Anthropogenic landscape decreases mosquito biodiversity and drives malaria vector proliferation in the Amazon rainforest

OTMFA (r2 = -0.35), Campinarana (r2 = -0.28) and FC (r2 = -0.32). The results of path analysis are detailed in S3 Table in S1 File. The model showed a plausible causal direction on Ny. dar- lingi abundance that involves land use change, represented by negative effects of (1) Anthropo- genic vegetation on FC, (2) Campinarana and OTMFA on the Shannon-index (mosquito community diversity). These effects can increase Ny. darlingi abundance. The forest loss pro- cess (deforestation), particularly in Campinarana and OTMFA, can decrease the diversity of the mosquito community and therefore increase Ny. darlingi abundance. The Path analysis results are presented in S4 Table in S1 File. The canonical correspondence analysis (Fig 6) demonstrated that the four landscape cate- gories were pooled according to species composition of the 79 sampling units. In addition, Ny. darlingi abundance was associated with Culicidae communities represented by the landscapes A, C, and partially D, with the highest positive values associated with A. The components CCA1 and CCA2 explained 50% and 27% respectively, and together they explained 77% of the variation species-landscapes and 5.6% of the total data variation. Landscape B sampling units span the field collections, and landscape A was grouped on the CCA1 axis but separated out well on the CCA2 axis, suggesting that the lower forest cover habitat component is an impor- tant determinant of landscape A and B mosquito sample assemblages. The sampling units of landscape A were distinct, separating best both on the CCA1 and CCA2, suggesting that open

habitat component was most important in determining landscape A mosquito assemblage. Discussion Based on our results, it is possible to construct a network of anthropogenic changes and their effects on Culicidae diversity and Ny. darlingi in the natural tropical rainforest landscape. Here, the forest cover loss causes habitat loss and fragmentation, increasing the forest edge effects and changing the Culicidae species composition. Mosquito communities are strongly impacted by the mechanism associated with changes in land-use. Some species can readily invade new niches that emerged because of forest fragmentation and increased forest edges. High percentage of forest cover and increased Culicidae diversity can lead to a decrease of 533 and 226 mosquitoes, respectively. Deforestation leads to biodiversity loss [72], decreasing the dilution effect, and increasing diffuse competition. In these settings, the reduction of shading, raising the local temperature around human dwellings and in the neighboring larval habitats, reduces the larva to adult development time, and shifts primary vector species [3, 24, 35]. Therefore, habitat fragmentation is a key factor in the dynamics of this species because the increase in forest edge density facilitates the species dispersion and proliferation, creating a serious public health problem. In Brazil, 99% of the 193,838 reported malaria cases in 2018 were in the Amazon biome, and more than 89% (173,006) were caused by P. vivax and 10% (19,283) by P. falciparum [73].

Mosquitoes of the subfamily Anophelinae are responsible for transmitting Plasmodium between infectious and susceptible humans. In endemic areas across the Amazon basin, malaria is associated with activities that require forest clearing, such as infrastructure construc- tion, agricultural expansion, mining, logging, and increased urbanization [28, 74]. Increased malaria incidence is a trade-off of poorly planned or unplanned land occupation for socioeco- nomic development [32, 75–77]. It is well known that anthropogenic change in natural forest environments is a major driver of increased malaria incidence in subtropical and tropical endemic countries [30, 39, 78]. Recently, Chaves et al. (2018) demonstrated that increased malaria incidence is associated with complex mechanisms of change associated with deforestation, forest fragmentation, habitat degradation, geopolitical and social elements that facilitate malaria propagation. In addition, PLOS ONE Anthropogenic landscape and mosquito biodiversity drives malaria vector proliferation PLOS ONE | https://doi.org/10.1371/journal.pone.0245087 January 14, 2021 16 / 25