Quantifying flight aptitude variation in wild Anopheles gambiae in order to identify long-distance migrants

Roy Faiman,Tovi Lehmann,Moussa Diallo,Adama Dao,Zana L Sanogo,Samake Djibril,Benjamin J Krajacich,Margery Sullivan,Alpha S Yaro,Asha Krishna

doi:10.1186/s12936-020-03333-2

Abstract

BackgroundIn the West African Sahel, mosquito reproduction is halted during the 5–7 month-long dry season, due to the absence of surface waters required for larval development. However, recent studies have suggested that both Anopheles gambiae sensu stricto (s.s.) and Anopheles arabiensis repopulate this region via migration from distant locations where larval sites are perennial. Anopheles coluzzii engages in more regional migration, presumably within the Sahel, following shifting resources correlating with the ever-changing patterns of Sahelian rainfall. Understanding mosquito migration is key to controlling malaria—a disease that continues to claim more than 400,000 lives annually, especially those of African children. Using tethered flight data of wild mosquitoes, the distribution of flight parameters were evaluated as indicators of long-range migrants versus appetitive flyers, and the species specific seasonal differences and gonotrophic states compared between two flight activity modalities. Morphometrical differences were evaluated in the wings of mosquitoes exhibiting high flight activity (HFA) vs. low flight activity (LFA).MethodsA novel tethered-flight assay was used to characterize flight in the three primary malaria vectors- An. arabiensis, An. coluzzii and An. gambiae s.s. The flights of tethered wild mosquitoes were audio-recorded from 21:00 h to 05:00 h in the following morning and three flight aptitude indices were examined: total flight duration, longest flight bout, and the number of flight bouts during the assay.ResultsThe distributions of all flight indices were strongly skewed to the right, indicating that the population consisted of a majority of low-flight activity (LFA) mosquitoes and a minority of high-flight activity (HFA) mosquitoes. The median total flight was 586 s and the maximum value was 16,110 s (~ 4.5 h). In accordance with recent results, flight aptitude peaked in the wet season, and was higher in gravid females than in non-blood-fed females. Flight aptitude was also found to be higher in An. coluzzii compared to An. arabiensis, with intermediate values in An. gambiae s.s., but displaying no statistical difference. Evaluating differences in wing size and shape between LFA individuals and HFA ones, the wing size of HFA An. coluzzii was larger than that of LFAs during the wet season—its length was wider than predicted by allometry alone, indicating a change in wing shape. No statistically significant differences were found in the wing size/shape of An. gambiae s.s. or An. arabiensis.ConclusionsThe partial agreement between the tethered flight results and recent results based on aerial sampling of these species suggest a degree of discrimination between appetitive flyers and long-distance migrants although identifying HFAs as long-distance migrants is not recommended without further investigation.

Highlights

In the West African Sahel, mosquito reproduction is halted during the 5–7 month-long dry season, due to the absence of surface waters required for larval development
Flight activity and identification of putative long‐distance flyers (LDMs) To determine if flight activity was concentrated in certain parts of the night, we examined three indices, namely (1) number of hourly flight bouts, (2) longest flight bout, and (3) total hourly flight (Fig. 3)
There was a mild modality, suggesting elevated total flight and flight bouts between 11:00 and 02:00 h, this modality was not found to be statistically supported by the 95% CI which overlapped widely

Summary

Introduction

In the West African Sahel, mosquito reproduction is halted during the 5–7 month-long dry season, due to the absence of surface waters required for larval development. The primary focus of this work is with the Sahelian Zone of West Africa, where mass seasonal migrations of pest insects, such as grasshoppers and pyrrhocorid bugs, into- and back out of the Sahel in Mali and Niger have been described [19,20,21,22]. These migrations follow cyclical shifts in wind direction as the Inter-Tropical Convergence Zone (ITCZ) moves north during March–August, south during September–February, with the migrants taking advantage of ephemeral, but seasonally available, dependable habitats. Because it is easier to notice immigration into areas depleted of conspecific populations, many other cases of insect migration have likely been discounted

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Conclusion