The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel

Abstract

Background: Persistence of African anophelines throughout the long dry season (4-8 months) when no surface waters are available remains one of the enduring mysteries of medical entomology. Recent studies demonstrated that aestivation (summer diapause) is one mechanism that allows the African malaria mosquito, Anopheles gambiae, to persist in the Sahel. However, migration from distant localities - where reproduction continues year-round - might also be involved.

Methods: To assess the contribution of aestivating adults to the buildup of populations in the subsequent wet season, two villages subjected to weekly pyrethrum sprays throughout the dry season were compared with two nearby villages, which were only monitored. If aestivating adults are the main source of the subsequent wet-season population, then the subsequent wet-season density in the treated villages will be lower than in the control villages. Moreover, since virtually only M-form An. gambiae are found during the dry season, the reduction should be specific to the M form, whereas no such difference is predicted for S-form An. gambiae or Anopheles arabiensis. On the other hand, if migrants arriving with the first rain are the main source, no differences between treated and control villages are expected across all members of the An. gambiae complex.

Results: The wet-season density of the M form in treated villages was 30% lower than that in the control (P < 10-4, permutation test), whereas no significant differences were detected in the S form or An. arabiensis.

Conclusions: These results support the hypothesis that the M form persist in the arid Sahel primarily by aestivation, whereas the S form and An. arabiensis rely on migration from distant locations. Implications for malaria control are discussed.

Figure 1

A schematic map showing locations of the four focal villages (red large dots). The nearest village (gray dots) and nearest permanent surface waters (blue dots) to each of the focal villages are shown as well as the site of a previous study (Thierola), to which several citations were made. Roads (unpaved) are shown in gray and the largest town (Banamba) is marked as a gray square. Additional information is provided in Table 1.

Figure 2

Species and molecular form composition in the four villages over time, based on 4,584 mosquitoes which were successfully genotyped to species and molecular form (see text for details). Note that the time intervals are variable. Pooling of adjacent dates was carried out if samples were small and only if minimal differences in composition were found. Except for the period marked '2Feb10' that covered samples from January to March, other pooled samples represent periods shorter than three weeks between June and October 2010. Numbers above bars show cases where sample size per village/period were smaller than 20. Significant heterogeneity among villages (P < 0.05, after the sequential Bonferroni procedure) is denoted by stars.

Figure 3

Overall density (number of mosquitoes/house) in treated (red) and control (black) villages over time, measured by pyrethrum spray collections in 25 houses/village every month until the first rain and every 10 d thereafter. The density of the molecular forms of An. gambiae and of An. arabiensis was estimated by multiplying the density of An. gambiae s.l. (upper panel) by the corresponding fraction representing the relevant taxon in the corresponding village and time period. The yellow shading denotes the period of treatment in treated villages (from the desiccation of the last larval site 10 km around the village and until the first rain).

Figure 4

Density (number of mosquitoes/house) in each pair of treated (red) and control (black) villages over time (for further details, see legend of Figure 3).