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 distributed across a gradient of fully domesticated to fully pristine ecosystems in southern Tanzania
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Date
2023
Authors
Walsh, Katrina
Journal Title
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Publisher
University College Cork
Published Version
Abstract
The effectiveness of current first-choice vector control interventions on the semi-zoophagic vector Anopheles arabiensis are limited, among other things, by insecticide resistance and their ability to acquire non-human bloodmeals. Across much of southern Tanzania, in areas where humans and cattle are readily available, it is the predominant member sibling species of the Anopheles gambiae complex. However, little is known about its population dynamics or blood utilization behaviours in pristine natural ecosystems, where these known preferred hosts are scarce or completely absent.
This study investigated larval habitat occupancy and species composition of the An. gambiae complex, together with the availability of various potential mammalian blood host species, across a gradient of fully domesticated to fully pristine ecosystems in southern Tanzania. Potential aquatic habitats were surveyed at 40 locations encompassing permanent human settlements, a community-owned Wildlife Management Area with varying degrees of human activity, and Nyerere National Park (NNP), which had very little. To investigate the effects of potential host availability on the species composition of the complex, all direct observations, tracks and signs of humans, livestock and wild animals observed around the surveyed larval habitats were recorded in parallel. The resulting data were analysed by logistic regression using generalized linear mixed models.
Odds of habitat occupancy by An. gambiae complex larvae decreased by 62% (P<0.0001) across the full range of natural ecosystem integrities observed, from fully domesticated to completely pristine areas, suggesting that the availability of suitable blood hosts had a modest effect on overall habitat utilization by this taxon. However, while only An. arabiensis, a key vector of residual malaria transmission, was found in fully domesticated ecosystems, its non-vector sibling species An. quadriannulatus also occurred in conserved areas and dominated the most pristine natural ecosystems. The proportion of An. arabiensis versus An. quadriannulatus was positively associated with the number of times humans and/or cattle (P=0.0007) were detected at a location and negatively associated with distance inside NNP and away from human settlements (P<0.0001). Nevertheless, An. arabiensis was found even in absolute pristine environments that were >40km away from any signs of human or livestock, suggesting this species can survive on blood from one or more wild animal species. High proportions of An. quadriannulatus inside NNP were positively associated with the number of times impala were detected (P<0.0001), suggesting they may be a preferred blood source for this non-vector, giving it a competitive advantage over An. arabiensis where this antelope is abundant. Despite being detected less frequently, bushpig were also positively associated with high proportions of An. quadriannulatus, suggesting they provide a second preferred blood source, particularly in the miombo woodlands of the buffer zone where impala were scarce.
Overall, it seems that the availability of preferred hosts influences the competitive balance between these sibling species and that refugia populations of An. arabiensis can persist in wild areas, thus presenting both challenges and opportunities for control interventions: While such refuge populations deep inside pristine conservation area may confound attempts to repeat historical successes with eliminating this species from areas outside its natural range, it may also constitute a reservoir of diverse, unselected genomes with original wild-type insecticide susceptibility traits that could repopulate areas around human settlements that had otherwise been considered lost from the natural gene pool.
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Keywords
Malaria vector , Mosquito ecology , Species interactions , Blood host preferences , Larval habitats
Citation
Walsh, K. 2023. 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 distributed across a gradient of fully domesticated to fully pristine ecosystems in southern Tanzania. MSc Thesis, University College Cork.