Blood host preferences and competitive inter-species dynamics within an African malaria vector species complex inferred from signs of animal activity around aquatic larval habitats.

Abstract

The dual-specialized behavioural adaptions of Anopheles arabiensis, to feed readily upon either people or cattle, enable it to thrive and mediate persistent residual malaria transmission across much of Africa, despite widespread use of long-lasting insecticidal nets (LLINs). Indeed, LLIN scale up has often resulted in it dominating the more efficient but vulnerable malaria vector Anopheles gambiae, its sibling species within a complex of the latter name. However, the feeding behaviours and competitive relationships of An. arabiensis with other sibling species in well conserved natural ecosystems, where its known preferred hosts are scarce or absent, remain largely unexplored. Potential aquatic habitats were surveyed for An. gambiae complex larvae across a gradient of natural ecosystem integrity in southern Tanzania, encompassing fully domesticated human settlements, a partially encroached Wildlife Management Area (WMA), and well conserved areas of the recently gazetted Nyerere National Park (NNP) before substantive development of tourist access or accommodation. Direct observations, tracks, spoor and other signs of human, livestock or wild animal activity around these water bodies were recorded as indirect indicators of potential blood source availability. While only An. arabiensis was found in fully domesticated ecosystems, its non-vector sibling species An. quadriannulatus occurred in conserved areas and dominated the most intact natural ecosystems. Proportions of larvae identified as An. arabiensis were positively associated with human and/or cattle activity and negatively associated with distance inside NNP and away from human settlements. Proportions of An. quadriannulatus were positively associated with activities of impala and bushpig, implicating both as likely preferred blood hosts. While abundant impala and lack of humans or cattle in intact acacia savannah within NNP apparently allowed it to dominate An. arabiensis, presence of bushpig seemed to provide it with a foothold in miombo woodlands of the WMA, despite encroachment by people and livestock. While this antelope and suid are essentially unrelated, both are non- migratory residents of small home ranges with perennial surface water, representing preferred hosts for An. quadriannulatus that are widespread across extensive natural ecosystems all year round. Despite dominance of An. quadriannulatus in well-conserved areas, An. arabiensis was even found in absolutely intact environments >40km inside NNP, suggesting it can survive on blood from one or more unidentified wild species. While self-sustaining refuge populations of An. arabiensis inside conservation areas, supported by wild blood hosts that are fundamentally beyond the reach of insecticidal interventions targeted at humans or their livestock, may confound efforts to eliminate this key malaria vector, they might also enable insecticide resistance management strategies that could restore the effectiveness of pyrethroids in particular.