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

AbstractThe dual-specialized behavioural adaptions ofAnopheles 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 vectorAnopheles gambiae, its sibling species within a complex of the latter name. However, the feeding behaviours and competitive relationships ofAn. arabiensiswith 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 forAn. gambiaecomplex 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 onlyAn. arabiensiswas found in fully domesticated ecosystems, its non-vector sibling speciesAn. quadriannulatusoccurred in conserved areas and dominated the most intact natural ecosystems. Proportions of larvae identified asAn. arabiensiswere positively associated with human and/or cattle activity and negatively associated with distance inside NNP and away from human settlements. Proportions ofAn. quadriannulatuswere 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 dominateAn. 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 forAn. quadriannulatusthat are widespread across extensive natural ecosystems all year round.Despite dominance ofAn. quadriannulatusin well-conserved areas,An. arabiensiswas 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 ofAn. arabiensisinside 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.