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

increasing vector abundance and putting settlers at risk of malaria [79], the socioeconomic conditions from localities were similar (i.e., subsistence rural practices in low populational density (< 1,500 people per km2), medium-low Human Development Index (HDI ~ 0.6), lack of basic sanitation and precarious housing). However, the landscape structure differed in each sampling unit of our study design, verifying that landscape (without socioeconomic confusion variables) operates as a regulator of the mosquito community and malaria risk. Relative to the landscape habitat of the primary malaria vector, females will seek more shaded and safer larval habitats (realized niche) for egg laying [34]. In this context, moderate forest cover (i.e., a range between 45 ¬ 65%, partially shaded) increases the occurrence of larval habitats and adult resting places. On the other hand, low forest cover (full sunlight larval habi- tats) might pressure the species to disperse, because the females require appropriate water bod- ies (partially shaded) to deposit eggs. Some authors have demonstrated that the microclimate, pH, microbiota and other factors affect the productivity of Ny. darlingi larval habitats [41, 80, 81]. Results of the present study demonstrated that changes in the natural landscape structure, defined by the measurement of three metrics, significantly impacted adult productivity. Adult abundance is likely associated with an increase in the presence of suitable larval habitats and vertebrate hosts for blood feeding. Similarly, a positive relationship between clearing natural

forest and the presence of Ny. darlingi was found in French Guiana [82]. Results of our study indicate that deforestation and forest clearing for human occupation and changes in land-use create new ecological and environmental conditions, which drive changes in the composition and community structure of plants [83, 84] and animals [85, 86], including insects of the family Culicidae. The anthropogenic changes in the tropical rainforest environment are linked to processes of ecological succession that can be initiated by a distur- bance in a community [87]. Forest streams can be impacted by deforestation, i.e., once a tree is cut its trunk or branches can block the water flow, increasing resting places for adults, habitat for female oviposition, and microhabitat for immature development (S13 Fig in S1 File) [88]. Following deforestation, blocked water flow, and readily available blood meals, mosquitoes can proliferate. The introduction of new sources of blood for mosquitoes, and biotic compo- nents of malaria ecology such as ecological interactions among vector-host species also affect the dominance of vector species [56]. Humans and domestic animals, as well as local weather conditions are important factors in the changing landscape due to environmental disturbance [89, 90]. These factors together contribute to a dynamic process of change, dominated by fast- growing, resilient, generalist species that will be replaced by more competitive species as suc- cession proceeds or new anthropogenic changes interfere in the natural succession process

[91–93]. Medeiros-Sousa and colleagues [94] found strong evidence that biodiversity loss increases the risk of pathogen transmission. This can be observed in mosquito communities, for example, when a taxonomic group increases or decreases its species assemblages in a chain of ecological succession. In our study, Culicidae diversity (β diversity) responded inversely to Ny. darlingi vector abundance across changes in PLAND metrics (S14 Fig in S1 File), a process that can influence diffuse competi- tion and transmission dynamics of vector-borne pathogens [10]. This ecological process was used to explain malaria dynamics in the tropical rain forest, where access to vertebrate blood sources can be mediated by the threshold tolerance of a host to mosquito bites, and defensive host behavior [3]. The increased β diversity in higher PLAND can increase diffuse competition and decrease in malaria risk. In S15 Fig in S1 File landscapes with less than 25% of PLAND had fewer rare species (rich- ness) according to the collector curve effort. This evidence reinforces the hypothesis that forest cover can drive the dominance of Ny. darlingi. Therefore, if we define risk as the chance of a susceptible host being bitten by an infected vector, landscapes with lower forest cover PLOS ONE Anthropogenic landscape and mosquito biodiversity drives malaria vector proliferation PLOS ONE | https://doi.org/10.1371/journal.pone.0245087 January 14, 2021 18 / 25