Diurnal biting of malaria mosquitoes in the Central African Republic indicates residual transmission may be "out of control"

Abstract

Malaria control interventions target nocturnal feeding of the Anopheles vectors indoors to reduce parasite transmission. Mass deployment of insecticidal bed nets and indoor residual spraying with insecticides, however, may induce mosquitoes to blood-feed at places and at times when humans are not protected. These changes can set a ceiling to the efficacy of these control interventions, resulting in residual malaria transmission. Despite its relevance for disease transmission, the daily rhythmicity of Anopheles biting behavior is poorly documented, most investigations focusing on crepuscular hours and nighttime. By performing mosquito collections 48-h around the clock, both indoors and outdoors, and by modeling biting events using circular statistics, we evaluated the full daily rhythmicity of biting in urban Bangui, Central African Republic. While the bulk of biting by Anopheles gambiae, Anopheles coluzzii, Anopheles funestus, and Anopheles pharoensis occurred from sunset to sunrise outdoors, unexpectedly ∼20 to 30% of indoor biting occurred during daytime. As biting events did not fully conform to any family of circular distributions, we fitted mixtures of von Mises distributions and found that observations were consistent with three compartments, corresponding indoors to populations of early-night, late-night, and daytime-biting events. It is not known whether these populations of biting events correspond to spatiotemporal heterogeneities or also to distinct mosquito genotypes/phenotypes belonging consistently to each compartment. Prevalence of Plasmodium falciparum in nighttime- and daytime-biting mosquitoes was the same. As >50% of biting occurs in Bangui when people are unprotected, malaria control interventions outside the domiciliary environment should be envisaged.

Keywords: Anopheles; Central African Republic; biting behavior; residual malaria; vector control.

Fig. 1.

Overview of diel biting events by malaria vectors in the Central African Republic. (A) Mosquito collection sites in the city of Bangui (source: https://OpenStreetMap.org). (B) Circular representation of biting events, kernel distributions (lines), sample mean directions ⍬, and resultant lengths R depicted as arrow vectors on the unit circle for each species and location. Darker colors represent indoor collections, and lighter colors outdoor collections. (C) Linear representation of biting events during the day expressed by the cumulative sample distribution curves of the relative frequency of landings on human collectors. The gray areas represent nighttime.

Fig. 2.

Fitting mixtures of von Mises circular distributions. (A) Frequency distribution of number of compartments that best fit the observed circular distribution of biting events in monthly samples. Colors pertain to the nature of the sample: A. gambiae (red/dark red), A. coluzzii (blue/dark blue), A. funestus (yellow/brown), and A. pharoensis (violet/purple). Darker colors represent indoor collections, lighter colors outdoor collections. (B) Circular and linear representations of assignment of biting events to compartments assuming conservatively K = 3 across species and locations. Blue, cluster 1; green, cluster 2; and red, cluster 3. Arrows represent mean directions of each cluster, with lengths indicating the concentration parameter. x axis, time in hours. Gray areas visualize nighttime.

Fig. 3.

Impact of diurnal biting activity on residual malaria transmission in Bangui. (A) Sampling coverage of the studies reviewed by Sherrard-Smith et al. (24) denoted by the hour-by-hour frequency of recorded biting activity. Gray areas represent nighttime. None of the reviewed studies cover the period from 0900 to 1700 hours (white dots). (B) Hourly distribution along the day of the proportion of mosquitoes’ bites (λ, dots in the figure) in relation to the average proportion of people indoors (orange dashed line) or in bed (orange continuous line). White dots designate the period when biting occurs when people are not in households. (C) Combined mosquito and human activity data estimating mosquito biting risk expressed by the mean proportion of bites (black dots in B) taken while humans are indoors (Φ_I) or in bed (Φ_B). A. gambiae (red), A. coluzzii (blue), A. funestus (yellow), and A. pharoensis (violet). Each gray dot represents the corresponding values of individual studies of the systematic review (24). (D) Summary of the observed proportion of mosquito bites by species according to location and period of the day: A. gambiae (red), A. coluzzii (blue), A. funestus (yellow), and A. pharoensis (violet). (E) Prevalence of P. falciparum DNA in the head/thorax of a subset of Anopheles specimens (n = 271) randomly chosen from the dataset according to the period of the day when they were collected.