Memórias do Instituto Oswaldo Cruz Fundação Oswaldo Cruz, Fiocruz ISSN: 1678-8060 EISSN: 1678-8060 Vol. 91, Num. 1, 1996, pp. 75-79

The Sand Fly Fauna (Diptera: Psychodidae: Phlebotominae) of a Focus of Cutaneous Leishmaniasis in Ilheus, State of Bahia, Brazil

Alfredo CR Azevedo, Maur1cio L Vilela, Nataly A Souza, Claudia A Andrade-Coelho, Andre F Barbosa, Antonio LS Firmo*, Elizabeth F Rangel

Laboratario de Vetores de Leishmaniose e Oncocercose, Departamento de Entomologia, Instituto Oswaldo Cruz, Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brasil *Fundacao Nacional de Saúde, Ilheus, BA, Brasil

Work supported by CNPq, Brazil grant no. 40.337l/90-2

Code Number: OC96012
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The municipality of Ilheus, State of Bahia, has a focus of cutaneous leishmaniasis where entomological studies were carried out to determine the sand fly species and their habits. Lutzomyia migonei, L. sallesi, L. tupynambai, L. schreiberi, L. intermedia, L. whitmani, L. yuilli yuilli, L. fischeri, L. pessoai, L. shannoni and L. misionensis were identified.

Lutzomyia whitmani was the predominant species. Specimens were collected indoors, at peridomestic sites, in the cocoa plantations and in other types of collections. Females fed readily on humans and were attracted to domestic animals. Our evidence suggests that L. whitmani is a probable vector.

Key words: sand fly fauna - cutaneous leishmaniasis - State of Bahia - Brazil

American Cutaneous Leishmaniasis (ACL), caused by Leishmania (V.) braziliensis, is one of the parasitic diseases of high incidence in some states of northeast Brazil. The municipality of Ilheus, State of Bahia, is an endemic area of ACL. There are several cases of mucosal involvement (FNS - Fundaçao Nacional de Saúde 1991, personal comunication). We decided, in collaboration with FNS in 1990, to identify the local sand fly fauna and to study those aspects of the biology of the sand fly species as related to their role as vectors in some endemic areas in this region.

At present, no control measures have been applied in this region. Therefore, data obtained from these studies may be helpful in planning control programmes.

MATERIALS AND METHODS

Study area and meteorological data - The municipality of Ilheus is located about 462 km from Salvador City (14^o50' latitude South and 39^o06' longitude West). It has a wet, hot tropical climate and high annual rainfall (1,500-2,000 mm). In the past, it was covered by 'Mata Atlantica' forest, but now consists of plantations of cocoa-tree, the regions major economical agricultural activity.

We worked at two sites: Violeta and Cipo farms, where the average temperature ranged between 19 C and 29 C, and relative humidity was 87%.

Sand fly captures - These were carried out between 18:00 hr and 20:00 hr one week per month (December 1990, February, March, September and October 1991, March until August, and November 1992). Sand flies were captured in houses, on the inside and outside walls, using manual aspirators; at peridomestic sites (up to 10m from houses) using manual aspirators on equines, and by CDC light traps (Sudia & Chamberlain 1962, Gomes et al. 1985, Natal et al. 1991) in domestic animal shelters. In cocoa plantations, a Shannon trap (Sherlock & Pessoa 1964) was used for collections up to 50m and 100m from houses, and a Falcao light trap (Falcao 1981, Aguiar et al. 1985) was used only to capture 100m from houses.

The degree of anthropophily was determined by considering the number of females collected bitting man, in peridomestic sites and in cocoa plantations.

Identification of sand fly species - Sand flies were stored in 70% ethyl alcohol and later preserved on slides, using BerleseÆs medium, for taxonomic studies.

Search for natural infections of sand flies - Some captured females were kept in cages, in plastic bags with high humidity, and dissected in physiological saline, within 24hr. These were identified by their spermathecae during the dissections.

RESULTS

Sand fly fauna - During 242 hr we collected a total of 8695 specimens belonging to the following Lutzomyia species, listed according to the classification by Young and Duncan (1994):

Group Migonei Theodor, 1965

L. migonei (Franca, 1920)

L. sallesi (Galvao & Coutinho, 1939)

L. tupynambai (Mangabeira, 1942)

Subgenus Micropygomyia Barretto, 1962

L. schreiberi Martins, Falcao & Silva, 1975

Subgenus Nyssomyia Barretto, 1962

L. intermedia (Lutz & Neiva, 1912)

L. whitmani (Antunes & Coutinho, 1939)

L. yuilli yuilli Young & Porter, 1972

Subgenus Pintomyia Costa Lima, 1932

L. fischeri (Pinto, 1926)

L. pessoai (Coutinho & Barretto, 1940)

L. sp.

Subgenus Psathyromyia Barretto, l962

L. shannoni (Dyar, 1929)

Subgenus Psychodopygus Mangabeira, 1941

L. sp.

Ungrouped species

L. misionensis (Castro, 1959)

The predominance of L. whitmani (97.7%) over the other collected species was very evident. Lutzomyia intermedia (1%) followed in abundance and the other species appeared in much lower percentages (Table).

TABLE

Sand flies collected in Ilheus, Bahia, Brazil. December 1990, February, March, September and October 1991, March-August and November 19922.

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Sand flies species        Females    Males   Total    % 
----------------------------------------------------------
L. migonei                 8         11      19     0.2 
L. sallesi                 1         -       1      0.0 
L. tupynambai              2         -       2      0.0 
L. schreiberi              5         1       6      0.1 
L. intermedia              52        39      91     1.0
L. whitmani                3099      5390    8489   97.7
L.y.yuilli                 1         -       1      0.0 
L. fischeri                34        14      48     0.6 
L. pessoai                 7         1       8      0.1 
L. (Pi)sp.                 6         -       6      0.1 
L. shannomi                1         -       1      0.0 
L. (Ps) sp.                1         2       3      0.0
L. minionensis             20        -       20     0.2
----------------------------------------------------------
Total                    3237      5458     8695   100.0
----------------------------------------------------------

Fig. 1: fequency of Lutzomyia whitmani on A: inside houses, B: animal bait (equine) and C, D: in domestic animal shelters (C = chicken house, D = cowshed).

Fig. 2: frequency of Lutzomyia whitmani in plantations of cocoa A, B: using Shannon trap, and C: using light trap.

Frequency of species caught with differents type and site of captures - In 108 hr we collected 6327 specimens from inside and outside houses: L. whitmani (97.8%) was the most common captured species. We also collected L. migonei, L.sallesi, L. tupynambai, L. schreiberi, L. intermedia, L. fischeri, L. pessoai, L. (Pi) sp, L. shannoni and L. misonensis. (Fig.1).

From light traps in domestic animals shelters, we collected 274 specimens. In a chicken-house most sand flies captured in 22 hr were L. whitmani (93.8%). Lutzomyia migonei, L. tupynambai, L. intermedia, L. fischeri , L. pessoai and L. (Pi) sp. were also found. In the cowshed, only two species were caught (56 specimens in 10 hr): L. whitmani (75%) and L. fischeri (25%). The number of sand flies attracted to equines, during 16 hr, was 318 and again most were L .whitmani (98.5%), followed by L. fischeri (0.9%) and L. (Pi) sp. (Fig.1).

In cocoa plantations (during 86 hr) we collected 1720 specimens. Near houses (994 specimens), L. migonei, L. y. yuilli and L. misionensis were found, with L. whitmani predominating (97.9%). As far as 100m from houses (694 specimens), only two species were collected - L. whitmani (99.9%) and L. misionensis (0.1%). Further away from houses when a Falcao light trap was used (32 specimens), L. whitmani (75.8%), L. pessoai (9.1%), L. fischeri and L. misionensis were collected (Fig. 2).

The specimens identified as Lutzomyia spp. are related to subgenera Psychodopygus (possibly L. ayrozai) and Pintomyia sp. that may be an undescribed species.

Search for natural infections - We dissected 225 specimens, but no infections were detected.

Although we have not yet identified the Leishmania isolated from patients, the clinical and parasitological features indicate that the disease in Ilheus is caused by Le. (V.) braziliensis.

DISCUSSION

Our survey in Ilheus indicated the presence of 13 species of sand flies, most of which were captured in houses and in peridomiciliary surroundings. At both areas L. whitmani was predominant, and was present in each type of collection. This finding supports previous studies, in the States of Sao Paulo (Barretto 1943, Forattini 1960, Taniguchi et al. 1991), Minas Gerais (Mayrink et al. 1979), Bahia (Barretto et al. 1982, Vexenat et al. 1986) and Ceara (Azevedo & Rangel 1991), where L. whitmani was recorded in domestic habitats.

In spite of its high degree of anthropophily, L. whitmani is also attracted to domestic animals, suggesting its adaptation to the domestic habitat.

This sand fly species is considered a vector of Le. (V.) braziliensis in other endemic areas of northeast and southeast Brazil, where it enters dwellings places and sites near houses (Pessoa & Coutinho 1941, Mayrink et al. 1979, Azevedo et al. 1990, Queiroz et al. 1991). In Três Bracos, State of Bahia, the high percentage of L. whitmani inside houses and in peridomestic sites, associated with the presence of infected specimens with Le.(V.) braziliensis in peridomi-ciliary areas, suggests a domestic or peridomestic transmission cycle of ACL (Hoch et al. 1986, Ryan et al. 1990).

Because the primary forest in this area has been replaced by several types of agriculture, mostly cocoa tree cultivation, we suggest that domestic and peridomestic transmission is occuring. Although no natural infection of Leishmania was found in L. whitmani, our studies suggest that this sand fly species is the vector because it feeds readily on humans and is the predominant species in domestic and peridomestic sites, where a peridomestic transmission cycle involving a domestic reservoir may be occurring. On the other hand, we cannot dismiss the likelihood that transmission may also occur in cocoa plantations, indicating, that it is also an occupational disease.

Recently, Rangel (1993) studied L. whitmani by comparing populations from States of Para, Ceara and Bahia. Sand flies from these areas are morphologically very similar but have distinct behaviorial characteristics. When the author used morphometric characters, genomic DNA fragments as diagnostic probes and phylogenetic analysis, this survey showed strong evidence that there are at least two distinctive forms of this sand fly species, that are geographically isolated: one occurrring in State of Pará (north Brazil) and the other in northeast Brazil (States of Ceara and Bahia, including Ilheus, this type locality). This suggests the possibility that these two forms are involved in the transmission of ACL in two different environments.

We found two other sand fly species in Ilheus, L. intermedia and L. migonei, which are involved in the transmission of ACL due to Le. (V.) braziliensis in other states from northeast and southeast Brazil (Araújo Filho 1979, Rangel et al. 1984, 1986, 1990, Azevedo et al. 1990). In the present study area, these species are uncommon and we believe that they are not transmiting the disease to man.

ACKNOWLEDGEMENTS

To Jorair Souza e Silva, Eliesio Bezerra da Silva, Augustinho Freire Demetrio, Moacir Vieira de Oliveira, Paulo Raimundo Barbosa and Antonio Carlos Conceica Menezes, technicians from Fundacao Nacional de Saude, Brazil for support in field works.

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Received 19 January 1995

Accepted 18 September 1995

Copyright 1995 Fundacao Oswaldo Cruz

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