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

RESEARCH ARTICLE Anthropogenic landscape decreases mosquito biodiversity and drives malaria vector proliferation in the Amazon rainforest Leonardo Suveges Moreira ChavesID1*, Eduardo Sterlino BergoID2, Jan E. Conn3,4, Gabriel Zorello LaportaID5, Paula Ribeiro Prist6, Maria Anice Mureb Sallum1‡ 1 Departamento de Epidemiologia, Faculdade de Sau´ de Pu´ blica, Universidade de São Paulo, São Paulo, SP, Brazil, 2 Superintendência de Controle de Endemias, Secretaria de Estado da Sau´de de São Paulo, Araraquara, SP, Brazil, 3 Wadsworth Center, New York State Department of Health, Albany, NY, United States of America, 4 Department of Biomedical Sciences, School of Public Health, State University of New York, Albany, NY, United States of America, 5 Setor de Po´s-graduac¸ão, Pesquisa e Inovac¸ão, Centro Universita´rio Sau´ de ABC, Fundac¸ão ABC, Santo Andre´, SP, Brazil, 6 Department of Ecology, Institute of Bioscience, University of São Paulo, São Paulo, SP, Brazil ‡ Senior author. * leonardosuveges@usp.br Abstract Inter-relationships among mosquito vectors, Plasmodium parasites, human ecology, and biotic and abiotic factors, drive malaria risk. Specifically, rural landscapes shaped by human activities have a great potential to increase the abundance of malaria vectors, putting many vulnerable people at risk. Understanding at which point the abundance of vectors increases in the landscape can help to design policies and interventions for effective and sustainable control. Using a dataset of adult female mosquitoes collected at 79 sites in malaria endemic

areas in the Brazilian Amazon, this study aimed to (1) verify the association among forest cover percentage (PLAND), forest edge density (ED), and variation in mosquito diversity; and to (2) test the hypothesis of an association between landscape structure (i.e., PLAND and ED) and Nyssorhynchus darlingi (Root) dominance. Mosquito collections were per- formed employing human landing catch (HLC) (peridomestic habitat) and Shannon trap combined with HLC (forest fringe habitat). Nyssorhynchus darlingi abundance was used as the response variable in a generalized linear mixed model, and the Shannon diversity index (H’) of the Culicidae community, PLAND, and the distance house-water drainage were used as predictors. Three ED categories were also used as random effects. A path analysis was used to understand comparative strengths of direct and indirect relationships among Ama- zon vegetation classes, Culicidae community, and Ny. darlingi abundance. Our results dem- onstrate that Ny. darlingi is negatively affected by H´ and PLAND of peridomestic habitat, and that increasing these variables (one-unit value at β0 = 768) leads to a decrease of 226 (P < 0.001) and 533 (P = 0.003) individuals, respectively. At the forest fringe, a similar result was found for H’ (β1 = -218; P < 0.001) and PLAND (β1 = -337; P = 0.04). Anthropogenic changes in the Amazon vegetation classes decreased mosquito biodiversity, leading to increased Ny. darlingi abundance. Changes in landscape structure, specifically decreases in PLAND and increases in ED, led to Ny. darlingi becoming the dominant species,

PLOS ONE PLOS ONE | https://doi.org/10.1371/journal.pone.0245087 January 14, 2021 1 / 25 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Chaves LSM, Bergo ES, Conn JE, Laporta GZ, Prist PR, Sallum MAM (2021) Anthropogenic landscape decreases mosquito biodiversity and drives malaria vector proliferation in the Amazon rainforest. PLoS ONE 16(1): e0245087. https://doi. org/10.1371/journal.pone.0245087 Editor: Deborah Faria, Universidade Estadual de Santa Cruz - UESC, BRAZIL Received: October 30, 2020 Accepted: December 21, 2020 Published: January 14, 2021 Copyright: © 2021 Chaves et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the manuscript and its Supporting Information files. Funding: This work was supported by Fundac¸ão de Amparo à Pesquisa do Estado de São Paulo (FAPESP; grants 2014/26229-7, 2014/26855-5 and 2014/09774-1), and by National Institutes of Health, USA, grant 2R01AI110112-06A1 to JEC. Competing interests: The authors have declared that no competing interests exist.