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Revista da Sociedade Brasileira de Medicina Tropical

Print version ISSN 0037-8682On-line version ISSN 1678-9849

Rev. Soc. Bras. Med. Trop. vol.48 no.3 Uberaba May/June 2015

http://dx.doi.org/10.1590/0037-8682-0088-2015 

Major Articles

Phlebotominae sand flies (Diptera: Psychodidae): potential vectors of American cutaneous leishmaniasis agents in the area associated with the Santo Antônio Hydroelectric System in Western Amazonian Brazil

Allan Kardec Ribeiro Galardo 1  

Clícia Denis Galardo 1  

Guilherme Abbad Silveira 2  

Kaio Augusto Nabas Ribeiro 2  

Andréa Valadão Hijjar 3  

Liliane Leite Oliveira 3  

Thiago Vasconcelos dos Santos 4  

1Laboratório de Entomologia Médica, Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá, Macapá, Amapá, Brasil.

2Santo Antônio Energia S/A, Porto Velho, Rondônia, Brasil.

3Saneamento Ambiental Projetos e Operações Ltda, Rio de Janeiro, Brasil.

4Instituto Evandro Chagas, Secretaria de Vigilância em Saúde, Ministério da Saúde, Ananindeua, Pará, Brasil.

ABSTRACT

INTRODUCTION:

An entomological study was conducted as part of a vector-monitoring program in the area associated with the Santo Antônio hydroelectric system in State of Rondônia, Western Amazonian Brazil.

METHODS:

Fourteen sampling sites were surveyed to obtain data on the potential vectors of Leishmania spp. in the area. Sand flies were collected from 2011 to 2014 during the months of January/February (rainy season), May/June (dry season), and September/October (intermediary season) using light traps arranged in three vertical strata (0.5, 1, and 20m).

RESULTS

: A total of 7,575 individuals belonging to 62 species/subspecies were collected. The five most frequently collected sand flies were Psychodopygus davisi (Root) (36.67%), Trichophoromyia ubiquitalis (Mangabeira) (8.51%), Nyssomyia umbratilis (Ward &amp Fraiha) (6.14%), Bichromomyia flaviscutellata (Mangabeira) (5.74%), and Psychodopygus complexus (Mangabeira) (5.25%). These species have been implicated in the transmission of American cutaneous leishmaniasis agents in the Brazilian Amazon region and described as potential vectors of this disease in the study area.

CONCLUSIONS:

Additional surveillance is needed, especially in areas where these five species of sand fly are found.

Key words: Vectors; Cutaneous leishmaniasis; Amazonian region

INTRODUCTION

Phlebotominae sand flies (Diptera: Psychodidae: Phlebotominae) belong to a group of insects with public health relevance that are vectors of certain pathogens, including agents of leishmaniasis(1) (2). Currently, there are 274 recognized species of sand fly in Brazil, and approximately 10% of these species have been implicated in the transmission of American cutaneous leishmaniasis (ACL)(3) (4). Most of these species are endemic to the Brazilian Amazon region. The high biodiversity of the region may contribute to the variety of ecological systems that Leishmania Ross parasites and their respective mammalian reservoir hosts inhabit(5).

In the State of Rondônia in Western Amazonian Brazil, ACL is considered to be a major public health problem, with an annual incidence of 115 cases per 100,000 inhabitants. From 2011 to 2013, 2,945 confirmed autochthonous cases of the disease were reported(6). In Rondônia, at least four Leishmania species have been associated with human infection, including Leishmania (Viannia) braziliensis Vianna, Leishmania (Viannia) lainsoni Silveira, Shaw, Braga &amp Ishikawa, Leishmania (Viannia) guyanensis Floch, and Leishmania (Leishmania) amazonensis Lainson &amp Shaw(7) (8).

Previous studies have compiled interesting data on sand fly populations in State of Rondônia(9) (10) (11) (12) (13) (14) (15) (16). These studies and secondary data compiled in earlier checklists(17) (18) identified 111 Phlebotominae species in State of Rondônia; at least 18 of these species have been associated with Leishmania infections(14).

As in other states of the Brazilian Amazon region, the territory of Rondônia contains infrastructure such as hydroelectric systems that impact the environment by suppressing the growth of vegetation. Because this human activity might influence the emergence of unknown epidemiological profiles of ACL, it is necessary to improve current knowledge of Leishmania species diversity and the temporal/spatial distribution of vector fauna in these areas using surveillance programs aimed at monitoring the transmission of disease. Thus, the aim of the present study was to provide data on the sand fly fauna of an area associated with a hydroelectric system in western Amazonian Brazil and identify potential vectors of ACL agents in this area.

METHODS

Study area

Porto Velho (8° 45′ 43″ S, 63° 54′ 14″ W) is the capital of and largest city in the State of Rondônia. The average altitude ranges from 70 to 600m above sea level. The climate has been classified as tropical super humid (medium annual temperature 25.5°C), and the predominant vegetation is Amazonian tropical rain forest. This area is directly impacted by the construction of the Santo Antônio Hydroelectric System in the Madeira River. Porto Velho, which has an estimated population of 495,000 inhabitants, experienced 314 reported autochthonous cases of ACL in 2011, 2012, and 2013, accounting for more than 10% of the cases of ACL in the State of Rondônia(6). Fourteen collection sites were selected as priority areas for a survey based on the recommendations of previous studies conducted as part of the Basic Environmental Plan (BEP) of the Santo Antônio Hydroelectric System (Table 1). These sites are located in the terra firme forest, which is characterized by distantly spaced apart trees (open canopy) with an average of 40m of canopy. Larger trees with a canopy of up to 55m such as Castanha-do-Pará (Lecythidaceae), Muiaracatiara (Anacardiaceae), Tauari (Lecythidaceae) and Angelim (Fabaceae) were also observed. The composition of palms (Arecaceae) is variegated in these dense forest environments.

Table 1: Collection sites used to catch sand flies in the area associated with the Santo Antônio Hydroelectric System. 

Sampling

Before and after the dam was filled, eleven samples were collected between January 2011 and June 2014 during the rainy (January/February), dry (May/June), and intermediary (September/October) Amazonian seasons using light traps from the Center of Diseases Control (CDC) that were run from 06:00 p.m. to 06:00 a.m. for two consecutive nights. To ensure that the sampling effort was sufficient, a cumulative curve was constructed to calculate the Chao 1, Chao 2, Jackknife 1, and Jackknife 2 diversity indices using the data from all 121 sampled points. The sampling points comprised three traps positioned in different vertical strata, i.e., 0.5, 1, and 20m into the tree canopy, providing 72h of sampling time per collection site. Individual data on the vertical stratification were not available, and each collection site provided a single trapping sample. All collections were approved by the Brazilian Institute of Environment and Renewable Natural Resources (Authorization IBAMA n. 219/2013).

Sand fly processing

The collected individuals were identified according to their external morphological characteristics. Specimens that could not be identified in the field were stored in 70% alcohol, transported to the laboratory and mounted on glass slides with Berlese liquid (G.B.I. Laboratories, Manchester, England) using a modified version of the Young &amp Duncan(1) temporary mounting technique. The phylogenetic taxonomic criteria of Galati(19) were used to identify species, and generic abbreviations proposed by Marcondes(20) were used.

Acquisition of secondary data

Data on the average rainfall during the 2012-2013 period were obtained from the Porto Velho automatic station (National Institute of Meteorology, www.inmet.com.br).

RESULTS

A total of 7,575 phlebotomine sand flies belonging to 64 taxa (62 species/subspecies) were collected over the course of 11,888h of sampling (Table 2). Fifteen genera were identified, including Psychodopygus Mangabeira (13 spp.), Evandromyia Mangabeira (10 spp.), Psathyromyia Barreto (8 spp.), Trichophoromyia Barreto (6 spp.), Nyssomyia Barreto (6 spp.), Micropygomyia Barreto (5 spp.), Migonemyia Galati (3 spp.), Bichromomyia Artemiev (2 spp.), Sciopemyia Barreto (2 spp.), Viannamyia Mangabeira (1941) (2 spp.), Pressatia Mangabeira (2 spp.), Pintomyia Costa Lima (1 spp.), Lutzomyia França (1 spp.), Trichopygomyia Barreto (1 spp.), and Brumptomyia França and Parrot (1 spp.).

Table 2: Sand fly species from the eleven collection sites associated with the Santo Antônio Hydroelectric System in State of Rondônia, Western Amazonian Brazil, from 2011 to 2014. 

The sampling sufficiency curve showed stabilization, reaching an asymptote for the four analyzed diversity indices (Figure 1). The presence of six species (Trichophoromyia eurypyga (Martins, Falcão &amp Silva), Pressatia choti (Floch &amp Abonnenc), Sciopemyia fluviatilis (Floch &amp Abonnenc), Evandromyia pinottii (Damasceno &amp Arouck), Nyssomyia yuilli pajoti (Abonnenc, Léger &amp Fauran), and Trichophoromyia ruii (Arias &amp Young) was documented for the first time in State of Rondônia.

Figure 1: Accumulation curve for sand fly species richness in 121 sites sampled from 2011 to 2014. 

As shown in Figure 2, an increasing number of sand flies was collected between the rainy and dry seasons (i.e., January/June), and the number of sand flies collected tended to decrease during the intermediary season (July/October). In 2012-2013, the first and second years after the dam was filled, the number of individuals collected increased during all of the collection seasons; thereafter, the number plateaued until June 2014.

The five most frequently collected species of sand flies have been implicated in the epidemiology of ACL in the Brazilian Amazonian region. These species included Psychodopygus davisi (Root) (36.7%), Trichophoromyia ubiquitalis (Mangabeira) (8.51%), Nyssomyia umbratilis (Ward &amp Fraiha) (6.14%), Bicrhomomyia flaviscutellata (Mangabeira) (5.74%), and Psychodopygus complexus (Mangabeira) (5.25%). The frequency with which each species was encountered in 2012 and 2013 was compared with the rainfall; the population size of these insects was found to increase at the beginning of the dry season (May/June) when pluviometric precipitation began to decrease (Figure 3).

Figure 2: The seasonal variation in number of sand flies collected during the rainy, intermediary, and dry seasons from 2011 to 2014 in the area associated with the Santo Antônio Hydroelectric System. 

Figure 3:  Frequency with which Psychodopygus davisi, Trichophoromyia ubiquitalis, Nyssomyia umbratilis, Bicrhomomyia flaviscutellata, and Psychodopygus complexus were encountered and rainfall during the entomological collections of 2012 and 2013. 

DISCUSSION

A total of 118 species were identified in State of Rondônia, including seven new records. Two previous studies conducted in this state had identified 22 new records(14) (16). Therefore, it appears that new records of phlebotomine sand flies are continuously being discovered in Rondônia. The Chao/Jackknife indices calculated in the present study indicated that the sampling effort was sufficient to completely estimate the species richness in the studied region.

Several recent studies have described a high level of biodiversity of sand flies (>50 species registered in some of environments) in areas associated with hydroelectric systems in Brazil(21) (22) (23). The present study is the first to provide a longitudinal evaluation of sand fly populations before and after the filling of a dam. The results of this study indicate that the filling of the dam may be associated with an immediate increase in the density of the sand fly population.

The proportion of sand fly populations that had been disturbed by environmental changes tended do decline over time, as evidenced by comparison with subsequent collections, suggesting an apparent reestablishment of the ecological system. The factors associated with these fluctuations have not been well defined. Environmental changes influence the biodiversity, population size, and proportion of dominant species of sand fly(24). Long-term surveys are needed to evaluate whether sand fly populations are able to be replenished after a long period. A preliminary analysis found no correlation between the number of cases of ACL and variations in the number of flies (data not shown).

Psychodopygus davisi is a medically important species of sand fly. The anthropophilic behavior and widespread distribution of these insects in the Amazon basin(25) and previous records of natural Leishmania infections with this species suggest that this species is a potential vector of ACL agents in the studied region. This species has been shown to carry L. (V.) braziliensis and L. (V.) naiffi Lainson and Shaw in Serra dos Carajás(26) (Southern State of Pará, Brazil) and L. (V.) braziliensis in State of Rondônia(14) (27). Recently, two females of this species from the area associated with the Belo Monte Hydroelectric System in State of Pará were found to carry peripylarian Leishmania­-like flagellates (unpublished observations). These findings and data from the present study further suggest that Ps. davisi is involved in the transmission of Leishmania (Viannia) parasites (mainly L. (V.) naiffi) in the Amazon region(14). Trichophoromyia ubiquitalis, Nyssomyia umbratilis, Bichromomyia flaviscutellata, and Ps. complexus are also likely involved in the transmission of agents of ACL in Brazilian Amazonia.

Trichophoromyia ubiquitalis is the only sand fly vector associated with the transmission of L. (V.) lainsoni (28), a parasite recently identified in State of Rondônia(8). However, Trichophoromyia species are also thought to be carriers of L. (V.) lainsoni, as deoxyribonucleic acid (DNA) of this parasite was found in Trichophoromyia auraensis specimens in the Peruvian Amazon(29). Furthermore, two pooled samples of Th. ubiquitalis were recently observed to carry the DNA of an ambiguously identified Leishmania (Viannia) parasite [most likely L. (V.) braziliensis] in the rural area of Cerrado in the State of Mato Grosso(30).

In the present study, Th. ubiquitalis, a known vector of L. (V.) lainsoni, was the second most frequently identified species of sand fly in the study area. These observations are in conflict with the hypothesis that other species more anthropophilic than Th. ubiquitalis transmit L. (V.) lainsoni-like parasites in State of Rondônia(8) which was suggested by the fact that Th. ubiquitalis was infrequently encountered in entomological studies conducted in the municipality of Monte Negro(14). Although it has previously been suggested that Th. ubiquitalis does not exhibit high levels of anthropophilic behavior under field conditions(28), previous studies have described the intradomiciliar transmission of L. (V.) lainsoni via indoor-collected Th. ubiquitalis in an island of the metropolitan area of Belém, State of Pará (unpublished observations). These findings suggest that Th. ubiquitalis is a putative vector of L. (V.) lainsoni in State of Rondônia.

Nyssomyia umbratilis has been identified as the main vector of L. (V.) guyanensis in northern Brazil, particularly in the Guianan ecoregion complex(31). The findings of the present study suggest that Ny. umbratilis is a frequently encountered species in the Porto Velho municipality, which is consistent with findings of Azevedo et al(13). These authors found that Ny. umbratilis was the second most (19.9%) prevalent species in the Samuel Ecological Station, accounting for 48.5% of the specimens collected in the canopy at 20m. Although the distribution of L. (V.) guyanensis near the southern Amazon River remains unknown, recent findings related to the circulation of a L. (V.) guyanensis -like parasite in State of Rondônia(8) suggest that there is a transmission cycle for this parasite/vector in the studied region. However, additional observations are needed to confirm this hypothesis.

Bichromomyia flaviscutellata (2) (7), the major vector of L. (L.) amazonensis, was frequently encountered in the present survey. This was surprising because light traps were used for collection, and these species typically cannot be collected in large numbers without the use of rodent-baited traps(32). This unexpected result could be explained by the fact that the traps were placed 50cm above the ground at each CDC collection station where low-flying specimens may have been attracted to the light and intercepted.

Bichromomyia olmeca nociva (Young &amp Arias), a suspected vector(33) closely related to Bichromomyia species which are associated with the epidemiology of L. (L.) amazonensis, was detected in this study. This species is similar to Bi. reducta (Feliciangeli, Ramirez Pérez &amp Ramirez), a species that was not observed in the present survey but has previously been described as a natural vector of L. (L.) amazonensis in studies conducted in Cachoeira Samuel, State of Rondônia(12). Because Bi. flaviscutellata was detected most frequently in the present study, this species is suspected to be the main species involved in the transmission of ACL attributed to L. (V.) amazonensis in Rondônia(7).

Psychodopygus complexus is currently recognized to be associated with L. (V.) braziliensis-associated ACL in areas where the closely related species Psychodopygus wellcomei is absent(34). In the present study, Ps. complexus was unambiguously identified in the collection because of the absence of Ps. wellcomei males. However, the transmission of L. (V.) braziliensis by Ps. complexus cannot be assumed because no reports of natural infection with this species or evidence of ecological association between the presence of this species and ACL have been reported in the study region. L. (V.) braziliensis is widely distributed throughout Brazil, and several species of sand fly that were not encountered in this study, including Ps. wellcomei Fraiha, Shaw &amp Lainson, Migonemyia migonei (França), Nyssomyia whitmani (Antunes &amp Coutinho), and Ny. intermedia (Lutz &amp Neiva)(2) (7) , have been implicated in the transmission of these agents.

The epidemiological background of the highly anthropophilic species Ps. davisi should be considered in the context of the transmission of various L. (Viannia) species in areas of the Amazon region such as Rondônia(14). The evidence encountered in the present study cannot exclude the possibility that this particular species of sand fly was involved in human infections recently attributed to L. (V.) braziliensis (8) in Rondônia.

The area associated with the Santo Antônio hydroelectric system currently has the highest recorded diversity of Phlebotominae in State of Rondônia. The seasonal fluctuations in sand fly populations from the studied region have been shown to be associated with the end of the rainy period, which is consistent with findings from other entomological studies. However, changes in the populations of these insects are also influenced by the filling of the dam. The increased number of sand flies was not found to be associated with an increase in the incidence of ACL.

Psychodopygus davisi, Trichophoromyia ubiquitalis, Nyssomyia umbratilis, Bichromomyia flaviscutellata, and Ps. complexus were the five most frequently collected species in this study, and they are all considered to be potential vectors of ACL agents in the Amazon region. The large number of Ps. davisi specimens collected in the present study suggests a need for the entomological surveillance of this sand fly species, as these insects are potential vectors of zoonotic cutaneous leishmaniasis in Rondônia.

ACKNOWLEDGMENTS

The authors wish to thank to Redivaldo Francisco Almeida de Souza, Aderbal Amanajás Santana and Jorge Pereira Duarte for their technical support in the field and laboratory work. The authors also appreciate the cooperation of the Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá.

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Santo Antônio Energia S/A.

Received: March 16, 2015; Accepted: April 24, 2015

Correspondence author: Dr. Thiago Vasconcelos dos Santos. Laboratório de Leishmanioses Prof. Dr. Ralph Lainson/Instituto Evandro Chagas/SVS/MS. Rodovia BR 316, Km 07, 67030-000 Ananindeua, Pará, Brasil. Phone: 55 91 3214-2003 e-mail: thiagovasconcelos@iec.pa.gov.br

The authors declare that there is no conflict of interest

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