Microorganism-mediated behaviour of malaria mosquitoes

Host-seeking is an important component of mosquito vectorial capacity on which the success of the other behavioural determinants depends. Blood-seeking mosquitoes are mainly guided by chemical cues released by their blood hosts. This thesis describes results of a study that determined the effect of microorganisms – host skin bacteria as well as malaria parasites – on host-seeking behaviour of female Anopheles gambiae sensu stricto and An. arabiensis in Homabay county, western Kenya. Semi-field and field experiments were conducted to determine the response of mosquitoes with different host preference to synthetic and natural odour blends from three vertebrate hosts, a human, a cow and a chicken. Screen house experiments were conducted to test whether specific skin bacteria or a mix of skin bacterial volatiles from the three vertebrate hosts mediate mosquito response. A review chapter in this thesis discusses how malaria parasites can manipulate human hosts to enhance their own transmission, by making the hosts more attractive to mosquitoes. Another experiment, using a dual-choice olfactometer, determined whether infection with malaria parasites increases human attractiveness to malaria mosquitoes, and whether the attractiveness of infected humans is Plasmodium falciparum-stage specific. Here, the same children participated in the study during infection with malaria parasites and after treatment with antimalarial drugs, artemisinin lumefantrine. Cage assays were further used to test mechanisms of attractiveness of P. falciparum-infected individuals using body odours or skin bacterial volatiles collected from the children at the two time points. Overall results show that skin bacterial volatiles play an important role in guiding mosquitoes with different host preferences to their specific host. For An. gambiae s.s., high (microscopic) densities of P. falciparum gametocytes (and not parasite-free, submicroscopic gametocytes or asexual stages of Plasmodium parasites) results into higher attractiveness of hosts, and body odours play a role in attractiveness of P. falciparum-infected humans. The results may help to develop more effective health policies and enable targeted interventions towards the most attractive hosts, which could contribute to reductions in malaria transmission. Identification of general or common attractive volatiles produced by the natural hosts as well as those from the gametocyte carriers may contribute to the development of an improved synthetic odour blend that may be used for sampling of mosquitoes with different host preferences. The use of powerful attractive odorants may result in reductions of vector-borne diseases transmitted by mosquitoes.