villages. In Mom- fermentation can support considerable breeding of basa (TEESDALE,1959) and also in smaller towns in this species (IWUALA,1979). Kenya (WIJERSand KIILU,1978), latrines are the most In rural areas polluted-water breeding places are common breeding places. A rather similar obser- very rare. Twenty years ago in the southern part of vation has been made in Zanzibar (MANSFIELD-ADERS,Nigeria, C. p. quinquefasciatus was not yet found in 1927) and in continental Tanzania (WHITE, 1967, domestic water containers. It was also absent from 1971b; MENUand KILAMA,1972; BANGet al., 1975). certain natural breeding places such as tree-holes Soakage pits also provide breeding places for C. p. (SURTEES,1959), although DUNN (1927) had made quinquefasciatus (ADERS, 1917; TEESDALE,1959; similar observations but found the species in a few WIJERSand KIILU, 1978), although in some localities crab-holes in the region of Lagos and Ebute Metta. in north-east Tanzania, larvae were not found (KOL- More recently, it was also found colonizing crab-holes STROP,personal communication). A noteworthy case in Accra (CHINERY,1969). was observed by WIJERSand KIILU(1978), in which Discussion. An examination of the various types of latrines received waste-water in the absence of soak- C. p. quinquefasciatus breeding places in the Ethiopian * age pits and therefore mosquito larvae developed for faunal region as a whole shows two differences: the a longer time than breeding places supplied only from types of larval habitats in urban and rural areas are the water-table. Waste-water from sisal factories is not always identical, and the particular types of im- particularly suitable for the development of C. p. quin- portant breeding place vary in degree of infestation in quefasciatus larvae. different regions of the continent. There is a relation- Various containers and peridomestic breeding ship between the establishment and breeding of C. p. Biology and control of Culex pipiens quinquefasciatus 325

quinquefasciatus and its vectorial capacity. Where the mean sterility, for KITZMILLER(1959) has described species has been established for a long time, it is cases of parthenogenesis in C. p. quiilquefasciatus in present in all environments and is an effective vector the laboratory. of W. bancrofti. Where it has only recently become In the laboratory in Upper Volta, this period established, it is restricted to urban areas and is still between emergence and the first blood-meal was only a potential vector. This suggests that, in the found to be 60 hr by examination of the ovarioles of future, West and Central Africa may witness a spread nulliparous females. However, in nature, it is believed of C. p. quiilquefasciatus to the rural areas followed by to be only about 48 hr (SUBRA,1972a). the beginning of transmission of W. bancrofti. The blood-meal. Endo-exophagy. Anthropophilic mosquitoes feeding at night, bite man either inside dwellings (endophagy) or outside (exophagy). It may Adults happen that certain individuals of the same species After first describing the various phases of adult facultatively feed indoors and others outdoors. mosquito life, the work particularly concerned with Furthermore, this behaviour may differ from one each of those phases will be reviewed. Most of the region to another. In South-East Asia, at Bangkok, observations involve essentially the females, which are SASAet al. (1965bj, observed that most females of C. p. of more public health interest than the males because quinquefasciatus fed indoors. DE MEILLONand SEBAS- of their role as vectors. TIAN (1967a) had observed the exact opposite in Ran- Phases ofadult life. After leaving the breeding place goon, where the exophagous tendency predominated. where their pre-imaginal development has taken place The results recorded in Africa seem to show more adults usually fly for a short distance (rarely more uniform behaviour of C. p. quinquefasciatus, which is than 100 m). By 24 to 36 hr later, most of the females markedly endophagous in the Comoro Islands will have been fertilized and will then take a blood- (BRUNHES,1975), in East Africa (VANSOMEREN et al., meal at quite a stable rhythm. After the blood has 1958; SMITH, 1961; VAN SOMERENand FURLONG, been entirely digested, and the eggs have formed, they 1964) and in West Africa (SUBRA,1972b). In Mayotte will be laid on the surface of various bodies of water in the Comoro Islands, BRUNHES(1975) observed that generally of man-made origin. A period of from a few the percentage of endophagous females could vary hours up to a half a day will elapse between oviposit- according to locality. In Bobo Dioulasso, endophagy ion and the next blood-meal, which will be the begin- was more marked during the cold season, when the ning of the next gonotrophic cycle. difference between lower and upper extreme tempera- Adult activities before the first blood-meal. Equal tures was greater (SUBRA,1972b). numbers of males and females continuously emerge Biting cycle. The large majority of female C. p. quin- from the breeding sites but there are nevertheless two quefasciatus feed at night. When they bite man it is peaks, one before sunset and the other, which is very mainly below the knee if the person is sitting, or on marked, between 20.00 hr and 21.00 hr (DE MEILLONet any part of the body if he is lying down (SELFet al., al., 1967~).Before adults leave the larval breeding 1969). Similar observations have been made by other place, a rest phase of varying length occurs when they authors studying the biting cycle of endophagous will rest on the banks of ditches or sides of the con- females. Most biting specimens were collected after tainer. It is followed by a mass departure of the males midnight in the Comoro Islands (BRUNHES,1975), in and females at nightfall (YASUNOand HARINASUTA,East Africa (VAN SOMERENet al., 1958; TEESDALE, 1967). DE MEILLONet al. (1967cj have demonstrated 1959; SMITH, 1961; VAN SOMERENand FURLONG, that in these flights there are two categories of indi- 1964) and in West Africa (SUBRA,1972b). In Réunion, vidual: some aged a few hours, which have emerged however, HAMON(1965) observed most bites in the during the day and during the emergence peak pre- first part of the night. This discrepancy with the ceding sunset, the others older, originating from the results of other authors might be due to the marked day before the hatching peak of 20.00 hr to 21.00 hr, fall in temperature during the night, which led to a which leave the breeding place the following day. In decrease in the number of females seeking a blood- regions where the seasons are more distinct than in meal. SUBRA(1972b) and BRUNHES(1975), who each the tropics, the females emerge in larger numbers than collected several thousand specimens, place the peak the males during the colder months (HATS, 1975). more precisely between 01.00hr and 02.00hr. The Mating does not take place immediately after leav- maximum number of bites outside dwellings occurs in ing the larval breeding place, but occurs 36 to 48 hr some instances at the same time as indoors (SMITH, after emergence according to YASUNOand HARINA- 1961) and sometimes earlier (BRUNHES,1975). In SUTA (1967) or even later (72hr) according to the Bobo Dioulasso exophagous females sometimes bite laboratory observations of SEBASTIANand DE MEIL- earlier and sometimes at the same time as endopha- LON (1967). These two groups of authors observed gous females, depending on the season of the year that it took place mainly before and after sunset. (SUBRA,1972b). Their age only occasionally seems to Usually, the females are fertilized before their first affect the biting cycle of C. p. quinquefasciatus females. blood-meal, but sometimes fertilization occurs when Among specimens that feed away from dwelling the females have already taken blood (YASUNOand places, there is no difference between parous and nul- HARINASUTA, 1967). Climatic conditions may liparous females at any season. In endophagous influence the time of fertilization. In India, it takes females and only in the rainy season, a majority of place at all seasons when the females are 2 to 3 days parous individuals has been observed at the beginning old, except during the winter when it is sometimes and end of the night. This special behaviour of the delayed up to the sixth day after hatching (YASUNOet parous females during the rainy season might be con- al., 1972). Absence of fertilization does not necessarily nected with their oviposition rhythm (SUBRA,1972b). 326 R. SUBRA

Host preferences. While most authors (HAMONand (agreement between the number of blo’od-meals and MOUCHET,1967) agree that C. p. quinquefasciatus is the number of ovipositions) Is the general rule. Just anthropophilic, the host preferences of that mosquito two cases of autogeny in C. p. quinquefasciatus have have been the subject of numerous investigations, been reported from Africa, one by MICHELat Thies in often with contradictory results, in the different parts Senegal (in HAMONet al., 1967), the other by BUSHROD of its area of distribution. This applies also to Africa, (1978) in Tanzania. Autogenesis has not been demon- where MATHIS(1935) described C. p. quinquefasciatus strated in the laboratory in Dakar (MATHIS,1935), in as highly ornithophilic, whereas the majority of Sierra Leone (THOMAS,1956) or in Bobo-Dioulasso authors, both in West Africa (Sierra Leone, THOMAS, (SUBRA,1972a). As for the pre-gravid phase said to 1956; and Upper Volta, SUBRA,1970) and in East indicate gonotrophic discordance, it has been ob- Africa (HEISCHet al., 1959, and CHANDLERet al., 1975, served in West Africa but involved only a limited in Kenya; WHITE,1971% in Tanzania) have agreed number of cases-less than 10% of the specimens that it is anthropophilic. studied (SUBRA, 1972a). Thus knowledge of the The degree of this anthropophily, moreover, varies duration of the gonotrophic cycle can be used for according to the place where fed females are trapped, determination of chronological age. and C. p. quinquefasciatus may be attracted by various The duration of digestion of the blood-meal has types of bait (LEEet al., 1954). Catches carried out been studied during the rainy season in the laboratory inside occupied dwellings provided a larger percent- and in the field at Bobo Dioulasso, Upper Volta age of anthropophilic females than those out of doors. (SUBRA,1972a). In the laboratory, the author used Thus, in Upper Volta, 98% of the females captured nulliparous females and found that digestion pro- inside dwellings had fed on man, as against 1.3% on ceeded at approximately the same rate whatever the birds and 0.7% on various mammals. On the other time of the blood-meal. In all specimens it was com- hand, with females captured outdoors, the percentage pleted by 60 hr, in some it required only 48 hr. The of anthropophilic specimens was only 73%, while results of field trials using specimens marked with the ornithophilic proportion was 20.9%, and those fluorescent powder confirm these observations. Ovi- feeding on various mammals (particularly dogs) position, if it is not delayed by the taking of a non- accounted for 6.1% (SUBRA,1970). However, here also blood-meal, occurs a few hours after completion of as in Rangoon (DE MEILLONand SEBASTIAN,1967b), maturation of the ovaries, at least in the rainy season. anthropophily still predominated, whereas in north- The blood-meal following oviposition occurs within ern Nigeria the percentage of females that had fed on just a few hours. different host species was greater than the percentage The first gonotrophic cycle would therefore appear of anthropophilic females (SERVICE,1965). These data, to last a minimum of 5 days, the second 3 days, and however, were based on a few dozen specimens only. the subsequent ones 4 days or more, since old parous The practical consequences of host selection are females require a longer time than primiparae. seen in differences in fertility (see section on ‘Biology’, Oviposition. Oviposition cycle. If there are no atmos- subsection ‘Egg’). pheric disturbances, sunrise and sunset are the pre- Non-blood-meals. The taking of meals other than ferred times for oviposition in C. p. quinquefasciatus blood has been discussed by only a few authors, females as observed at Rangoon in South-East Asia although in this species it may affect the length of the (DE MEILLONet al., 1967e) and in Bobo Dioulasso in gonotrophic cycle and hence its vectoral capacity and West Africa (SUBRA,1971b). In the latter case, the population dynamics. DE MEILLONet al. (1967d) most important peak was at sunset. Several authors demonstrated that feeding on sugar-water delayed who have studied other mosquito species estimate oviposition but also reduced daily mortality. These that variations in luminosity trigger off the oviposit- authors discovered this phenomenon under natural ion reflex. However, luminosity does not seem to be conditions, and established that C. p. quinquefasciatus the only factor determining the oviposition cycle since has a feeding cycle on sugarcane. The specimens col- DE MEILLONet al. (1967e) demonstrated a relation- lected under these circumstances included not only ship between the date of the blood-meal and the date newly emerged mosquitoes but also older ones. of oviposition. Under the humidity and temperature Similarly, in Upper Volta, SUBRA(1970) caught conditions in which these authors were working, the parous females that had taken a non-blood-meal. The sunset peak corresponded to females which had taken proportion of this type of female was much higher a blood-meal after midnight 3 nights before, while the outdoors than inside dwellings. There seemed to be sunrise peak corresponded to the females which had no such difference in nulliparous females. taken a blood-meal before midnight 2 nights earlier. The gonotrophic cycle. In the past, the concept of In Bobo Dioulasso, fluctuations in the number of ovi- the gonotrophic cycle has been interpreted in two positions made daily could not be precisely linked ways. The present author accepts the definition of with any other phenomenon (SUBRA,1971b). BEKLEMISHEV(in DETINOVA,1963) who believed that Chemical factors determining selection of ouiposition the gonotrophic cycle was the period between two sites. On the whole, C. p. quinquefasciatus females do successive ovipositions (or the period between emer- not oviposit at random in all potential breeding gence and oviposition in the case of nulliparous places, but only in those which contain certain females). This interpretation makes it possible to de- attractive substances. IKESHOJI(1966) showed that termine the chronological age of females in which the breeding-site water contained a factor attractive to number of ovipositions is known and to calculate the gravid female C. p. quinquefasciatus and stimulated average duration of the gonotrophic cycle. Determi- oviposition. In 1968, the same author separated by nations of this kind are obviously possible in anauto- gas chromatography four compounds that are attract- genous females and if gonotrophic concordance ive to C. p. quinquefasciatus females. Later, IKESHOJI Biology and control of Culex pipiens quiiiquefasciatus 321 and MULLA(1970a) demonstrated that this mosquito known hitherto. Thus, it seems that in its classical sometimes responded positively to attractants pecu- environment, an inhabited region, C. p. quinquefas- liar to other species. ciatus rarely flies more than a few hundred metres. In the field in Upper Volta, SUBRA(1971b) tested However, this distance does not represent potentiali- the attraction of various potential breeding places in ties inherent in the species which, in an uninhabited the human environment in Bobo Dioulasso, and ob- area, can travel much further. served that the water in soakage pits attracted the The distances covered may be influenced by the largest number of gravid females. Furthermore, he wind (FUSSELL,1964) and by climatic conditions. found in the laboratory that the attraction of certain YASUNOet al. (1973) found that C. p. quiiiquefasciatus of these pits varied from season to season. In particu- moved faster and covered a greater distance in the hot lar, some negative breeding places in the dry season rather than in the cold season. Study of sexual differ- were much less attractive than the positive ones. The ences has led to contradictory results. According to absence of pre-imaginal specimens could be ascribed, FUSSELL(1964) and YASUNOet al. (1973) sex does not at least in part, to the lack of attractiveness for the affect the distance covered, but LINDQUISTet al. (1967) females of the water in these breeding places. found that females had a greater flight range than Structure of the breeding place deterinining selection males. of ovipositioiz sites. The chemical composition of the In Africa, in Réunion, HAMON(1953a) estimated water in larval breeding places is not the only factor that C. p. quinquefasciatus could fly a distance of 8 km that determines the selection of oviposition sites by by relating the densities observed at a given point to gravid C. p. quiiiquefasciatus females. The structure of the nearest breeding place capable of producing such the breeding places also plays an essential part. In numbers of mosquitoes. Movements in urban and Rangoon, DE MEILLONet al. (1966) placed pans con- rural environments were studied in Bobo Dioulasso, taining water from larval breeding places at different Upper Volta, with the help of insects marked with levels (from ground level to 2m), and the number of fluorescent powders (SUBRA,1972a). In the urban en- ovipositions was greater near ground level. In Upper vironment, it was found that there was a preferred Volta, SUBRA(1971b) using as a model the natural direction of travel for males and females. No satisfac- breeding places (soakage pits) studied the influence of tory explanation could be found for this' phenomenon, three factors: volume of water, distance between the which in any case does not seem to be the general surface of the water in the breeding places and ground rule, since YASUNOet al. (1973) observed uniform dis- level, and the degree to which the opening into the persion from the release point. In Bobo Dioulasso, breeding places was obstructed. For an equal surface males covered between 400 and 500m, whereas the area, breeding places with the most water attracted females could fly up to 1 km. The distance travelled the largest number of ovipositions. The number of by females seems to be related to their state of nu- ovipositions was greater, the further below ground trition, since the greatest distances were covered by level and surface of the water. Finally, females unfed females, some of which flew for several hundred oviposited more readily in breeding places with an metres following emergence. In rural areas, the unobstructed entrance than in those in which it was females covered greater distances at a greater speed obstructed. than in urban areas-up to 3.5 km from the release Flight range. Research on this topic has not been point (SUBRA,1972a). very extensive and most of it has been done in South- Resting places. As already stated, some C. p. quin- East Asia. Most of the papers referred to here are quefasciatus females have an endophagic behaviour concerned with studies using marked mosquitoes and others an exophagic. In the same way, some released at various points. Large differences (ranging specimens choose resting places inside dwellings, from a few hundred metres to several kilometres) in while others find shelter outdoors. The tendency of the flight range of C. p. quiiiquefasciatus have been mosquitoes to stay inside dwellings will be called recorded by the various authors who have dealt with endophily, and the opposite tendency exophily, this question. In reality, these facts are more intellig- although it should be made clear that during the ible and easier to interpret if they are considered in gonotrophic cycle the same female may exhibit both relation to the environment in which the test mos- tendencies. quitoes were released-urban, rural or uninhabited. Numerous studies have been carried out on endo- In Rangoon (Burma), LINDQUISTet al. (1967) esti- philic mosquitoes, undoubtedly because they are mated the flight range of C. p. quinquefasciatus at easier to catch. In this category, adults of both sexes 1 km. In the same city, SELFet al. (1971) later made a rest inside dwelling places by day. In Upper Volta, more or less identical estimate, mosquitoes flying a SUBRA(1970) observed that males were significantly greater distance being the exception. In fact, most more numerous in huts with corrugated iron roofs specimens fly less than 500 to 600 m from the point of than in those with roofs of dried mud, the difference release. In uninhabited areas, on the other hand, mos- perhaps being due to the climatic conditions prevail- quitoes are able to fly for several kilometres (ARIDI ing in the two types of houses. No such difference was and MAJID, 1938). YASLJNOet al. (1975) captured found in females. While the proportions of the differ- nearly 8% of the marked mosquitoes at 1km from the ent stages varied with the type of house studied or the release point. These authors worked in a situation series of observations concerned, in every case it was half-way between the two examples quoted above: recently fed females that made up the largest propor- they released the mosquitoes in an uninhabited area tion of the specimens caught. The physiological age of but near a village in the New Delhi region. However, these females varies from one season to another. in the same region in a rural area BROOKSet al. (1976) Unfed females, on the other hand, always include a recorded a distance of 11 km-much greater than any high proportion of nulliparous specimens, which indi- 328 R. SUBRA cates that newly emerged insects use dwellings as between rainfall and the peak breeding periods. A shelters. single peak corresponds to a single rainy season (West Outside dwellings, there are numerous shelters Africa and the Comoro Islands), while two peaks cor- where C. p. quinquefasciatus adults take refuge (DE respond to the two rainy seasons (East Africa). MEILLONet al., 1967a; SUBRA,1970). In Upper Volta, The differences between maximum and minimum metal shelters such as cans and cabins of lorries, seem densities are generally very great. Thus, in West particularly attractive to males. Furthermore, speci- Africa, mean densities in the rainy season are often 10 mens of both sexes were caught in unoccupied houses, times as high as in the dry season (SUBRA,1973). Simi- sheds and hen-coops, in jars, and in dry wells. The larly, in the Comoro Islands, BRUNHES(1975) found large catches made by SUBRA(1970) in dry wells an almost complete absence of the species during the showed that recently fed females represented the dry season in Grand Comoro and in some villages in smallest part of the population present in that type of Mayotte. This was not, however, a general phenom- shelter, pnfed females and gravid specimens were the enon, since in other villages, according to the same more numerous. These unfed females, as in the case of author, the reduction observed is only by a half the endophilic mosquitoes, consist mainly of nulli- between the two seasons; this difference is doubtless parous specimens which seem to shelter in wells after due to the nature of the breeding places and sites of leaving the breeding places where they emerged. the villages studied. On the basis of the above data, it is possible to sketch an outline of the behaviour of C. p. quinqziefas- CONTROL ciatus adults during the different phases of the gono- trophic cycle. The mosquito generally spends only a General background few hours in the vicinity of the breeding place from C. p. quinquefasciatus is a species that has proved which it emerged. It then makes one or more flights, difficult to control in many areas although the use of which take it to another shelter either inside a house insecticides has given satisfactory results in many or outdoors. When they reach the appropriate age, instances. This species has shown a relatively high the females take their first blood-meal, mostly inside tolerance to DDT and other organochlorine com- dwellings where they then pass the first few hours pounds (BROWNand PAL, 19731, thus requiring appli- after the blood-meal. Most of them then leave the cation of high doses of the pesticides. dwellings and digestion is completed outdoors in The increasing resistance to organochlorine insecti- some shelter. Exophagic females, once they have cides and then to certain organophosphorus insecti- taken a blood-meal, undergo their gonotrophic cycles cides has restricted the use of these compounds and in in the outdoor shelters already mentioned. Some may some cases has led to a return to petroleum larvicides even enter inhabited houses after biting man or ani- which had been abandoned when organochlorine mals outside. In any case the females, whether endo- compounds were originally introduced. New sub- philic or exophilic, carry out a series of movements by stances (chemosterilants, growth regulators and over- day and night, throughout their gonotrophic cycle crowding factors) have also been tested, particularly (DEMEILLON and KHAN,1967). in the laboratory, as have new methods of control Population dynamics. Most of the data on seasonal (genetic and biological, the use of parasites and preda- fluctuations of C. p. quinquefasciatus adults have been tors); but very few trials have been carried out on the based on human-bait catches, since the results African continent. Environmental improvement and obtained by other methods may lead to conclusions integrated control through a combination of several of doubtful validity. methods have produced positive results and appear to In Upper Volta, peak female densities in urban be the most promising solution to .the problem of areas have been recorded in the rainy season and at controlling C. p. quinquefasciatus. the beginning of the dry season (SUBRA,1973). The same applies to rural areas, where the species is, how- Methods of control ever, very much less common (HAMON,1963). In Chemical control. Synthetic insecticides. In the years northern Nigeria, near Kaduna, peak densities occur following the Second World War, the use of orga- at the beginning of the rainy season (SERVICE,1963). nochlorine insecticides spread throughout Africa and The coastal areas of East Africa have two rainy the islands of the Indian Ocean. However, few data seasons, one in April and May and the other, less are available on the successive or alternative use of important and less constant, from October to the compounds involved. In general, the periods of December. In the town of Mombasa in Kenya, TEES- maximum utilization and effectiveness of these insecti- DALE (1959) observed two periods of peak densities, cides fall within the years 1950 to 1960, while the during and after these two rainy seasons. In rural appearance of some cases of resistance antedate 1960. areas, VANSOMEREN et al. (1958) made similar obser- Thus, in Brazzaville DDT and HCH were used every vations, as did WIJERSand KIILU(1978). In north-east year from 1951 to 1957, inclusive. Dieldrin was used Tanzania, in a suburban locality, C. p. quinquefas- in 1957 and alternated with DDT and HCH in the ciatus densities had two peaks corresponding to the years that followed (ADAMand SOUWEINE,1962). two rainy seasons (WHITE,1971a), the peak densities In some cases, the use of combination of insecti- occurring during the lesser rainy season. In the Com- cides and oils has enabled a wider use of organochlor- oro Archipelago, which has only one rainy season, ine preparations: for example, malariol (DDT + oil) peak densities occur during that season both in was applied for many years in Tanzania (MENUand Grand Comoro and in Mayotte (BRUNHES,1975). KILAMA,1972). From this review, covering several areas of Africa, From 1960 onwards, however, organophosphorus it clearly emerges that there is a marked relationship larvicidal compounds gradually began to replace Biology and control of Culex pipieris quiiiquefasciatus 329 organochlorines. Experiments carried out in Rangoon Four organophosphorus compounds can be especi- (Burma) showed that the routine use of such insecti- ally used as larvicides : chlorpyrifos (Dursban), fen- cides and especially fenthion as a larvicide gives ex- thion, fenitrothion (= sumithion, = folithion) and tremely satisfactory results against C. p. quiiiquefas- temephos. As most C. p. quinquefasciatus breed in ciatus (GRAHAMet al., 1972) at a cost lower than that rather small areas (a few square metres or less) it is of the oil-based applications used previously (GRATZ, difficult to estimate a dosage per hectare as is done 1973a). for other mosquito species. The idea is to introduce In Africa, starting from 1955, diazinon gave promis- into the breeding place a certain amount of insecticide ing results on a small scale against C. p. quiiiquefas- adapted to each case and expressed in p.p.m. The ciatus larvae in heavily polluted waters (HARVEY, places to be treated include mainly cesspools, latrines, 1956). The most widely used OP compound has been drains, ditches and some artificial containers (drums, malathion but it has the disadvantage of deteriorating cisterns) which contain contaminated water. Pirimi- rapidly in polluted waters (WHITE,1971b). Very good phos methyl (OMS 1424) has also been tried as a results seem to have been obtained with other com- larvicide against this mosquito by the WHO Vector pounds of the same group. Thus in Bagamoyo, in Biology Control Research Unit No. 2 in Indonesia: Tanzania, C. p. quiiiquefasciatus densities have been one part per million was effective for 2 weeks. considerably reduced when granular chlorfenvinphos Although indoor residual application of insecticides (Birlane) was applied to latrines (MENUand KILAMA, is not the method of choice against C. p. quinquefas- 1972). In Zanzibar (Tanzania) the use of chlorpyrifos ciatus, two OP compounds (malathion and fenitroth- (Dursban) has produced encouraging results (KILAMA, ion) and one carbamate (propoxur) can be considered personal communication) as it has in Dar es Salaam under special situations. At 2 g/m2 the effectiveness (BANGet al., 1975). may last for about 3 months. The areas to be treated Experiments on a more restricted time-scale and include inside walls, ceilings, sometimes furniture, and space, but carried out in a more rational way, have verandah, if any. also shown the effectiveness of other organophos- Malathion has been used in the United States of phorus compounds for controlling C. p. quinquefas- America in ultra-low volume (ULV) exterior treat- ciatus larvae. In towns in West Africa temephos ments to control encephalitis outbreaks (WHO, 1970). (Abate) and chlorpyrifos have proved very effective A dosage of 225 ml per hectare proved to be sufficient against this mosquito (SUBRAet al., 1969). On the to control C. p. quinquefasciatus outside. Nevertheless, East African coast in a rural area of Tanzania, the this rate had to be increased to 450ml to control utilization of these two compounds has reduced by mosquitoes inside urban housing. See Tables 1-4 for a 95% the number of man-biting females (BUSHROD, summary of residual toxicities of larvicides and sus- 1979). In the same area, excellent results have been ceptibility to larvicides. obtained with chlorpyrifos in the town of Morogoro, Methods of chemical application. In most cases, in Tanzania (MROPEet al., 1973), and with temephos ground equipment is used to apply pesticides for the on the Kenyan coast (WIJERS,personal communi- cation). In Mayotte, in the Comoro Archipelago, the Table 1. Susceptibility of fourth-instar colony larvae of use of temephos has led to reductions in adult C. p. quinquefasciatus after 24 hr exposure to various densities in rural areas (SUBRAet al., 1973). However, larvicides it is interesting to note that in some African countries, the national or local vector control services prefer to OMS Lc50 LC95 use these products (excepting temephos) as adulticides Compound number (p.p.m.) (p.p.m.) for intradomiciliary spraying and that larviciding, Chlorpyrifos 97 1 0.00071 0.0013 when carried out at all, is merely supplementary to Chlorpyrifos methyl 1155 0.004 adulticidal measures. It has been so in Mali with fen- Parathion 19 0.0017 0.0026 thion (SUBRAet al., 1970a) and in Madagascar with Temephos 786 0.0016 0.0029 malathion (SUBRA,personal observation). OMS 1211* 0.0023 0.0048 It should be noted, however, that such intradomici- Fenthion 2 0.0028 0.0051 liary spraying is not directed against C. p. quinquefas- Bromophos 658 0.0058 0.0083 ciatus alone but also against anophelines, for which OMS 1210 0.0042 0.0084 this control measure is often the most appropriate. In OMS 437 0.0057 0.011 OMS 1290 0.0078 0.025 addition, they often control populations of other Fenitrothion 43 0.014 0.028 insects (bedbugs) that sometimes cause as much nuis- Bromophos ethyl 659 0.018 0.045 ance as mosquitoes, so the human population would Dichlorvos 14 0.044 0.063 favour spraying rather than larvicidal application, OMS 1287 0.053 0.072 and this explains why adulticiding is sometimes given OMS 711 0.042 0.085 preference. Malathion 1 0.064 0.098 Choice of pesticides. While C. p. quinquefasciatus Tetramethrint 0.043 0.120 can develop a high degree of tolerance followed by OMS 236 >0.10 resistance to these insecticides, it nevertheless is true Bendiocarb 1394 0.500 that, if financially feasible, there is a range of new Pirimiphos methyl 1424 0.020 Methoprene 1804 0.010 products particularly larvicides, which if rationally used produce good control results. Judicious alter- *0-(2,5-dichloro-4-iodophenyl)O,O-dimethylphosphoro- nation of the various compounds available seems, thioate. moreover, to be the best way of controlling C. p. quin- TA pyrethrum derivative. quefasciatus (see HAMONand MOUCHET,1967). Source: SELFand TUN(1970). 330 R. SUBRA

Table 2. Residual toxicities of larvicides against C. p. quin- periods of the species and the persistence of the com- quefasciatus in polluted concrete drains pound used. In the case of adulticides, it depends amongst other things, on the nature of the substrate Dosage No. of days on which the product is sprayed. Thus, it is only poss- Treatment (P.Pd effective ible to speak of the mean duration of effectiveness Emulsifiable concentrates (WHO, 1970): in the case of the most commonly used compounds (malathion and fenitrothion), it is about 3 Chlorpyrifos 1.o 25 Chlorpyrifos o. 1 10 months. The duration of effect of larvicides also varies Temephos 2.0 15 and depends on the degree of pollution of the breed- Temephos 1.o 13 ing places, a high degree of pollution reducing the Temephos o. 1 6 duration of effectiveness as well as the flow of water. Fenthion 2.5 15 Thus, in Bobo Dioulasso in West Africa, temephos Fenthion 1.o 11 remained effective in soakage pits for about 2 weeks Fenthion 0.5 7 (SUBRAet al., 1970b), but in Mayotte in the Comoros Fenthion o. 1 5 it was effective for over a month in the same type of OMS-1290 2.5 16 breeding place which was apparently less polluted OMS-1290 1.o 11 (SUBRAet al., 1973). OMS-437 4.0 14 OMS-437 0.8 11 Precautions necessary for pesticides. Indoor spray- Bromophos-ethyl 0.5 6 ing against adults can be applied only when food and Bromophos-ethyl 0.25 4 clothing have been removed. OMS-1210 5.0 10 The larvicides available cannot be used indiscrimin- OMS-1210 1.o 7 ately in all types of breeding places. Those containifig OMS-1211 5.0 8 water which may be used for watering animals, or OMS-1211 1.o 7 those situated near drinking water wells, must be Bromophos 5.0 7 treated with compounds of low mammalian toxicity. Bromophos o. 1 2 In such cases, temephos is preferred to chlorphyrifos, Tetramethrin 5.0 6 Tetramethrin 1.0 3 although the latter has a much longer-lasting effect. OMS-1287 5.0 5 As far as insecticide storage and use are concerned, OMS-1287 1.o 3 several measures have to be kept in mind in all Parathion 7.5 10 circumstances. Pesticides have to be stored in safe Parathion 0.04 1 places, inaccessible to children. Staff responsible for OMS-236 12.5 9 treatment operations have to be supplied with well- Fenitrothion 15.0 10 maintained spraying equipment and protective cloth- Fenitrothion 0.4 2 ing. In addition to this, they must be under regular OMS-711 18.0 18 medical surveillance. Pirimiphos-methyl (OMS-1424) 1.0 14 Altosid (OMS-1697) 1.o 21 Insecticide resistance. The first case of resistance to Methoprene (OMS-1804) 1.0 7 organochlorine compounds in C. p. quinquefasciatus was demonstrated by HAMON(1953b) in Réunion. Dosage No. of days In subsequent years, other strains became resistant: in Treatment (USgal/acre;l./ha) effective West Africa in 1958, Central Africa (Zaire) and East Emulsifiable concentrates* + oil? Africa in 1959, Madagascar in 1961 (BROWNand PAL, Dursban + gas oil 10 Abate + gas oil 80; 760 10 Table 3. Residual toxicities of larvicides against C. p. quin- Fenthion + gas oil 10 quefasciatus in polluted earthen drains Oil alone Flit MLO* 80; 760 8 No. of days Malariol 80; 760 6 Treatment Dosage (p.p.m.) effective Gas oil 80; 760 6 Emulsifiable concentrates *Applied at a rate of 1.0 p.p.m. Temephos 0.5 12 ?Applied at a rate of 0.19 US gallons per 100 ft2 of water Temephos 0.1 9 surface. Bromophos 3.75 21 $Obtained from the Esso Research and Engineering Co. Bromophos 0.75 10 Source: SELFand TUN(1970). Bromophos 0.50 9 Fenthion 5.0 21 Fenthion 1.o 11 control of C. p. quinquefasciatus. It can be either OMS-1290 1 .O 11 hand- or power-operated. In many African countries, OMS-437 1.o 11 hand-operated equipment has been preferred as it is Fenitrothion 0.25 7 less expensive (in terms of cost and maintenance) and Parathion 3.0 9 easier to carry (in terms of weight and volume) in Parathion 2.0 8 sometimes very confined spaces. Aerial equipment OMS-236 5.0 14 OMS-711 2.5 10 was used in the United States of America for the ULV OMS-1287 1.0 3 treatments with malathion. Tetramethrin 1.0 3 Treatment frequency of pesticides. The frequency of insecticide applications depends on the breeding Source: SELFand TUN(1970). Biology and control of Culex pipieris quinquefusciutus 331

Table 4. Residtial toxicities of larvicides against C. p. quin- considered for certain types of breeding pIaces or in quefusciutus in polluted pit latrines special circumstances such as when other products are not available. After the treatment of latrines with No. of days sump oil in Amani (Tanzania) WHITE(1967) observed Treatment Dosage (p.p.m.) effective a reduction in C. p. quinquefasciatus densities and the Emulsifiable concentrates disappearance of the species from breeding places of this type where it was later replaced by Culex cinereus Chlorpyrifos 1.o 77 and Culex nebulosus. Special oils (‘Flit MLO) devel- Chlorpyrifos o. 1 31 oped during the last few years for mosquito control Temephos 5.0 63 Temephos 1.o 35 have proved to be excellent larvicides. They were Fenthion 2.0 24 recently shown to kill C. p. quinquefasciatus eggs Fenthion 1.o 21 (MCDONALD,1976), although trials carried out by Fenthion 0.5 10 WHITE(1971b) in Tanga (Tanzania) were disappoint- OMS-1210 2.5 25 ing. According to him, the lack of success could be OMS-1210 1.0 20 ascribed to the rapid emulsification of the oil by OMS-1211 2.5 25 soaps, detergents and urine contained in the breeding OMS-1211 1.o 18 places. The rising price of oils, however, will certainly OMS-1290 2.5 27 reduce if not eliminate their use against mosquito lar- OMS-1290 1.o 15 OMS-1290 0.5 6 vae. OMS-437 5.0 49 Insect growth regulators. Insect growth regulators OMS-437 1.o 10 are a new group of products which could be used as Bromophos 5.0 35 substitutes for the larvicides mentioned above. These Bromophos 2.5 21 new pest control agents, in general, pose less hazard Bromophos 1.0 11 to the non-target fauna, man and animals. Fenitrothion 5.0 12 Several trials have been carried out with OMS- Fenitrothion 1.0 10 1804, diflubenzuron (= dimilin) (1-(4-~hlorophenyl)-3- Parathion 5.0 20 Parathion 1.o 7 (2,6-difluorobenzoyl)-urea), used as larvicide. This OMS-1287 2.5 8 growth regulator interferes with the formation of the OMS-1287 1.0 6 cuticle and thus causes disturbances during ecdysis. In Malathion 5.0 10 India, SHARMAet al. (1975) fpund the duration of its Dichlorvos 5.0 10 efficacy to be about one week. The same product has Dichlorvos 1.0 7 given much better results in Africa at Bobo Dioulasso Tetramethrin 5.0 4 (Upper Volta) where SALESand HERVY(1977) found Tetramethrin 1.0 2 that its effect persisted for about a month. This com- pound has also been tested in Indonesia by WHO/ Emulsifiable concentrates gas oil* + VBCRU-2 and found effective for 2 weeks (SELFet al., Chlorpyrifos 1.0 56 1978). Chlorpyrifos 0.5 53 Another compound, OMS-1697 (methoprene or Chlorpyrifos o. 1 30 Altosid) has been tested at Jakarta by NELSONet al. Temephos 1.0 42 (1976) and SELFet al. (1978). It simulates juvenile hor- Temephos 0.1 12 mone, and disturbs pupation causing the death of Fenthion 1.o 21 pupae or of adults when they emerge. Its effectiveness Bromophos-ethyl 0.5 13 was assessed on the basis of the reduction in female Gas oil alone -* 7 population densities in the treated zone. This reduc- *Applied at a rate of 120 US gal/acre, i.e. 0.03 US gal- tion, which was observed over a long period (between lons per 11 ft2 of water surface (approximately 1140 l./ha). the second and seventh week following treatment), Source: SELFand TUN(1970). was about 84% in specimens caught on human-bait and 69% in those caught inside dwellings. Overcrowding. Pre-imaginal forms of mosquitoes 1973). This resistance became so general that suscepti- breeding in very large numbers in a small space may bility tests carried out in 1966 by MOUCHETet al. release substances that slow up growth and cause (1968) on West African strains showed that only a high mortality among young specimens of the same very small number were still sensitive to DDT. species. This phenomenon, which was observed as Resistance to the HCH-dieldrin group followed re- long ago as 1930 by ROUBAUDand TOUMANOFFin sistance to DDT, and showed a similar spread. It was C. pipiens, has recently been studied in C. p. quinque- reported in West Africa in 1957, then in Mali (1961) fasciatus by IKESHOJIand MULLA(1970b). These same and the Ivory Coast (1966). In 1959 it was found in authors (1974%b) have isolated and chemically identi- Central Africa (Zaire); East Africa and Zanzibar; in fied the factors responsible for these developmental 1964 in continental Tanzania, and in 1961 in Mada- anomalies. If they prove effective in the field, they gascar (BROW and PAL, 1973). could play a considerable role in controlling mos- At the present moment, resistance in C. p. quiiique- quitoes, especially C. p. quinquefasciatus, on which fasciatus to all organochlorine insecticides seems to most of the research has been done (HWANGand be general and covers vast regions in Central Africa MULLA, 1976; MULLA,1976). At the moment, they are (MOUCHETet al., 1972). still in early stages of testing. Oils. Oils were employed before the use of synthetic Genetic control. Genetic control would doubtless insecticides became general. Their utilization is still constitute one of the most satisfactory ways of dealing 332 R. SUBRA with the problem of mosquito control since it does especially because it became obvious that synthetic not require the use of any chemical product in the insecticides could not by themselves solve all the field and the risks of pollution are therefore nil. problems of C. p. quinquefasciatzts control. The first Furthermore, only the target species is affected by obstacle to the use of these predators lay in their such control operations, and thus there is very little inability to adapt themselves to highly polluted disturbance of the natural balance. waters which are the most productive breeding places Studies on cytoplasmic incompatibility have been for this mosquito. However, work by SASAet al. carried out on C. pipiens (MARSHALLand STALEY, (1965a) showed that in some places, such as Bangkok, 1937) and later on C. p. quinquefasciatus (ROUBAUD, Poecilia reticulata (ROZENand BAILY,1963) developed 1956). Crossing experiments in Africa on the latter satisfactorily in polluted breeding places. BAY and species have used strains from different areas, and SELF (1972), studying the problem in other towns in some have resulted in incompatibilities. In West South-East Asia, considered that larvivorous fish Africa SUBRA(1972~) achieved 57 crosses (out of 72 could be used effectively to control mosquito larvae possible) with nine different strains. With a strain but in restricted situations, since various factors work from Thies in Senegal it was possible to classify the against their establishment in all types of breeding various strains tested into six different types accord- places. The Maldive Islands would seem to offer a ing to success or failure in crossing, and in which situation exceptionally favourable to the use of fish as direction or directions. Thirty crosses carried out by the main means of controlling several mosquito LAVEN(1969) with six strains from West (two), Cen- species, including C. p. quinquefasciatus (VELIMIROVIC tral (two) and East (two) Africa also demonstrated and CLARKE,1975). The larval breeding places are several cases of incompatibility. On the other hand, mainly wells in which three different fish species can six strains of C. p. quinquefasciatus caught in Tanzania be introduced (Poecilia reticulata, Mollienesia sphenops and Kenya and crossed by MAGAYUKAand WHITE and Kuhlia taeniurus, a marine species adapted to life (1972) showed no incompatibilities in 26 crosses in wells). achieved (30 possible). In addition to fish, attention has also been given to In an experiment carried out in Asia (LAVEN,1967), other predators, including the mosquito larvae be- non-indigenous males incompatible with the females longing to the Lutzia genus, which are able to develop of the local strain were released in a Burmese village. in some of the C. p. quinquefasciatus breeding places After a few weeks none of the eggs laid by these (GRATZ,1973b). females was viable. In a trial based on the release of Parasites. Field trials have been carried out in males sterilized in the pupal stage with thiotepa in the South-East Asia and also in the South Pacific. United States of America (PATTERSONet al., 1970), the REYNOLDS(1972) succeeded in introducing a micro- indigenous population of C. p. quinquefasciatus was sporidan, Plistophora czrlicis Weiser, into a natural suppressed 10 weeks after the beginning of the trial. population of C. p. qirinquefasciatus in Nauru Island Although these two trials were carried out on a small in Micronesia but did not succeed in appreciably scale in well-isolated zones, they nevertheless proved reducing the density of populations of that mosquito. that the released males competed with the males of Nematodes belonging to the Romanomermis culici- the wild population. vorm species have also been tested experimentally to Two trials carried out in the Delhi region (YASUNO control C. p. quinquefasciatus. In the laboratory, a et al., 1978; BROOKSet al., 1976), the first using strain of this mosquito from Taiwan proved to be chemosterilized males and the second using males in- very susceptible to infection by R. culicivorax, with compatible with the local strains and in which a sex- infection rates ranging from 90 to 100% (MITCHELLet linked translocation had been introduced, resulted in al., 1974). Nevertheless, a trial carried out in Bangkok a high percentage of sterility. However, in both cases by CHAPMANet al. (1972) proved quite disappointing, the trials did not have the success anticipated because since the percentage of mosquitoes infected by the of reinvasion of mosquitoes from the outside. parasite was low. Moreover, these authors were not While genetic control in theory remains one of the certain that the parasite could survive under natural most attractive methods of control, at present none of conditions. Later on, CHEN(1976) in Taiwan observed the methods is operational. Prospects of their use on that this same parasite could complete its life cycle in a large scale are not very promising due to reinvasion nature but emphasized the importance of pH as a problems, human factors, and high cost. As GRATZ limiting factor. More recently, in the United States of (1973a) observed, vast difficulties must be overcome America, LEVYand MILLER(1977) were able to get and further knowledge acquired before such methods 53.7% parasitism in C. p. quinquefasciatus larvae can be used routinely. breeding in an abandoned sewage settling tank, and it Biological control. Predators. Use of larvivorous fish was concluded that this mermithid had potential as a is one of the oldest and best-known methods of con- control agent against this species. Nevertheless, it is trolling mosquitoes. In East Africa, they were intro- worth noting that C. p. quinquefasciatus can develop duced several centuries ago by the Arabs who had resistance to R. culicivorax which might reduce the founded towns and villages along the coast. The fish possibilities of its use on a large scale. This has were placed in tanks (‘birikas’) where the water was already been reported by PETERSEN(1978). kept for ritual ablutions and where Aedes aegypti and One of the most promizing pathogen agents seems C. p. quinquefasciatirs developed (WIJERSand SUBRA, to be a spore-forming bacterium discovered a few personal observation). After the Second World War, years ago by GOLDBERGand MARGALIT(1977) and fish (Lebistes) were used in Tanzania in breeding identifed as Bacillus thuringiensis serotype H-14 (DE places of the same type (BANGet al., 1973a). BARJAC,1978). It produces a crystal of toxin protein The recent resumption of their use was envisaged ,(delta-endotoxin) which acts as a stomach poison Biology and control of Culex pipiens quinqirefasciatus 333 when eaten by the insect. It is active, against several the spraying of latrines and polluted water with chlor- mosquito species, including species of the Culex pyrifos led to a reduction of 92% in adult densities of pipiens complex (GARCIAand DESROCHERS,1979), and C. p. quinquefasciatus evaluated on the basis of room- it has a high degree of safety for non-target organisms pyrethrum spray catches. This is ample proof of the (DEJOUX,1979; SINEGREet al., 1979). To determine success of the operation. whether it might be one of the main tools for future control of C. p. quinquefasciatus in developing coun- Evaluation tries will require large-scale field experiments. Evaluation is an essential component of any vector Environmental management. These measures aim at control operation. Its aim is to assess the effects of eliminating the breeding places that enable mosquito these operations on vector densities and disease im- larvae to develop. A distinction will be drawn pact. In areas of Africa where C. p. quinquefasciatus is between operations aimed at eliminating these sites only important as a nuisance, the evaluation will deal on a relatively permanent basis (environmental modi- only with mosquito population densities. When it is fication), and those which tend only to get rid of un- considered mainly as a filariasis vector, evaluation stable and generally small breeding places tempor- will also involve reduction in disease transmission arily (environmental manipulation). and prevalence. Waste water can be discharged either through well- Mosquito densities. It is essential to collect data on designed soakage pits in which mosquito larvae can mosquito densities prior to any control operation, no longer develop, or by building sewers which at the then to compare them with the data obtained during same time avoid accumulation of stagnant rainwater and after these operations. When possible, there and replace latrines. Disappearance of breeding places should be an uncontrolled experimental area in order of this type would considerably reduce the densities of to evaluate density variations which may not be C. p. quinquefasciatus and would lead to large savings related to control operations. in both insecticides and manpower. However, the de- Mosquito densities can be measured at each of the velopment of such systems requires large investments development stages : eggs, pre-imaginal forms, and often beyond the available resources of a particular adults. Finding and collecting egg rafts of C. p. quin- state. It is nevertheless the aim to which all concerned quefasciatus is not always very easy, especially in should be directing their efforts, even if it is not im- breeding places which may be several meters deep. mediately attainable. Accurate identification requires larvae bred to the Besides the breeding places mentioned above which fourth stage, which requires time and laboratory are characterized by their stability and large size, are space. In addition, important fluctuations in the small collections of water resulting from human ac- number of egg rafts laid in the same breeding place tivity or negligence (tin cans, broken bottles, etc.). from day to day (SUBRA,1971) may give a false idea of Their elimination by the health services or the inhabi- the size of the mosquito population. In this respect tants themselves can also help to reduce adult egg sampling cannot contribute to proper evaluation. densities. The most important problem here is to con- Larvae and pupae are sampled at the same time. vince populations of the need to continue their efforts Several devices have been developed which have been and thus to avoid a return to the status quo ante once reviewed by SERVICE(1976). Most C. p. quinquefas- the first enthusiasm has died down. Here health edu- ciatus breeding places have a rather limited surface, cation must play a primary role, since there can be no and it is usually relatively easy to check whether or permanent environmental improvement without the not they are colonized by this species. However, in cooperation of the local population (WHO, 1975). cases where water surface is not easy to reach (very Integrated control. Integrated control aims primar- deep latrines, cesspools covered with a cement cap), ily at combining methods, which if applied separately, proper pre-imaginal sampling may then be difficult would not achieve the desired result but together are and inappropriate for evaluation. mutually complementary. Adult mosquitoes may be sampled using numerous Several pilot field trials have been carried out in mcthods and devices (SERVICE,1976). The most com- South-East Asia. In Rangoon, MATHIS(1972) success- monly used in Africa to assess the effects of control fully combined the use of larvivorous fish (P. reticu- operations have been night catches on human baits lata) and the larvicide fenthion with a view to con- (SUBRAet al., 1973; BUSHROD,1979; WIJERS,un- trolling the pre-imaginal females of C. p. quinquefas- published report) and day catches (either by hand or ciatus developing in a ditch. In Bangkok PRAKONG pyrethrum spray catches) of females resting inside the PHAN-URAIet al. (1975) had achieved a reduction of houses (SUBRAet al., 1970). The favourable or un- something like 75% in size of pre-imaginal population favourable reactions of people living in the area where by twice a week removing the debris floating on the control operations are taking place is another way of top of two pools colonized by C. p. quinquefasciatus. assessing the success of mosquito control. Although it The introduction of P. reticulata also reduced the cannot be measured on a scientific basis, it is an indi- number of pre-imaginal forms down to only 2% of the cation which has to be taken into account by those level observed before the beginning of the trials. Inter- responsible for these operations. ruption of the removal of this debris was followed by Reduction in disease transmission and prevalence. an increase in the culicid population. Reduction in disease transmission as well as reduction At Dar es Salaam in East Africa, in a large-scale in disease prevalence are the two major factors which trial affecting several species (Anopheles, Ae. aegypti, have to be assessed, in addition to density reduction, C. p. quinquefasciatus), BANGet al. (1975) combined when the target mosquito is a disease vector. Thus in environmental improvement and insecticides. A Tanzania, the success obtained in reducing densities reduction in the number of larval breeding places and of C. p. quinquefasciatus and Anopheles ganibiae 334 R. SUBRA complex species was confirmed by an important control of urban mosquitoes in Dar es Salaam using reduction of filariasis transmission (BUSHROD,1979). community sanitation supplemented by larviciding. E. On the other hand, in Réunion, a large decrease of the Afr. med. J. 52, 578-588. number of cases of bancroftian filariasis was observed BARJACH. DE (1978) Une nouvelle variété de Bacillus thur- after intensive antimosquito measures mainly aimed ingiensis tres toxique pour les moustiques : B. thur- towards malaria vectors (BRUNHES,1975). ingiensis var. israelensis sbrotype 14, C.R. Acad. Sci. Paris. (Sér. D) 286, 797-800. Conclusions BAYE. C. and SELFL. S. (1972) Observations of the guppy, Poecilia reticulata Peters, in Culex pipiens fatigam breed- Complete success in operations to control C. p. ing sites in Bangkok, Rangoon and Taipei. Bull. Wld quinquefusciutus is rare. In most instances, the species Hlth Org. 46, 407-416. has been able to overcome the obstacles placed by BHATH. R. (1975) A survey of hematophagous arthropods man in the way of its breeding. It is true that often in western Himalaya, Sikkim and Hill districts of West these efforts to control the mosquito were unsuccess- Bengal: records of mosquitoes collected from Himalayan ful because new breeding sites were created by man. region and Uttar Pradesh with ecological notes. Ind. J. med. Res. 63, 1583-1608. This situation has led many authorities responsible BRENGUESJ. (1975) La filariose de Bancroft en Afrique de for vector control to believe that the control of C. p. l'Ouest. Mém. ORSTOM, Paris 79, 299 pp. quinquefusciatus is ineffective or at least requires BROOKSG. D., CURTISC. F., GROVERK. K., KRISHNA- means that are out of reach of their financial MURTHY B. s., RAJAGOPALANP. L., SHARMA L. s., Ø resources. SHARMAV. P., SINGHK. R. P., YASUNOM., ANASARDM. An interesting paper by GRAHAMand GRATZ(1975) A., ADAKT., AGARWALH. V., BATRAC. P., CHANDRAHAS has shown that in numerous developing tropical R. K., MALHOTRA P. R., MENONP. K. B., MENONR., countries the sums devoted to vector control were DASS., RAZDANR. K. and VAIDYANATHANV. (1976) A . often considerable. The bulk of the failures seem to be field trial on control of Culex pipiens fatigans Wied. by release of males of strain integrating cytoplasmic incom- due to faulty planning, execution and surveillance of patibility and a translocation. Document WHO/ operations. Thus it. becomes essential to strengthen VBCl76.635. the already existing cadre of mosquito control BROWNA. W. A. and PALR. (1973) Insecticide resistance in workers (MACDONALD,1978) and to carry out cost/ arthropods. Wld Hlth Org. Monogr. Ser. 38, 541 pp. benefit studies for the control operations on the basis BRUNHESJ. (1975) La filariose de Bancroft dans la sous- laid down by CVJETANOVICand GRAB(1976) to ensure région malgache (Comores-Madagascar-Réunion). Mém better utilization of the available funds. Perhaps, it ORSTOM, Paris 81, 212 pp. would then be possible to maintain C. p. quinquefas- BRUNHESJ. and DANDOY6.11973) Géographie de la filar- ciutus densities at a sufficiently low level to ensure iose de Bancroft dans les îles d'Anjouan et Mayotte. Doc. mim. ORSTOM, Tananarive, 19 pp. that the mosquito ceases to be one of the major BRYGOOE. R. and SUREAUP. (1962) Culex fatigam et virus health problems in the human environment in the poliomyélitique. Arch. Inst. Pasteur Madagascar 30, tropics. 155-157. BUSHRODF. M. (1978) Autogeny in East African Culex f Acknowledgements-I would like to thank those who pipiens quinquefasciatus (=fatigam). Trans. R. Soc. trop. assisted in reviewing this manuscript, especially to Dr A. Med. Hyg. 72, 323. W. A. BROWN,Dr W. A. CHINERY,Dr N. G. GRATZ,Mrs BUSHRODF. M. (1979) Studies on filaria transmission in M. KING,Dr J. MOUCHET,Dr M. MULLA,Dr R. REUBEN, Kwale, a Tanzanian coastal village, and the results of . Dr H. F. SCHOOF,Dr V. THOMASand Dr Y. WADA. mosquito control measures. Ann. trop. Med. Parasit. 73, 277-285. CHANDLERJ. A., BOREHAMP. F. L., HIGHTONR. B. and REFERENCES* HILLM. N. (1975) Feeding habits of mosquitoes in the ABDULCADERW. H. M., RMAKONEP., THARUMARAJAHK. Kisumu area and their possible relationship to disease and MAHADEVAR. (1965) Vectorial capacity of Culex transmission. E. Afr. med. J. 52, 413-417. pipiens fatigam in Ceylon. J. trop. Med. Hyg. 68, CHANDLERJ. A. and HIGHTONR. B. (1975) The succession 254-256. of mosquito species (Diptera, Culicidae) in rice fields in ADAMJ. P. and SOUWEINEG. (1962) Etude de la sensibilité the Kisumu area of Kenya, and their possible control. aux insecticides des Culicidae de Brazzaville (République Bull. ent. Res. 65, 295-302. du Congo) avec quelques notes de faunistique et de bio- CHAPMANH. C., PONTC. P., MATHISH. L., NELSONM. J. logie. Bull. Inst. Rech. sc. 1, 31-44. and BOONLUANPHATOMACHINDA (1972) Field release of ADERSW. M. (1917) Insects injurious to man and stock in the nematode Reesimerniis nielseni for the control of Zanzibar. Bull. ent. Res. 7, 391-401. Culex pipiens fatigam in Bangkok (Thailand). Document AFRIDI M. K. and MATIDS. A. (1938) Observations on the WHOIVBCl72.412. I DP. range of dispersion of Culex fatigans and its infiltration CHAUVETG.'and RASÔ~ONIAINAL. DE G. (1966) Culex into Delhi urban area. J. Mal. Inst. India. 1, 155-167. pipiens fatigam Wied. en milieu urbain à Madagascar: BANGY. H., MSANGIA. S. and WRIGHTJ. W. (1973a) pullulation, résistance aux insecticide chlorés. Incidence Mosquito control service in Tanzania. Part I. Historical possible sur l'endémie filarienne, lutte. Reo. méd. Mada- review. Document WHOlVBC/73.438. gasc. Afr. austr. 41, 5-36. BANGY. H., SABUNII. B. and TONNR. J. (1973b) Mosquito CHAUVETG. and RASOLONIAINAL. DE G. (1968) Culex control service in Tanzania. III. The effects of mosquito pipiens fatigam en milieu urbain à Madagascar. Cah. control and urbanization on mosquito population in ORSTOM, Sér. Ent. me'd. Parasit. 6, 145-159. Dar es Salaam, from 1954 to 1971. Document WHO/ CHENP. S. (1976) A study of Reesimermis nielseni for con- VBC173.440. trol of Culex pipiens fatigans in Taiwan. Bull. Inst. Zool. BANGY. H., SABUNII. B. and TONNR. J. (1975) Integrated Acad. sin. (Taipei) 15, 21-28. CHINERYW. A. (1968) Mosquito control in an urban environment with reference to the anti-mosquito oper- *The literature survey ended in January 1980 ations in Accra and Tema. Ghana med. J. 7, 205-209. Biology and control of Culex pipieris quinquefasciatus 335

CHINERYW. A. (1969) A survey of mosquito breeding in GRATZN. G. (1974a) The persistence and recrudescence of Accra, Ghana, during a two-year period of larval mos- some arthropod and rodent borne diseases. Pub. Hlth quito control. I. The mosquitoes collected and their Reo. 3, 117-148. breeding places. Ghana med. J. 8, 266-274. GRATZN. G. (1974b) Urbanization and filariasis. Document CHINERYW. A. (1970) A survey of mosquito breeding in WHO/FIL/74.119. Accra, Ghana, during a two-year period of larval mos- HAMONJ. (1953a) Etude biologique et systématique des quito control. II. The breeding of Culex (Culex) pipiens Culicidae de l’île de la Réunion. Mini. Inst. scient. Mada- fatigam Wiedemann and Anopheles (Cellia) gaittbiae gascar (E)4,521-541. Giles, in Accra, Ghana. Ghana nied. J. 9, 109-116. HAMONJ. (1953b) Apparition à la Réunion d’une résistance CHOWC. Y. (1973) Filariasis vectors in the Western Pacific au DDT chez Culex fatigam Wiedemann, principal vec- Region. Z. Tuopetiined. Parasit. 24, 404-418. teur de la filariose à Wuchereria bancrofti dans l’île. Bull. CLEMENTSA. N. (1963) The Physiology of Mosquitoes. Soc. Path exot. 46(3), 454-463. 393 pp. Pergamon Press, Oxford. HAMONJ. (1956) Seconde note sur la biologie des mous- COLLESSD. H. (1957) Notes on the culicine mosquitoes of tiques de l?le de la Réunion. Ann. Parasit. hum comp. 31, Singapore. III. Larval breeding places. Amtrop. Med. 598-606. Parasit. 51, 102-1 16. HAMONJ. (1963) Les moustiques anthropophiles de la COSTAMOURAO M. DO (1964) Relatario de Missao de région de Bobo-Dioulasso (République de Haute-Volta). Estudo e Combate de Endemias de S. Tomé e Principe Cycles d’aggressivité et variations saisonnières. Ann. Soc. (Ier semester de 1962). Anais Inst. Med. trop. 21, ent. France 312, 85-144. 501-539. HAMONJ., BURNETTG. F.,ADAM J. P., RICKENBACHA. and CVJETANOVICB. and GRABB. (1976) Rough determination GRJEBINE A. (1967) culex pipiens fatigam Wiedemann, of the cost-benefit balance point of sanitation pro- Wuchereria bancrofti Cobbold, et le développement grammes. Bull. Wld Hlth Org. 54, 207-215. économique de l’Afrique tropicale. Bull. Wld Hltli Org. DEJOUXC. (1979) Recherches préliminaires concernant 37, 217-237. l’action de Bacillus thuringiensis israelensis De Barjac sur HAMONJ. and MOUCHETJ. (1967) La résistance aux insecti- la faune d’invertébrés d’un cours d’eau tropical. Docu- cides chez Culex pipieris fatigatis Wiedemann. Bull. Wld nient WHO/VBC/79.721. Hlth Org. 37, 277-286. D’EMMEREZDE CHARMOYD. (1908-1909) On three new HARRISW. V. (1942) Notes on culicine mosquitoes in Tan- species of Culex collected during the anti-malarial cam- ganyika territory. Bull. ent. Res. 33, 181-193. paign in Mauritius in 1908. Ann. trop. Med. Parasit. 2, HARVEYA. E. C. (1956) Preliminary tests with diazinon 257-262. against culicine larvae in septic and waste water tanks. DETINOVAT. S. (1963) Méthodes à appliquer pour classer E. Afr. med. J. 33(4), 117-123. par groupes d’âge les diptères présentant une importance HAWKINGF. (1973) The world distribution of Wuchereria médicale. Wld Hlth Org. Monogr. Ser. 47, 220 pp. bancrofti and of Brugia malayi. 9th Intern. Congr. trop. DOBROTWORSKYN. V. (1967) The problem of the Culex Med. Mal., Abstr. inv. Pap. 1, 104. pipiens complex in the South Pacific (including Austra- HAYESJ. (1975) Seasonal changes in population structure lia). Bull Wld Hlth Org. 37, 251-255. of Culex pipiens quinquefasciatus Say (Diptera: Culici- DUNNL. H. (1927) Further observations on mosquito dae): study of an isolated population. J. med. Ent. 12, breeding in tree-holes and crab-holes. Bull. ent. Res. 18, 167-178. 247-250. HEISCHR. B., NELSONG. S. and FURLONGM. (1959) FUSSELLE. M. (1964) Dispersal studies on radioactive- Studies on filariasis in East Africa. I. Filariasis on the tagged Culex quinquefasciatus Say. Mosquito News 24, Island of Pate, Kenya. Trans. R. Soc. trop. Med. Hyg. 53, 422-426. 41-53. GAABOUBI. A., MANSOURN. A. and KAMELF. M. (1971) HENRARDG., PEELE. and WANSONM. (1946) Quelques Evaluation of nine insecticides with three pyrethrin localisations de Wuchereria bancrofti Cobbold au Congo synergists against the mosquito Culex pipiens quinquefas- belge, cycle de développement chez Culex fatigam Wied., ciatus. Z. ang. Ent. 68, 432-438. Anopheles funestus Giles, Aedes aegypti L. et Anopheles GALVEZGOMEZ A. (1947) El mosquito, agente, transmisor gambiae Giles. Rec. Tr. Sc. med. Congo Belge 5, 212-232. de la poliomielitis. Medicina (Mexico) 27, 537, 351- HIGHTONR. B. and VAN SOMERANE. C. C. (1970) The 357. transportation of mosquito between international air- GARCIAR. and DESROCHERSB. (1979) Toxicity of Bacillus ports. Bull. Wid Hlth Org. 42, 344-335. thuringiensis var. israelensis to some California mos- HWANGY. S. and MULLAM. S. (1976) Overcrowding and quitoes under different conditions. Mosquito News 39(3), its chemistry. Chert?. Technol. 6, 358-363. 541-544. IKESHOJIT. (1966) Attractant and stimulant factors for ovi- GILLETTJ. D. (1972) The Mosquito: Its Life, Activities, and position of Culex pipiens fatigam in natural breeding Impact on Human Afluirs. 358 pp. Doubleday, Garden sites. Bull. Wld Hltli Org. 35, 905-912. City, New York. IKESHOJIT. (1968) Studies on mosquito attractants and GOLDBERGL. J. and MARGALITJ. (1977) A bacterial spore stimulants. V. Gas-chromatographic separation of the demonstrating rapid larvicidal activity against Anopheles attractants for oviposition of Culex pipiens fatigans from sergenti, Uranotaenia unguiculata, Culex univittatus, field water. Appl. Ent. Zoo/. 3, 176-188. Aedes uegypti and Culex pipiens. Mosquito News 37(3), IKESHOJIT. and MULLAM. S. (1970a) Oviposition attrac- 355-358. tants for four species of mosquitoes in natural breeding GRAHAMJ. E., ABDULCADER M. H. M., MATHISH. L., SELF waters. Ann. ent. Soc. Am. 63, 1322-1327. L. S. and SEBASTIAN A. (1972) Studies on the control of IKESHOJIT. and MULLAM. S. (1970b) Overcrowding Culex pipiens fatigam Wiedemann. Mosquito News 32, factors of mosquito larvae. J. econ. Ent. 63, 9&96. 399-416. IKESHOJIT. and MULLAM. S. (1974aj Overcrowding GRAHAMJ. and GRATZN. G. (1975) Urban vector control factors of mosquito larvae: isolation and chemical iden- services in the developing countries. Pans. 21, 365-379. tification. Environ. Ent. 3, 482-486. GRATZN. G. (1973a) The control of urban filariasis by the IKESHOJIT. and MULLAM. S. (1974b) Overcrowding control of Culex pipiens fatigans. 9th intern. Congr. trop. factors of mosquito larvae: activity of branched fatty Med. Mal., Abstr. inn Pap. 1, 10. acids against mosquito larvae. Environ. Ent. 3, 487-491. GRATZN. G. (1973b) Mosquito-borne disease problems in IWUALAM. O. E. (1979) Cassava fermentation pools as the urbanization of tropical countries. Critic. Rev. en- major breeding foci for culicine mosquitoes in Nsukka, viron. Contr. 3, 455-495. Nigeria. Niger. med. J. 9, 327-335. 336 R. SUBRA

IYENGARM. O. T. (1952) Filariasis in the Maldive Islands. the morphological and biological differentation of Culex Bull. Wld Hlth Org. 7, 375403. pipiens Linnaeus and Culex molestus Forskal (Diptera, KITZMILLERJ. B. (1959) Parthenogenesis in Culex fatigans. Culicidae). Proc. R. ent. Soc. Lond. (A). 12, 17-26. Science 129, 3352, 837-838. MATHISM. (1935) Biologie de Culex fatigans, de Dakar, KNIGHTK. L. and ABDELMALEK A. A. (1951) A morpho- élevé en série au laboratoire. Bull. Soc. Path. exot. 28, logical and biological study of Culex pipiens in the Cairo 577-581. area of Egypt (Diptera-Culicidae). Bull. Soc. Fouad I. MATHISH. L. (1972) Culex pipiens fatigans control in Ran- Ent. 35, 175-185. goon, Burma, utilizing both fish and insecticide. Docu- KRAMERL. D. and SCHERERW. F. (1976) Vector com- ment WHOJVBCJ72.401. petence of mosquitoes as a marker to distinguish central MATTINGLYP. F. (1962) Population increases in Culex American and Mexican epizootic from enzootic strains pipiens fatigans. A review of present knowledge. Bull. of Venezuelan encephalitis virus. Am. J. trop. Med. Hyg. Wld Hlth Org. 27, 579-594. 25, 336-346. MATTINGLYP. F. and BROWNE. S. (1955) The mosquitoes KRISHNAMURTIB. S. and PAL R. (1958) A note on the of the Seychelles. Bull. ent. Res. 46, 69-110. comparative effect of different blood feed on egg produc- MEILLONB. DE and KHAN2. H. (1967) Observations on the tions of Culex fatigans. Bull. nat. Ind. Mal. Mosquito Dis. flight activities of Culex pipiens fatigans in Rangoon, 7, 27-29. Burma. Bull. Wld Hlth Org. 36, 15-20. KUHLOWF. (1976) Untersuchungen über die Empfanglich- MEILLONB. DE, PAINGM., SEBASTIANA. and KHANZ. H. keit von Culex pipiens für Infektionen mit Wuchereria (1967a) Outdoor resting of Culex pipiens fatigans in Ran- bancrofti. Z. ang. Ent. 82, 50-52. goon, Burma. Bull. Wld Hlth Org. 36, 67-73. KURIHARAT. (1963) Laboratory experiments on the effects MEILLONB. DE and SEBASTIANA. (1967a) The biting cycle of some environmental conditions on the growth of lar- of Culex pipiensfatiguns on man in Rangoon, Burma, vae of the mosquito Culex pipiens s.1. Jap. J. sanit. Zool. and the microfilarial periodicity. Bull. Wld Hlth Org. 36, 14, 7-15. 174-176. LAMBRECHTF. L. (1971) Notes on the ecology of Seychelles MEILLONB. DE and SEBASTIANA. (1967b) Examination of mosquitoes. Bull. ent. Res. 60, 513-532. the stomach contents of Culex pipiens fatigans in Ran- LAVENH. (1967) Eradication of Culex pipiens fatigans goon, Burma, to determine the origin of the blood-meal. through cytoplasmic incompatibility. Nature 216, Bull. Wld Hlth Org. 36, 168-169. 383-384. MEILLONB. DE, SEBASTIANA. and KHANZ. H. (1966) Posi- LAVENH. (1969) Incompatibility tests of Culex pipiens tive geotaxis in gravid Culex pipiens fatigans. Bull. Wld cgmplex. Part I. African strains. Mosquito News 29, Hlth Org. 35, 808-809. 70-74. MEILLONB. DE,SEBASTIAN A. and KHANZ. H. (1967b) The LEED. J., CLINTONK. J. and OGOWERA. K. (1954) The duration of egg, larval and pupal stages of Culex pipiens blood sources of some Australian .mosquitoes. Aust. J. fatigam in Rangoon, Burma. Bull. Wld Hlth Org. 36, biol. Sci. 7, 282-301. 7-14. LEE D. J., FENNERF. and LAWRENCEJ. J. (1958) Mos- MEILLONB. DE, SEBASTIANA. and KHAN Z. H. (1967~) quitoes and fowl pox in the Sydney area. Aust. vet. J. 34, Exodus from a breeding place and the time of emergence 230-237. from the pupa of Culex pipiens fatigans. Bull. Wld Hlth LEVYR. and MILLERT. W., JR (1977) Experimental release Org. 36, 163-167. of a mermithid nematode to control mosquitoes breed- MEILLONB. DE., SEBASTIANA. and KHAN2. H. (1967d) ing in sewage settling tanks. Mosquito News 37(3), Cane-sugar feeding in Culex pipiens fatigans. Bull. Wld 41W14. Hlth Org. 36, 53-65. LINDQUISTA. W., IKESHOJIT., GRABB., MEILLONB. DE and MEILLONB. DE, SEBASTIANA. and KHANZ. H. (1967e) KHANZ. H. (1967) Dispersion studies of Culex pipiens Time of arrival of gravid Culex pipiens fatigans at an fatigans tagged with 32P in the Kemmendine area of oviposition site, the oviposition cycle and the relation- Rangoon, Burma. Bull. Wld Hlth Org. 36, 21-37. ship between time of feeding and time of oviposition. MAASCHH. J. (1973) Quantitative Untersuchungen zur Bull. Wld Hlth Org. 36, 3946. Ubertrangung von Wuchereria bancrofti in der Kustenre- MENUJ. P. and KILAMAW. L. (1972) Prevalence of Ban- gion Liberias. Z. tropenmed. Parasit. 24, 419434. croftian filariasis in a rural community in Coastal Tan- MCCRAEA. W. R., BELLT. M., HENDERSONB. E., MUNUBE zania. In Proceedings of 1972 East African Medical G. M. R. and MUKWAYAL. G. (1968) Trans-stadial Research Council Scientijìc Conference (Ed. by ANDERSON maintenance of revirus type 3 in the mosquito Culex (C.) and KILAMAW. L.), pp. 345-352. East African Literature pipiens fatigans Wiedemann and its implication. E. Aj?. Bureau, Nairobi. med. J. 45(10), 677-686. MITCHELLC. J., CHENP. S. and CHAPMANH. C. (1974) MCDONALDJ. L. (1976) Response of Culex pipiens quinque- Exploratory trials utilizing a mermithid nematode as a fasciatris Say eggs, larvae, and pupae to additions of Flit control agent for Culex mosquitoes in Taiwan. J. Formo- MLO to their breeding site water. Mosquito News 36, san med. Assoc. 73(5), 241-254. 97-98. MOUCHETJ., CORDELLIERR., GERMAINM., CARNEVALEP., MCDONALDW. W. (1978) Advances in the ecology and BARATHEJ. and SANNIERC. (1972) Résisfance aux insec- control of urban mosquito populations. In Medical ticides &Aedes Aegypti L. et Culex pipiens fatigans en Entomology Centenary (Ed. by WILLMOTS.), pp. 62-69. Afrique Centrale. Document WHOJVBCJ72.381. Royal Society of Tropical Medicine and Hygiene, Lon- MOUCHETJ., DEJARDINJ. and SUBRAR. (1968) Sensibilité don. aux insecticides de Culex pipiens fatigans en Afrique de MACFIEJ. W. S. and INGRAMA. (1916) The domestic mos- l'Ouest. Méd. trop. 28, 374-394. quitoes of Accra. Bull. ent. Res. 7, 161-177. MOUCHETJ., ELLIOT R., GARIOVJ., VOECKELJ. and MAGAWKAS. A. and WHITEG. B. (1972) Hybrid compati- VARIERASJ. (1960) La résistance aux insecticides chez bilities and susceptibility of Culex pipiens fatigans Wied. Culex pipiens fatigans Wied. et les problèmes d'hygiène to Wuchereria bancrojti (Cobbold) in East Africa. Bull. urbaine au Cameroun. Méd. trop. 20,447456. Wld Hlth Org. 46, 801-805. MROPEF. M., BANGY. H.and TONNR. J. (1973) Compara- MANSFIELD-ADERSW. (1927) Notes on malaria and filar- tive trial of three larvicides against Culex pipiens fatigans iasis in the Zanzibar protectorate. Trans. R. Soc. trop. in Morogoro, Tanzania. Document WHOJVBCf73.452. Med. Hyg. 21, 207-214. MULLAM. (1976) Evolution of chemical control strategies MARSHALLJ. F. and STALEYJ. (1937) Some notes regarding for mosquitoes. Conventional, novel and natural chemi- ..---- Biology and control of Culex pipiens quinquefasciatus 337

cals. Proc. Pap. 44th Ann. Cot$ Calif: Mosquito Com. M. and SEBASTIANA. (1971) Studies on infiltration of ASSOC.Inc., pp. 71-77. marked Culex pipiens fatigam into sprayed areas in Ran- MUSPRATTJ. (1956) The Stegomyia mosquitoes of South goon, Burma. Bull. Wld Hlth Org. 45, 379-383. Africa and some neighbouring territories (including SELFL. S., USMANS., PANTC. P. and NELSONM. J. (1976) chapters on the mosquito-borne virus diseases of the A field trial with the insect growth regulator OMS-1805 Ethiopian zoo-geographical region of Africa). Mem. ent. (TH 6040) against Culex pipiens fatigam in Jakarta, Soc. sthp. Aj?. 4, 138 pp. Indonesia. Document WHOIVBC/76.625. NELSONG. S., HEISCHR. B. and FURLONGM. (1962) SELFL. S., NELSON,M. J., PANTC. P. and USMANS. (1978) Studies in filariasis in East Africa. II. Filarial infection in Field trials with two insect growth regulators against man, animals and mosquitoes on the Kenya Coast. Culex quiquefasciatus. Mosquito News 38(1), 74-79. Trans. R. Soc. trop. Med. Hyg. 56, 202-217. SERVICEM. W. (1963) The ecology of the mosquitoes of the NELSONM. J., SELFL. S. and PANTC. P. (1976) Field trials Northern Guinea savannah of Nigeria. Bull. ent. Res. 54, with the insect growth regulator OMS 1697 (Altocid, 601-632. Methoprene) against Culex pipiens fatigam in Jakarta, SERVICEM. W. (1965) The identification of blood-meals Indonesia. Document WHOIVBCJ76.604. from Culicine mosquitoes from Northern Nigeria. Bull. OGUNBAE. O. (1971) Observations on Culex pipiens fati- ent. Res. 55, 637-643. gam in Ibadan, Western Nigeria. Ann. trop. Med. Para- SERVICEM. W. (1966) The replacement of Culex nebulosus sit. 65, 399402. Theo. by Culex pipiens fatigam Wied. (Diptera, Culici- PATTERSONR. S., WEIDHAASD. E., FORDH. R. and LOF- dae) in towns in Nigeria. Bull. ent. Res. 56, 407415. GREN C. S. (1970) Suppression and elimination of an SERVICEM. W. (1976) Mosquito Ecology. Field Sampling island population of Culex pipiens quinquefasciatus with Methods. Applied Science, London. 583 pp. sterile males. Science 168, 1368-1370. SHARMAV. P., BATRAC. P. and BROOKSG. D. (1975) PETERSENJ. J. (1978) Development of resistance by the Laboratory and field evaluation of a growth-regulating southern house mosquito to the parasitic nematode compound (OMS-1804) against Culex pipiens fatigam. Rornanomerinis culicivorax. Environ. Ent. 7(4), 518-520. Document WHOIVBC/75.549. PRAKONGPHAN-URAI, NELSON M. J. and BOONLUAN SIMASATHIENP. and OLSONL. C. (1973) Factors influencing PHANTHUMACHINDA(1975) Control of Culex pipiens fati- the vector potential of Aedes aegypti and Culex gans (W.) by the larvivorous fish Poecilia reticulata and quinquefasciatus for Wesselbron virus. J. med. Ent. 10, by removal of debris from the breeding habitat. Docu- 587-590. ment WHOfVBCJ75.572. SINÈGREG., GAVENB. and JULLIENJ. L. (1979) Securité RAO T. R. (1975) Arboviruses and their vectors in India. d'emploi du sérotype H-14 de Bacillus thuringiensis pour Ind. J. med. Res. 63, 1219-1233. la faune non-cible des gîtes à moustiques du littoral REYNOLDSD. G. (1972) Experimental introduction of a méditerranéen fiançais. Docurllent WHOJVBC/79.742. microsporidian into a wild population of Culex pipiens SIRIVANAKARNS. and WHITEG. B. (1978) Neotype designa- fatigam Wied. Bull. Wld Hlth Org. 46, 807-812. tion of Culex quinquefasciatus Say (Diptera: Culicidae). RIBEIROH. and MEXIAJ. T. (1966) Research on the mos- Proc. ent. Soc. Wash. 80(3), 36G372. quitoes of Angola (Diptera: Culicidae). III. A survey in SMITHA. (1961) Observations on the man-biting habits of the Lobito-Catumbela region. Ann. Inst. Med. trop. 13, some mosquitoes in the South Pare area of Tanganyika. 167-182. E. Afr. med. J. 38, 246. ROUBAUDE. (1956) Phénomènes d'amixie dans les inter- SUBRAR. (1965) Culex pipiens fatigam Wiedemann, vecteur croisements de souches géographiques indifférenciées possible de la filariose urbaine à Wuchereria bancrofti extérieurement du moustique commun tropical Culex Cobbold en Afrique de l'ouest. Rap. fin. multigr. 58me fatigam Wied. C.R. Acad. Sci. (Paris) 242, 1557-1559. COI$ tech. OCCGE, Bobo-Dioulasso 1, 193-195. ROUBAUDE. and TOUMANOFFC. (1930) Intoxications d'en- SUBRAR. (1970) Etudes écologiques sur Culex pipiens fati- combrement, chez les larves de Culex en milieu non gans Wiedemann, 1828, (Diptera, Culicidae) dans une renouvelé. Bull. Soc. Path. exot. 23, 978-986. zone urbaine de savane soudanienne ouest-africaine. SALESS. and HERVYJ. P. (1977) L'évaluation au stade IV Lieux de repos des adultes. Cah. ORSTOM, Sir Bit. de l'éfficacité de l'OMS-1804 (Dimilin) contre les larves mid. Parasit. 8, 353-376. de Culex pipiens fatigam Wiedemann et Aedes aegypti SUBRAR. (1971a) Etudes écologiques sur Culex pipiens fati- Linne. Docunient WHOlVBCf77.655. gan~Wiedemann, 1828, (Diptera, Culicidae) dans une SARKARJ. K., HATIA. K. and MITRAA. G. (1973) Role of zone urbaine de savane soudanienne ouest-africaine. mosquitoes in the spread of smallpox (Dipt., Culicidae). Dynamique des populations préimaginales. Cah. J. iilfect. Dis. 128, 781-783. ORSTOM, Sir Ent. méd. Parasit. 9, 73-102. SASAM., KURIHARAT., DHAMVENIJO. and HARINSUTAC. SUBRAR. (1971b) Etudes écologiques sur Culex pipiens fati- (1965a) Studies on mosquitoes and their natural enemies gans Wiedemann, 1828, (Diptera, Culicidae) dans une ir, Bangkok. 3. Observations on a mosquito-eating fish zone urbaine de savane soudanienne ouest-africaine. 'guppy', Lebistes reticulatus, breeding in polluted waters. Rythme de ponte et facteurs conditionnant l'oviposition. Jap. J. exp. Med. 35, 63-80. Cali. ORSTOM, Sér. Ent. méd. Parasit. 9, 317-332. SASAM., KURIHARAT. and HARINASUTAC. (1965b) Studies SUBRAR. (1972a) Etudes écologiques sur Culex pipiens fati- on mosquitoes and their natural enemies in Bangkok. gam Wiedemann, 1828, (Diptera, Culicidae) dans une Part I. Observations on the bionomics of Culex pipiens zone urbaine de savane soudanienne ouest-africaine, fatigam Wiedemann. Jap. J. exp. Med. 35, 2349. Longévité et déplacements d'adultes marqués avec des SEBASTIANA. and MEILLOND. DE (1967) Experiments on poudres fluorescentes. Cah. ORSTOM. Sir. Ent. mid. the mating of Culex pipiens fatigam in the laboratory. Parasit. 10, 3-36. Bull. Wld Hlth Org. 36, 47-52. SUBRAR. (1972b) Etudes écologiques sur Culex pipiens fati- SELFL. S. and TUNM. M. (1970) Summary of field trials in gans Wiedemann, 1928, (Diptera, Culicidae) dans une 1964-1969 in Rangoon, Burma, of organophosphorus zone urbaine de Savanne soudanienne ouest-africaine. larvicides and oils against Culex pipiens fatigam larvae Tendances endo-exophages et cycle d'aggressivité. Cah. in polluted water. Bull. Wld Hltk Org. 43, 841-851. ORSTOM. Sér. Ent. méd. Parasit. 10, 335-345. SELFL. S., ABDULCADERM. H. M. and TUN M. M. (1969) SUBRAR. (1972~)Etudes écologiques sur Culex pipiens fati- Preferred biting sites of Culex pipiens fatigam on adult gans Wiedemann, 1828, (Diptera, Culicidae) dans une Burmese males. Bull. Wld Hlth Org. 40(2), 324-327. zone urbaine de savane soudanienne ouest-africaine. SELFL. S., TUNM. M., MATHISH. L., ABDULCADERM. H. Differenciation de diverses souches par leur relations

I.S.A. l/&--r 338 R. SUBRA

d'incompatibilité. Cah. ORSTOM, Sér. Ent. méd. Parasit. VAN SOMERENE. C. C., TEESDALEC. and FURLONGM. 10, 37-45. (1955) The mosquitoes of the Kenya coast; records of SUBRAR. (1973) Etudes écologiques sur Culex pipiens fati- occurrence, behaviour and habitat. Bull. ent. Res. 46, gans Wiedemann, 1828, (Diptera, Culicidae) dans une 463-493. zone urbaine de Savanne soudanienne ouest-africaine. VAN SOMERENE. C. C., HEISCHR. B. and FURLONGM. Dynamique des populations imaginales. Cah. ORSTOM, (1958) Observations on the behaviour of some mos- Sir. Ent. méd. Parasit. 11, 79-100. quitoes of the Kenya Coast. Bull. ent. Res. 49, 643-660. SUBRAR. (1975) Urbanisation et filariose de Bancroft en VELIMIROVICB. and CLARKEJ. L. (1975) Use of larvivorous Afriaue et à Madagascar. Cah. ORSTOM. Sir. Ent. méd. fish for vector control in the Maldives Republic. Tro- Parasit. 13, 193-26. penmed. Parasitol. 26, 503-506. SUBRAR.. BOUCHITEB. and Coz J. (1969) Evaluation sur le VERMEILC. (1955) Nouvelle contribution à l'étude du com- terrain' de l'efficacité de deux insecticides organophos- plexe Culex pipiens en Tunisie: sur un biotype recontré phorés l'abate et le dursban, contre les larves de Culex dans le secteur sub-saharien de ce pays. Bull. Soc. Sci. pipiens fatigans Wiedemann, 1828. Méd. trop. 29, nat. Tunis. 8, 33-35. 607-614. WANSONM. (1935) Note sur les trous de crabes, gîtes lar- SUBRAR., BOUCHITER. and GAYRALPH. (1970b) Evalu- vaires. Ann. Soc. Belge Mid. trop. 15, 575-585. ation à grande echelle du dursban et de l'abate pour le WHITEG. B. (1967) Mosquito breeding in Amani latrines, contrôle des larves du Culex pipiens fatigans Wiede- Annual Rep. E. Afr. Mal. Vect.-Borne Dis. 75-76. mann, 1828, dans la ville de Bobo-Dioulasso (Haute- WHITEG. B. (1971a) Studies on transmission of Bancrof- Volta). Mid. trop. 30, 393-402. tian filariasis in North-Eastern Tanzania. Trans. R. Soc. SUBRAR. and HEBRARDG. (1975) Ecologie larvaire de trop. Med. Hyg. 65, 819-829. Culex pipiens fatigans Wiedemann, 1828, (Diptera, Culi- WHITEG. B. (1971b) The present importance of domestic cidae) dans une zone de haute endémie filarienne mosquitoes (Culex pipiens fatigans Wiedemann) in East (Mayotte, Archipel des Comores). Tropenmed. Parasit. Africa and recent steps towards their control. E. Afr. 26,48-59. med. J. 48, 266274. SUBRAR., HEBRARDG. and RABENIRAINYL. (1973) Essai de WIJERSD. J. B. and KIILUG. (1978) Bancroftian filariasis lutte contre Anopheles gambiae s.l. et Culex pipiens fati- in Kenya. III. Entomological investigations in Mambrui, gans Wiedemann, 1828, par les larvicides dans une zone a small coastal town, and Jaribuni, a rural area more d'endémie filarienne (Mayotte, Archipel des Comores). inland (Coast Province). Ann. trop. Med. Parasit. 71(3), Cah. ORSTOM, Sir. Ent. mid. Parasit. 11, 225-231. 347-359. SUBRAR., ROY L., ACCROMBESSIR. and PANGALETP. WILLSW., SAIMOTG., BROCHARDCH., BLUNBERGB. S., (1970a) Projet pour l'exécution d'une campagne anti- LONDONW. T., DECHENER. and MILLMANP. (1976) moustique dans la ville de Bamako. Doc. mim OCCGE, Hepatitis B. surface antigen (Australia antigen) in mos- Bobo-Dioulasso, 169/Ent./70. quitoes collected in Senegal, West Africa. Am. J. trop. SUBRAR., SALESS. and DYENMKOUMAA. (1965) Prospec- Med. Hyg. 25, 186-190. tion entomologique en République du Mali. Doc. mim. WORLDHEALTH ORGANIZATION (1970) Insecticide resist- non publié OCCGE, Bobo-Dioulasso. ance and vector control. Wld Hlth Org. Techn. Rep. 443, SURTEESG. (1959) On the distribution and seasonal inci- 280 pp. dence of culicine mosquitoes in southern Nigeria. Proc. WORLDHEALTH ORGANIZATION (1974) WHO Expert Com- R. ent. Soc. Lond. (A)34, 110-120. mittee on Filariasis. Wld Hltlt Org. Techn. Rep. 542,54 pp. SURTEESG. (1970) Large-scale irrigation and arbo-virus WORLDHEALTH ORGANIZATION (1975) Ecology and con- epidemiology, Kano plain, Kenya I. Description of the trol of vectors of public health importance. Wld Hlth area and preliminary studies on the mosquitoes. J. med. Org. techn. Rep. 561, 35 pp. Ent. 7, 509-517. WORLDHEALTH ORGANIZATION (1978) Rift Valley fever. TEESDALEC. (1941) Pineapple and banana plants as sources Wkly epidem. Rec. 53(32), 238. of Aedes mosquitoes. E. Afr. med. J. 18, 260-267. YASUNOM. and HARINASUTAC. (1967) The studies of the TEESDALEC. (1959) Observations on the mosquito fauna of behaviour of Culex pipiens fatigans with special reference Mombasa. Bull. ent. Res. 50, 191-208. to dispersal, mating and feeding. Jap. J. exp. Med. 37, TESHR. B. and GUBLERD. J. (1975) Laboratory studies of 525-534. transovarial transmission of La Crosse and other arbo- YASUNOM., MACDONALDW. W., CURTISC. F., GROVERK. viruses by Aedes albopictus and Culex fatigans. Am. J. K., RAJAGOPALANP. K., SHARMAV. P., SINGHD., SINGH trop. Med. Hyg. 24, 876-880. K. R. P., AGARWALH. V., KAZMIS. J., MENONR., RAZ- TESH R. B. and ROSENL. (1975) Failure of rubella virus to DAN R. K., SAMUELD. and VAIDYANATHANV. (1978) A replicate in mosquitoes. Intervirology 5, 216-219. control experiment with chemosterilized male Culex THOMAST. C. ,E. (1956) A note on the occurrence of Culex pipiens fatigans Wied. in a village near Delhi surrounded (Culex pipiens$atigans) in Sierra Leone. Ann. trop. Med. by a breeding-free zone. Jap. J. sanit. Zool. 29, 325-343. Parasit. 50, 421-425. YASUNO M., RAJAGOPALANP. K. and LABRECQUEG. C. TOUMANOFFC., SIMONDN. and BAH BOUBACAR(1956) (1975) Migration patterns of Culex fatigans around Quelques observations sur la faune culicidienne de la Delhi, India. Trop. Med. 17, 91-96. Basse-Guinée (Conakry et la Presqufle de Kaloum) (Sai- YASUNO M., RAJAGOPALANP. K., RUSSELES. and LA- son sèche de l'année 1956). Bull. Soc. path exot. 49, BRECQUE G. C. (1973) Influence of seasonal changes in 661-674. climate on dispersal of released Culex pipiensfatigans. A TRPISM., HARTBERGW. K., TEESDALEC. and MCCLEL- study in villages in Delhi Union Territory, India. Bull. LAND G. A. H. (1971) Aedes aegypti and Aedes simpsoni Wld Hlth Org. 48, 317-321. breeding in coral rock holes on the coast of Tanzania. YASUNOM., SINGHN. and CHOWDHURYD. S. (1972) Field Bull. Wld Hlth Org. 45, 425-531. studies on the mating behaviour of Culex fatigans. Docu- VANSOMEREN E. C. C. and FURLONGM. (1964) The biting ment WHO/VBC/72.390. habits of Aedes (Skusea) pembaensis Theo. and some ZIELKEE. and KUHLOWF. (1977) On the inheritance of other mosquitoes of Faza, Pate Island, East Africa. Bull. susceptibility for infection with Wuchereria bancrofti in ent. Res. 55, 97-124. Culex pipiens fatigans. Tropenmed. Parasit. 28, 68-70.