Corrientes is located in the Mesopotamian region in northeastern Argentina. The province shares international borders with Paraguay to the north, through the Paraná River, and with Uruguay and Brazil through the Uruguay River in the east, and national borders with the provinces of Misiones, Entre Ríos Chaco and Santa Fe. The climate is humid in winter and dry in summer, with an average annual temperature of 21 °C, irregular periods of rainfall with an annual average of 1200 mm (NMS 2018). The Esteros del Iberá wetlands are found in the north-central region of the province, with an area of ~700,000 ha.

Data sources and search strategies: To obtain information on the citations of the different Phlebotominae species in the province of Corrientes, scientific sources (scientific articles published in indexed journals and congress abstracts) containing first records or focal samplings were analyzed. An active bibliographic search was carried out in electronic databases such as PubMed, Scielo and Google Scholar. The combined keywords (in English and Spanish) used were: Leishmaniases, Visceral Leishmaniases or Tegumentary Leishmaniases or Cutaneous Leishmaniases and Corrientes Argentina. Phlebotominae or sandflies or flebotomos and Corrientes, Argentina, Leishmaniasis Tegumentaria or Leishmaniasis Cutanea or Leishmaniasis Visceral and Corrientes Argentina. Publications between 1900 and 2020 were considered.

Unpublished data: Data from samplings conducted in the town of Mercedes on 10 and 11 November 2011 and 22, 23, 27 and 28 January 2013; in Colonia Carlos Pellegrini on 12, 13 and 15 November 2011 and in Santo Tomé on 7 and 9 April 2014, 11 March 2015, 19 April 2016, 18 and 20 September, 15 November and 12 December 2017 and 26 February 2019 were included. Sandflies samplings were carried out with REDILA light traps (Fernández et al., 2015), in sites selected under worst-case scenario criterion (Salomón et al., 2002). All these sites were geo-referenced by means of a GARMIN eTrex® 30 handheld GPS.

The captured Phlebotominae were diaphanized with lactophenol (lactic acid and phenol 1:1). Subsequently, their determination was performed according to a taxonomic key (Galati, 2018).

Reports of Nyssomyia intermedia (Lutz & Neiva) and Psathyromyia shannoni (Dyar) according to original works were recorded here as Ny. neivai (Pinto) and Pa. bigeniculata (Floch & Abonnenc) due to nomenclatural changes and species re-assignment (Andrade Filho et al., 2003; Sábio et al., 2014; Szelag et al., 2016). Females of Evandromyia cortelezzii (Brètes), Ev. sallesi (Galvao & Coutinho) and Ev. chacuensis (Szelag et al., 2018) cannot be distinguished by their morphological characteristics, so specimens were included as Cortelezzii Complex (Galati, 2018).

Localities with reports of CL and LV cases: Confirmed human cases records by year and reporting locality were obtained from the Sistema Nacional de Vigilancia en Salud (SNVS). Data correspond to a query on 12/02/2019 and include cases recorded until then.

The first non-systematic captures of sandflies in the province of Corrientes were published in the 1950s (Bejarano & Duret, 1950; Castro, 1959; Duret, 1952). From 1990 onwards, sandflies captures were related to research projects or epidemic outbreaks. To date, 26 capture sites have been reported throughout the province (Fig. 1), with a total of 30 published articles and 10 additional unpublished samples. Sampling sites are located mainly along the river boundaries of the province, along National Route 12, bordering the Paraná River to the north and west, and Route 14 bordering the Uruguay River to the east. Not all districts within the province were sampled and no sampling records were found in the southwestern area.

Fig. 1.
Distribution of the 26 sampling sites.

1 Apipé, 2 Alvear, 3 Bella Vista, 4 Corrientes, 5 Colonia Liebig, 6 Colonia Pellegrini, 7 Curuzú Cuatiá, 8 Estación biológica de Corrientes, 9 Garruchos, 10 Gobernador Virasoro, 11 Itatí, 12 Ituzaingó, 13 La Cruz, 14 Mercedes, 15 Monte Caseros, 16 Paso de los libres, 17 Paso de la Patria, 18 Riachuelo, 19 San Cayetano-Riachuelo, 20 San Cayetano, 21 San Antonio, 22 Santo Tomé, 23 San Carlos, 24 Santa Tecla, 25 Ita-Ibaté y 26 Villa Olivari. Base maps obtained from OpenStreetMap (https://www.openstreetmap.org/).

A total of 15 species of Phlebotominae have been recorded: Lutzomyia longipalpis (Lutz & Neiva), Ny. neivai, Migonemyia migonei (França), Cortelezzii Complex, Pintomyia fischeri (Pinto), Pi. pessoai (Coutinho & Barretto), Pi. montícola (Costa Lima), Pi. misionensis (Castro), Micropygomyia quinquefer (Dyar), Ny. Whitmani (Antunes and Coutinho), Pa. bigeniculata, Brumptomyia avellari (Costa Lima), Br. gimaraesi (Coutinho & Barretto), Br. sp. y Ev. correalimai (Martins, Coutinho & Lutz) (Fig. 2). This latter species was captured for the first time in the city of Santo Tomé during the surveys in 2015, 2016 and 2017.

Fig. 2.
Distribution of Phlebotominae species in the province of Corrientes.

Each map shows the sites where the different species were recorded: Br. avellari 3 sites, Br. guimaraesi 2 sites, Brymptomyia sp 3 sites, Cortelezzii Complex 8 sites, Ev. correalimai 1 site, Lu. longipalpis 13 sites, Mg. migonei 8 sites, Mi. quinquefer 2 sites, Ny. neivai 22 sites Ny. whitmani 4 sites, Pa. bigeniculata 6 sites, Pi. fischeri 2 sites, Pi. misionensis 1 site, Pi. monticola 1 site, Pi. pessoai 5 sites.

The sites with the highest number of species records were Santo Tomé, Santa Tecla, Corrientes capital, San Cayetano-Riachuelo and San Cayetano. Santo Tomé and Corrientes capital are cities with little vegetation or patches of vegetation within the urban area. More than 10 samplings were carried out in these cities with different objectives and study methods, the first one taking place in the 1950s. On the other hand, Santa Tecla, San Cayetano-Riachuelo and San Cayetano are less urbanized, and even with rainforest areas with a high percentage of vegetation cover, and with up to four samplings each (Table I).

Table I.
Phlebotominae reported in Corrientes province from 1951 to 2019 by species, locality, sampling year, and source of information (reference).

Human cases of VL have been recorded in four cities of the province: Corrientes capital, Ituzaingó, Santo Tomé and Paso de los Libres (Fig. 3). In the first three cities there were records of Lu. longipalpis, while in Paso de los Libres, only Ny. neivai was found (Salomón et al., 2009; Salomón et al., 2011).

Focal sampling associated with three cases of human VL has been carried out. The focal studies in Corrientes Capital (Araujo et al., 2015) and Santo Tomé confirmed the presence of the vector Lu. longipalpis and infected dogs in the surroundings of the detected human case (unpublished data). In contrast, in the study in Paso de los Libres only infected dogs were found, but no presence of Lu. longipalpis (Blanco et al., 2014)

Regarding positive sites for human CL reports, co-occurrence of human cases and presence of Ny. neivai have been recorded in Apipé, Corrientes, Bella Vista, Itatí, Riachuelo, Santo Tomé, Villa Olivari and Paso de la Patria (Borda et al., 2006; Salomón et al., 2002; 2006a; 2009; Martínez et al., 2019), human cases without vector presence were only recorded in Mercedes while no Phlebotominae samplings were carried out in the remaining eight localities with human cases (Fig. 3).

Fig. 3.
Distribution of human cases of VL and CL reported by the Sistema Nacional de Vigilancia en Salud (SNVS) and sites where Lu. longipalpis and Ny. neivai were found.

Cities with human VL cases are indicated as follows: 1 Santo Tomé, 2 Paso de los Libres, 3 Ituzaingó, and 4 Corrientes. Cities with human CL cases are: 5 Apipé, 6 Corrientes, 7 Manuel Derqui, 8 Bella Vista, 9 Riachuelo, 10 Empedrado, 11 Perugorria, 12 Goya, 13 Paso de la Patria, 14 Mercedes, 15 San Luis del Palmar, 16 Santa Lucía, 17 Itatí, 18 Santo Tomé, 19 Santa Ana, 20 Villa Olivari, 21 San Miguel.

Evandromyia correalimai (Martins, Coutinho & Lutz) Corrientes province, Santo Tomé City 1 ♀ (Lat: -28.551079°, Long: -56.029922°) 11-III-2015; 1 ♀ (Lat: -28.546722°, Long: -56.033361°) 19-IV-2016, 3 ♀ (Lat: -28.541965°, Long: -56.032168°) 18-IX-2017, 20-IX-2017 and 15-XI-2017; collected by Villarquide, María Lucrecia. Captures are available at Fundacion Barcelo. All individuals were captured in henhouses surrounded by vegetation, at 315 m, 470 m and 240 m approximately from the Uruguay River. These dwellings are located on the edge of the city, adjacent to the river containment vegetation. All sites had chickens and dogs. Distribution. The only previous record for the country was in Puerto Iguazú, within few meters from the Parana river (Fernández et al., 2020), 440 km from Salto Tomé, on the Uruguay river.

The present study reported 15 Phlebotominae species in the province of Corrientes out of the 46 recorded in Argentina (Moya et al., 2021), with most of the reports distributed in the north and east of the province. Samplings were distributed throughout the peripheral area of the province, generally in cities of high population density that are located on or a few km apart from national routes 12 and 14. Towards the center of the province there are few samples and the cities have generally low population density. Lutzomyia longipalpis was found in 13 cities located mainly on the periphery of the province and the distribution of Ny. neivai was observed in 22 cities mainly in the north and east. However, the 17 cities with reported CL cases were mainly distributed in the west and southwest.

The greater number of phlebotominae species recorded in localities such as Corrientes and Santo Tomé, could be related to a greater probability of collecting species usually found in low abundances, due to the greater number of studies, and the greater number of sites sampled in these cities. Consistently, the occurrence of species such as Mi. quinquefer, Ps. bigeniculata, Cortelezzii complex, Pi. pessoai, Ny. neivai, Ny. whitmani and Mg. migonei in urbanized environments, could be related to peri-urban areas or intra-urban vegetation patches, since these species are favored by both anthropic modifications and arboreal vegetation as it was observed in previous studies in the province of Corrientes (Santini et al., 2015; Berrozpe et al., 2019; Martínez et al., 2019). A study carried out in Brazil, which assessed the presence of species in urban, transition and rainforest areas, found also the greatest species diversity in the transition zone (de Castilho Sanguinette et al., 2015). This increase in diversity in transitional areas could explain why species such as Pi. misionensis and Pi. monticola are found so far only in Santa Tecla and Apipe, sites with mixed environmental characteristics such as high vegetation coverage intermingled with domestic areas of human low density.

The cities with CL risk have been associated with environmental heterogeneity and edges with secondary vegetation, especially in small cities (Salomón et al., 2006a). The distribution of recorded CL cases could be associated with the latter condition, given that most of the cities with human CL are small or with large areas or riparian forest. However, although the sites where the vector and cases were recorded coincide, it is not possible to state that the site of the reporting is the same as the transmission site, as only the residence or place of diagnosis is the usually recorded data. Meanwhile, the place of transmission may be even in localities far away of the residence related to recreational or work activities within areas of wild vegetation (e.g., fishing, hunting, or forest clearing work), where the vectors involved in transmission are generally found (Salomón, 2019). In order to evaluate the possible sites of transmission and predict the appearance of new cases, it is important to record and detect new vector-competent species in time, for which vector surveillance and knowledge of the species present are essential.

Visceral leishmaniases is the most severe form of the disease and can be fatal if not diagnosed or inadequately treated. During 2018, the case fatality rate of VL reached 8% for the Americas (OPS 2019). In the records collected for this study, only 4 cities in the province of Corrientes showed cases of VL. In the focal study conducted in the city of Paso de los Libres in response to the human case of VL, infected dogs were found, but no sandflies were detected, probably due to unfavorable weather conditions at the time of sampling. However, previous studies had detected the presence of Ny. neivai, and the epidemiological interview did not indicate whether the patient had traveled to other localities prior to symptoms manifestation (Blanco et al., 2014; Salomón et al., 2011). Likewise, the presence of Lu. longipalpis could not be ruled out.

The new record in the province, Ev. correalimai, though it is not of sanitary importance, contributes to increase the specific richness, in addition to its importance for being the second record for Argentina. Ev. correalimai was first recorded in Puerto Iguazú, Misiones, in protected areas (Iguazú National Park) and forest patches (Fernández et al., 2020). In Santo Tomé, the new record reported here, Ev. correalimai was captured in two sites located on the edge of riparian and secondary vegetation, inside henhouses.

This compilation of vector species records and cases of leishmaniases allowed us to identify spatial gaps in information, especially in the southwestern area of the province of Corrientes. In general, the studies carried out in the province were motivated by epidemic outbreaks, while others were aimed at evaluating the presence or dispersal of Lu. longipalpis or Ny. neivai given their implication in the transmission of leishmaniases (Salomón et al., 2002, 2006a, 2009, 2011). The last distribution study about Lu. longipalpis in the province was in 2010 and did not cover all the main cities of the province (Salomón et al., 2011). It is highly likely then, that the species could be present in more cities. Likewise, in places where only Lu. longipalpis was recorded in the south, other species might be found if further studies were carried out, especially, taking into account that in the province of Entre Ríos to the south of Corrientes a profile of five species was found, including Ny. neivai and Ny. whitmani. Hence, these species could be present having not been recorded in southern Corrientes.They could even be implicated in some of the CL cases in the 8 positive cities where Phlebotominae sandflies were not sampled (Salomón et al., 2006b; Gould et al., 2013; Santini et al., 2018).

In conclusion, the record of 15 Phlebotominae species places Corrientes as the third province in terms of specific richness for Argentina, after the provinces of Misiones and Chaco. Most of the species are found in the north. Meanwhile, the variety of environments in the province suggests that there may still be more species that have not been recorded yet. Regarding the distribution of CL cases, they are mainly found along the coast of Paraná River, while VL cases, according to their date of occurrence, seem to be moving southward along the coast of Uruguay River. Although confirmation of the site of infection depends on both, reliable information from epidemiological interviews and the movement of individuals to areas of transmission, the number of sites with human cases in areas with no vector records calls for more vector studies. This would complement the information compiled here and would allow to contribute to the design of strategies and allocation of resources for operational research, control and sanitation policies to address the problem of leishmaniases.

lvillarquide@barcelo.edu.ar