Plant-Feeding Behaviour and its Effects on the Fitness and Competence of the Malaria Vector Anopheles Gambiae (Diptera: Culicidae)

Abstract

Malaria remains a serious threat in sub-Saharan Africa Available control tools are now largely ineffective. Because of the role of vectors in malaria transmission, integrated vector management strategies that are environmentally safe, economically feasible and acceptable to resource-limited communities are one way to achieve effective malaria control. However, adequate knowledge of the biology, behaviour and ecology of the malaria vectors are imperative. Sugar-feeding from plants is a basic requirement for adult mosquitoes, and so far have received little attention. The present study, conducted in Suba district (a malaria endemic area of western Kenya), aimed to investigate the plant-feeding behaviour and its effects on the fitness and competence of Anopheles gambiae. Females of two species of Anopheles gambiae s. l. namely Anopheles gambiae s.s., and Anopheles arabiensis were sampled during both dry and wet seasons. Approximately 12% were fructose-positive at the time of collection, indicating recent plant-feeding. Proportions of plant-fed mosquitoes were similar in all the 2 Anopheles species (P=0.90), at all their gonotrophic status (unfed, blood-fed, half-gravid, and gravid) (P=0.69), at all ages (parous and nulliparous) (P=0.98), and during both seasons (P=0.06). However, more mosquitoes had fed on plants when collected far from larval habitats (P=0.001). When offered 13 dominant plant species [Cassia hirsuta L., Senna bicopsularis L., Senna didymobotrya F. (Leguminosae), Daturo stramonium L. (Solanaceae), Flaveria trinervia M., Parthenium hysterophorus L., I'siada punctulata V., Tithonia diversifolia H. (Asteraceae), Hamelia patens J. (Rubiaceae), Ipomea hildebrandtie V. (Convolvulaceae), Lantana camara L. (Verbenaceae), Ricinus communis L. (Euphorbiaceae), Tecoma stans L. (Bignoniaceae)) growing around human dwellings and mosquito larval habitats in the study area, behavioural responses of mosquitoes to those candidate plants were recorded in the greenhouse, each plant being presented to mosquitoes singly, and concurrently with other plants species in the no-choice and choice bioassays respectively. Gas chromatography analysis was carried out to determine and compare plants and mosquito sugar profiles. Five plants species were found to be most preferred by Anopheles gambiae, namely; Ricinus communis L., Senna didymobotrya F., Parthenium hysterophorus L., Tecoma stans L., and Hamelia patens J (P<0.001). Flowers were most fed on by mosquitoes, but leaves were most preferred in two plants species (Lantana camara and Parthenium hysterophorus); leaves and stems in Ricinus communis. With the exception of one plant species (Parthenium hysterophorus), survival (P<0.001) and fecundity (P=0.01) were high in the mosquitoes which fed on most of the preferred plants, compared to those which fed on the less preferred plant. Sugar composition and concentration in the preferred plants were positively correlated to the survival (r=1, P<0.001) and fecundity (r-0.87, P=0.04) of mosquitoes. Four plants species (Lantana camara, Senna didymobotrya, Ricinus communis and Parthenium hysterophorus) significantly reduced the prevalence of infection in mosquitoes (P<0.01). There was also a drastic decrease on the parasite load (oocyst intensity) in the midguts of the infected mosquitoes which fed on 3 plants species (Lantana camara, Senna didymobotrya and Pathernium hysterophorus) (P<0.01). The inhibitory effects of those plants were more pronounced when mosquitoes plant-fed throughout (before and after) an infectious blood meal, followed by plant-feeding post-infection. The greatest impact of deleterious plants was found in the transitions macrogamete-ookinete (only in pre-infection plant-feeding) and ookinete-oocyst (only in post-infection plant-feeding). These studies imply that certain plant species preferred by Anopheles gambiae in the endemic area significantly decrease their fitness and competence to develop Plasmodium falciparum, and therefore can reduce malaria transmission.