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Revista Brasileira de Entomologia

Print version ISSN 0085-5626

Rev. Bras. entomol. vol.58 no.1 São Paulo Jan./Mar. 2014

http://dx.doi.org/10.1590/S0085-56262014000100013 

MEDICAL AND VETERINARY ENTOMOLOGY

 

Phlebotomine sand flies (Diptera, Psychodidae) from Rio de Janeiro State, Brazil: species distribution and potential vectors of leishmaniases

 

 

Bruno Moreira CarvalhoI,*; Cristina Maria Giordano DiasII; Elizabeth Ferreira RangelI

ILaboratório de Transmissores de Leishmanioses, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz. Avenida Brasil, 4365, Pavilhão Carlos Chagas, 5º andar, sala 43, Manguinhos, 21040–360 Rio de Janeiro-RJ, Brasil, brunomc@ioc.fiocruz.br; efrangel@ioc.fiocruz.br
IICentro de Estudos e Pesquisas em Antropozoonoses Máximo da Fonseca Filho, Secretaria de Estado de Saúde do Rio de Janeiro. Rua do Resende 118, sala 201 – Centro, 20231–092 Rio de Janeiro-RJ, Brasil, cristina.giordano@saude.rj.gov.br

 

 


ABSTRACT

Phlebotomine sand flies (Diptera, Psychodidae) from Rio de Janeiro State, Brazil: Species distribution and potential vectors of leishmaniases. Rio de Janeiro State, in Brazil, has endemic areas of both cutaneous and visceral leishmaniases. In these areas, entomologic surveillance actions are highly recommended by Brazil's Ministry of Health. The present work describes the results of sand fly captures performed by the Health Department of Rio de Janeiro State between 2009 and 2011 in several municipalities. An updated species list and distribution of phlebotomine sand flies in the state are provided based on an extensive literature review. Currently, the sand fly fauna of Rio de Janeiro State has 65 species, belonging to the genera Brumptomyia (8 spp.) and Lutzomyia (57 spp.). Distribution maps of potential leishmaniases vector species Lutzomyia (Nyssomyia) intermedia, L. migonei, L. (N.) whitmani, L. (N.) flaviscutellata and L. (Lutzomyia) longipalpis are provided and their epidemiological importance is discussed.

Keywords: Insecta; monitoring; Phlebotominae; review; species list.


 

 

Brazil is the country with the highest estimated annual incidences of American Visceral Leishmaniasis (AVL) and American Cutaneous Leishmaniasis (ACL) (Alvar et al. 2012). Both AVL and ACL are widespread in the Brazilian territory, where their notification is mandatory (Brasil 2006, 2007). The current spread of these diseases in the country reveals a change in their epidemiological profiles, shifting from rural to periurban areas, with human cases recorded even in capital cities such as Campo Grande (Brazuna et al. 2012), Belo Horizonte (Passos et al. 1993) and Rio de Janeiro (Marzochi et al. 2009).

Back in 1912, Adolpho Lutz and Arthur Neiva described three sand fly species, speculating in their possible role as disease vectors (Lutz & Neiva 1912). Two of these species were captured in Rio de Janeiro State: i) Lutzomyia (Lutzomyia) longipalpis in Mangaratiba and Rio de Janeiro municipalities; ii) Lutzomyia (Nyssomyia) intermedia in Rio de Janeiro municipality, in the neighborhoods of Santa Teresa and Laranjeiras.

The earliest report of ACL human cases in Rio de Janeiro State was published by D'Utra e Silva (1915), but the first documented outbreak of the disease occurred later in 1921 in Rio de Janeiro municipality, with about 50 human cases recorded in "Santa Thereza Hill", an area that today corresponds to Laranjeiras, Cosme Velho and Santa Teresa neighborhoods (Cerqueira & Vasconcelos 1922). At the same time, Aragão (1922, 1927) noticed the high frequency of sand flies associated with areas of ACL human cases and demonstrated the importance of L. (N.) intermedia on the transmission of Leishmania (Viannia) braziliensis.

Other important ACL outbreaks occurred in 1974 in Jacarepaguá, also in Rio de Janeiro municipality (Lima et al. 1988), and in 1975 in Ilha Grande, in Angra dos Reis municipality (Araújo Filho & Coura 1981). Currently, ACL is widely spread in the state, with 1,951 autochthonous human cases recorded in the past 10 years (2002 to 2011) (Oliveira-Neto et al. 2000; Kawa & Sabroza 2002; Bustamante et al. 2009).

According to the literature, the main ACL vector in Rio de Janeiro State is L. (N.) intermedia, with L. migonei being considered as secondary vector, especially in Rio de Janeiro municipality (Araújo Filho et al. 1981; Rangel et al. 1986; Pita-Pereira et al. 2005). Other potential vector species have been registered in endemic areas of the state, such as L. (N.) whitmani, L. (N.) flaviscutellata, L. (Pintomyia) fischeri and L. (P.) pessoai (Araújo Filho et al. 1981; Rangel et al. 1984, 1986, 1990; Souza et al. 2002).

The number of human cases of AVL in the state is much lower than ACL cases. In the same 10-year period (2002 to 2011), 49 autochthonous human cases were recorded. It was in the late 1970s that the first AVL autochthonous case was recorded: a then deceased 55 year old man who lived in Bangu (Rio de Janeiro municipality) (Salazar et al. 1979). Currently, in the state, the disease has been registered in several municipalities, but most human cases are concentrated in Rio de Janeiro, around the Pedra Branca Massif, and in continental slopes of the Gericinó Massif, in Bangu, Senador Camará, Realengo, Campo Grande, Guaratiba, Barra de Guaratiba, Barra da Tijuca, Grumari, Vargem Grande, Camo-rim, Curicica, Taquara and Gericinó neighborhoods (Marzochi et al. 2009). The main vector of Leishmania (Leishmania) infantum chagasi in Brazil, L. (Lutzomyia) longipalpis, was also already detected in Rio de Janeiro State on several studies (Araújo Filho et al. 1981; Souza et al. 1981, 2003a; Marzochi et al. 1985, 2009).

Brazil's Ministry of Health recommends that every leishmaniases outbreak must be surveyed for occurrence of sand fly vectors (Brasil 2006, 2007). When planning an entomologic survey of a particular area, it is essential to know if the area has been surveyed before and which sand fly species have been detected there. Most recent studies on the distribution of sand flies from Brazil list 53 species occurring in Rio de Janeiro State (CIPA Group 1999; Aguiar & Medeiros 2003; Galati 2003). The last publication on the sand fly fauna from the state in a finer scale was Martins et al. (1978). Here, an updated sand fly species list and distribution in Rio de Janeiro State is provided, based on the entomologic surveillance activities of the Health Department of Rio de Janeiro State and an extensive literature review.

 

MATERIAL AND METHODS

Entomologic surveys have been done systematically by the Health Department of Rio de Janeiro State. Whenever a new human case of leishmaniasis is notified, sand fly captures are performed to survey the probable area of infection and detect potential vector species. Sand flies were captured with CDC (Sudia & Chamberlain 1962) or HP (Pugedo et al. 2005) light traps, following recommendations by Brazil's Ministry of Health (Brasil 2006, 2007). Species identification was based on the taxonomic key of Young & Duncan (1994).

Literature search was performed on the following online databases: Medline (http://www.ncbi.nlm.nih.gov/pubmed/), Scopus (http://www.scopus.com), Scielo (http://www.scielo.org), Biblioteca Virtual em Saúde (http://regional.bvsalud.org) and Google Scholar (http://scholar.google.com). Thesis databases from Fundação Oswaldo Cruz were also consulted (http://www.arca.fiocruz.br). Every reference that was not available online was searched on two libraries from Fundação Oswaldo Cruz: Biblioteca de Ciências Biomédicas (http://www.fiocruz.br/bibcb) and Biblioteca de Saúde Pública (http://www.fiocruz.br/bibsp). Each retrieved reference was carefully reviewed for sand fly records from Rio de Janeiro State, and a database was compiled with species records by municipality.

Distribution maps were created for potential vectors of Leishmania spp. and leishmaniases human cases recorded by the Health Department of Rio de Janeiro State between years 2002 and 2011. Maps were designed with the municipality territorial division of IBGE (2010), in ArcGIS 10 software.

As expected, during this review, different species nomenclatures were found. In order to facilitate text comprehension, every sand fly species name was adapted to the nomenclature proposed by Young & Duncan (1994).

 

RESULTS

Between 2009 and 2011, 22 municipalities were surveyed by the Health Department of Rio de Janeiro: Armação dos Búzios, Barra Mansa, Cambuci, Campos dos Goytacazes, Cantagalo, Duas Barras, Itaguaí, Itaperuna, Itatiaia, Macaé, Miguel Pereira, Porciúncula, Porto Real, Rio Bonito, Rio de Janeiro, Santa Maria Madalena, São Fidélis, Trajano de Moraes, Três Rios, Valença, Vassouras and Volta Redonda. In these surveys, 25 sand fly species were detected: Brumptomyia brumpti, B. nitzulescui, Lutzomyia (L.) longipalpis, L. (L.) ischyracantha, L. (L.) alencari, L. (S.) sordellii, L. edwardsi, L. migonei, L. sallesi, L. tupynambai, L. termitophila, L. firmatoi, L. walkeri, L. (P.) pessoai, L. (P.) fischeri, L. (P.) bianchigalatiae, L. aragaoi, L. (T.) longispina,L. (N.) whitmani, L. (N.) intermedia, L. (P.) davisi, L. (P.) hirsuta hirsuta, L. (P.) ayrozai, L. quinquefer and L. oswaldoi.

The literature review resulted in a database with 61 sand fly species from 70 references, including 64 published articles, 2 dissertations, 2 monographs, 1 research report and 1 book chapter.

Rio de Janeiro sand fly fauna consists of 65 species, from genus Brumptomyia (8 spp.) and Lutzomyia (57 spp.). The Lutzomyia species was represented by nine subgenus and five species groups, as well as two ungrouped species. Species list and distribution by municipality is provided next. New records for the state, when compared with previous distribution reviews (Martins et al. 1968; CIPA Group 1999; Aguiar & Medeiros 2003; Galati 2003) are marked with (*). Type localities are marked with (**) and doubtful records with (***).

Genus Brumptomyia França & Parrot, 1921 (8 spp.):

B. avellari (Costa Lima, 1932): Angra dos Reis (Rendeiro 2007), Bom Jesus do Itabapoana (Rezende et al. 2009), Cardoso Moreira (Mangabeira Filho 1942b; Martins et al. 1978), Itaguaí (Aguiar et al. 1996).

B. brumpti (Larrousse, 1920)*: Campos dos Goytacazes, Mangaratiba (Novo et al. 2013), Miguel Pereira, Petrópolis (Souza et al. 2002, 2005a), Rio de Janeiro (Gouveia et al. 2012), São Fidélis, Três Rios, Valença.

B. cardosoi (Barretto & Coutinho, 1941): Duque de Caxias (Martins et al. 1978), Magé (Aguiar et al. 1985c; Aguiar & Vilela 1987), Nova Iguaçu (Martins et al. 1978), Petrópolis (Souza et al. 2002, 2005a), Valença (Martins et al. 1978).

B. cunhai (Mangabeira, 1942): Angra dos Reis (Araújo Filho et al. 1981; Carvalho et al. 2013), Itaguaí (Aguiar et al. 1996), Maricá (Rodrigues et al. 2013), Niterói (Rodrigues et al. 2013), Nova Iguaçu (Martins et al. 1978), Rio de Janeiro (Souza et al. 2000), Saquarema (Brazil et al. 2011).

B. guimaraesi (Coutinho & Barretto, 1941): Angra dos Reis (Rendeiro 2007), Casimiro de Abreu (Souza et al. 2001), Itaguaí (Aguiar et al. 1996), Itatiaia (Afonso et al. 2007), Magé (Aguiar et al. 1985c; Aguiar & Vilela 1987), Mesquita (Oliveira-Neto et al. 2000; Meneses et al. 2002), Paraty (Carvalho et al. 1995, 2000), Petrópolis (Souza et al. 2002, 2005a), Rio de Janeiro (Cabrera et al. 2003), Saquarema (Brazil et al. 2011).

B. nitzulescui (Costa Lima, 1932): Angra dos Reis (Araújo Filho et al. 1981; Carvalho et al. 2013), Duque de Caxias (Martins et al. 1978), Itaguaí, Mesquita (Meneses et al. 2002), Niterói (Rodrigues et al. 2013), Nova Iguaçu (Martins et al. 1978), Rio de Janeiro (Gouveia et al. 2012), Valença (Martins et al. 1978).

B. pintoi (Costa Lima, 1932): Cardoso Moreira (Martins et al. 1978).

B. troglodytes (Lutz, 1922): Itatiaia (Afonso et al. 2007), Magé (Aguiar et al. 1985c; Aguiar & Vilela 1987), Nova Iguaçu (Martins et al. 1978).

Genus Lutzomyia França, 1924 (57 spp.):
Subgenus L. (Lutzomyia) França, 1924 (5 spp.):

L. (L.) amarali (Barretto & Coutinho, 1940): Bom Jesus do Itabapoana (Rezende et al. 2009), Itatiaia (Afonso et al. 2007), Magé (Aguiar et al. 1985c), Petrópolis (Martins et al. 1978; Souza et al. 2002, 2005a).

L. (L.) longipalpis (Lutz & Neiva, 1912): Angra dos Reis (Araújo Filho & Sherlock 1981; Araújo Filho et al. 1981; Carvalho et al. 2013), Armação dos Búzios, Barra Mansa, Casimiro de Abreu (Souza et al. 2001), Itaguaí (Aguiar et al. 1987, 1996), Macaé (Martins et al. 1978), Mangaratiba (Lutz & Neiva 1912; Novo et al. 2013), Mesquita (Rangel et al. 1990; Oliveira-Neto et al. 2000; Meneses et al. 2002), Niterói (Rodrigues et al. 2013), Paraty (Moutinho et al. 2010), Petrópolis (Souza et al. 2002), Rio Bonito (Brazil et al. 1989), Rio de Janeiro (Lutz & Neiva 1912; Fundação Oswaldo Cruz 1974; Martins et al. 1978; Lima et al. 1981; Souza et al. 1981, 2003b; Rangel et al. 1986; Cabrera et al. 2003; Brazil 2013), São Fidélis, Saquarema (Brazil et al. 2011, 2012), Valença, Volta Redonda.

L. (L.) ischyracantha* Martins, Falcão & Silva, 1962: São Fidélis.

L. (L.) alencari Martins, Souza & Falcão, 1962: São Fidélis.

L. (L.) gasparviannai Martins, Godoy & Silva, 1962: Nova Iguaçu** (Martins et al. 1962b, 1978).

Subgenus L. (Sciopemyia) Barretto, 1962 (2 spp.):

L. (S.) sordellii (Shannon & Del Ponte, 1927): Armação dos Búzios, Macaé, Rio de Janeiro (Oliveira et al. 1995; Gouveia et al. 2012), Três Rios.

L (S.) microps (Mangabeira, 1942): Angra dos Reis (Carvalho et al. 2013), Magé (Aguiar & Soucasaux 1984; Aguiar et al. 1985a; Aguiar & Vilela 1987), Mangaratiba (Martins et al. 1978), Niterói (Rodrigues et al. 2013), Nova Iguaçu** (Mangabeira Filho 1942a; Martins et al. 1978), Petrópolis (Martins et al. 1962a, 1978; Souza et al. 2002, 2005a).

Species Group Migonei Theodor, 1965 (11 spp.):

L. lenti (Mangabeira, 1938): Bom Jesus do Itabapoana (Rezende et al. 2009), Carmo (Alves 2007), Macaé (Martins et al. 1978), Rio de Janeiro (Oliveira et al. 1995).

L. edwardsi (Mangabeira, 1941): Angra dos Reis (Araújo Filho et al. 1981; Rendeiro 2007; Carvalho et al. 2013), Bom Jardim (Souza et al. 2003a), Duque de Caxias (Martins et al. 1978), Itaguaí (Aguiar et al. 1996), Itatiaia (Martins et al. 1978; Afonso et al. 2007), Magé (Aguiar et al. 1985c; Aguiar & Vilela 1987), Mangaratiba (Martins et al. 1978; Novo et al. 2013), Maricá (Rodrigues et al. 2013), Mesquita (Rangel et al. 1990), Niterói (Rodrigues et al. 2013), Nova Iguaçu** (Martins et al. 1978; Mangabeira Filho 1941), Paraty (Aguiar et al. 1993; Costa et al. 2004; Carvalho et al. 1995, 2000), Petrópolis (Martins et al. 1962a; Martins et al. 1978; Souza et al. 2002, 2005a), Rio de Janeiro (Cabrera et al. 2003; Souza et al. 2003b; Gouveia et al. 2012), Silva Jardim (Souza et al. 2001), Valença (Martins et al. 1978), Vassouras.

L. migonei (França, 1920): Angra dos Reis (Araújo Filho et al. 1981; Martins et al. 1978; Rendeiro 2007; Souza et al. 2009; Carvalho et al. 2013), Bom Jardim (Souza et al. 2003a), Bom Jesus do Itabapoana (Rezende et al. 2009), Cambuci, Cantagalo, Carmo (Alves 2007), Casimiro de Abreu (Souza et al. 2001), Duque de Caxias (Martins et al. 1978), Itaguaí (Aguiar et al. 1987, 1996), Itatiaia (Afonso et al. 2007), Macaé (Martins et al. 1978), Magé (Martins et al. 1978), Mangaratiba (Costa Lima 1932; Martins et al. 1978; Novo et al. 2013), Mesquita (Rangel et al. 1990; Oliveira-Neto et al. 2000; Meneses et al. 2002), Miguel Pereira, Niterói (Brazil et al. 1989; Brazil et al. 1991; Rodrigues et al. 2013), Nova Iguaçu (Martins et al. 1978), Paracambi (Santos 1998), Paraty (Aguiar et al. 1993; Carvalho et al. 1995, 2000; Costa et al. 2004; Moutinho et al. 2010), Petrópolis (Barretto & Zago Filho 1956; Martins et al. 1962a, 1978; Souza et al. 2002, 2005a), Resende (Martins et al. 1978), Rio Bonito (Martins et al. 1978; Brazil et al. 1989), Rio de Janeiro (Aragão 1927; Costa Lima 1932; Fundação Oswaldo Cruz 1974; Martins et al. 1978; Lima et al. 1981, 1988; Souza et al. 1981, 2000, 2003b; Rangel et al. 1986; Cabrera et al. 2003; Pita-Pereira et al. 2005; Gouveia et al. 2012), Santa Maria Madalena, São Fidélis, Saquarema (Brazil et al. 2011), Seropédica (Cardoso et al. 2009), Valença, Vassouras (Martins et al. 1978).

L. cortelezzii (Brèthes, 1923)*: Mangaratiba (Novo et al. 2013), Mesquita (Rangel et al. 1990), Niterói (Rodrigues et al. 2013), Nova Iguaçu (Santana 2003), Rio de Janeiro (Souza et al. 1981), Rio de Janeiro (Souza et al. 2003b).

L. sallesi (Galvão & Coutinho, 1939): Barra Mansa, Cambuci, Cantagalo, Itaperuna, Itatiaia (Afonso et al. 2007), Mesquita (Meneses et al. 2002), Niterói (Brazil et al. 1991), Nova Iguaçu (Santana 2003), Petrópolis (Martins et al. 1962a, 1978), Porciúncula, Resende (Martins et al. 1978), Rio de Janeiro (Oliveira et al. 1995; Souza et al. 2003b), São Fidélis, Valença.

L. tupynambai (Mangabeira, 1942): Angra dos Reis (Carvalho et al. 2013; Souza et al. 2009), Campos dos Goytacazes (Martins et al. 1978), Cardoso Moreira** (Mangabeira Filho 1942a), Itatiaia (Afonso et al. 2007), Mangaratiba (Martins et al. 1978), Maricá (Rodrigues et al. 2013), Niterói (Rodrigues et al. 2013), Paraty (Moutinho et al. 2010), Petrópolis (Martins et al. 1962a, 1978; Souza et al. 2002, 2005a), São Fidélis.

L. costalimai (Mangabeira, 1942): Bom Jardim (Souza et al. 2003a), Campos dos Goytacazes (Martins et al. 1978), Cardoso Moreira** (Mangabeira Filho 1942a), Mangaratiba (Martins et al. 1978), Petrópolis (Souza et al. 2002, 2005a), Rio de Janeiro (Souza et al. 2003b).

L. petropolitana Martins & Silva, 1968: Petrópolis** (Martins & Silva 1968; Martins et al. 1978).

L. termitophila Martins, Falcão & Silva, 1964: Angra dos Reis (Carvalho et al. 2013), Cambuci, Petrópolis (Souza et al. 2002), Petrópolis (Souza et al. 2005a), Rio de Janeiro (Oliveira et al. 1995).

L. firmatoi (Barretto, Martins & Pellegrino, 1956): Angra dos Reis (Carvalho et al. 2013), Bom Jardim (Souza et al. 2003a), Itaguaí (Aguiar et al. 1996), Mangaratiba (Novo et al. 2013), Mesquita (Rangel et al. 1990), Miguel Pereira, Niterói (Brazil et al. 1989), Nova Iguaçu (Martins et al. 1978), Paraty (Aguiar et al. 1993; Moutinho et al. 2010), Petrópolis (Souza et al. 2002, 2005a), Rio de Janeiro (Souza et al. 1981, 2000, 2003b; Rangel et al. 1986; Lima et al. 1988), São Pedro da Aldeia (Martins et al. 1978).

L. walkeri (Newstead, 1914)*: São Fidélis.

Species Group Verrucarum Theodor, 1965 (1 sp.):

L. serrana (Damasceno & Arouck, 1949): Mesquita (Meneses et al. 2002), Nova Iguaçu (Martins et al. 1978).

Subgenus L. (Pintomyia) Costa Lima, 1932 (3 spp.):

L. (P.) pessoai (Coutinho & Barretto, 1940): Angra dos Reis (Rendeiro 2007), Itaguaí (Aguiar et al. 1987, 1996), Itatiaia (Afonso et al. 2007), Magé (Aguiar & Soucasaux 1984; Aguiar et al. 1985a, 1985b; Aguiar & Vilela 1987), Mangaratiba (Martins et al. 1978), Niterói (Brazil et al. 1989, 1991), Paracambi (Santos 1998), Paraty (Aguiar et al. 1993), Petrópolis (Barretto & Zago Filho 1956; Martins et al. 1978; Souza et al. 2002, 2005a), Rio de Janeiro (Souza et al. 2000, 2003b), Saquarema (Brazil et al. 2011), Vassouras.

L. (P.) fischeri (Pinto, 1926): Angra dos Reis (Martins et al. 1978; Rendeiro 2007; Souza et al. 2009), Bom Jardim (Souza et al. 2003a), Bom Jesus do Itabapoana (Rezende et al. 2009), Cantagalo, Casimiro de Abreu (Souza et al. 2001), Duque de Caxias (Martins et al. 1978), Itaguaí (Aguiar et al. 1987, 1996), Magé (Martins et al. 1978; Aguiar & Soucasaux 1984; Aguiar et al. 1985a, 1985b, 1985c, 1986; Aguiar & Vilela 1987), Mangaratiba (Novo et al. 2013), Mesquita (Rangel et al. 1990), Niterói (Brazil et al. 1989, 1991), Nova Iguaçu (Martins et al.

1978), Paracambi (Santos 1998), Paraty (Aguiar et al. 1993; Carvalho et al. 1995, 2000; Costa et al. 2004; Moutinho et al. 2010), Petrópolis (Barretto & Zago Filho 1956; Martins et al. 1962a, 1978; Souza et al. 2002, 2005a), Resende (Martins et al. 1978), Rio Bonito (Brazil et al. 1989), Rio de Janeiro (Fundação Oswaldo Cruz 1974; Martins et al. 1978; Lima et al. 1981; Souza et al. 1981, 2000, 2003b; Rangel et al. 1986; Gouveia et al. 2012), Saquarema (Brazil et al. 2011), Valença, Vassouras (Martins et al. 1978).

L. (P.) bianchigalatiae (Andrade-Filho, Aguiar, Dias & Falcão, 1999): Itaguaí (Andrade Filho et al. 1999); Itatiaia (Afonso et al. 2007); Magé (Andrade Filho et al. 1999); Mangaratiba (Novo et al. 2013); Mesquita (Meneses et al. 2002); Niterói (Rodrigues et al. 2013); Saquarema (Brazil et al. 2011), Valença.

Subgenus L. (Pressatia) Mangabeira, 1942 (1 sp.):

L. (P.) mamedei Oliveira, Afonso, Dias & Brazil, 1994: Paraty (Carvalho et al. 1995, 2000), Rio de Janeiro** (Oliveira et al. 1994, 1995).

Species Group Rupicola Lewis et al., 1977 (1 sp.):

L. rupicola Martins, Godoy & Silva, 1962: Angra dos Reis (Carvalho et al. 2013), Itatiaia (Afonso et al. 2007), Magé (Aguiar et al. 1985c), Petrópolis** (Martins et al. 1962a, 1978).

Subgenus L. (Psathyromyia) Barretto, 1962 (2 spp.):

L. (P.) lutziana (Costa Lima, 1932): Cardoso Moreira (Martins et al. 1978), Macaé (Martins et al. 1978), Magé (Martins et al. 1978), Mesquita (Oliveira-Neto et al. 2000; Meneses et al. 2002), Nova Iguaçu (Martins et al. 1978), Paraty (Carvalho et al. 1995, 2000), Petrópolis (Souza et al. 2005a), Rio de Janeiro (Gouveia et al. 2012).

L. (P.) shannoni (Dyar, 1929): Angra dos Reis (Rendeiro 2007), Casimiro de Abreu (Souza et al. 2001), Itatiaia (Afonso et al. 2007), Magé (Aguiar & Soucasaux 1984; Aguiar et al. 1985a, 1985b, 1985c, 1986), Mesquita (Rangel et al. 1990), Nova Iguaçu (Martins et al. 1978), Paracambi (Santos 1998), Paraty (Aguiar et al. 1993), Petrópolis (Barretto & Zago Filho 1956), Petrópolis (Martins et al. 1962a, 1978; Souza et al. 2002, 2005a), Resende (Martins et al. 1978), Rio de Janeiro (Martins et al. 1978), Silva Jardim (Souza et al. 2001).

Species Group Aragaoi Theodor, 1965 (4 spp.):

L. barrettoi barrettoi (Mangabeira, 1942): Angra dos Reis (Rendeiro 2007), Casimiro de Abreu (Souza et al. 2001), Itaguaí (Aguiar et al. 1996), Magé (Aguiar et al. 1985c; Aguiar & Vilela 1987), Mesquita (Oliveira-Neto et al. 2000; Meneses et al. 2002), Petrópolis (Martins et al. 1962a, 1978; Souza et al. 2002, 2005a), Rio de Janeiro (Rangel et al. 1986), Silva Jardim (Souza et al. 2001).

L. pascalei (Coutinho & Barretto, 1940): Angra dos Reis (Araújo Filho et al. 1981; Carvalho et al. 2013), Itatiaia (Afonso et al. 2007), Mesquita (Meneses et al. 2002), Nova Iguaçu (Martins et al. 1978), Paraty (Aguiar et al. 1993).

L. aragaoi (Costa Lima, 1932): Angra dos Reis (Rendeiro 2007), Magé (Aguiar & Vilela 1987), Três Rios.

L. brasiliensis (Costa Lima, 1932): Cardoso Moreira (Martins et al. 1978).

Species Group Lanei Theodor, 1965 (2 spp.):

L. pelloni (Sherlock & Alencar, 1959): Angra dos Reis (Souza et al. 2009; Carvalho et al. 2013), Bom Jardim (Souza et al. 2003a), Duque de Caxias (Martins et al. 1978), Magé (Martins et al. 1978), Mangaratiba (Martins et al. 1978; Novo et al. 2013), Niterói (Brazil et al. 1989), Nova Iguaçu (Martins et al. 1978), Rio de Janeiro (Fundação Oswaldo Cruz 1974; Rangel et al. 1986; Lima et al. 1988; Souza et al. 2000, 2003b; Gouveia et al. 2012).

L. lanei (Barretto & Coutinho, 1941): Angra dos Reis (Araújo Filho et al. 1981), Itaguaí (Aguiar et al. 1996), Itatiaia (Afonso et al. 2007), Magé (Aguiar et al. 1985c), Mangaratiba (Martins et al. 1978), Maricá (Rodrigues et al. 2013), Mesquita (Rangel et al. 1990; Meneses et al. 2002), Niterói (Rodrigues et al. 2013), Nova Iguaçu (Martins et al. 1978), Petrópolis (Barretto & Zago Filho 1956), Petrópolis (Martins et al. 1962a, 1978), Resende (Martins et al. 1978), Rio de Janeiro (Rangel et al. 1986).

Subgenus L. (Trichopygomyia) Barretto, 1962 (1 sp.):

L. (T.) longispina (Mangabeira, 1942)*: Valença.

Subgenus L. (Nyssomyia) Barretto, 1962 (3 spp.):

L. (N.) flaviscutellata (Mangabeira, 1942): Angra dos Reis (Araújo Filho et al. 1981; Carvalho et al. 2013), Nova Iguaçu (Martins et al. 1978), Petrópolis (Martins et al. 1962a, 1978).

L. (N.) whitmani (Antunes & Coutinho, 1939): Angra dos Reis (Rendeiro 2007), Bom Jardim (Souza et al. 2003a), Bom Jesus do Itabapoana (Rezende et al. 2009), Cantagalo, Carmo (Alves 2007), Casimiro de Abreu (Souza et al. 2001), Itaguaí (Aguiar et al. 1987, 1996), Itaperuna, Itatiaia, Mesquita (Rangel et al. 1990; Oliveira-Neto et al. 2000; Meneses et al. 2002), Miguel Pereira, Paracambi (Santos 1998), Paraty (Aguiar et al. 1993; Carvalho et al. 1995, 2000), Petrópolis (Souza et al. 2002, 2005a, 2005b), Rio de Janeiro (Lima et al. 1981; Rangel et al. 1986; Oliveira et al. 1995; Souza et al. 2000, 2003b; Cabrera et al. 2003), São Fidélis, Saquarema (Brazil et al. 2011), Seropédica (Cardoso et al. 2009), Silva Jardim (Souza et al. 2001), Três Rios, Valença, Volta Redonda.

L. (N.) intermedia (Lutz & Neiva, 1912): Angra dos Reis (Martins et al. 1978; Araújo Filho et al. 1981; Rendeiro 2007; Souza et al. 2009; Carvalho et al. 2013), Araruama (Martins et al. 1978), Bom Jardim (Souza et al. 2003a), Bom Jesus do Itabapoana (Rezende et al. 2009), Cambuci, Cantagalo, Carmo (Alves 2007), Casimiro de Abreu (Souza et al. 2001), Duas Barras, Itaboraí (Martins et al. 1978), Itaguaí (Aguiar et al. 1987, 1996), Itaperuna (Martins et al. 1978), Itaperuna, Itatiaia, Macaé (Martins et al. 1978), Magé (Nery-Guimarães & Bustamante 1954; Nery-Guimarães 1955; Martins et al. 1978), Mangaratiba (Martins et al. 1978; Novo et al. 2013), Mesquita (Rangel et al. 1990; Oliveira-Neto et al. 2000; Meneses et al. 2002, 2005; Afonso et al. 2005), Miguel Pereira, Niterói (Brazil et al. 1989, 1991; Rodrigues et al. 2013), Nova Iguaçu (Martins et al. 1978; Santana 2003), Paracambi (Santos 1998), Paraty (Aguiar et al. 1993; Carvalho et al. 1995, 2000; Costa et al. 2004; Moutinho et al. 2010), Petrópolis (Barretto & Zago Filho 1956; Martins et al. 1962a, 1978; Souza et al. 2002, 2005a, 2005b), Porto Real, Resende (Martins et al. 1978), Rio Bonito (Martins et al. 1978; Brazil et al. 1989), Rio de Janeiro (Lutz & Neiva 1912; Aragão 1927; Costa Lima 1932; Fundação Oswaldo Cruz 1974; Martins et al. 1978; Lima et al. 1981, 1988; Souza et al. 1981, 2000, 2003b; Rangel et al. 1984, 1986; Oliveira-Neto et al. 1988; Oliveira et al. 1995; Cabrera et al. 2003; Pita-Pereira et al. 2005; Gouveia et al. 2012), Santa Maria Madalena, São Fidélis, Saquarema (Brazil et al. 2011), Seropédica (Cardoso et al. 2009), Silva Jardim (Souza et al. 2001), Trajano de Moraes, Três Rios, Valença (Martins et al. 1978), Vassouras (Martins et al. 1978), Volta Redonda.

Subgenus L. (Psychodopygus) Mangabeira, 1941 (10 spp.):

L. (P.) geniculata (Mangabeira, 1941): Paraty (Aguiar et al. 1993).

L. (P.) matosi (Barretto & Zago Filho, 1956): Itatiaia (Afonso et al. 2007), Petrópolis** (Barretto & Zago Filho 1956; Martins et al. 1978), Resende (Martins et al. 1978), Vassouras (Martins et al. 1978).

L. (P.) arthuri (Fonseca, 1936): Paraty (Aguiar et al. 1993), Petrópolis (Barretto & Zago Filho 1956; Martins et al. 1978).

L. (P.) lloydi (Antunes, 1937): Bom Jardim (Souza et al. 2003a), Petrópolis (Barretto & Zago Filho 1956; Souza et al. 2002, 2005a; Martins et al. 1978).

L. (P.) davisi (Root, 1934): Angra dos Reis (Souza et al. 2009); Duque de Caxias (Martins et al. 1978), Itatiaia (Afonso et al. 2007), Magé (Martins et al. 1978; Aguiar & Soucasaux 1984; Aguiar et al. 1985a, 1985b); Nova Iguaçu (Martins et al. 1978), Paraty (Carvalho et al. 1995, 2000), Valença, Vassouras (Martins et al. 1978).

L. (P.) hirsuta hirsuta (Mangabeira, 1942): Casimiro de Abreu (Souza et al. 2001), Itatiaia (Afonso et al. 2007), Magé (Aguiar & Soucasaux 1984; Aguiar et al. 1985a, 1985b, 1985c, 1986; Aguiar & Vilela 1987), Nova Iguaçu (Martins et al. 1978), Paracambi (Santos 1998), Petrópolis (Martins et al. 1962a, 1978), Rio de Janeiro (Souza et al. 2003b; Gouveia et al. 2012), Silva Jardim (Souza et al. 2001), Valença.

L. (P.) paraensis (Costa Lima, 1941)***: Bom Jardim (Souza et al. 2003a).

L. (P.) ayrozai (Barretto & Coutinho, 1940): Angra dos Reis (Souza et al. 2009; Rendeiro 2007; Carvalho et al. 2013), Carmo (Alves 2007), Duque de Caxias (Martins et al. 1978), Itatiaia (Afonso et al. 2007), Magé (Martins et al. 1978; Aguiar & Soucasaux 1984; Aguiar et al. 1985a, 1985b, 1985c, 1986; Aguiar & Vilela 1987), Mesquita (Meneses et al. 2002), Nova Iguaçu (Martins et al. 1978), Paraty (Aguiar et al. 1993), Petrópolis (Barretto & Zago Filho 1956; Martins et al. 1962a, 1978), Resende (Martins et al. 1978), Silva Jardim (Souza et al. 2001), Valença, Vassouras (Martins et al. 1978).

L. (P.) carrerai carrerai (Barretto, 1946): Itatiaia (Barretto 1955), Resende (Martins et al. 1978).

L. (P.) fairchildi Barretto, 1966: Itatiaia** (Barretto 1966, Martins et al. 1978).

Subgenus L. (Micropygomyia) Barretto, 1962 (3 spp.):

L. (M.) minasensis (Mangabeira, 1942)*: Petrópolis (Souza et al. 2002, 2005a).

L. (M.) schreiberi Martins, Falcão & Silva, 1975: Angra dos Reis (Araújo Filho et al. 1981; Souza et al. 2009; Carvalho et al. 2013), Duque de Caxias (Martins et al. 1978), Itaboraí (Martins et al. 1978), Itaguaí (Aguiar et al. 1987, 1996), Itaperuna (Martins et al. 1978), Macaé (Martins et al. 1978), Magé (Martins et al. 1978), Mangaratiba (Martins et al. 1978), Mangaratiba (Martins et al. 1978; Novo et al. 2013), Maricá (Rodrigues et al. 2013), Mesquita (Oliveira-Neto et al. 2000; Meneses et al. 2002), Niterói (Brazil et al. 1989), Niterói (Martins et al. 1978; Rodrigues et al. 2013), Nova Iguaçu (Martins et al. 1978), Paraty (Aguiar et al. 1993; Carvalho et al. 1995, 2000; Moutinho et al. 2010), Petrópolis (Martins et al. 1962a, cited as L. micropygus; Martins et al. 1978), Rio Bonito (Martins et al. 1978; Brazil et al. 1989), Rio de Janeiro (Martins et al. 1978; Rangel et al. 1986; Lima et al. 1988; Oliveira et al. 1995; Souza et al. 2000, 2003b Cabrera et al. 2003; Gouveia et al. 2012), São Pedro da Aldeia (Martins et al. 1978), Teresópolis (Martins et al. 1978).

L. (M.) micropyga (Mangabeira, 1942)***: Rio de Janeiro (Fundação Oswaldo Cruz 1974; Souza et al. 1981).

Species Group Oswaldoi Theodor, 1965 (6 spp.):

L. borgmeieri Martins, Falcão & Silva, 1972: Itaboraí (J. D. Andrade Filho, personal communication).

L. quinquefer (Dyar, 1929): Angra dos Reis (Souza et al. 2009), Armação dos Búzios, Bom Jardim (Souza et al. 2003a), Bom Jesus do Itabapoana (Rezende et al. 2009), Cantagalo, Carmo (Alves 2007), Itaguaí (Aguiar et al. 1996), Itaperuna (Martins et al. 1978), Mangaratiba (Novo et al. 2013), Mesquita (Rangel et al. 1990; Oliveira-Neto et al. 2000; Meneses et al. 2002), Paraty (Aguiar et al. 1993), Petrópolis (Martins et al. 1978; Souza et al. 2002, 2005a), Rio de Janeiro (Cabrera et al. 2003; Souza et al. 2003b; Gouveia et al. 2012), Santa Maria Madalena, São Fidélis, Trajano de Moraes, Três Rios.

L. longipennis (Barretto, 1946)*: Bom Jardim (Souza et al. 2003a).

L. peresi (Mangabeira, 1942): Itatiaia (Afonso et al. 2007), Rio de Janeiro (Oliveira et al. 1995).

L. capixaba Dias, Falcão, Silva & Martins, 1987*: Mangaratiba (Novo et al. 2013).

L. oswaldoi (Mangabeira, 1942)*: Angra dos Reis (Souza et al. 2009), Bom Jardim (Souza et al. 2003a), Cambuci, Paraty (Carvalho et al. 1995, 2000), Rio de Janeiro (Souza et al. 2000, 2003b), Seropédica (Cardoso et al. 2009).

Ungrouped Lutzomyia Species (2 spp.):

L. monticola (Costa Lima, 1932): Angra dos Reis (Rendeiro 2007), Bom Jardim (Souza et al. 2003a), Casimiro de Abreu (Souza et al. 2001), Itaguaí (Aguiar et al. 1987, 1996), Itatiaia (Afonso et al. 2007), Magé (Aguiar & Soucasaux 1984; Aguiar et al. 1985a, 1985b, 1985c, 1986; Aguiar & Vilela 1987), Paracambi (Santos 1998), Paraty (Aguiar et al. 1993), Petrópolis (Barretto & Zago Filho 1956; Martins et al. 1978; Souza et al. 2002, 2005a), Resende (Martins et al. 1978), Rio de Janeiro (Rangel et al. 1986), Silva Jardim (Souza et al. 2001), Vassouras (Martins et al. 1978).

L. misionensis (Castro, 1959)*: Casimiro de Abreu (Souza et al. 2001), Itatiaia (Afonso et al. 2007).

Five species were considered potential leishmaniases vectors in the state: L. (N.) intermedia, L. migonei, L. (N.) whitmani, L. (N.) flaviscutellata and L. (L.) longipalpis. Distribution maps of these species and leishmaniases human cases by municipality are presented separately for ACL (Fig. 1) and AVL (Fig. 2).

 

DISCUSSION

Published lists of sand fly species from Brazil commonly demonstrate species distribution by state, such as studies by Aguiar & Medeiros (2003), the online database of CIPA Group (1999) and the taxonomic key of Galati (2003). Species distributions from each state are commonly published separately, like those from Minas Gerais (Andrade & Dantas-Torres 2010), São Paulo (Shimabukuro et al. 2010), Pernambuco (Dantas-Torres et al. 2010), Mato Grosso (Missawa & Maciel 2007) and Rio Grande do Norte (Ximenes et al. 2000). The present work is the first to summarize the distribution of sand fly species from Rio de Janeiro State.

Several epidemiological studies and entomologic surveys confirmed L. (N.) intermedia as the predominant species in peridomestic environment in many municipalities of Rio de Janeiro State, such as Angra dos Reis (Souza et al. 2009; Carvalho et al. 2013), Bom Jardim (Souza et al. 2003a), Bom Jesus do Itabapoana (Rezende et al. 2009), Carmo (Alves 2007), Casimiro de Abreu (Souza et al. 2001), Magé (Nery-Guimarães 1955), Mangaratiba (Novo et al. 2013), Niterói (Brazil et al. 1989), Paraty (Aguiar et al. 1993; Carvalho et al. 1995, 2000; Costa et al. 2004; Moutinho et al. 2010), Rio Bonito (Brazil et al. 1989), Rio de Janeiro (Lima et al. 1981; Souza et al. 2000; Gouveia et al. 2012), Saquarema (Brazil et al. 2011) and Seropédica (Cardoso et al. 2009). In addition to these cited references, the findings of naturally infected females of L. (N.) intermedia by Leishmania (V.) braziliensis (Rangel et al. 1984; Pita-Pereira et al. 2005; Rocha et al. 2010) and experimental infection by the same parasite (Rangel et al. 1992) reinforce the hypothesis that this sand fly species is the main ACL vector of Rio de Janeiro State.

Lutzomyia migonei is considered secondary vector of Leishmania (V.) braziliensis in Rio de Janeiro State. This was first suggested by Araújo Filho et al. (1981), who noticed it as the second most abundant species inside houses where ACL human cases had been recorded in Ilha Grande (Angra dos Reis). In Jacarepaguá (Rio de Janeiro), L. migonei showed high abundance and preference to feed on dogs, suggesting it would be maintaining the canine ACL cycle in the area (Rangel et al. 1986). In Itaguaí, Aguiar et al. (1996) compared the sand fly fauna of different altitude levels (100 and 300 m) and noticed that L. migonei had higher abundances than L. (N.) intermedia at 300 m, suggesting a possible involvement in ACL transmission. Lutzomyia migonei is commonly found in high abundances next to L. (N.) intermedia, as it was also shown in Rio de Janeiro (Lima et al. 1981; Gouveia et al. 2012), Mesquita (Rangel et al. 1990; Meneses et al. 2002) and Paraty (Aguiar et al. 1993; Carvalho et al. 1995, 2000; Moutinho et al. 2010). In the state, this species was also captured naturally infected by Leishmania (V.) braziliensis (Pita-Pereira et al. 2005).

Besides L. (N.) intermedia and L. migonei, other sand fly species found in Rio de Janeiro State show evidences of participation on ACL transmission cycles, such as L. (N.) whitmani (Forattini 1953; Souza et al. 2002; Costa et al. 2007), L. (P.) fischeri (Coutinho & Barreto 1941; Lainson 1983; Souza et al. 2002) and L. (P.) pessoai (Forattini 1954; Silva & Grunewald 1999), all of them with observed anthropophily and adaptability to domestic environments (Rangel & Lainson 2009). From these cited species, the ones that were already found naturally infected by Leishmania (V.) braziliensis in southeastern and southern Brazil are only L. (N.) whitmani and L. (P.) fischeri (Pita-Pereira et al. 2005, 2011; Rocha et al. 2010).

Although L. (N.) whitmani has been suggested as the most important vector of ACL in Brazil, being widespread in the country (Costa et al. 2007; Rangel & Lainson 2009), it is not very abundant in Rio de Janeiro State. Its role in the state's ACL transmission was further discussed by Souza et al. (2002, 2005a, 2005b) during studies in Petrópolis. The authors suggested that the two most frequent species, L. (N.) intermedia and L. (N.) whitmani, would be sharing ACL transmission throughout several months of the year, since both showed high anthropophily. In addition, L. (N.) intermedia was more predominant during the hotter months (December, January and February), while L. (N.) whitmani was more frequent during colder months (June, July and August). The authors also noticed that L. (N.) whitmani was more frequent in captures inside the forest and near banana plantations, while L. (N.) intermedia predominated in peridomestic environments.

Lutzomyia (Nyssomyia) flaviscutellata is the main vector of Leishmania (L.) amazonensis, causative agent of Diffuse Cutaneous Leishmaniasis (DCL) (Lainson & Shaw 1968; Ward et al. 1977; Lainson et al. 1987; Rangel & Lainson 2009). In 2007, Rio de Janeiro State's first autochthonous DCL human case was detected in Paraty (Azeredo-Coutinho et al. 2007). Until today, there are no records of other human cases in the state, although in São Paulo State, dogs and rodents (Akodon sp.) were detected infected with Leishmania (L.) amazonensis (Tolezano et al. 1988, 2007). Lutzomyia (N.) flaviscutellata is widespread in Brazil, and frequently associated with primary and secondary forests of Amazon, Atlantic Forest and Cerrado biomes. It is strongly attracted to rodents, but not so much to humans (Shaw & Lainson 1968; Shaw et al. 1972; Rangel & Lainson 2009), explaining why captures with Disney traps (Disney 1966), using rodents as baits, are often more successful in capturing this species (Araújo Filho et al. 1981; Dorval et al. 2010). In Rio de Janeiro State, L. (N.) flaviscutellata was found only in Angra dos Reis (Araújo Filho et al. 1981; Carvalho et al. 2013), Nova Iguaçu (Martins et al. 1978) and Petrópolis (Martins et al. 1962a, 1978). Its real distribution and abundance is underestimated, probably because there is only one published study that used Disney traps to capture sand flies in the state (Araújo Filho et al. 1981). Even with its major occurrence on north and northeast Brazil, the species was also found in São Paulo State (Gomes & Galati 1989, Gomes 1994), in Atlantic Forest areas very similar to those in Rio de Janeiro State.

Lutzomyia (Lutzomyia) longipalpis is highly adaptable to man-modified environments, probably because it feeds on a wide variety of vertebrate hosts and is highly anthropophilic (Lainson & Rangel 2005; Afonso et al. 2012). The presence of this species in urban areas of Brazil is a determinant factor for AVL urbanization process (Rangel & Vilela 2008; Werneck 2008). In Rio de Janeiro State, this species have been recorded in low abundances on several studies, frequently in rural or periurban areas (Araújo Filho & Sherlock 1981; Araújo Filho et al. 1981; Rangel et al. 1986, 1990; Souza et al. 1981, 2001, 2002; Cabrera et al. 2003; Carvalho et al. 2013). Recently, L. (L.) longipalpis was detected in an urban area of Rio de Janeiro City (in the locality of Caju). This finding, coupled with the record of canine VL cases and one human AVL case, demonstrates the first AVL focus in an urban area of Rio de Janeiro City (Brazil 2013).

In some AVL areas of the state, L. (L.) longipalpis could not be found (Souza et al. 2000, 2009). In these areas, Souza et al. (2003b) hypothesized the possible epidemiologic importance of L. migonei in maintaining and expanding canine infection, based on its strong attraction to dogs. Lutzomyia migonei shows evidences of AVL transmission in Pernambuco State, where it was found naturally infected by Leishmania (L.) infantum chagasi in areas without records of L. (L.) longipalpis (Carvalho et al. 2010). Definitely more studies are necessary to test the hypothesis of this alternative AVL vector species in Rio de Janeiro State.

The records of L. (P.) paraensis and L. (M.) micropyga in Rio de Janeiro State should be interpreted with caution, since both are considered Amazonian species (Young & Duncan 1994).

The entomologic records from the Health Department of the State contributed with knowledge of the sand fly fauna from 22 municipalities. About 60% of these were not surveyed in scientific studies, such as São Fidélis. If this municipality had not been surveyed by the Health Department of the State, three sand fly species would not have been registered in Rio de Janeiro State: Lutzomyia (L.) ischyracantha, L. (L.) alencari and L. walkeri. This evidence reinforces the importance of collaboration between researchers and health department professionals, so that these data reach the scien-tific literature. Leishmaniases control actions are mainly based on entomologic surveillance, so it is fundamental that endemic areas be constantly surveyed.

This list shows records of 65 sand fly species from 46 municipalities. Since this corresponds to only 50% of the 92 municipalities of Rio de Janeiro State, some other species could certainly be found in other areas with future studies.

 

ACKNOWLEDGMENTS

To Patrícia Ganzenmüller Moza and Carlos Henrique Assis, from the Health Department of Rio de Janeiro State, for providing data on leishmaniases human cases. To José Dilermando Andrade Filho, from Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, for giving information about specimens deposited in Coleção de Referência Nacional e Internacional de Flebotomineos (CRNIF-CPqRR). To two anonymous reviewers, who made significant contributions to this manuscript. To Mariana Vale, from the Ecology Department of Federal University of Rio de Janeiro for English review. To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for funding.

 

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Received 16 July 2013;
Accepted 24 November 2013

 

 

Associate Editor: Maria Anice M. Sallum
* Corresponding author.

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