Fauna of phlebotomine sand flies (Diptera, Psychodidae) in areas with endemic American cutaneous leishmaniasis in the State of Mato Grosso do Sul, Brazil

MEDICAL AND VETERINARY ENTOMOLOGY

Fauna of phlebotomine sand flies (Diptera, Psychodidae) in areas with endemic American cutaneous leishmaniasis in the State of Mato Grosso do Sul, Brazil

Paulo Silva de Almeida^I; Jhoy Alves Leite^I; Aldecir Dutra de Araújo^I; Paulo Mira Batista^I; Rosineide Barbosa da Silva Touro^I; Vânia Santos Araújo^I; Edson José de Souza^I; João Batista Rodrigues^I; Gerson Antunes de Oliveira^I; Jeovaldo Vieira dos Santos^I; Odival Faccenda^II; José Dilermando Andrade Filho^III

^ILaboratório Regional de Entomologia, Núcleo Regional de Saúde da Secretaria Estadual de Saúde, Rua Hilda Bergo Duarte, 940, Centro, 79806–020 Dourados-MS, Brasil. [e-mail]

^IIUniversidade Estadual de Dourados, Rod. Dourados Itaum, km 12, Cidade Universitária, 79804–970 Dourados-MS, Brasil. [e-mail]

^IIICentro de Pesquisas René Rachou/Fiocruz-MG. Av. Augusto de Lima, 1715, Barro Preto, 30190–002 Belo Horizonte-MG, Brasil. [e-mail]

ABSTRACT

Fauna of phlebotomine sand flies (Diptera, Psychodidae) in areas with endemic American cutaneous leishmaniasis in the State of Mato Grosso do Sul, Brazil. The aim of this study was to investigate the ecological aspects of the main vectors of American cutaneous leishmaniasis (ACL) in four monitoring stations situated in the municipalities of Naviraí, Nova Andradina, Novo Horizonte do Sul and Rio Verde de Mato Grosso. For each monitoring station, the captures of sand flies were undertaken each month from July 2008 to June 2010 using CDC and Shannon traps. The CDC traps were installed simultaneously for three consecutive nights in three collection sites: intradomicile, peridomicile and edge of the forest. A Shannon trap was installed from dusk to 10 pm, inside the forest, one night per month. A total of 7,651 sand flies belonging to nine genera and twenty-nine species were captured. Nyssomyia neivai (52.95%), Psathyromyia hermanlenti (10.91%), Psathyromyia runoides (9.16%), Nyssomyia whitmani (7.95%), Psathyromyia aragaoi (4. 89%), Nyssomyia antunesi (3.14%) and Evandromyia bourrouli (2.20%) were the most frequent species. Approximately 65% of the sand flies were collected in the forest environment. The municipalities presented significantly different indexes of species diversity. Naviraí presented the lowest species diversity index, however, it showed the highest abundance. Novo Horizonte do Sul had the highest species diversity index, but the lowest abundance (< 5%). It is noteworthy the occurrence of vector species of Leishmania in the areas studied, especially in Naviraí, where Ny. neivai presented high frequencies which may explain the increased number of ACL cases in this municipality.

Keywords: Insecta; Neotropical; Phlebotominae; species diversity.

Knowing the main vector species found in an area of transmission of American cutaneous leishmaniasis (ACL) is very important in order to understand how the disease is transmitted and thus guide the measures of prevention and control, as well as to evaluate their effectiveness (Ministério da Saúde 2007). In Brazil, there are few studies on the diversity of sand fly species that are vectors of ACL Leishmania. However, bio-ecological studies on suspected or incriminated vector species can contribute to the development of indicators for disease risk assessment.

The sand fly fauna of Mato Grosso do Sul is relatively well known and currently consist of 59 species (Young & Duncan 1994; Galati et al. 2006; Oliveira et al. 2006; Almeida et al. 2010). Regarding the vectors of ACL agents in Mato Grosso do Sul, studies in the municipality of Corguinho and in the Bodoquena area demonstrated the presence of Nyssomyia whitmani (Antunes & Coutinho, 1939) (Galati et al. 1996; Galati et al. 2003) and Nyssomyia neivai (Pinto, 1926) in six municipalities of Mato Grosso do Sul (Almeida et al. 2010), which are important species involved in the transmission of ACL leishmaniasis in Brazil (Luz et al. 2000; Andrade Filho et al. 2007; Costa et al. 2007; Saraiva et al. 2010). Recently, in the municipalities of Bela Vista and Bonito the presence of Bichromomyia flaviscutellata (Mangabeira, 1942) in areas with occurrence of Leishmania (Leishmania) amazonensis was confirmed (Nunes et al. 2008; Dorval et al. 2010).

Between January 2008 and July 2010, the SINAN (Sistema de Informações de Agravos de Notificação), Epidemiological Surveillance Service of the Mato Grosso do Sul State Health Secretariat confirmed 388 cases of ACL in 60 municipalities, among them Naviraí, Nova Andradina, Novo Horizonte do Sul and Rio Verde de Mato Grosso. This study aimed to assess: 1) the sand fly fauna, and 2) the ecological aspects of the main vectors of ACL agents in Naviraí, Nova Andradina, Novo Horizonte do Sul and Rio Verde de Mato Grosso municipalities, where the prevalence of ACL is high.

MATERIAL AND METHODS

Study area. For each municipality, a Monitoring Station (MS) was selected, considering the number of autochthonous human cases of ACL in recent years and the absence of previous researches about the sand flies fauna in these areas.

Naviraí (23º03'54"S and 54º11'26"W, 362 meters altitude) with an area of 2,193.83 km² is located in the southwestern region of the state, 350 km from Campo Grande, the State capital. Its population consists of 46,355 inhabitants (IBGE, 2011). The municipality borders the state of Paraná and the original vegetation was seasonal semi-deciduous forest. The agriculture and commerce are the major economic resources of the municipality. The main crops are sugar cane, beans, lemon, corn and wheat. In this municipality, the entomological survey was conducted near "Usinavi", a sugar cane mill, situated at the farm Santa Maria.

Nova Andradina (22º14'00"S and 53º20'35"W, 380 meters altitude) with an area of 4,776.09 km² is located in the southeastern region, 288 km from Campo Grande. Its population consists of 45,599 inhabitants (IBGE, 2011). The municipality is part of the Paraná river basin and its original vegetation was seasonal semi-deciduous forest. Livestock (mainly buffalo) and commerce are the major economic resources of the municipality. The main crops are sugar cane and cassava. The CDC light traps were installed in the farm Três Irmãos and the Shannon trap, in a forest fragment, near the neighborhood "COHAB III".

Novo Horizonte do Sul (22º39'11"S and 53º51'21"W) with an area of 849.11 km² is also located in the southwest region, 303 km from Campo Grande. The population consists of 4,944 inhabitants (IBGE, 2011). It is also situated in the Paraná river basin and the original vegetation was characterized by seasonal semi-deciduous forest and livestock is the major economic activity of the municipality. The rearing of silkworms and cassava plantations are also widespread in the municipality. The survey was undertaken in an area known as Linha Volta Redonda.

Rio Verde de Mato Grosso (18º55'05"S and 54º50'39"W, 330 meters altitude) with an area of 8,151.97 km², is located in the Pantanal, in the north of the State, 201 km from Campo Grande, its population consisting of 18,892 inhabitants (IBGE 2011). The municipality is located in the Paraguay river basin with a dominant vegetation of Cerrado and Pantanal. Trade and farming are major economic activities in the municipality. Cattle, sheep, horses, wool production and orange, coconut and guava plantations are widespread around the city. The survey was conducted in the Serra Grande Farm resort.

Collection of the sand flies. The survey was conducted from July 2008 to June 2010. In each monitoring station, four locations were sampled: 1) intradomicile; 2) peridomicile; 3) edge of the forest and 4) inside the forest. Sand fly collections were carried out with automatic light traps during three consecutive nights on the first, second and third sites, monthly. The Shannon trap was installed from dusk to 10 pm, one night per month in the fourth point (forest). The field methodology followed the guidelines of the Manual for the Surveillance of ACL (Ministério da Saúde 2007). Species were identified in the Laboratório Regional de Entomologia de Dourados/SES-MS according to Galati's classification (2003). Abbreviations for the genera follow that proposed by Marcondes (2007).

Analysis of the data. The characteristics of the population studied were described using a single frequency through percentages, tables and graphs. Furthermore, the data were stratified by municipality and point of capture to check the diversity index and proximity among the descriptors, through correspondence analysis (Mingoti 2005).

In order to assess the diversity of the phlebotomine species in the four sites of capture, in each municipality, the Shannon-Wiener index was used (with correction factor and the natural logarithm) according to the number of species occurrences. The t test was used to compare the diversity index. The level of significance was 0.83%, which corresponds to 5% divided by the number of multiple comparisons (six).

RESULTS AND DISCUSSION

A total of 7,651 sand flies were captured, belonging to nine genera and twenty-nine species. The most frequent species were: Nyssomyia neivai (52.9%), Psathyromyia hermanlenti (Martins, Falcão & Silva, 1970) (10.9%), Psathyromyia runoides (Fairchild & Hertig, 1953) (9.2%), Nyssomyia whitmani (8.0%), Psathyromyia aragaoi (Costa Lima, 1932) (4.9%), Nyssomyia antunesi (Coutinho, 1939) (3.1%), and Evandromyia bourrouli (Barretto & Coutinho, 1941) (2.2%). The other species totalized 8.8% of the captured sand flies (Table I).

Naviraí presented a high frequency of Ny. neivai (99.6%). The other species accounted for less than 1% of the total. Nyssomyia whitmani was only captured at the edge of the forest (Table II). Both species are involved in the transmission of Leishmania protozoa in Brazil (Andrade Filho et al. 2007; Pita-Pereira et al. 2009; Marcondes et al. 2009; Saraiva et al. 2009).

A total of 65.0% of the sand flies were collected inside the forest, unlike other studies, in which most specimens were found in anthropic environments (Saraiva et al. 2008; Galati et al. 2010). This fact may be due to the use of a Shannon trap in the forest and CDC light traps in the other environments, which demonstrates the importance of using more than one type of trap in studies of sand fly fauna.

The seasonal variation of Ny. neivai in Naviraí is showed in Fig. 1. The highest frequency of the species occurs in the months that follow periods of heavy rain. This period coincides with the late winter and spring. This result is different than that showed by Galati et al. (2010) in the Iporanga municipality, São Paulo state, where the predominance of the species occurs in the summer, however, it corroborates the observations of Odorizzi & Galati (2007) in the northwestern region of São Paulo state.

In Nova Andradina, the species Evandromyia lenti (Mangabeira, 1938) showed the highest frequency (47.0%), followed by Evandromyia termitophila (Martins, Falcão & Silva, 1964) (19.3%). Brumptomyia brumpti (Larrouse, 1920), Psathyromyia campograndensis (Oliveira, Andrade Filho, Falcão & Brazil, 2001), Sciopemyia sordellii (Shannon & Del Pont, 1927), all with 6.0%, and Psathyromyia punctigeniculata, with 4.8%, presented distinct frequencies from the other species, which together accounted for 10.9% of the species captured (Table III). Evandromyia lenti was found naturally infected with Leishmania braziliensis in Minas Gerais (Margonari et al. 2010), and Sherlock (1996) suggests that this species may be involved in the transmission of canine visceral leishmaniasis in the State of Bahia.

Psathyromyia shannoni (Dyar, 1929) was the species with the greatest abundance (28.2%) in Novo Horizonte do Sul, followed by Pintomyia christenseni (Young & Duncan, 1994) (13.3%), Ny. neivai (11.8%), Ny. whitmani (8.1%), Pa. aragaoi and Pintomyia pessoai (Barretto & Coutinho, 1940), both with 7.5%, Ev. lenti (6.9%) and Brumptomyia avellari (Costa Lima, 1922) (6.6%). The other species accounted for the remaining 10.1%. Psathyromyia shannoni was predominant inside the forest. This species has been found naturally infected in several countries (Young & Duncan 1994) and may be involved in the transmission of Leishmania mexicana in Mexico (Sanchéz-García et al. 2010). It is also important to emphasize the predominance of Ny. neivai in the intradomicile environment.

In Rio Verde do Mato Grosso, the species with the highest frequency was Pa. hermanlenti (26.0%), followed by Pa. runoides (21.9%), Ny. whitmani (17.7%), Pa. aragaoi (10.8%), Ny. antunesi (7.5%), Ev. bourrouli (5.1%), Pa. campograndensis (1.9%) and Ev. lenti (1,7%). The other species totalized 7.4%. The majority of specimens were collected at the edge of the forest (68.4%). Psathyromyia hermanlenti and Pa. runoides were more frequent in the intradomicile environment (Table III). This is the first report of Pa. runoides in the Mato Grosso do Sul state. The vectors species of Leishmania (Viannia) spp. collected in Rio Verde do Mato Grosso were Ny. whitmani and Ny. antunesi, the latter presenting a highly anthropophilic behavior (Andrade Filho et al. 2001) and they were found naturally infected by flagellates in the State of Pará (Ryan et al. 1984; Silveira et al. 2002). Bichromomyia flaviscutellata, a species involved in the transmission of Leishmania (Leishmania) amazonensis in several regions of Brazil, including Mato Grosso do Sul (Lainson & Shaw 1968; Shaw & Lainson 1968; Dorval et al. 2010), was also captured.

During the two years of the study, the seasonal distribution of Ny. whitmani in Rio Verde de Mato Grosso showed a higher density in drier periods (fall and winter) (Fig. 1), as occurred in the Bodoquena and Corguinho municipalities, both in Mato Grosso do Sul state (Galati et al. 1996; Galati et al. 2003), and Maringá, in Paraná state (Teodoro et al. 2003).

The municipalities presented significantly different species diversity indexes (Table I), with Naviraí, which presented the highest frequency of specimens (52.6%), showing the lowest value, influenced by the abundance of Ny. neivai (Table III). Nova Andradina had less than 2% of specimens captured, and showed the second lowest diversity value (Table I, Fig. 2). Novo Horizonte do Sul had the highest species diversity, although its abundance was lower than 5% (Table I, Fig. 2) and Rio Verde do Mato Grosso presented the second highest diversity and abundance, with approximately 42% of the sand flies captured (Table I, Fig. 2).

The correspondence analysis (Fig. 2) revealed that the position of the different species is not close to the center, which means that their prevalence differs among the municipalities. The incidence is similar in Novo Horizonte do Sul and Nova Andradina. Naviraí had an incidence of few species, but is associated with the most abundant species, Ny. neivai. Rio Verde de Mato Grosso is associated with more species and greater abundance.

Nyssomyia neivai was the most frequent and abundant species. It was present in all ecotypes surveyed in the state of Mato Grosso do Sul. This observation confirms the results obtained by Massafera et al. (2005) and Silva et al. (2008) in the State of Paraná. In the state of São Paulo, Condino et al. (1998) also observed a higher density of Ny. neivai in the city of Teodoro Sampaio. In the city of Piçarras, in the state of Santa Catarina, Marcondes et al. (2005) observed the predominance of Ny. neivai in areas with occurrence of ACL.

Nyssomyia whitmani was the fourth most frequently captured species (Table I), occurring in Naviraí, Novo Horizonte do Sul and Rio Verde do Mato Grosso and was considered as a potential vector of Leishmania braziliensis in Mato Grosso do Sul (Galati et al. 1996). This species was more abundant in environments with anthropic modifications, such as peridomicile and the edge of the forest.

Despite the use of different traps, the diversity is distinct among the different collecting sites, being higher in the edge of the forest, followed by peridomicile and intradomicile. The lowest diversity was found inside the forest. The diversity index was statistically different for all comparisons between two environments (Table II). The diversity of sand flies of the four municipalities should be related, probably with peculiar characteristics of each, such as geographical location, vegetation and climate, important factors for the faunal composition.

The geometric proximity between the site of capture and species of sand flies is represented by Fig. 3. Dimension 1 explains almost all of the variation (92.7%), allowing the results to be read horizontally, from left to right. The species located to the left of the center are associated with the edge of the forest and peridomicile, and those located to the right of the center, with intradomicile and inside the forest and, therefore, they represent the most abundant species there. Near the center, indicating that there is no trend, i.e., the abundance is divided proportionally among the environments, few species appear in this location. Lutzomyia longipalpis (Lutz & Neiva, 1912) and Pi. christenseni appear closer to the center, being their frequencies proportional in all places of capture. On the other hand, the majority of species are found outside the center, showing that their incidence is not proportionally equal among the sites of capture.

From 2001 to 2010, Naviraí reported 82 cases of ACL, Nova Andradina reported 41, Novo Horizonte do Sul reported 48 and Rio Verde de Mato Grosso reported 51 cases (Sinan 2011). Important vector species of ACL agents were found in these municipalities, especially Ny. neivai in Naviraí, which may explain the high number of cases of ACL in this municipality, suggesting that this species may be responsible for the disease transmission in this region.

ACKNOWLEDGEMENTS

To the technicians from the Ministry of Health for their collaboration in the field research: Agabito Arguelho, in the municipality of Novo Horizonte do Sul and the colleagues from Laboratório Regional de Entomologia de Dourados, Ademar Dimas Ferreira, José Oliveira da Silva, Nilza Sizue Fukuda Nogueira Mariano and Maria Aparecida Ferreira de Souza, for helping in the mounting and in the identification of the sand flies. To Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for financial support.

Received 19 September 2012; accepted 26 October 2012

Associate Editor: Maria Anice M. Sallum

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Publication Dates

• Publication in this collection
  01 Apr 2013
• Date of issue
  Mar 2013

History

• Received
  19 Sept 2012
• Accepted
  26 Oct 2012