Effect of non-human hosts on the human biting rate of primary and secondary malaria vectors in Tanzania

Abstract

Background: Malaria vectors vary in feeding preference depending on their innate behaviour, host availability and abundance. Host preference and human biting rate in malaria vectors are key factors in establishing zooprophylaxis and zoopotentiation. This study aimed at assessing the impact of non-human hosts in close proximity to humans on the human biting rate of primary and secondary malaria vectors, with varying host preferences. Methods: The effect of the presence of non-human hosts in close proximity to the human host on the mean catches per person per night, as a proxy for mosquito biting rate, was measured using mosquito-electrocuting traps (METs), in Sagamaganga, Kilombero Valley, Tanzania. Two experiments were designed: (1) a human versus a calf, each enclosed in a MET, and (2) a human surrounded by three calves versus a human alone, with each human volunteer enclosed individually in a MET spaced 10 m apart. Each experiment was conducted on alternate days and lasted for 36 nights per experiment. During each experiment, the positions of hosts were exchanged daily (except the human in experiment 2). All anopheline mosquitoes caught were assayed for Plasmodium sporozoites using enzyme-linked immunosorbent assay. Results: A total of 20,574 mosquitoes were captured and identified during the study, of which 3608 were anophelines (84.4% primary and 15.6% secondary malaria vectors) and 17,146 were culicines. In experiment 1, the primary malaria vector, Anopheles arabiensis, along with Culex spp. demonstrated a preference for cattle, while the primary vectors, Anopheles funestus, preferred humans. In experiment 2, both primary vectors, An. arabiensis and An. funestus, as well as the secondary vector Anopheles rivolurum, demonstrated behaviours amenable to zooprophylaxis, whereas Culex spp. increased their attraction to humans in the presence of nearby cattle. All anopheline mosquitoes tested negative for sporozoites. Conclusions: The findings of this study provide support for the zooprophylaxis model for malaria vectors present in the Kilombero Valley, and for the zoopotentiation model, as it pertains to the Culex spp. in the region. However, the factors regulating zooprophylaxis and zoopotentiation are complex, with different species-dependent mechanisms regulating these behaviours, that need to be considered when designing integrated vector management programmes.