New record and update on the geographical distribution of Pintomyia monticola ( Costa Lima , 1932 ) ( Diptera : Psychodidae ) in South America

The phlebotomine sand fly Pintomyia monticola (Costa Lima, 1932) is recorded for the first time in Brasília, central-west Brazil. A review of the geographical distribution of the species in South America is presented, and its distribution is extended. The potential geographical distribution of P. monticola is predicted based on ecological niche modeling. Ecological aspects of this species are discussed.

Ecological niche models were produced using Maxent version 3.2.1 (Phillips et al. 2006).We used a random seed to generate 10 replicate analyses based on bootstrap subsampling.We used median output grids as a hypothesis of suitability, and imported the results into ArcView 3.3 for assessment and analysis.Distributional data were separated into two sets: one for model calibration (75% of points) and one for model evaluation (25% of points).We assessed model accuracy by examining omission rate associated with test points (Anderson et al. 2002) and also used Maxent's jackknife test to identify variables that most influenced model predictions (Phillips et al. 2006).
We obtained 144 records for P. monticola and its updated geographical distribution map presents the bona fide records in South America and the new record (seven females) reported in the present study (Figure 1).All test points were included in the predicted suitable area (0% omission).Highest climate suitability for has been reported in Mato Grosso do Sul (Galati et al. 1996).Furthermore, DNA of Leishmania braziliensis was detected in P. monticola in Minas Gerais (Margonari et al. 2010).
The present study reports the presence of P. monticola in Brasília, central-west Brazil, and discusses the finding of this species in Peru in Pará state.It also updates the distribution of P. monticola and presents a potential geographical distribution model for this species.
In November 2013, sand fly specimens were captured in a gallery forest (15°57′41″ S, 047°56′38″ W) in the Fazenda Água Limpa (FAL) of the University of Brasília, located in a protected area (Área de Proteção Ambiental [APA] Gama e Cabeça de Veado).Two Shannon traps were set up for three hours and specimens were captured using a Castro aspirator.Sand flies were cleared (Forattini 1973), mounted and identified (Galati 2003b).
To characterize climate variation across the distribution of P. monticola, we used eight climatic variables: annual mean temperature, diurnal temperature range, temperature seasonality, maximum temperature in the warmest month, minimum temperature in the coldest month, annual precipitation, and precipitation in the wettest and driest months.We obtained these variables from the WorldClim project (Hijmans et al. 2005).All environmental databases used in this study covered areas of South America, resampled to a spatial resolution of 2.5′ (~5 km) (Almeida et al. 2013).Andrade and Gurgel-Gonçalves | Distribution of Pintomyia monticola in South America P. monticola was observed along the Brazilian Atlantic coast in the Atlantic Forest (Figure 1).Annual mean temperature, temperature seasonality, and minimum temperature in the coldest month were the variables that most influenced models of P. monticola.
Our study updates the occurrence map of P. monticola in South America and predicts a wide potential geographical distribution that possibly includes other Brazilian states, such as Alagoas, Sergipe, Paraíba, Pernambuco and Mato Grosso where the species have not yet been recorded.The same was observed in relation to Bolivia.The species is also probably present in the southern region of Peru.The sand fly fauna is well known in Pernambuco and Mato Grosso (Dantas-Torres et al. 2010; Missawa and Maciel, 2007).The Pintomyia species that occurs in Pernambuco is Pintomyia fisheri (Costa Lima, 1932) and three have been recorded in Mato Grosso, but no species of the monticola series.The absence of P. monticola in these climatically suitable areas could represent situations where the species has not yet dispersed or where the species has not become established due to competition with species previously present in that area.In addition, it is possible that human action, such as deforestation, could hinder the maintenance of P. monticola in forest remnants.Future studies using different trapping methods, with higher capture efforts, in the Atlantic Forest and Cerrado areas in these states should confirm the predictions presented herein.
In the state of São Paulo, P. monticola was the most frequent and abundant species in the Atlantic Forest and Cerrado biomes (Cutolo and Von Zuben 2008;Galati et al. 2010;Cutolo et al. 2013).In the 'Parque Estadual Intervales' (São Paulo), P. monticola was found inside and near caves.Moreover, one specimen was infected with unidentified microfilariae (Galati et al. 2010).A previous study found P. monticola females naturally infected by flagellates in a cutaneous leishamaniasis focus (Galati et al. 1996).Aspirations in armadillo burrows detected P. monticola females with Brumptomyia species indicating this ecotope as a possible breeding site (Forattini 1973;Galati et al. 2010).
Evidence indicates that P. monticola is attracted to humans, as demonstrated in the states of São Paulo (Galati et al. 2010), Minas Gerais (Hermeto et al. 1994), Rio de Janeiro (Afonso et al. 2007), and Rio Grande do Sul (Dias et al. 1997).In Espírito Santo, P. monticola was found in a hen house (Pinto et al. 2012).In Minas Gerais, P. monticola was found near caves, and in remnants of a deforested area (Carvalho et al. 2013).In Bahia, this species occurred in areas deforested for cocoa plantations and pasture (Dias-Lima et al. 2003).The presence of P. monticola in urban areas was recorded in the states of São Paulo (Colla-Jacques et al. 2010), Mato Grosso do Sul and in Pedro Juan Caballero, Paraguay (Andrade et al. 2012).
In Rio Grande do Sul, P. monticola was captured in the Atlantic Forest by different methods such as Chaniots and Damasceno traps and by using mouth aspirators (Dias et al. 1997).Alternative collection methods, such as the Malaise trap, can be used to collect this species and apparently is the only method that permits the capture of more males than females (Andrade Filho et al. 2008).
Pintomyia monticola has been recorded from 60−1,200 m above sea level (a.s.l.) (Galati et al. 2010;Colla-Jacques et al. 2010;Carvalho et al. 2013;Nascimento et al. 2013), with temperatures between 16°C−23.5°C(Sherlock and Santos, 1964;Dias-Lima et al. 2003;Teodoro et al. 1999Teodoro et al. , 2010;;Dias-Sversutti et al. 2007;Galati et al. 2010;Andrade et al. 2012) and precipitation ranging from 1,100-1,700 mm (Teodoro et al. 1999(Teodoro et al. , 2010;;Dias-Sversutti et al. 2007).The record of P. monticola in Peru was published in two checklists.In the first, the species was reported in Calca province, Cusco department (Cáceres et al. 2000) and, in the second, no locality record was provided (Cáceres and Galati 2001).Although Calca has average temperatures close to those recorded in Brazil (15−20°C), the altitude is much higher (2,928 m a.s.l.) and average rainfall is lower (600−880 mm) than areas where P. monticola is recorded.Pintomyia monticola has been recorded in the Atlantic Forest and Cerrado biomes of Brazil, as well as in Argentina and Paraguay.However, no suitable area passing through Bolivia and reaching Peru was observed in the predictive distribution model (Figure 1).Nonetheless, future studies are necessary to confirm the presence of the species in these countries.
The record of P. monticola in Pará is doubtful.Ryan (1986) recorded the species along km 12 of the Trans-Amazonian Highway between Marabá and Itaituba municipalities.The specimens were deposited in the 'Coleção de Flebotomíneos do Instituto Evandro Chagas' (COLFlebIEC) and the vouchers also include two males mounted in Berlese medium from Serra dos Carajás and Jari, both noted as needing confirmation (T.V. Santos pers.comm.).The male genitalia of P. monticola present bristles on the median region of the gonocoxite and in those males, these setae are absent.
Information about the biology, ecology and distribution of P. monticola is limited.Based on data available, P. monticola seems to be less abundant when compared with other sand flies present in the same areas.The sex ratio in all studies was female-biased and this species presents diurnal activity in forested areas with a higher occurrence during the crepuscular period between 6:00 and 7:00 pm or between 9:00 pm and 3:00 am in the coldest areas.It is a suspected vector of L. enriettii, the causative agent of cutaneous leishmaniasis in guinea pigs, in southern Brazil.Males and females of P. monticola are attracted to light sources and animal baits used in traps.The species can be found in the forest canopy, on the ground and at the edge, but also inside caves and in anthropized areas, occurring in the Atlantic Forest and in the Brazilian Cerrado.Armadillo burrows and opossum nests are potential breeding sites for P. monticola.Further research is needed to better understand the ecology and vector role of this species.

Figure 1 .
Figure 1.Geographical distribution of Pintomyia monticola in South America.White squares represent the known records.The blue square represents the new record from Brasília, central-west Brazil.Non-confirmed record in Peru and in the Brazilian state of Pará are represented by a question mark (see text for details).Areas identified as suitable based on climatic variables using ecological niche modeling (Maxent method) are shown on a scale of red: light red (low suitability) to dark red (high suitability).