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Biological Variation in Anopheles Darlingi Root Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(4): 391-398, Jul./Aug. 1996 391 Biological Variation in Anopheles darlingi Root JD Charlwood Swiss Tropical Institute, Socinstrasse 57, Basel CH 4002, Switzerland Behavioural variation in the South American malaria vector Anopheles darlingi is described. At the centre of its distribution, in forest areas close to the city of Manaus, Brazil, it is primarily exophagic and exophilic. Mosquitoes from this area are chromosomally diverse. Towards the northern edge of its distribution (in Guyana and Venezuela) it is more endophagic and less diverse chromosomally. Simi- larly in the south (in the state of Minas Gerais) it is less polymorphic. In this area, however, it is prima- rily zoophilic and exophagic. Evidence is presented that female wing size may vary between popula- tions. The possibility that this widely distributed species may be a complex could have important impli- cations for future malaria control schemes. Key words : Anopheles darlingi - biting - host preference - resting - species complex According to the theory of forest refugia (Haffer sect to transmit disease: (1) abundance; (2) con- 1969, 1974) the Amazonian rain forest contracted tact with man; (3) susceptibility to infection; and into isolated patches, or refuges, during dry peri- (4) longevity (Gillies 1988). Factors which influ- ods in the Pleistocene with secondary ence human mosquito contact, such as the propen- intergradiation when the rainfall increased. The sity to enter houses to feed, the host preference fragmentation of the forest would have provided and the behaviour after feeding are particularly an excellent templet for the occurrence of allopat- important. ric differentiation within a species, which may have Apart from a few isolated instances (Arruda et eventually resulted in speciation. The observed al. 1986, Branquinho et al. 1993) where it occurs variation within Heliconius (Brown et al. 1974), Anopheles darlingi Root is the major, or only, vec- Drosophila (Spassky et al. 1971), Anolis (Vanzolini tor of human malaria (Forattini 1962, Lourenço- & Williams 1970) as well as birds (Haffer 1969, de-Oliveira et al. 1989). It is largely responsible 1974), mammals (Hershkovitz 1969) and plants for the upsurge of malaria in Brazil (Charlwood et (Prance 1974) is regarded as supporting evidence al. 1995 a). It has a range that extends from south- for the refugia hypothesis. ern Mexico to the south of Brazil (Forattini 1962). Even if this were not the case, isolation by dis- This broad range implies a priori that variations in tance could be important in promoting genetic di- its biology are likely to exist (Giglioli 1956, Rachou vergence (Endler 1977) since most species do not 1958, Zimmerman 1992). This paper summarises have continuously distributed populations and gene some of the information concerning An. darlingi flow between clumped demes is normally and discusses the effect that the insects’ behaviour leptokurtic (because many more individuals move may have on malaria transmission. The role that smaller distances than would be expected if they environmental or genetic factors may have on de- moved at random). Hence, species distributed over termining aspects of behaviour are discussed as broad geographic ranges are more likely to be di- potential methods of control especially in the rela- vided by changes in geomorphology and climate tively isolated settlements such as are often found than species with limited ranges. They are also in newly opened areas of rainforest, where malaria more likely to have greater habitat diversity and is particularly prevalent. are likely to develop clines and subspecies. This Abundance and survival - In order for disease is of more than academic interest in insects such transmission to be sustained sufficient numbers of as mosquitoes which are vectors of disease, be- vectors must occur in relatively close proximity to cause variations in their biology and behaviour may humans. Numbers of adult An. darlingi are often influence their vectorial capacity (Elliot 1972). clustered in relatively small areas. This is prob- Four factors may influence the capacity of an in- ably a function of relative distance to breeding sites since abundance is largely dependant on lar- val ecology. An. darlingi breeds in partially shaded, neutral, unpolluted and relatively still pools of water. In newly opened up areas of rainforest these Received 6 January 1995 pools are often man made and are the result of Accepted 21 March 1996 badly made culverts that act as bridges for roads 392 Biological Variation in A. darlingi Root JD Charlwood whenever a stream is encountered. On the upstream its domesticity (Davis 1931, Shannon 1933). In side of such crossings long, snaking lakes are Guyana Giglioli (1948) found that it was the most formed that act as year round breeding sites for common anopheline captured inside houses (over mosquitoes. Since water is a valuable asset to set- 99%). It was also reported resting inside houses in tlers, houses are often located close to such blocked Surinam by Van der Kuyp (1954) and was reported streams. This reduces the need for long flights by to be common inside houses in some areas of Bra- the mosquito which facilitates malaria transmis- zil, particularly the south (Galvão et al. 1942, Deane sion. Improvement in the construction of drain- et al. 1948). This endophilism contributed to the age ditches, particularly on the smaller dirt roads, initial success of the DDT house spraying cam- could perhaps have a profound effect on malaria paign in Guyana and Venezuela (Giglioli 1951, transmission. It is also found in pools alongside Gabaldon & Berti 1954). The resting position rivers. Annual population cycles are dependant within the house is also of obvious importance in on a complex series of factors, such as rainfall assessing the likely effect of insecticides. The (Bruyning 1952, Charlwood 1980) or water table preferred resting site within houses appears to dif- (Klein & Lima 1990, Rozendaal 1992). In many fer between areas. In Colombia the majority of areas peak numbers occur at the end of the rainy females rest within 1m of the floor (Quinones & season when abundant water remains available and Suarez 1990) whereas in a study from Acre, Brazil when the likelihood of flushing by excessive rain- most were collected from the ceiling (Roberts et fall is reduced. In Costa-Marques in Rondônia and al. 1987). It is known that the material used in the on BR 174 between Manaus and Boa Vista there construction of the house, the number of openings is an associated peak in the number of malaria cases and amount of smoke in the house may affect time among settlers at these times. For much of the an- spent inside the house and resting site in African nual cycle An. darlingi populations are very small anophelines (Gillies & DeMeillon 1968). This is (Hayes & Charlwood 1979, Charlwood 1980, also likely to be true for South American endophilic Hudson 1984, Rozendaal 1992). This low density anophelines. makes it difficult to monitor populations even in In many areas, however readily it enters houses the absence of control measures. to feed, An. darlingi only spends a few minutes The problems associated with catching suffi- inside. In Surinam, Hudson (1984) estimated that ciently large samples has meant that very little work the mosquitoes spent an average of 7.7 min inside has been performed on survival rate determination a house before and 17.1 min after feeding. In Mato of An. darlingi. No substantial information con- Grosso, Brazil, the pre-biting period was approxi- cerning seasonal or geographical variation in sur- mately 10 min (Charlwood 1980) and Colombia vival have been reported, although a greater pro- the total time spent inside houses was estimated to portion of potential vectors (i.e. those that were be 150 min (Elliott 1972). In these areas, and also three parous or older) were found during a limited in Minas Gerais, Brazil, females are commonly series of dissections from Amazonas (Charlwood seen on the exterior walls of houses (Bustamante 1980) compared to a population from Mato Grosso & Guedes 1950). Such behaviour has been re- (Charlwood & Wilkes 1979). Survival in these ported for mosquitoes from areas where the inside populations was age dependant and fitted a walls of houses have been sprayed with DDT Gompertz curve (Clements & Paterson 1981). In (Hayes & Charlwood 1977, Charlwood & capture-recapture experiments in Rondônia An. Paraluppi 1978, Charlwood & Wilkes 1979, darlingi was the most long lived of the local spe- Charlwood 1980). In Surinam Rozendaal (1989) cies and the only one caught in any numbers close considered that, despite a limited period spent in- to the house used in the experiments. All other side houses, indoor spraying with DDT would still species, including An. triannulatus and An. provide effective control. Physiological resistance oswoldoi, two vectors from other states of Brazil to DDT by An. darlingi has only been reported from were only caught away from the house close to a single population from Columbia despite many water (Charlwood & Alecrim 1988). years of spraying by malaria control programs Man mosquito contact - Endophiliy - A great throughout South America (Suarez et al. 1990). deal of interest attaches to the sites of contact be- Nevertheless, perhaps because of this heightened tween man and vector, largely because of their exophiliy, control with DDT has not been achieved importance for control by house-spraying. Two in many malarious areas. The use of rapid action factors influence the relative numbers biting in- synthetic pyrethroids has recently been shown to doors and outdoors: reactions to the house itself achieve a much greater degree of control and the timing of biting activity. (Charlwood et al. 1995a) and shows promise for Throughout its range An. darlingi readily en- the future. Selection for an even greater degree of ters houses to feed and early observers emphasised outdoor biting, as occurred in An.
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