Abstract

Rapidly emerging insecticide resistance is creating an urgent need for new active ingredients to control the adult mosquitoes that vector malaria. Biopesticides based on the spores of entomopathogenic fungi have shown considerable promise by causing very substantial mortality within 7–14 days of exposure. This mortality will generate excellent malaria control if there is a high likelihood that mosquitoes contact fungi early in their adult lives. However, where contact rates are lower, as might result from poor pesticide coverage, some mosquitoes will contact fungi one or more feeding cycles after they acquire malaria, and so risk transmitting malaria before the fungus kills them. Critics have argued that ‘slow acting’ fungal biopesticides are, therefore, incapable of delivering malaria control in real-world contexts. Here, utilizing standard WHO laboratory protocols, we demonstrate effective action of a biopesticide much faster than previously reported. Specifically, we show that transient exposure to clay tiles sprayed with a candidate biopesticide comprising spores of a natural isolate of Beauveria bassiana, could reduce malaria transmission potential to zero within a feeding cycle. The effect resulted from a combination of high mortality and rapid fungal-induced reduction in feeding and flight capacity. Additionally, multiple insecticide-resistant lines from three key African malaria vector species were completely susceptible to fungus. Thus, fungal biopesticides can block transmission on a par with chemical insecticides, and can achieve this where chemical insecticides have little impact. These results support broadening the current vector control paradigm beyond fast-acting chemical toxins.

Highlights

  • Current strategies for malaria control center on the use of chemical insecticides against the adult mosquito vectors [1]

  • Since initial reports demonstrated the basic premise of this approach [7,8], studies have explored the impact of fungal pathogens on the survival of a range of mosquitoes that vector disease [9,10,11,12,13,14,15], virulence against insecticide-resistant mosquitoes [16,17,18], possible methods of biopesticide delivery [19,20], and the impact of sub- and pre-lethal effects of infection on vectorial capacity [7,21]

  • How do dose and exposure time affect efficacy on a natural substrate sprayed with a simple formulation of fungal spores? Second, what is the combined impact of lethal and pre-lethal effects of fungal infection on the capacity of mosquitoes to transmit malaria? Third, are insecticide resistant mosquitoes vulnerable to fungal attack? We find that through a combination of lethal and pre-lethal effects, the candidate biopesticide can produce extensive transmission blocking within a single feeding cycle

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Summary

Introduction

Current strategies for malaria control center on the use of chemical insecticides against the adult mosquito vectors [1]. Since initial reports demonstrated the basic premise of this approach [7,8], studies have explored the impact of fungal pathogens on the survival of a range of mosquitoes that vector disease [9,10,11,12,13,14,15], virulence against insecticide-resistant mosquitoes [16,17,18], possible methods of biopesticide delivery [19,20], and the impact of sub- and pre-lethal effects of infection on vectorial capacity [7,21].

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