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Diversity Patterns of Hematophagous Insects in Atlantic Forest Fragments and Human-Modified Areas of Southern Bahia, Brazil

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Diversity Patterns of Hematophagous Insects in Atlantic Forest Fragments and Human-Modified Areas of Southern Bahia, Brazil Vol. 43, no. 2 Journal of Vector Ecology 293 Diversity patterns of hematophagous insects in Atlantic forest fragments and human-modified areas of southern Bahia, Brazil Lilian S. Catenacci1,2,3,4, Joaquim Nunes-Neto2, Sharon L. Deem4, Jamie L. Palmer4, Elizabeth S. Travassos-da Rosa2, and J. Sebastian Tello5,6 1Curso de Medicina Veterinária, Federal University of Piauí State/CPCE, Bom Jesus, PI, Brazil, [email protected] 2Division of Arbovirology and Hemorrhagic Fevers, Evandro Chagas Institute, Anannindeua, PA, Brazil 3Royal Zoological Society of Antwerp, Centre for Research and Conservation, Antwerp, Belgium 4Saint Louis Zoo, Institute for Conservation Medicine, St. Louis, MO, U.S.A. 5Missouri Botanical Garden, Center for Conservation and Sustainable Development, St. Louis, MO, U.S.A. 6Pontificia Universidad Católica del Ecuador, Escuela de Biología, Quito, Ecuador Received 7 June 2018; Accepted 16 August 2018 ABSTRACT: There have been several important outbreaks of mosquito-borne diseases in the Neotropics in recent years, particularly in Brazil. Some taxa are also considered to be indicators of environmental health. Despite the importance of understanding insect abundance and distribution to the understanding of disease dynamics and design strategies to manage them, very little is known about their ecology in many tropical regions. We studied the abundance and diversity of mosquitoes and sand flies in the Bahia State of Brazil, a point of origin for arbovirus outbreaks, including Zika and Chikungunya fever. During 2009-2014, 51 mosquito taxa were identified, belonging to three dipteran families, Ceratopogonidae, Culicidae, and Psychodidae. The family Culicidae, including the Sabethini tribe, were the most abundant (81.5%) and most taxa-rich (n=45). While season (winter and summer) was a strong factor determinant of the occurrence of the most abundant taxa, the stratification level in the forest (ground or tree level) had a strong effect and the dominant taxa at ground level were completely different from the dominant species collected at tree level. We suggest that sites with a mix of forest and agroforestry systems support the highest biodiversity of hematophagous insects as compared to highly disturbed landscapes. Journal of Vector Ecology 43 (2): 293-304. 2018. Keyword Index: Arbovirus, mosquito, Culicidae, abundance, richness, Brazil. INTRODUCTION (CPCV), and recently, West Nile virus (WNV), chikungunya virus (CHIK), and Zika virus (ZIKV) (Figueiredo et al 2010, Many species of hematophagous insects, particularly Serra et al. 2016). In sylvatic areas, culicid mosquitoes also species in the families Ceratopogonidae, Culicidae, transmit pathogens to wild animals (Medeiros-Sousa et al. Psychodidae, and Simuliidae, are vectors of important 2013). Thus, rural communities where people, mosquitoes, tropical diseases (Vasconcelos and Calisher 2016, Cardoso and wild animals co-exist in close proximity are at an increased et al. 2017, Harbach 2017). Considering the emerging risk for the emergence of infectious diseases, particularly those arbovirus outbreaks in recent years throughout the world that are vector-borne, such as arboviruses. Understanding the (Figueiredo and Figueiredo 2014, Figueiredo and Figueiredo spatial and temporal variation in abundance and diversity of 2015, Vasconcelos and Calisher 2016), knowledge of disease culicid mosquitoes, as well as the role of climate in shaping vector distribution and biodiversity is essential to identify this variation, is important to assess disease risks in natural potential areas of high risk for pathogen transmission and environments (Pinto et al. 2009). Furthermore, the condition to conduct assessments of environmental health in protected of culicid populations can be used as a bioindicator for and anthropogenically disturbed areas (Navarro et al. 2015). environmental health assessments (Montes 2005, Paula et al. Among vectors, mosquitoes (Diptera: Culicidae) are 2015). particularly prominent. Approximately 3,500 species of Unfortunately, the ecology of mosquitoes in many parts Culicidae have been described worldwide, and Brazil is home of the tropics is poorly understood. Even though recent to about 450 species (Paula et al. 2015, Harbach 2017). The outbreaks of Zika and chikungunya in Brazil can be traced hematophagous Culicidae are divided into two subfamilies, back to rural areas of southern Bahia State (Brazil 2016), little Anophelinae and Culicinae. The Anophelinae are vectors of information exists about mosquito diversity, demography, many arboviruses and Plasmodium species and the subfamily or abundance. Moreover, this region contains remnants of Culicinae are vectors of a great variety of arboviruses, such as Atlantic forest, which are home to a large number of mammals, yellow fever virus (YFV), dengue virus (DENV) serotypes, St. birds, and arthropods (Ribeiro et al. 2009, Cassano et al. Louis encephalitis virus (SLEV), Ilheus virus (ILHV), Rocio 2011), some of which may be important for the circulation virus (ROCV), Bussuquara virus (BSQV), Cacipacore virus dynamics of many arboviruses (Souza et al. 2015). The goal 294 Journal of Vector Ecology December 2018 of this study was to investigate the entomofauna in sylvatic from November to April. Winter is the colder, drier part of and rural areas of southern Bahia, Brazil, and to evaluate the the year from May to October (Figure 2). effect of seasonality and the stratification level of the forest Samples were collected at seven different sites in sylvatic on arthropod taxa diversity. We also discuss in more detail and rural environments (Table 1). These sites were selected the Culicidae that are potential bioindicators and vectors of based on type of vegetation and proximity to areas where wild human and wildlife diseases. mammals have been monitored as part of other ecological and health studies (Oliveira et al. 2011, Catenacci et al. 2016). MATERIALS AND METHODS The sites with higher amounts of primary or second-growth forests were REBIO-Una, Ecoparque de Una, and Lagoa Study area Encantada, respectively. Three of the seven sites were sampled This study was conducted in the municipalities of Ilhéus in both “summer season” and “winter season,” accounting for and Una, located in the southern Bahia Atlantic Forests ten sampling events (Table 1 and Figure 2). of Brazil from 2006 to 2014 (Figure 1). Across this region, anthropogenic activities have resulted in a mosaic of land- Mosquito sampling use strategies. Native Atlantic forest is highly fragmented The Brazilian Federal and State Entomological and embedded within an agricultural matrix dominated by Services conducted the mosquito collections as part of cacao agroforestry systems, as well as plantations of rubber their surveillance program from 2009 to 2014. At each tree, coconut, banana, and cassava. The region also contains site, sampling lasted between three to ten days. Each day, the Una Biological Reserve and its Buffer Zone, the Una mosquitoes were surveyed during three time intervals: two Biological Wildlife Refuge (Alger and Caldas 1994, Sollberg during daylight (08:00-12:00 and 16:00-18:00) and one at et al. 2014). The area is surrounded by small villages where night (18:00-06:00). During daylight sampling, mosquitoes the majority of people are living by subsistence agriculture on were collected at ground and tree levels. At ground level, small family-based farms. Here, people have limited access three or more team members collected mosquitoes using to basic infrastructure, such as electricity, potable water, hand nets (polyester net bag 30 cm in diameter, attached to a sanitation, and health care (Carneiro Santos et al. 2014, 30 cm aluminum handle) constructed by the research team. Sollberg et al. 2014). With regards to climate, the mean annual At tree level, climbing equipment or a platform were used, temperature is 24° C, and annual rainfall averages 1,500 mm. and a trained person collected mosquitoes with a hand net at Based on the average temperature over the last three decades, 15 m high. Adult mosquitoes were transferred immediately to we define summer as the warmer and wetter part of the year, Eppendorf tubes using a manual suction tube (Castro catcher, Figure 1. Study sites of hematophagous arthropod surveys: Ilhéus city (top) and Una city (bottom). Vol. 43, no. 2 Journal of Vector Ecology 295 Table 1. Study sites, including the dominant landscape, the municipality, and the geographic coordinates. Study site Predominant type of vegetation* Cities Coordinates - Agroforestry with second-growth forest b,c 14º39’49.4’’S Almada Farm (site 1) - cacao farm Ilhéus - Neighbor of Bonfin and Santa Rita Farm 39º11’36.8’’W Bonfim Farm (site 2) - rural settlement -Agroforestry with second-growth forest b,c 14º39’31.24’’S Ilhéus with cacao farm - Neighbor of Almada and Santa Rita Farm 39º11’37.6’’W - Agroforestry with second-growth forest b,c 14º40’35.6’’S Santa Rita Farm (site 3) - cacao farm Ilhéus - Neighbor of Bonfim and Almada Farm 39º11’10.8’’W Colônia de Una Farm (site 4) - - Agriculture with second-growth forest b,d 15º17’11.1’’S Una Familiar agriculture farm - Close to REBIO-UNA 39º08’25.0’’W -Second-growth forest b with few agroforestry c, Lagoa Encantada (site 5) – 14º37’10.5’’S close to a big lake Ilhéus conservation area 39º08’14.6’’W - Close to Bonfim, Santa Rita and Almada Farm -Mostly old-growth foresta in the East side and Una Biological Reserve (Rebio-Una) Second-growth b forest with old-growth foresta 15º10’55.3’’S (site 6) – conservation area Una in the West side 39º04’20.7’’W -Neighbor of Ecoparque de Una Ecoparque de Una (site 7) – -Second-growth forest b 15º10’11.7’’S Una conservation área -Neighbor of Ecoparque de Una 39º03’16.4’’W *Vegetation types: aold-growth forest: forest with little or no sign of past human disturbance, a closed canopy, trees in general at least 20 m high with large diameters, bromeliads in a wide range of sizes and an extensive layer of vines; bSecond-growth forest: forest with visible signs of previous human disturbance, which has been subjected to either ‘general’ (recovering from complete deforestation) or ‘selective’ logging (recovering from the cutting of selected species).
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