Natural exposure to Chikungunya virus in golden-headed lion tamarin (Leontopithecus chrysomelas, Kuhl, 1820) from non-protected areas in southern Bahia, Brazil: Implications and significance

Abstract

Chikungunya virus (CHIKV) is primarily associated with non-human-primates (NHPs) in Africa, which also infect humans. Since its introduction to Brazil in 2014, CHIKV has predominantly thrived in urban cycles, involving Aedes aegypti mosquitoes. Limited knowledge exists regarding CHIKV occurrence and implications in rural and sylvatic cycles where neotropical NHPs are potential hosts, from which we highlight Leontopithecus chrysomelas (Kuhl, 1820), the golden-headed lion tamarin (GHLT), an endangered species endemic to the Atlantic Forest (AF) in Southern Bahia State, Brazil. The present study investigated wild GHLT groups across two municipalities, Ilhéus and Una, Bahia. Surveys were conducted in three groups within cocoa agroforests (cabrucas) in Ilhéus, and four groups in anthropized forest and agroforestry fragments in Una, between 2021 and 2022. Thirty-two GHLT specimens were captured and chemically immobilized, examined and submitted to blood sample collection; nine specimens were later recaptured in 2022, totaling 41 samples. CHIKV viremia was not detected in any specimens (as assayed by RT-qPCR). Plaque reduction neutralization test (PRNT90) detected CHIKV antibodies in two (6.3%) GHLTs, with 10-20 antibody titers. Seroprevalence in 2021 was 5.6% and in 2022 was 8.7% with an incidence of 4.5%, whereas, a male adult tested seropositive in both years, suggesting either natural re-exposure and antibody maintenance over time. All samples tested seronegative for Mayaro Virus. Eight mosquito species from the Culicidae family were collected, identified and assayed for CHIKV genomes, showing negative results. This study provides the first evidence of natural CHIKV exposure among free-living GHLTs in Brazil, emphasizing their susceptibility and potential role as reservoirs. These findings underscore the possible consequences of anthropic disturbances in the Brazilian AF, without a seroprevalence difference between non-protected forest formations, agroforest fragments and various mosaic farming landscapes in South Bahia, and highlight the importance of conservation efforts for this endemic and endangered primate species.

Fig 1. Sampling areas of the groups of free-living Leontopithecus chrysomelas, Kuhl, 1820 (Golden-Headed Lion Tamarin, GHLT) and mosquitoes in Una and Ilhéus municipality, south Bahia State, Brazil, collected during the years 2021 and 2022.

Group name: Almada (ALM), Bom Pastor (BMP)–sampled in two points, Santa Rita (SRI)–sampled in two points, Ribeiro (RIB), Elias (ELI)–sampled in two points, Manoel Rosa (MRO), and Ozawa (OZW). This image of basemap was performed by using satellite images of bands green, red and infrared (10m resolution) of Sentinel-2 (date: 22/06/09), which are of public domain available from U.S. Geological Survey at Copernicus browser (https://browser.dataspace.copernicus.eu). Map generated with the free and open source geographic information system (QGIS,version 3.32; licensed under general public license [40]).

Fig 2. Types of land cover and use of soil based on MapBiomas [59,60] within the study areas in the municipalities of Ilhéus and Una, Bahia, Brazil during the years 2021 and 2022.

The depicted areas encompass a 354 m radius home range buffer surrounding the sampling points of Leontopithecus chrysomelas (golden-headed lion tamarin, GHLT). MapBiomas Project—Collection 8 of the Annual Series of Land Use Land Cover Maps of Brazil, accessed on 01/02/2024 through the link: https://brasil.mapbiomas.org/colecoes-mapbiomas/ e MapBiomas Cacau–Mapeamento do Cultivo Sombreado de Cacau no Sul da Bahia. accessed on 01/02/2024 through the link: https://brasil.mapbiomas.org/mapbiomas-cacau/. Map generated with the free and open source geographic information system (QGIS,version 3.32; licensed under general public license [40]).

Fig 3. Comparison between median percentages of the different land cover and soil uses (LCSU) types within a 39,4ha (354m radius) home range buffer surrounding the sampling points of Leontopithecus chrysomelas (golden-headed lion tamarin, GHLT).

Fig 4. Closest distance edge points of the home range buffer (39.4ha, 354m radius) represented by their group’s names and the human settlements indicated by numbers 1–6, based on IBGE census sectors [61], in the study areas of Leontopithecus chrysomelas (golden-headed lion tamarin, GHLT).

Group name: Almada (ALM), Bom Pastor (BMP), Santa Rita (SRI), Ribeiro (RIB), Elias (ELI), Manoel Rosa (MRO), and Ozawa (OZW). This image of basemap was performed by using satellite images of bands green, red and infrared (10m resolution) of Sentinel-2 (date: 22/06/09), which are of public domain available from U.S. Geological Survey at Copernicus browser (https://browser.dataspace.copernicus.eu). Map generated with the free and open source geographic information system (QGIS,version 3.32; licensed under general public license [40]).