The effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)

Abstract

BackgroundAnopheles arabiensis is a major malaria vector in Africa. Adult females are likely to imbibe multiple blood meals during their lifetime. This results in regular exposure to potential toxins and blood-meal induced oxidative stress. Defence responses to these stressors may affect other factors of epidemiological significance, such as insecticide resistance and longevity. The aims of this study were to examine the effect of multiple blood-feeding on insecticide tolerance/resistance with increasing age, to assess the underlying biochemical mechanisms for the responses recorded, and to assess the effect of multiple blood-feeding on the life histories of adult females drawn from insecticide resistant and susceptible laboratory reared An. arabiensis.MethodsLaboratory reared An. arabiensis females from an insecticide resistant and an insecticide susceptible colony were offered either a single blood meal or multiple blood meals at 3-day intervals. Their tolerance or resistance to insecticide was then monitored by WHO bioassay four hours post blood-feeding. The biochemical basis of the phenotypic response was assessed by examining the effect of blood on detoxification enzyme activity and the effect of blood-meals on detoxification enzyme activity in ageing mosquitoes.ResultsControl cohorts that were not offered any blood meals showed steadily decreasing levels of insecticide tolerance/resistance with age, whereas a single blood meal significantly increased tolerance/resistance primarily at the age of three days. The expression of resistance/tolerance in those cohorts fed multiple blood meals generally showed the least variation with age. These results were consistent following exposure to DDT and pyrethroids but not to malathion. Multiple blood-meals also maintained the DDT and permethrin resistant phenotype, even after treatment females had stopped taking blood-meals. Biochemical analysis suggests that this phenotypic effect in resistant females may be mediated by the maintenance of increased glutathione s-transferase activity as a consequence of multiple blood-feeding. Multiple blood-feeding increased the longevity of insecticide resistant females regardless of their mating status, but only increased the longevity of unmated susceptible females.ConclusionThese data suggest that multiple blood-feeding confers a competitive advantage to insecticide resistant females by increased longevity and maintenance of the expression of resistance with age.

Empirical and theoretical investigation into the potential impacts of insecticide resistance on the effectiveness of insecticide‐treated bed nets

“…SENN‐BASE exhibits moderate resistance to pyrethroids only (Oliver & Brooke, ). SENN‐DDT was established in 1995 by selecting SENN‐BASE for resistance to DDT: each generation, the survivors of an hour‐long exposure to 4% DDT are allowed to breed and start the next generation (Oliver & Brooke, ). SENN‐DDT is resistant to DDT, permethrin, deltamethrin, and malathion due to increased detoxification enzyme activity and fixation of the L1014F kdr mutation (Oliver & Brooke, , ).…”

Climate change exacerbates pest damage through reduced pesticide efficacy

“…15 In Anopheles arabiensis, increasing the temperature reduced pyrethroid sensitivity. 16 In the brown plant hopper Nilaparvata lugens, a serious rice (Oryza sativa) pest in Asia, the sensitivity of the pest to triazophos was significantly decreased in enriched, compared to ambient, CO 2 levels. 17 In plant pests, the most common examples of conditional resistance are related to the effects of environmental conditions on herbicide sensitivity.…”

Putting evolution in elimination: Winning our ongoing battle with evolving malaria mosquitoes and parasites

“… Susceptibility tests: Insecticide susceptibility as determined with standard bioassays may not reflect susceptibility under actual field conditions as such tests are performed with young (2‐ to 5‐day‐old) female mosquitoes following single, limited‐time exposure to an insecticide under constant insectary conditions. As a result, the effect of natural mosquito traits such as sex, age, blood‐feeding status and circadian rhythm (Kulma, Saddler, & Koella, ; Oliver & Brooke, ) but also climatic variables (Glunt, Blanford, & Paaijmans, ) on the toxicity of insecticides is not captured, neither are sublethal effects on blood‐feeding and host‐seeking factors (Glunt et al., unpublished), infection with entomopathogens such as Plasmodium (Alout et al., ), or delayed mortality (Viana, Hughes, Matthiopoulos, Ranson, & Ferguson, ). Vector species: Resistance is typically characterized for a few major malaria vectors in a given area, but there may be several other malaria vectors present. Although we have always assumed that there are roughly 30‐40 malaria vectors worldwide, recently molecular tools show us we may be dealing with a larger diversity of vector species as well as population diversity within one species (Lobo et al., ). Behavioural changes: Apart from the conventional resistance mechanism (target site, metabolic or cuticular resistance), vectors that can avoid contact with insecticides have a clear selective advantage.…”