Biting time of day in malaria mosquitoes is modulated by nutritional status

Background: Transmission of vector-borne pathogens follows daily rhythms, occurring at the time of day that vectors forage for blood. Control measures, such as insecticide-treated bed nets (ITNs), have been particularly successful for reducing malaria transmission because they exploit the nocturnal biting behaviour of the Anopheles spp. that vector malaria. However, shifts in biting behaviour to earlier or later hours when people are unprotected can undermine the efficacy of ITNs. Despite the implications for malaria transmission, the mechanisms underlying these shifts remain poorly understood. Because food availability mediates activity and foraging rhythms, and ITNs block access to human blood as a food source, it was hypothesized that nutritional deprivation could cause mosquitoes to shift their biting behaviour to earlier or later in the diel cycle. Methods: Female Anopheles gambiae sensu lato (s.l.) mosquitoes were provided with a blood meal on day 3 post-emergence, and access to one of three feeding treatments that varied in nutritional resources: (i) 0.5% sucrose, (ii) 10% sucrose, or (iii) 10% sucrose plus an additional blood meal on day 6. Mosquitoes were released into a semi-field system on day 10 with human-mimic traps to investigate how food availability impacted the time of day that mosquitoes host seek. Results: Nutritional resources determine both the likelihood and time of day that host-seeking occurs. Specifically, low-resourced mosquitoes were 2–3-fold more likely to host seek overall, and 5–10-fold more likely to host seek at an earlier time of day than well-resourced mosquitoes (fed 10% sucrose with and without an additional blood meal), which predominantly sought a host in the second half of the night time. Conclusions: This study reveals that mosquito nutritional condition drives plasticity in biting time of day, suggesting it is an underappreciated contributor to residual malaria transmission. Furthermore, the findings suggest that targeting mosquito nutrition (e.g. sugar-baited traps) could influence mosquito behaviour in ways that affect the success of ITNs. More broadly, understanding the drivers of biting time of day variation is crucial for the future success of vector control tools and controlling malaria transmission.