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

development of immature stages [20, 41]. Aquatic habitats include anthropogenic and natural water bodies such as freshwater streams, small forest rivers (igarape´s), and partially shaded fishponds, usually located along the forest border [34]. Continuous changes in the landscape also influence the spatiotemporal dynamics of the malaria vectors, that normally exhibit sea- sonal peaks in abundance depending on the environmental distribution and availability of habitats in the wet-dry and dry-wet transition seasons [42–44]. Anthropogenic changes in nat- ural environments either can increase the distribution and availability of standing water despite season or increase the duration of habitats, thus diminishing the seasonal impact on the dynamics of vector populations (Rohr et al. 2019). Culicidae diversity and landscape composition or configuration, distinct patterns of land occupation and land-use have all been considered important drivers of malaria, changing the biodiversity of ecosystem services [3], shifting primary vector species [24, 45, 46], and exposing the human population to risk [47]. In endemic areas, a decrease in Anophelinae diversity increases both the risk of human exposure to vector mosquitoes and the likelihood of acquir- ing malaria, especially in areas where the landscape structure is conducive to vector-human contact [24, 27, 48]. In Amazonian rural landscapes, malaria risk is dynamic and associated with a complex network of environmental changes, ecological, entomological, socioeconomic, and political determinants [20, 49, 50].

The source-sink dynamics concept was originally proposed to describe variation in habitat quality that can affect population growth or decline for a target species [51]. More recently, this concept was embraced by the field of landscape ecology [52] and has joined the theory of island biogeography. Immigration and extinction rates across a heterogenous habitat com- posed of continuous forest (source) and small forest patches (sinks) in an anthropogenic matrix define the persistence of a given species. In the case of mosquitoes, the source-sink dynamics can be applied to understand and predict transmission of sylvatic pathogens to humans, or vice-versa. This study aims to better understand the effects of change in the diversity, community structure and composition of mosquito species in a continuous range of landscape elements, i.e., percent forest cover and forest edge density configurations, in endemic malaria areas in Amazonian Brazil. We hypothesized that (1) decreased forest cover and increased forest edge density lead to a change in mosquito diversity; (2) Ny. darlingi dominance is dynamic and highest in areas where forest cover is actively being decreased by human occupation. Methods Study area Mosquitoes were collected in 79 sampling units in 12 municipalities in the Brazilian Amazon states of Acre (twice in Acrelaˆndia, Cruzeiro do Sul, Maˆncio Lima, Rodrigues Alves), Amazo- nas (Itacoatiara, Guajara´, Humaita´, La´brea, São Gabriel da Cachoeira), Para´ (Pacaja´), and Ron-

doˆnia (Machadinho D’Oeste) (S1 Fig in S1 File). The selection of field localities for conducting mosquito collections is the same protocol described by Sallum et al. [53]. Rural settlements comprised mainly subsistence farms, with Manihot esculenta (manioc, cassava), Dioscorea trifida (yam), Coffea arabica (coffee), Euterpe oleracea (ac¸aı´), Musa spp. (banana) and Oryza sp. (rice) plantations, and other vegetables for local consumption [54]. Local settlers grow fish in fish farms, and maintain small numbers of poultry, pigs, goats, and livestock for family consumption and local commerce. Details of regional climate, vegetation class, ecological zone, and rainfall are presented in S1 Table in S1 File and Fig 1. The Brazilian Amazon encompasses four major vegetation class: Tropical Moist Forest, Open Tropical Moist Forest, Seasonal Lowland Forest, and Campinarana [55]. PLOS ONE Anthropogenic landscape and mosquito biodiversity drives malaria vector proliferation PLOS ONE | https://doi.org/10.1371/journal.pone.0245087 January 14, 2021 3 / 25