Sandfly fauna (Diptera: Psychodidae) in an urban area, Central-West of Brazil

Wagner de Souza Fernandes Leandro Machado Borges Aline Etelvina Casaril Everton Falcão de Oliveira Jucelei de Oliveira Moura Infran Eliane Mattos Piranda Elisa Teruya Oshiro Suellem Petilim Gomes Alessandra Gutierrez de Oliveira About the authors

ABSTRACT

Biological and ecological relations among vectors and their pathogens are important to understand the epidemiology of vector-borne diseases. Camapuã is an endemic area for visceral and tegumentary leishmaniasis. The aim of this study was to characterize the sandfly fauna present in Camapuã , MS, Brazil. Sand flies were collected every fortnight from May 2014 to April 2015 using automatic light traps in the domicile and peridomicile of twelve neighborhoods and forest. The collected specimens were identified based on morphology according to the valid identification keys. In total, 2005 sandflies of five genera and nine species were collected. Nyssomyia whitmani and Lutzomyia cruzi were the most abundant species. Males were more abundant, with a male-to-female ratio of 2.14. The highest diversity was observed in peripheral neighborhood, with abundant plant cover. The peridomicile presented greater abundance of sandflies, with the predominance of Ny. whitmani . No significant correlation between the absolute frequencies of the most abundant species and the precipitation variable was observed; however, there was a predominance of Lu. cruzi in the rainy season. We observed a high frequency of sandflies in urban area, especially vector species. The presence of Nyssomyia whitmani and Lutzomyia cruzi indicate the necessity for health surveillance in the municipality. Additional method of collection such as sticky trap is also recommended for appropriate faunestic study.

Camapuã; Nyssomyia whitmani; Lutzomyia cruzi; Leishmaniases

INTRODUCTION

Different sandfly species with wild habits have been adapted to urban areas, where they find suitable sites for their development 11. Barata RA, França-Silva JC, Mayrink W, Silva JC, Prata A, Lorosa ES, et al. Aspectos da ecologia e do comportamento de flebotomíneos em área endêmica de leishmaniose visceral, Minas Gerais. Rev Soc Bras Med Trop. 2005;38:421-5. . Vector-borne diseases are related to the environment and changes in the ecosystem, such as urbanization, with increased density of vector insects, favoring the emergence and reemergence of diseases like Leishmaniasis 22. Barcellos C, Monteiro AM, Corvalán C, Gurgel HC, Carvalho MS, Artaxo P, et al. Mudanças climáticas e ambientais e as doenças infecciosas: cenários e incertezas para o Brasil. Epidemiol Serv Saude. 2009;18:285-304.,33. Rangel EF, Vilela ML. Lutzomyia longipalpis (Diptera, Psychodidae, Phlebotominae) and urbanization of visceral leishmaniasis in Brazil. Cad Saude Publica. 2008;24:2948-52. .

The leishmaniasis is a group of parasitic diseases caused by protozoa of the Leishmania genus (Ross 1903) transmitted through infected sandflies, affecting wild (rodents, marsupials, edentulous) and domestic animals (dogs) as well as the man 44. Lainson R, Shaw JJ. New World Leishmaniasis. In: Cox FE, Wakelin D, Gillespie SH, Despommier DD, editors. Topley & Wilson’s Microbiology and microbial infections. 10th ed. London: Hodder Arnold; 2005. v.6, p.313-49. . The notification and increase on incidence of the leishmaniasis in non-endemic areas indicate the necessity to study local sandfly fauna in order to know the dominance, diversity and dispersion of the species and to identify probable vectors 55. Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Manual de vigilância e controle da leishmaniose visceral. Brasília: Ministério da Saúde; 2014. .

Between 2007 and 2015, Mato Grosso do Sul notified 1985 cases of VL and 1232 of TL, of which 12 and 11, respectively, were reported in Camapuã (MS). The municipality is classified as a sporadic leishmaniasis transmission area 66. Brasil. Ministério da Saúde. Sistema de Informação de Agravos de Notificação (SINAN). Leishmaniose tegumentar americana: casos confirmados e notificados no Sistema de Informação de Agravos de Notificação: Mato Grosso do Sul. [cited 2017 Jan 30]. Available from: http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sinannet/cnv/ltaMS.def
http://tabnet.datasus.gov.br/cgi/deftoht...
,77. Brasil. Ministério da Saúde. Sistema de Informação de Agravos de Notificação. Leishmaniose visceral: casos confirmados e notificados no Sistema de Informação de Agravos de Notificação: Mato Grosso do Sul. [cited 2017 Jan 30]. Available from: http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sinannet/cnv/leishvMS.def
http://tabnet.datasus.gov.br/cgi/deftoht...
. However, a few studies conducted in the region were conducted in rural areas mainly in caves, with description of Lu. cruzi88. Mangabeira Filho O. Sobre duas novas espécies de Flebótomus (Diptera: Psychodidae). Mem Inst Oswaldo Cruz. 1938;33:349-61. incriminated as vector of Leishmania ( L .) infantum99. Galati EA, Nunes VL, Rego Junior FA, Oshiro ET, Chang MR. Estudo de flebotomíneos (Diptera: Psychodidae) em foco de leishmaniose visceral no Estado de Mato Grosso do Sul, Brasil. Rev Saude Publica. 1997;31:378-90.,1010. Missawa NA, Veloso MA, Maciel GB, Michalsky EM, Dias ES. Evidência de transmissão de leishmaniose visceral por Lutzomyia cruzi no município de Jaciara, Estado de Mato Grosso, Brasil. Rev Soc Bras Med Trop. 2011;44:76-8. and Lu. dispar , a very anthropophilic considered as a potential vector of Leishmania sp. 1111. Williams P, Carvalho AL, Description of the female of Lutzomyia (Lutzomyia) dispar, with a redescription of the male (Diptera: Psychodidae: Phlebotominae). J Med Entomol. 1979;16:325-30. .

Considering the cases of leishmaniasis in the municipality and the absence of vector information in the area, the aims of this study were to identify the sandfly fauna in the city of Camapuã , Mato Grosso do Sul, Brazil, and to analyze the temporal distribution of species of medical importance and their presence in different ecotypes (intradomicile, peridomicile and forest).

METHODS

Study Area

The study was conducted in Camapuã (19º31’53’’S and 54º02’38’’W, 409 m above sea level), located in Mato Grosso do Sul, Center-West region of Brazil ( Figure 1 ). The municipality has a total area of 6229.615 km 22. Barcellos C, Monteiro AM, Corvalán C, Gurgel HC, Carvalho MS, Artaxo P, et al. Mudanças climáticas e ambientais e as doenças infecciosas: cenários e incertezas para o Brasil. Epidemiol Serv Saude. 2009;18:285-304. , the city is located 137 km from the State capital and the population is estimated in 13,712 inhabitants 1212. Instituto Brasileiro de Geografia e Estatística. Mato Grosso do Sul: Camapuã. [cited 2016 Aug 20]. Available from: http://cidades.ibge.gov.br/xtras/perfil.php?codmun=500260
http://cidades.ibge.gov.br/xtras/perfil....
,1313. Camapuã. Secretaria Municipal de Saúde. Plano Municipal de Saúde 2014-2017. Camapuã: Prefeitura de Camapuã; 2014. .

Figure 1
Geographical location of the study area: municipality of Camapuã , State of Mato Grosso do Sul, Brazil

The climate is classified according to Köppen as tropical (AW). The average temperature varies between 20 and 24 ºC and rainfall between 1,000 and 1,500 mm per year, with the dry season from April to September and the rainy season from October to March 1313. Camapuã. Secretaria Municipal de Saúde. Plano Municipal de Saúde 2014-2017. Camapuã: Prefeitura de Camapuã; 2014. .

The municipality is located in the cerrado biome, and has two phytophysiognomies: campo cerrado (formed by undergrowth, trees and shrubs with thick bark and height of 4 to 8 m) and cerradão (consisting of grasses, shrubs up to 3 m and trees with height from 10 to 15 m) 1414. Borgonovi M, Chiarini JV. Cobertura vegetal do Estado de São Paulo I – Levantamento por fotointerpretação das áreas cobertas com cerrado, cerradão e campo, em 1962. Bragantia. 1965;24:159-72.,1515. Mato Grosso do Sul. Secretaria de Meio Ambiente, do Planejamento, da Ciência e Tecnologia. Caderno geoambiental das regiões de planejamento do MS. Campo Grande: SEMAC; 2011 [cited 2016 Jun 04]. Available from: http://www.servicos.ms.gov.br/semade_download/Caderno%20Ambiental/Caderno_Geoambiental.pdf
http://www.servicos.ms.gov.br/semade_dow...
. However, due to the livestock activities, most of the area is covered by pastures 1616. Martins JS, Calderano SB, Zaroni MJ, Coutinho HL, Baca JF. Levantamento semidetalhado dos solos da microbacia dos Córregos Barroso e Barrozinho, no município de Camapuã, MS. Rio de Janeiro: Embrapa; 2002.,1717. Pereira NR, Chagas CS, Carvalho Junior W, Bhering SB. Solos do município de Camapuã - MS. In: XXXIV Congresso Brasileiro de Ciência do Solo; 2013 Jul 28 a Ago 02; Florianópolis, SC, Brasil. [cited 2016 Fev 02]. Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/88907/1/camapua.pdf
http://ainfo.cnptia.embrapa.br/digital/b...
.

The urban area of Camapuã is on soils derived from the fine-grained sandstones of Pirambóia formation, with presence of clay that allows the soils to be non-friable. In the nearest collection sites of floodplains, the soils are dark due to the presence of organic matter, which helps to support humidity. The main differences between the capture sites were in relation to the degree of shadowing/sunshine and the proximity to remnants of native vegetation and the river.

Sandfly collection

Sand flies were collected fortnightly from May 2014 to April 2015, using modified Falcão light traps. The collection sites were defined according to the report of human cases of leishmaniasis in nearby areas, presence of animal shelters (chicken coop, stable, kennel) and organic matter per domicile. The traps were installed between 06:00 p.m. and 06:00 a.m. in the peridomicile and intradomicile of twelve residences and a trap in the forest. Table 1 shows the characteristics of the environment of each residence.

Table 1
Characteristics of capture sites, Camapuã , MS, Brazil

The insects were cleaned and assembled according to Forattini 1818. Forattini OP. Entomologia médica. São Paulo: Edgar Blücher; 1973. v. 4: Psychodidae, phlebotominae, leishmanioses, bartoneloses. . In order to identify the species, the structures of the head, thorax and abdomen were used, with emphasis on the genitalia, following the classification proposed by Galati 1919. Galati EA. Morfologia e taxonomia: classificação de Phlebotominae. In: Rangel EF, Lainson R, organizadores. Flebotomíneos do Brasil. Rio de Janeiro: Fiocruz; 2003. p. 23-51. . The abbreviation of the genera followed Marcondes 2020. Marcondes CB. A proposal of generic and subgeneric abbreviations for phlebotomine sandflies (Diptera: Psychodidae: Phlebotominae) of the world. Entomol News. 2007;118:351-6. .

Data Analysis

Diversity of species was calculated using the Shannon-Weaver Diversity Index (H’) 2121. Service MW. Mosquito ecology: field sampling methods. 2nd ed. London: Elsevier; 1993. and the measure of dominance/evenness was calculated using the Pielou’s Index (J). The evaluation of the most abundant species according to their spatial distribution was performed using the Standardized Index of Species Abundance (SISA) 2222. Roberts DR, Hsi BP. An index of species abundance for use with mosquito surveillance data. Environ Entomol. 2014;8:1007-13. . The frequencies of these species were calculated by the Williams geometric mean 2323. Haddow AJ. Studies on the biting habits and medical importance of east African mosquitoes in the genus Aedes. 1 – Subgenera Aedimorphus, Banksinella and Dunnius. Bull Entomol Res. 1960;50:759-79. .

The Wilcoxon test was used for comparisons of the absolute frequencies of total sandflies and of the two most abundant species between the sex and climate seasons (dry and rainy). The association between the accumulated rainfall per month and the absolute frequencies of the most abundant species was evaluated by the Spearman’s correlation.

RESULTS

A total of 2,005 specimens was collected and identified among five genera and nine species: Brumptomyia avellari (Costa Lima, 1932) , Brumptomyia galindoi (Fairchild & Hertig, 1947), Evandromyia lenti (Mangabeira, 1938), Evandromyia sallesi (Galvão & Coutinho, 1940) , Evandromyia teratodes (Martins, Falcão & Silva, 1964) , Nyssomyia whitmani (Antunes & Coutinho, 1939) , Psathyromyia aragaoi (Costa Lima, 1932), Psathyromyia bigeniculata (Floch & Abonnenc, 1941) and Lutzomyia cruzi (Mangabeira, 1938) ( Table 2 ).

Table 2
Distribution of sandflies species by neighborhood, Shannon’s Index (H), Pielou’s Index (J) and Standardized Index of Species Abundance (SISA), in urban areas of Camapuã , MS, 2014 to 2015 (n=2,005)

Considering all the capture sites, the predominant species were Nyssomyia whitmani (55.3%) and Lutzomyia cruzi (41.3%). Both were also the most abundant species according to the Standardized Index of Species Abundance (SISA=1.00), present in all the capture sites ( Table 2 ). The males were more frequent (n=1367, 68.2%) than females (n=638, 31.8%), with a male-to-female ratio of 2.14 (W=164860, p=0.002). Lu. cruzi showed a higher number of males (4.24, W=170990, p<0.001).

In peridomicile, 1702 (84.9%) specimens were captured, followed by intradomicile with 282 (14.06%), and 21 (1.04%) in the forest. Nyssomyia whitmani was predominant in peridomicile and forest, while Lu. cruzi was the most frequent in intradomicile.

The highest Shannon’s Diversity Index was reported in Olídia neighborhood (H=0.82) where five species were collected. São Bento neighborhood showed a lower diversity (H=0.74), but presented the greatest dominance of species, with seven of the nine species collected in the city. The index was not calculated for Chácara Pérola , Pedro Luiz Amorim, Alto and Mata due to the low density of collected insects ( Table 2 ).

There was no significant correlation between rainfall and frequency of Lu. cruzi (r=0.224; p=0.485) and Ny. whitmani (r=-0.335; p=0.287). The Williams’ average and monthly precipitation (mm 3 ) are shown in Figure 2 . We observed a predominance of Lu. cruzi in the rainy season, but not of Ny. whitmani . Table 3 shows the absolute frequency of sandflies between dry and rainy season.

Figure 2
Monthly Williams’ average of the most frequent species according to SISA and rainfall (mm), in urban areas of Camapuã , MS, Brazil, 2014 to 2015

Table 3
Absolute frequency of total collected sandflies and most abundant species according to SISA and climatic seasons, in urban areas of Camapuã , MS, 2014 to 2015

DISCUSSION

In Mato Grosso do Sul (MS), a total of 66 species of phlebotomine was identified 99. Galati EA, Nunes VL, Rego Junior FA, Oshiro ET, Chang MR. Estudo de flebotomíneos (Diptera: Psychodidae) em foco de leishmaniose visceral no Estado de Mato Grosso do Sul, Brasil. Rev Saude Publica. 1997;31:378-90.,2424. Almeida PS, Nascimento JC, Ferreira AD, Minzão LD, Portes F, Miranda AM, et al. Espécies de flebotomíneos (Diptera, Psychodidae) coletadas em ambiente urbano em municípios com transmissão de Leishmaniose Visceral do Estado de Mato Grosso do Sul, Brasil. Rev Bras Entomol. 2010;54:304-10.

25. Almeida PS, Leite JA, Araújo AD, Batista PM, Touro RB, Araújo VS, et al. Fauna of phlebotomine sand flies (Diptera, Psychodidae) in areas with endemic American cutaneous leishmaniasis in the State of Mato Grosso do Sul, Brazil. Rev Bras Entomol. 2013;57:105-12.

26. Casaril AE, Monaco NZ, Oliveira EF, Eguchi GU, Paranhos Filho AC, Pereira LE, et al. Spatiotemporal analysis of sandfly fauna (Diptera: Psychodidae) in an endemic area of visceral leishmaniasis at Pantanal, central South America. Parasit Vectors. 2014;7:364.

27. Galati EA, Nunes VL, Dorval ME, Oshiro ET, Cristaldo G, Espíndola MA, et al. Estudo dos flebotomíneos (Diptera, Pychodidae), em área de leishmaniose tegumentar, no Estado de Mato Grosso do Sul, Brasil. Rev Saude Publica. 1996;30:115-28.

28. Galati EA, Nunes VL, Boggiani PC, Dorval ME, Cristaldo G, Rocha HC, et al. Phlebotomines (Diptera, Psychodidae) in caves of the Serra da Bodoquena, Mato Grosso do Sul State, Brazil. Rev Bras Entomol. 2003;47:283-96.

29. Galati EA, Nunes VL, Boggiani PC, Dorval ME, Cristaldo G, Rocha HC, et al. Phlebotomines (Diptera: Psychodidae) in forested areas of the Serra da Bodoquena, state of Mato Grosso do Sul, Brazil. Mem Inst Oswaldo Cruz. 2006;101:175-93.
-3030. Infran JO, Souza DA, Fernandes WS, Casaril AE, Eguchi GU, Oshiro ET, et al. Nycthemeral rhythm of Phlebotominae (Diptera: Psychodidae) in a craggy region, transitioning between the Wetland and the Plateau, Brazil. J Med Entomol. In Press 2016. . The species recorded in Camapuã were already reported in MS and the composition is similar to that of other urban areas in the State 2424. Almeida PS, Nascimento JC, Ferreira AD, Minzão LD, Portes F, Miranda AM, et al. Espécies de flebotomíneos (Diptera, Psychodidae) coletadas em ambiente urbano em municípios com transmissão de Leishmaniose Visceral do Estado de Mato Grosso do Sul, Brasil. Rev Bras Entomol. 2010;54:304-10.,2626. Casaril AE, Monaco NZ, Oliveira EF, Eguchi GU, Paranhos Filho AC, Pereira LE, et al. Spatiotemporal analysis of sandfly fauna (Diptera: Psychodidae) in an endemic area of visceral leishmaniasis at Pantanal, central South America. Parasit Vectors. 2014;7:364.,2828. Galati EA, Nunes VL, Boggiani PC, Dorval ME, Cristaldo G, Rocha HC, et al. Phlebotomines (Diptera, Psychodidae) in caves of the Serra da Bodoquena, Mato Grosso do Sul State, Brazil. Rev Bras Entomol. 2003;47:283-96. .

The most frequent species were Ny. whitmani and Lu. cruzi , important in the epidemiology of leishmaniasis. Ny. whitmani has been implicated in the transmission of Leishmania sp. in Northeastern, Southeastern, Central-West, Southern and recently in South of Brazil 3131. Fonteles RS, Pereira Filho AA, Moraes JL, Kuppinger O, Rebêlo JM. Experimental infection of Lutzomyia (Nyssomyia) whitmani (Diptera: Psychodidae: Phlebotominae) with Leishmania (Viannia) braziliensis and Leishmania (L.) amazonensis, etiological agents of American Tugumentary Leishmaniasis. J Med Entomol. 2015;53:206-9.,3434. Costa SM, Cechinel M, Bandeira, V, Zannuncio JC, Lainson R, Rangel EF. Lutzomyia (Nyssomyia) whitmani s.l. (Antunes & Coutinho, 1939) (Diptera: Psychodidae: Phlebotominae): geographical distribution and the epidemiology of American cutaneous leishmaniasis in Brazil – mini-review. Mem Inst Oswaldo Cruz. 2007;102:149-53. , while Lu. cruzi has been incriminated in the transmission of L. ( L. ) infantum in the Central-West of Brazil 99. Galati EA, Nunes VL, Rego Junior FA, Oshiro ET, Chang MR. Estudo de flebotomíneos (Diptera: Psychodidae) em foco de leishmaniose visceral no Estado de Mato Grosso do Sul, Brasil. Rev Saude Publica. 1997;31:378-90.,1010. Missawa NA, Veloso MA, Maciel GB, Michalsky EM, Dias ES. Evidência de transmissão de leishmaniose visceral por Lutzomyia cruzi no município de Jaciara, Estado de Mato Grosso, Brasil. Rev Soc Bras Med Trop. 2011;44:76-8. . Ny. whitmani was collected in all the capture sites. The species shows different behavior in Brazil and is suspected to be a cryptic species complex with wild populations and some adapted populations to ecological changes and involved in the epidemiological chain of TL 3232. Rangel EF, Lainson R, Souza AA, Ready P, Azevedo AC. Variation between geographical populations of Lutzomyia (Nyssomyia) whitmani (Antunes & Coutinho, 1939) sensu lato (Diptera:Psychodidae:Phlebotominae) in Brazil. Mem Inst Oswaldo Cruz. 1996;91:43-50.

33. Brazil RP, Rodrigues AA, Andrade-Filho JD. Sand fly vectors of Leishmania in the Americas - a mini review. Entomol Ornithol Herpetol. 2015;4:144.

34. Costa SM, Cechinel M, Bandeira, V, Zannuncio JC, Lainson R, Rangel EF. Lutzomyia (Nyssomyia) whitmani s.l. (Antunes & Coutinho, 1939) (Diptera: Psychodidae: Phlebotominae): geographical distribution and the epidemiology of American cutaneous leishmaniasis in Brazil – mini-review. Mem Inst Oswaldo Cruz. 2007;102:149-53.
-3535. Rangel EF, Lainson R. Proven and putative vectors of American cutaneous leishmaniasis in Brazil: aspects of their biology and vectorial competence. Mem Inst Oswaldo Cruz. 2009;104:937-54. . It is probable that the species is involved in the transmission of Leishmania sp. in the studied area, considering the involvement in other regions 3434. Costa SM, Cechinel M, Bandeira, V, Zannuncio JC, Lainson R, Rangel EF. Lutzomyia (Nyssomyia) whitmani s.l. (Antunes & Coutinho, 1939) (Diptera: Psychodidae: Phlebotominae): geographical distribution and the epidemiology of American cutaneous leishmaniasis in Brazil – mini-review. Mem Inst Oswaldo Cruz. 2007;102:149-53. , infection capacity 3131. Fonteles RS, Pereira Filho AA, Moraes JL, Kuppinger O, Rebêlo JM. Experimental infection of Lutzomyia (Nyssomyia) whitmani (Diptera: Psychodidae: Phlebotominae) with Leishmania (Viannia) braziliensis and Leishmania (L.) amazonensis, etiological agents of American Tugumentary Leishmaniasis. J Med Entomol. 2015;53:206-9. , density, distribution and notification of cases in the municipality.

Although Ny. whitmani shows adaptation to anthropic environments, the species is still found in forest areas 3535. Rangel EF, Lainson R. Proven and putative vectors of American cutaneous leishmaniasis in Brazil: aspects of their biology and vectorial competence. Mem Inst Oswaldo Cruz. 2009;104:937-54. . In Camapuã, the species was more frequent in residences with abundant vegetation, mainly in peripheral neighborhoods. These sites offer ideal conditions for the development of sandflies 3636. Muniz LH, Rossi RM, Neitzke HC, Monteiro WM, Teodoro U. Estudo dos hábitos alimentares de flebotomíneos em área rural no sul do Brasil. Rev Saude Publica. 2006;40:1087-93. .

The second most frequent species was Lu. cruzi . Its importance was already reported in Corumbá (MS) 99. Galati EA, Nunes VL, Rego Junior FA, Oshiro ET, Chang MR. Estudo de flebotomíneos (Diptera: Psychodidae) em foco de leishmaniose visceral no Estado de Mato Grosso do Sul, Brasil. Rev Saude Publica. 1997;31:378-90. and Jaciara, Mato Grosso (MT) 1010. Missawa NA, Veloso MA, Maciel GB, Michalsky EM, Dias ES. Evidência de transmissão de leishmaniose visceral por Lutzomyia cruzi no município de Jaciara, Estado de Mato Grosso, Brasil. Rev Soc Bras Med Trop. 2011;44:76-8. , where the species was found naturally infected by Leishmania3737. Brito VN, Almeida AB, Nakazato L, Duarte R, Souza CO, Sousa VR. Phlebotomine fauna, natural infection rate and feeding habits of Lutzomyia cruzi in Jaciara, state of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz. 2014;109:899-904.

38. Pita-Pereira D, Cardoso MA, Alves CR, Brazil RP, Britto C. Detection of natural infection in Lutzomyia cruzi and Lutzomyia forattinii (Diptera: Psychodidae: Phlebotominae) by Leishmania infantum chagasi in na endemic area of visceral leishmaniasis in Brazil using a PCR multiplex assay. Acta Trop. 2008;107:66-9.
-3939. Santos SO, Arias J, Ribeiro AA, Hoffmann MP, Freitas RA, Malacco MA. Incrimination of Lutzomyia cruzi as a vector of American visceral leishmaniasis. Med Vet Entomol. 1998;12:315-7. , reinforcing its role as the vector of this agent. Lu. cruzi was described and redescribed from insects captured in Camapuã88. Mangabeira Filho O. Sobre duas novas espécies de Flebótomus (Diptera: Psychodidae). Mem Inst Oswaldo Cruz. 1938;33:349-61.,4040. Martins AV, Falcão AL, Silva JE, Dias ES. Nota sobre Lutzomyia (Lutzomyia) cruzi (Mangabeira, 1938), com a descrição da fêmea (Diptera, Psychodidae, Phlebotominae). Mem Inst Oswaldo Cruz. 1984;79:439-42. . It is commonly found in areas of savannah and wetland 4141. Missawa NA, Lima GB. Distribuição espacial de Lutzomyia longipalpis (Lutz & Neiva, 1912) e Lutzomyia cruzi (Mangabeira, 1938) no Estado de Mato Grosso. Rev Soc Bras Med Trop. 2006;39:337-40. , and already identified in six other municipalities of MS 99. Galati EA, Nunes VL, Rego Junior FA, Oshiro ET, Chang MR. Estudo de flebotomíneos (Diptera: Psychodidae) em foco de leishmaniose visceral no Estado de Mato Grosso do Sul, Brasil. Rev Saude Publica. 1997;31:378-90.,2424. Almeida PS, Nascimento JC, Ferreira AD, Minzão LD, Portes F, Miranda AM, et al. Espécies de flebotomíneos (Diptera, Psychodidae) coletadas em ambiente urbano em municípios com transmissão de Leishmaniose Visceral do Estado de Mato Grosso do Sul, Brasil. Rev Bras Entomol. 2010;54:304-10.,2626. Casaril AE, Monaco NZ, Oliveira EF, Eguchi GU, Paranhos Filho AC, Pereira LE, et al. Spatiotemporal analysis of sandfly fauna (Diptera: Psychodidae) in an endemic area of visceral leishmaniasis at Pantanal, central South America. Parasit Vectors. 2014;7:364.,4242. Oliveira AG, Andrade Filho JD, Falcão AL, Brazil RP. Estudo de flebotomineos (Diptera, Psychodidae, Phlebotominae) na zona urbana da cidade de Campo Grande, Mato Grosso do Sul, Brasil, 1999-2000. Cad Saude Publica. 2003;19:933-44. .

The species was collected in all the capture sites, mainly in central areas, demonstrating its predilection for anthropic environments, as noted in Corumbá (MS) 99. Galati EA, Nunes VL, Rego Junior FA, Oshiro ET, Chang MR. Estudo de flebotomíneos (Diptera: Psychodidae) em foco de leishmaniose visceral no Estado de Mato Grosso do Sul, Brasil. Rev Saude Publica. 1997;31:378-90.,2626. Casaril AE, Monaco NZ, Oliveira EF, Eguchi GU, Paranhos Filho AC, Pereira LE, et al. Spatiotemporal analysis of sandfly fauna (Diptera: Psychodidae) in an endemic area of visceral leishmaniasis at Pantanal, central South America. Parasit Vectors. 2014;7:364. and Jaciara (MT) 1010. Missawa NA, Veloso MA, Maciel GB, Michalsky EM, Dias ES. Evidência de transmissão de leishmaniose visceral por Lutzomyia cruzi no município de Jaciara, Estado de Mato Grosso, Brasil. Rev Soc Bras Med Trop. 2011;44:76-8.,3737. Brito VN, Almeida AB, Nakazato L, Duarte R, Souza CO, Sousa VR. Phlebotomine fauna, natural infection rate and feeding habits of Lutzomyia cruzi in Jaciara, state of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz. 2014;109:899-904. . Lu. cruzi shows similar behavior to Lu. longipalpis in relation to habitat, occupying urbanized areas 4343. Oliveira AG, Marassá AM, Consales CA, Dorval ME, Fernandes CE, Oliveira GR, et al. Observations on the feeding habits of Lutzomyia longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) in Campo Grande, an endemic area of visceral leishmaniasis in Mato Grosso do Sul, Brazil. Acta Trop. 2008;107:238-41.

44. Oliveira GM, Figueiró Filho EA, Andrade GM, Araújo LA, Oliveira ML, Cunha RV. Flebotomíneos (Diptera: Psychodidae: Phlebotominae) no município de Três Lagoas, área de transmissão intensa de leishmaniose visceral, Estado de Mato Grosso do Sul, Brasil. Rev Pan-Amaz Saude. 2010;1:83-94.
-4545. Vilela ML, Azevedo CG, Carvalho BM, Rangel EF. Phlebotomine fauna (Diptera: Psychodidae) and putative vectors of leishmaniases in impacted area by hydroelectric plant, State of Tocantins, Brazil. PLoS One. 2011;6:e27721. , especially with presence of abundant vegetation 4646. Fernández MS, Salomón OD, Cavia R, Perez AA, Guccione JD. Lutzomyia longipalpis spatial distribution and association with environmental variables in an urban focus of visceral leishmaniasis, Misiones, Argentina. Acta Trop. 2010;114:81-7.,4747. Santini MS, Utgés ME, Berrozpe P, Acosta MM, Casas N, Heuer P, Salomón OD. Lutzomyia longipalpis presence and abundance distribution at different micro-spatial scales in an urban scenario. PLoS Negl Trop Dis. 2015;9:e0003951. .

When comparing the number of specimens in the different ecotypes, peridomicile was the site with the highest density of sandflies, probably due to environmental ruralization, with abundance of organic matter and presence of animals such as chickens, pigs and dogs. In these places, the specimens find food and microhabitat for the development of their immature forms, increasing the quantity of these Diptera around the residence, which is considered a risk factor for the occurrence of leishmaniasis 4848. Sanguinette CC, Silva DF, Stumpp RG, Rego FD, Tonelli GB, Tanure A, et al. Comparison of the phlebotomine (Diptera: Psychodidae) fauna of urban, transitional, and wild areas in northern Minas Gerais, Brazil. Parasit Vectors. 2015;8:428. . In Camapuã , chicken coop was present in all residences, with the exception of Pedro Luiz Amorim neighborhood, which may explain the low density of insects in this capture site.

Even if these insects did not develop in the peridomicile, they could reach it easily by forest areas nearby, attracted by the light trap and available food source 11. Barata RA, França-Silva JC, Mayrink W, Silva JC, Prata A, Lorosa ES, et al. Aspectos da ecologia e do comportamento de flebotomíneos em área endêmica de leishmaniose visceral, Minas Gerais. Rev Soc Bras Med Trop. 2005;38:421-5. . The alternation habit between the forest and the anthropic environment favors the circulation of the parasite, since sandflies can feed on infected wild animals inside the forest and transmit the etiological agent to domestic animals present in the peridomicile, changing the classical pattern of TL transmission 4949. Carvalho MS, Bredt A, Meneghin ER, Oliveira C. Flebotomíneos (Diptera: Psychodidae) em áreas de ocorrência de leishmaniose tegumentar americana no Distrito Federal, Brasil, 2006 a 2008. Epidemiol Serv Saude. 2010;19:227-37. .

In the intradomicile, the most abundant species was Lu. cruzi . Inside the residences with the highest number of collected insects were, in addition to the residents, there were dogs. This species is eclectic with regard to food habits 5050. Chagas AC, Medeiros JF, Justiniano SC, Pessoa FA. Haematophagic behavior in laboratory of Lutzomyia cruzi (Mangabeira) (Diptera: Psychodidae) in relation to three mammalian blood sources in Manaus, Brazil. Acta Amaz. 2007;37:127-32. , which may have favored their collection inside the residences.

The greatest species dominance was found in São Bento neighborhood (n=7), however the Shannon’s Index was lower than the Olídia neighborhood with five different species collected. This is because the Shannon’s Index (H) also considers the species dominance, abundance and balance between them 5151. Hubálek Z. Measures of species diversity in ecology: an evaluation. Folia Zool. 2000;49:241-60. . The sites with the greatest species diversity were neighborhoods located in the periphery with favorable habitat for the presence of insects, like shading and abundance of organic matter.

Males were more abundant than females. The greater capture of this sex may have been favored by the collection methodology used, since the males are more attracted to the light of the trap 5252. Aguiar GM, Vilela ML, Schuback PA, Soucasaux T, Azevedo AC. Aspectos da ecologia dos flebótomos do Parque Nacional da Serra dos Órgãos, Rio de Janeiro. IV. Frequência mensal em armadilhas luminosas (Diptera: Psychodidae: Phlebotominae). Mem Inst Oswaldo Cruz. 1985;80:465-82. and are actively seeking hosts to attract females and increase the chances of copulation 5353. Dias ES, França-Silva JC, Silva JC, Monteiro EM, Paula KM, Gonçalves CM, et al. Flebotomíneos (Diptera: Psychodidae) de um foco de leishmaniose tegumentar no Estado de Minas Gerais. Rev Soc Bras Med Trop. 2007;40:49-52. . Considering that traps were installed near potential breeding sites and the fact that males hatch before females, these may also have facilitated male collection. Besides that, after blood feeding, females seek for safe shelters for digestion and maturation of ovarian follicles, which decreases their chance of being captured 11. Barata RA, França-Silva JC, Mayrink W, Silva JC, Prata A, Lorosa ES, et al. Aspectos da ecologia e do comportamento de flebotomíneos em área endêmica de leishmaniose visceral, Minas Gerais. Rev Soc Bras Med Trop. 2005;38:421-5.,2626. Casaril AE, Monaco NZ, Oliveira EF, Eguchi GU, Paranhos Filho AC, Pereira LE, et al. Spatiotemporal analysis of sandfly fauna (Diptera: Psychodidae) in an endemic area of visceral leishmaniasis at Pantanal, central South America. Parasit Vectors. 2014;7:364.,4242. Oliveira AG, Andrade Filho JD, Falcão AL, Brazil RP. Estudo de flebotomineos (Diptera, Psychodidae, Phlebotominae) na zona urbana da cidade de Campo Grande, Mato Grosso do Sul, Brasil, 1999-2000. Cad Saude Publica. 2003;19:933-44.,5252. Aguiar GM, Vilela ML, Schuback PA, Soucasaux T, Azevedo AC. Aspectos da ecologia dos flebótomos do Parque Nacional da Serra dos Órgãos, Rio de Janeiro. IV. Frequência mensal em armadilhas luminosas (Diptera: Psychodidae: Phlebotominae). Mem Inst Oswaldo Cruz. 1985;80:465-82.,5353. Dias ES, França-Silva JC, Silva JC, Monteiro EM, Paula KM, Gonçalves CM, et al. Flebotomíneos (Diptera: Psychodidae) de um foco de leishmaniose tegumentar no Estado de Minas Gerais. Rev Soc Bras Med Trop. 2007;40:49-52. .

Regarding the male-to-female ratio for Lu. cruzi , it was observed that the species presented higher male number in relation to the total specimens. Lu. cruzi is a sibling species of Lu longipalpis , and lekking has been documented for these species. During lekking, males release sex pheromones to attract females to mate, also attracting more males. This phenomenon also seems to occur among Lu. cruzi , once the pheromone 9-methyl-germacrene-B of insects from Corumbá (MS) was isolated 5454. Brazil RP, Hamilton JG. Isolation and identification of 9-methylgermacrene-B as the putative sex pheromone of Lutzomyia cruzi (Mangabeira, 1938) (Diptera: Psychodidae). Mem Inst Oswaldo Cruz. 2002;97:435-6. . In this municipality, Casaril et al . 2626. Casaril AE, Monaco NZ, Oliveira EF, Eguchi GU, Paranhos Filho AC, Pereira LE, et al. Spatiotemporal analysis of sandfly fauna (Diptera: Psychodidae) in an endemic area of visceral leishmaniasis at Pantanal, central South America. Parasit Vectors. 2014;7:364. have also captured more males of Lu cruzi .

Regarding the periodicity, the dry and rainy seasons in MS are well defined. A predominance of Lu. cruzi was observed in the rainy season, presenting peaks in October, January and April, similar to the previously reported trimodal behavior 99. Galati EA, Nunes VL, Rego Junior FA, Oshiro ET, Chang MR. Estudo de flebotomíneos (Diptera: Psychodidae) em foco de leishmaniose visceral no Estado de Mato Grosso do Sul, Brasil. Rev Saude Publica. 1997;31:378-90.,2626. Casaril AE, Monaco NZ, Oliveira EF, Eguchi GU, Paranhos Filho AC, Pereira LE, et al. Spatiotemporal analysis of sandfly fauna (Diptera: Psychodidae) in an endemic area of visceral leishmaniasis at Pantanal, central South America. Parasit Vectors. 2014;7:364. .

Nyssomyia whitmani showed no difference between the dry and rainy periods, and, for the precipitation, a negative but not significant correlation was observed between the species and the variable. The species shows great plasticity in relation to climatic changes and, although it is more frequent in the months of June, July and August 3434. Costa SM, Cechinel M, Bandeira, V, Zannuncio JC, Lainson R, Rangel EF. Lutzomyia (Nyssomyia) whitmani s.l. (Antunes & Coutinho, 1939) (Diptera: Psychodidae: Phlebotominae): geographical distribution and the epidemiology of American cutaneous leishmaniasis in Brazil – mini-review. Mem Inst Oswaldo Cruz. 2007;102:149-53. , in this study, the species was more captured in August, September and October.

In relation to other species found in the city of Camapuã , we have Ev. lenti which was originally considered refractory to Leishmania infection 5555. Brazil RP, Carneiro VL, Andrade Filho JD, Alves JC, Falcão AL. Biology of Lutzomyia lenti (Mangabeira) (Diptera:Psychodidae). An Soc Entomol Bras. 1997;26:191-3. , but has already been found naturally infected by L . ( V .) braziliensis5656. Paiva BR, Oliveira AG, Dorval ME, Galati EA, Malafronte RS. Species-specific identification of Leishmania in naturally infected sand flies captured in Mato Grosso do Sul State, Brazil. Acta Trop. 2010;115:126-30 . Pa. bigeniculata , species belonging to Shannon’s complex was found infected by flagellates in Bonito (MS) 5757. Brilhante AF, Dorval ME, Galati EA, Rocha HC, Cristaldo G, Nunes VL. Phlebotomine fauna (Diptera: Psychodidae) in an area of fishing tourism in Central-Western Brazil. Rev Inst Med Trop São Paulo. 2015;57:233-8. . Ev. sallesi was captured in the intradomicile and, although it is not anthropophilic, it is important to note that the species was found naturally infected by L . ( L .) infantum5858. Saraiva L, Carvalho GM, Gontijo CM, Quaresma PF, Lima AC, Falcão AL, et al. Natural infection of Lutzomyia neivai and Lutzomyia sallesi (Diptera: Psychodidae) by Leishmania infantum chagasi in Brazil. J Med Entomol. 2009;46:1159-63. and may contribute to the circulation of parasites in the environment.

Br. avellari, Br. galindoi, Ev. teratodes and Pa. aragaoi are found mainly in armadillo holes (Dasypodidae) and prefer wild environments 4242. Oliveira AG, Andrade Filho JD, Falcão AL, Brazil RP. Estudo de flebotomineos (Diptera, Psychodidae, Phlebotominae) na zona urbana da cidade de Campo Grande, Mato Grosso do Sul, Brasil, 1999-2000. Cad Saude Publica. 2003;19:933-44.,5959. Aguiar GM, Medeiros WM. Distribuição regional e habitats das espécies de flebotomíneos do Brasil. In: Rangel EF, Lainson R, organizadores. Flebotomíneos do Brasil. Rio de Janeiro: Fiocruz; 2003. p. 207-55. . These species together accounted for just over 3% of the total captured specimens and may have been attracted to light from residences and the trap.

It is noteworthy that Lu. longipalpis , the main vector of L. ( L .) infantum , was not collected during the study period, although there is indicative of their occurrence in the area based on geographic distribution models 6060. Almeida PS, Andrade AJ, Sciamarelli A, Raizer J, Menegatti JA, Hermes SC. Geographic distribution of phlebotomine sandfly species (Diptera: Psychodidae) in Central-West Brazil. Mem Inst Oswaldo Cruz. 2015;110:551-9. . Another species that has been previously reported in the municipality 1111. Williams P, Carvalho AL, Description of the female of Lutzomyia (Lutzomyia) dispar, with a redescription of the male (Diptera: Psychodidae: Phlebotominae). J Med Entomol. 1979;16:325-30. , Lu. dispar , was not captured in this study, probably because previous studies were conducted in the forest area and near the caves. Besides that, this species is highly anthropophilic and the appropriate trap was not used.

This study contributes to the knowledge of the sandfly fauna in Camapuã and State of MS. The presence of Lu. cruzi and Ny. whitmani reinforces the necessity for regular health education programs, associated with human and canine community surveys. These measures aim to prevent those cases of leishmaniasis occurring in Camapuã, since the increased incidence of these diseases has been observed in the municipality since 2007.

ACKNOWLEDGMENTS

We are grateful to the Health Surveillance of the Municipal Health Office of Camapuã , especially Leandro Machado Borges and Diego Hercules for the technical support on field activities, to the residents for their attention and to the staff of the Laboratory of Parasitology (Carla Cardozo Pinto de Arruda and Livia Garcia Bertollacci) for their collaboration.

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Publication Dates

  • Publication in this collection
    2017

History

  • Received
    12 Dec 2016
  • Accepted
    22 Feb 2017
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