First record of Aedeomyia squamipennis ( Lynch Arribálzaga , 1878 ) ( Diptera : Culicidae ) in the state of Maranhão : epidemiological implications and distribution in Brazil

We record Aedeomyia squamipennis from the state of Maranhão, Brazil (municipalities of Bacurituba, Barra do Corda, Cajapió, Governador Nunes Freire, and Santo Amaro do Maranhão). We show that this species is well distributed in the state. The potential in the epidemiology of avian malaria and arboviruses is discussed briefly in connection with its discovery in Santo Amaro do Maranhão, due to the great number of bird species on Lake Santo Amaro. Finally, we present the known distribution of the species in Brazil.

The family Culicidae is currently divided into two subfamilies: Anophelinae with 488 formally described species; and Culicinae with 3,067 (Harbach & Kitching 1998;Harbach 2017).Among the 11 tribes of Culicinae, Aedeomyiini is the smallest, with only seven described species in a single genus, Aedeomyia Theobald, 1901.Aedeomyia has two subgenera: Aedeomyia s.s. with six species occurring in the tropics, and the monotypic Lepiothauma Enderlein, 1923, recorded in the Afrotropical region only (Tyson 1970;Brunhes et al. 2011).
Aedeomyia is pantropical, with all species occurring in the southern hemisphere.Four species extend their distribution north of the Equator but do not reach the Tropic of Cancer (Belkin 1962;Tyson 1970).This genus is represented in the New World only by Aedeomyia (Aedeomyia) squamipennis (Lynch Arribálzaga, 1878: 151), an exclu-sively Neotropical species whose distribution extends from Argentina to Mexico (Lane 1953).Although Belkin et al. (1970) suggested that Ad. squamipennis may represent a species complex, until now no close new taxa have been described in the Neotropics.
Aedeomyia squamipennis is well distributed in Brazil, yet prior to this study this species had not been found in Maranhão (Xavier & Mattos 1989a), despite being known to occur in the neighboring Pará and Piauí states (Xavier & Mattos 1975;Xavier et al. 1979).
Maranhão is located in a privileged position with respect to geography, in the transition zone between the two largest Brazilian biomes, the Amazon and the Cerrado, thus forming several different physiognomies (Rebêlo et al. 2007).The state contains the largest continuous band of Brazilian mangrove (Rebelo-Mochel 2011) and a small portion of Caatinga biome, with a predominance of deciduous and seasonal sub-deciduous vegetation (Velloso et al. 2002).It also contains an extensive floodplain area called 'Baixada Maranhense' formed by flooded terrain, mangroves and sandbanks (Veloso 1964).The latter area is greatly affected by the rainy season, which causes the formation of large lakes that completely alter the local landscape, making it akin to the Brazilian Pantanal.Northeastern Maranhão contains a unique ecosystem called the 'Lençóis Maranhenses', consisting of Restinga vegetation, freshwater lagoons, and lush sandy dunes (Miranda et al. 2012).
According to the literature, prior to this study there were 78 species of mosquitoes recorded in Maranhão state (Vasconcelos et al. 1989;Xavier & Mattos 1989a;Motta & Lourenço-de-Oliveira 1995;Ahid & Lourenço-de-Oliveira 1999;Rebêlo et al. 2007).We present in this manuscript the first record of Ad. squamipennis in Maranhão, describing its range in the state and its distribution in Brazil, as did Blanton & Peyton (1957) for Panama and Gabaldon et al. (1981) for Venezuela.
The specimens used in this article are from three different studies.The first is an extensive inventory of phlebotomines conducted under the auspices of the Ministry of Health in the 11 municipalities with the highest rate of leishmaniasis in state.This research lasted two years (May 2012 to April 2014), in which samples were taken monthly and simultaneously in all municipalities studied.The second was the capture of sand flies, carried out in the vicinity of the Lençóis Maranhenses National Park, in villages of Barreirinhas and Santo Amaro do Maranhão, as described by PEREIRA-FILHO et al. (2015).The third is an inventory of sandflies in neighboring municipalities of Bacurituba and Cajapió in June 2016, both in region of Baixada Maranhense.All collections used incandescent, HP type CDC light traps (Pugedo et al. 2005) that were activated during 12 hours (18:00-06:00 h).
All specimens were taken to the Laboratório de Entomologia e Vetores at the Universidade Federal do Maranhão (LEV/UFMA), where insects were screened and identified.The capture methods used were not species-specific, thus in addition to sandflies other insect groups were eventually caught by these traps, including mosquitoes.Vouchers specimens were pinned and deposited in the Coleção de Culicidae da Fiocruz (Fiocruz-CCULI), Rio de Janeiro-RJ, Brasil (Table 1).No samples for DNA were taken from the vouchers.
Aedeomyia squamipennis distribution map was created using the Quantum GIS version 2.16.2 (Figure 1).Data of distribution were derived from extensive review of studies reporting Ad. squamipennis in Brazil (Appendix, Table A1).Geographic coordinates were found in literature and internet sources, in some cases this data were approximate, but some localities coordinates were not found.Datum used for geographic coordinates was South American Datum (SAD69).
Identification was carried out by first using the key to Culicidae genera proposed by Consoli & Lourenço de Oliveira (1994), then using the key proposed by Tyson (1970) to identify species within genus Aedeomyia, and Brunhes et al. (2011) as a supplementary tool.Furthermore, Dr. Monique Motta of the Laboratório de Mosquitos Transmissores de Hematozoários -Instituto Oswaldo Cruz (LATHEMA-IOC/Fiocruz) confirmed identifications by visual inspection of adults in stereomicroscope.
Aedeomyia squamipennis is the only representative of tribe Aedeomyiini in New World (Figure 2).Differs from all other mosquitoes of this region by following combination of characters: apex of mid and hindfemora with large tufts of outstanding scales (Figure 3); broad scales on torus, clypeus and flagellomere I; all flagellomeres thick and short; and flagellomeres II-XIII nearly equal in length (Figure 4); wings covered with broad yellowish, white and dark scales (Figure 5).
This species has also been implicated in arbovirus cycles, with prior investigators having isolated from adult mosquitoes Gamboa group virus, in which the natural cycle seems to involve birds (Dégallier et al. 1992), as well as Venezuelan Equine Encephalitis (VEE) virus complex (Mitchell et al. 1985).Although birds are not considered important hosts of VEE, Dickerman et al. (1976) showed that some Ciconiiformes can play a role in maintaining enzootic cycles.Such data demonstrate the capacity of Ad. squamipennis for contracting various parasites.
It is known that vector susceptibility to a parasite species can vary among populations, a phenomenon that may be explained by a combination of environmental conditions and ecological factors potentially altering vector-pathogen-host interactions (Santiago-Alarcon et al. 2012), in addition to behavioral and ecological variation.Although Ad. squamipennis has never been found infected with avian Plasmodium in Brazil (Santiago-Alarcon et al. 2012), this record in Santo Amaro do Maranhão indicates some epidemiological potential.The municipality lies on the Santo Amaro Lake, which borders the western edge of the Lençóis Maranhenses National Park.Soares & Rodrigues (2009) observed at least 41 species of birds occupying that lake, including resident and Nearctic migratory shorebirds (i.e., families Caradriidae and Scolopacidae).These two shorebird families are especially abundant in the dry season, which extends from September to November.Data from Soares & Rodrigues (2009) associated the presence of Ad. squamipennis in practically the same area as indicative of the potential vulnerability of the region to avian malaria and some arboviruses.The presence of migratory birds in the region may serve as a source of infection, and resident bird as point for dispersion of local parasite populations.Interestingly, of the 14 species of Ciconiiformes found by Gabaldon et al. (1985) to be infected by F. neotropicalis in Venezuela, six were later reported on Lake Santo Amaro by Soares & Rodrigues (2009).There have been no ecological studies of mosquito fauna in Santo Amaro do Maranhão (and studies of mosquitoes are generally lacking in other municipalities as well), thus this is the first record of Culicidae species in this municipality.
This new record of Ad. squamipennis raises the number of known mosquitoes species in Maranhão to 79.Based on its geographical position in transition zone and the wealth of ecosystems, lack of previous records of Ad. squamipennis may be explained by the lack of culicidofauna surveys.This finding indicates the need for entomological surveys in representative areas of the state, in order to better estimate the number of existing mosquito species.Studies that address ecological, behavioral and epidemiological facets of these organisms should also be carried out.
; Lourenço-de-Oliveira & Silva 1985; Consoli & Lourenço de Oliveira 1994; Naves et al. 1998; Forattini 2002).Ornithophilic mosquitoes are often suspected during avian disease outbreaks.For has been recorded in 21 federal states.The only states without records of this species are Roraima in the North region, Alagoas, Ceará, Paraíba and Sergipe in the Northeast, the Federal District in the Central-West.Specimens of Ad. squamipennis were collected in trap installed in a henhouse in the Riachão location, Santo

Figure 1 .
Figure 1.Geographic distribution of Aedeomyia squamipennis in Brazil based on literature records and collection data (black triangles), and new records from Maranhão state (black dots), based on present study.

Table 1 .
). Barra do Corda is located in the central region of the state, with a predominance of Cerrado vegetation and mixed forest (equatorial evergreen open forest with Cocal) (IBGE 1984).Governador Nunes Freire lies in the northwestern part of the Amazonian, although with quite deforested areas.Bacurituba and Cajapió are situated in north of state, near to the Rio Mearim mouth, in Baixada Maranhense region.Santo Amaro do Maranhão is located on the northeastern coast near the Lençóis Maranhenses National Park, which contains Restinga vegetation on paleodunes, associated with Cerrado (IBGE 1984).Data presented in this study indicate that Ad. squamipennis is well distributed in the state of Maranhão, occurring in the central, north, northeastern and northwestern portions.With the inclusion of Maranhão now this species Voucher specimens of Aedeomyia squamipennis collected in Maranhão state deposited in the Coleção de Culicidae da Fiocruz (Fiocruz-CCULI).