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Research article - Peer-reviewed, 2021

Wild populations of malaria vectors can mate both inside and outside human dwellings

Nambunga, Ismail H.; Msugupakulya, Betwel J.; Hape, Emmanuel E.; Mshani, Issa H.; Kahamba, Najat F.; Mkandawile, Gustav; Mabula, Daniel M.; Njalambaha, Rukiyah M.; Kaindoa, Emmanuel W.; Muyaga, Letus L.; Hermy, Marie R. G.; Tripet, Frederic; Ferguson, Heather M.; Ngowo, Halfan S.; Okumu, Fredros O.

Abstract

Background Wild populations of Anopheles mosquitoes are generally thought to mate outdoors in swarms, although once colonized, they also mate readily inside laboratory cages. This study investigated whether the malaria vectors Anopheles funestus and Anopheles arabiensis can also naturally mate inside human dwellings. Method Mosquitoes were sampled from three volunteer-occupied experimental huts in a rural Tanzanian village at 6:00 p.m. each evening, after which the huts were completely sealed and sampling was repeated at 11:00 p.m and 6 a.m. the next morning to compare the proportions of inseminated females. Similarly timed collections were done inside local unsealed village houses. Lastly, wild-caught larvae and pupae were introduced inside or outside experimental huts constructed inside two semi-field screened chambers. The huts were then sealed and fitted with exit traps, allowing mosquito egress but not entry. Mating was assessed in subsequent days by sampling and dissecting emergent adults caught indoors, outdoors and in exit traps. Results Proportions of inseminated females inside the experimental huts in the village increased from approximately 60% at 6 p.m. to approximately 90% the following morning despite no new mosquitoes entering the huts after 6 p.m. Insemination in the local homes increased from approximately 78% to approximately 93% over the same time points. In the semi-field observations of wild-caught captive mosquitoes, the proportions of inseminated An. funestus were 20.9% (95% confidence interval [CI]: +/- 2.8) outdoors, 25.2% (95% CI: +/- 3.4) indoors and 16.8% (+/- 8.3) in exit traps, while the proportions of inseminated An. arabiensis were 42.3% (95% CI: +/- 5.5) outdoors, 47.4% (95% CI: +/- 4.7) indoors and 37.1% (CI: +/- 6.8) in exit traps. Conclusion Wild populations of An. funestus and An. arabiensis in these study villages can mate both inside and outside human dwellings. Most of the mating clearly happens before the mosquitoes enter houses, but additional mating happens indoors. The ecological significance of such indoor mating remains to be determined. The observed insemination inside the experimental huts fitted with exit traps and in the unsealed village houses suggests that the indoor mating happens voluntarily even under unrestricted egress. These findings may inspire improved vector control, such as by targeting males indoors, and potentially inform alternative methods for colonizing strongly eurygamic Anopheles species (e.g. An. funestus) inside laboratories or semi-field chambers.

Keywords

Mosquito mating; Anopheles funestus; Anopheles arabiensis; Eurygamic species; Malaria; Tanzania

Published in

Parasites and Vectors
2021, volume: 14, number: 1, article number: 514
Publisher: BMC

Authors' information

Nambunga, Ismail H.
Ifakara Health Institute
Nambunga, Ismail H.
University of Glasgow
Msugupakulya, Betwel J.
Ifakara Health Institute
Msugupakulya, Betwel J.
Nelson Mandela African Institution of Science and Technology
Hape, Emmanuel E.
Ifakara Health Institute
Hape, Emmanuel E.
University of Glasgow
Mshani, Issa H.
Ifakara Health Institute
Mshani, Issa H.
University of Glasgow
Kahamba, Najat F.
University of Glasgow
Kahamba, Najat F.
Ifakara Health Institute
Kahamba, Najat F.
Nelson Mandela African Institution of Science and Technology
Mkandawile, Gustav
Ifakara Health Institute
Mabula, Daniel M.
Ifakara Health Institute
Njalambaha, Rukiyah M.
Ifakara Health Institute
Kaindoa, Emmanuel W.
Ifakara Health Institute
Kaindoa, Emmanuel W.
University of Witwatersrand
Kaindoa, Emmanuel W.
Nelson Mandela African Institution of Science and Technology
Muyaga, Letus L.
Ifakara Health Institute
Swedish University of Agricultural Sciences, Department of Plant Protection Biology
Tripet, Frederic
Keele University

Sustainable Development Goals

SDG3 Good health and wellbeing

UKÄ Subject classification

Ecology
Public Health, Global Health, Social Medicine and Epidemiology

Publication Identifiers

DOI: https://doi.org/10.1186/s13071-021-04989-8

URI (permanent link to this page)

https://res.slu.se/id/publ/114053