Zootaxa 1078: 25–32 (2005) www.mapress.com/zootaxa/
ISSN 1175-5326 (print edition)
Copyright © 2005 Magnolia Press
ISSN 1175-5334 (online edition)
ZOOTAXA
Sand flies (Diptera: Psychodidae) in Pernambuco State, northeastern Brazil: The presence of species incriminated as vectors of cutaneous leishmaniasis in the Amazon region V. Q. BALBINO1, M. S. ANDRADE4, I. COUTINHO-ABREU1, I. V. SONODA1, C. B. MARCONDES2, J. J. SHAW3 & S. P. BRANDÃO-FILHO4 1
Departamento de Genética, Universidade Federal de Pernambuco, 50732-970 Recife, Pernambuco, Brazil, e-mail:
[email protected] 2 Departamento de Microbiologia e Parasitologia, Universidade Federal de Santa Catarina, 88040-900 Florianópolis, Santa Catarina, Brazil, e-mail:
[email protected] 3 Departamento de Parasitologia, Universidade de São Paulo, São Paulo, E-mail:
[email protected] 4 Centro de Pesquisas Aggeu Magalhães, Fundação Oswaldo Cruz, 50670-420 Recife, Pernambuco, Brazil, E-mail:
[email protected] (corresponding author)
Abstract A total of 83,499 phlebotomine sand flies belonging to 23 species were captured in CDC light traps and from humans in three areas of the northeastern coastal region of Pernambuco State, Brazil. Two species had not been recorded previously from this region but have been incriminated as vectors of dermal leishmaniasis in the Amazon region. Lutzomyia claustrei, associated with the parasite Leishmania (Viannia) naiffi, and Lutzomyia flaviscutellata, associated with Leishmania (Leishmania) amazonensis, were captured in a small area of residual forest in the area of Recife. A third species, Lutzomyia complexa, which is considered a vector of Leishmania (V.) braziliensis, was also taken in the same forest, as well as in similar habitats of the municipalities of Amaraji and Paudalho. The commonest species in each locality were, respectively, Lutzomyia umbratilis, Lutzomyia whitmani, and Lutzomyia complexa. All are important vectors of the agents of leishmaniasis in the Amazon region. Key words: Phlebotominae, sand fly, Lutzomyia umbratilis, Lutzomyia complexa, Lutzomyia claustrei, Lutzomyia flaviscutellata, Lutzomyia whitmani, cutaneous leishmaniasis, Amazon, Brazil
Introduction Many phlebotomine sand fly species have been incriminated in the transmission of zoonotic cutaneous leishmaniasis on the American continent (Marcondes 2001, p. 26; Shaw 2002), and there is both epidemiological and experimental evidence of vectorAccepted by P. Adler: 29 Sept. 2005; published: 7 Nov. 2005
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parasite specificity. The enzootic cycle depends on intimate sand fly-reservoir contact and is considered a major factor limiting the geographical distribution of the disease. Experimental evidence also links vector-parasite specificity with leishmanial promastigote surface receptors, such as lipophosphoglycans (Sacks & Kamhawi 2001) and galactins of the sand fly’s intestinal wall (Kamhawi et al. 2004). Finding a species previously reported as a vector in a new region does not necessarily mean that it is transmitting the same parasite in this area; detailed ecological studies are required to determine its vectorial importance. Lutzomyia umbratilis, previously incriminated as the principal vector of Leishmania (Viannia) guyanensis in the Amazon Basin (Arias & Freitas 1978, Lainson et al. 1981) north of the Amazon River, was recently collected (Balbino et al. 2001) in the Recife area of Pernambuco State, in the extreme eastern part of northeastern Brazil. Lutzomyia complexa, a vector of L. (V.) braziliensis in eastern Amazonia (Souza et al. 1996), was collected (Andrade et al. 2005) in the ‘Zona da Mata’ region of Pernambuco where the occurrence of cutaneous leishmaniasis is common (Brandão-Filho et al. 1999, Brandão-Filho 2001). Lutzomyia flaviscutellata is a vector of L. (L.) amazonensis (Lainson & Shaw 1972), and L. (V.) naiffi has been found in Lutzomyia claustrei (Lainson & Shaw 1989). In the present paper, we discuss the presence and importance of these three vectors species in areas of Recife and ‘Zona da Mata’ of Pernambuco State, northeastern Brazil.
Materials and methods Studies were performed in three areas of Pernambuco State. Recife (8o 3’14’’S 34o52’52’’W, 4 m above sea level), which is the State’s capital, is situated on the coast. Its climate is hot, humid, and tropical with a mean temperature of 27 oC, a minimum temperature 18 oC, and an annual rainfall of 2,000 mm. Phlebotomine sand flies of this area were caught in the “Reserva Ecológica de Dois Irmãos,” which is situated in the western zone of the city. This nature reserve (400 hectares = 988.4 acres) has two lakes surrounded by secondary forest. The forest is very wet, especially during the rainy season (April-September). The reserve houses a small zoo, as well as some squatters, and is surrounded by a densely populated urban area that includes slums and shantytowns. Sand flies that were attracted to humans were collected from September 2002 to August 2004 with a hand-held aspirator and a killing bottle. Catches were made weekly during a 25minute period, starting one hour after sunset. This particular time was chosen because preliminary 24-hour observations had shown it was the period of highest activity. Amaraji (8o22’59’’S 35o27’09’’W, 289 m a.s.l.) and Paudalho (7o53’48’’S 35o10’47’’W, 69.5 m a.s.l.) are municipalities in the ‘Zona da Mata’ region, some 90 and 50 kilometers from Recife, respectively. In Amaraji, small patches of rain forest are surrounded by extensive areas of sugar cane and banana plantations, which are the predominant cash crops. Sand flies were captured manually and with CDC light traps in
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and around houses and animal sheds during four consecutive nights of each month, between 1996 and 1999. The conservation of the rain forest in Paudalho is superior to that of Amaraji, and it has a jungle warfare training center for the Brazilian army. Sand fly captures were performed in this area during 2002-2003, using CDC light traps and manual captures on four consecutive nights of each month in the primary and secondary forests. A number of soldiers contracted cutaneous leishmaniasis during military exercises in these forested areas. Sand flies were identified using the descriptions and keys of Young & Duncan (1994). The insects from Recife were deposited in the collection of the Departamento de Genética, Universidade Federal de Pernambuco (Recife, Pernambuco). Specimens from Amaraji and Paudalho were deposited in the Centro de Pesquisas Aggeu Magalhães, Fundação Oswaldo Cruz (Recife, Pernambuco). Some voucher specimens were sent to the Departamento de Parasitologia, Universidade de São Paulo (Dr J. J. Shaw), São Paulo, and the Departamento de Epidemiologia (Dr. E. A. B. Galati), USP, São Paulo.
Results A total of 83,499 specimens belonging to 23 Lutzomyia species were collected in the three areas (Table 1). Collections at Dois Irmãos (Recife) produced 10,287 sand flies of 10 species, of which 9,929 (96.5%, 2482 males, 7447 females) were L. umbratilis. Among the other species, 48 (1.13% of total, 3 males, 45 females) were identified as L. flaviscutellata, 35 (0.82%, 7 males, 28 females) as L. complexa, and 63 (1.48%, 20 males, 43 females) as L. claustrei. The 64,806 sand flies captured in Amaraji belonged to 8 species, of which 403 (0.62%) were L. complexa. Of the overall total, 97.84% were L. whitmani (Antunes & Coutinho), followed in order of predominance by L. evandroi (Costa Lima & Antunes), L. quinquefer (Dyar), L. walkeri (Newstead), L. sordelli (Shannon & Del Ponte), L. fischeri (Pinto), and L. naftalekatzi Falcão, Andrade Filho, Almeida & Brandão Filho. Sixteen species were captured in Paudalho, and of these, the dominant species was L. complexa, which represented 51.36% (4,317 of 8,406) of the total captured at this locality. Of the three study sites, Paudalho yielded the greatest variety of sand fly species.
Discussion Lutzomyia flaviscutellata was rare in the Recife collections. In studies carried out in the Amazonian region, this same species was not considered especially anthropophilic, preferring rodents (Lainson & Shaw 1968, Shaw & Lainson 1968). Populations of this species are particularly high in wet forests, especially those such as the “igapo” (i.e., seasonally flooded) (Shaw & Lainson 1972). This species readily adapts to modified forests and monoculture tree plantations (“gmelin”) in the north of Pará State (Ready et al. SAND FLIES
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1983). This adaptive ability suggests that L. flaviscutellata could spread to other areas of Pernambuco, where different types of vegetation have replaced the original Atlantic rain forest. Due to the close relationship of L. flaviscutellata with rodents, the mammalian fauna of the Recife site needs to be thoroughly investigated. Studies by other methods, such as rodent-baited traps (Disney 1966, Dégallier et al. 1983), probably would result in higher catches of L. flaviscutellata in this area. Dois Irmãos is very humid, and in the lower areas, the ground is flooded during and just after the rainy season, a situation similar to the habitats in which this species abounds in Pará. This same species was reported in the southern region of the State of Bahia in an area where L. (L.) amazonensis has been found. However, because there are no parasitological studies of leishmanial infections of this species in this region, its importance as a vector in this region of Brazil is only circumstantial (Vexenat et al. 1986). TABLE 1. Numbers of individuals of sand fly species (Lutzomyia species) collected in three study areas of Pernambuco State, Northeast Brazil, including totals by sex and male (M):female (F) ratios.
Species L. amazonensis
M
Amaraji F T
%
M/F
Localities Paudalho M F %
M/F
M
Recife F %
M/F
-
-
-
-
-
52
143
2.32
0.36
-
-
-
-
L. barrettoi
-
-
-
-
-
0
1
0.01
0
-
-
-
-
L. braziliensis
-
-
-
-
-
0
2
0.02
0
-
-
-
-
L. capixaba
-
-
-
-
-
0
8
0.10
0
-
-
-
-
L. choti
-
-
-
-
-
1,955
L. claustrei
-
-
-
-
-
-
L. complexa
172
231
403
0.62
0.74
462
L. evandroi
391
323
714
1.10
1.21
18
14
0.38
1.28
-
-
-
-
L. fischeri
6
9
15
0.02
0.67
-
-
-
-
-
-
-
-
L. flaviscutellata
-
-
-
-
-
-
-
-
-
3
45
0.47 0.07
L. furcata
-
-
-
-
-
-
-
-
-
7
5
1.18 1.40
L. longispina
-
-
-
-
-
36
58
1.12
0.62
-
-
1,705 43.54 1.15 -
-
-
3,855 51.36 0.89
19
18
0.36 1.05
20
43
0.61 0.46
7
28
0.34 0.25
-
-
L. naftalekatzi
-
-
-
-
-
2
4
0.07
0.50
-
-
-
-
L. quinquefer
27
35
62
0.10
0.77
0
1
0.01
0
-
-
-
-
L. sallesi
-
-
-
-
-
-
-
-
-
1
0
0.01
-
L. schreiberi
-
-
-
-
-
1
4
0.06
0.25
-
-
-
-
L. servulolimai
-
-
-
-
-
1
0
0.01
-
-
-
-
-
L. shannoni
-
-
-
-
-
-
-
-
-
123
32
1.51 3.84
L. sordelli
11
33
44
0.07
0.33
5
53
0.69
0.09
1
5
0.06 0.20
L. sp.
27
75
102
0.16
0.36
-
-
-
-
-
-
-
-
L. tupynambai
0
0
0
0
0
0
1
0.01
-
-
-
-
-
-
-
-
-
-
-
-
-
-
26
34
60
0.09
0.76
16
08
0.29
2.00
1
0
0.01
-
L. whitmani
28,354 35,052 63,406 97.84
0.81
0
1
0.01
0
-
-
-
-
Total
29,014 35,792 64,806 100.0
0.81
2548
5858
L. umbratilis L. walkeri
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100.0 0.43
2,273 7,656 96.52 0.30
2,455 7,832 100.0 0.31
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Lutzomyia complexa was incriminated as a vector of L. (V.) braziliensis in the State of Pará, where it is has an extensive geographical distribution (Souza et al. 1996), particularly in the eastern lowlands. This species is highly anthropophilic and preferentially bites humans rather than dogs or chickens (Campbell-Lendrun et al. 1999). Females of this species are morphologically similar to those of L. wellcomei (Frahia, Shaw & Lainson), but the males of these two species can be distinguished easily. Thus, the finding of only males of L. complexa means that the females caught in the same region as the males probably will be the same species. However, in areas where the two species are sympatric, females can be differentiated by multivariate analysis of morphological characters (Lane & Ready 1985), cuticular hydrocarbons (Ryan et al. 1986), and DNA probes (Ready et al. 1991). Lutzomyia complexa was more prevalent in the preserved forests (Paudalho) than in those disturbed by humans (Amaraji and Recife). Collection methods were not identical and might have accounted for differences in the prevalence of this species, although we think this is unlikely to have been the reason for the small numbers caught in Dois Irmãos Reserve. A recent study using CDC light traps by Silva & Vasconcelos (2005) failed to find L. complexa in the Dois Irmãos Reserve as well as in the reserves of Tapacura Mun.-São Lourenço da Mata, 8o00’08”S 35o01’06”W, 58 m a.s.l.), Curado (Mun.-Recife), and Charles Darwin (Mun.- Igarassu, 07o50’03”W, 20 m a.s.l.). All results to date suggest that L. complexa prefers larger areas of undisturbed, drier Atlantic rain forest. Another sand fly that has some morphological similarities with L. complexa is L. squamiventris. Lucena (1950) referred to the finding of “Phlebotomus squamiventris” in the states of Pernambuco and Paraíba; it certainly belongs to Psychodopygus Mangabeira. These specimens are not available so we cannot say to what species Lucena (1950) was referring. Lutzomyia wellcomei has been found in the State of Ceará (Ready et al. 1983), as well as in other areas of Northeast Brazil, and so Lucena’s “P. squamiventris” could be L. complexa and/or L. wellcomei. The specimens formerly identified as L. wellcomei in the Municipality of Paudalho (Brandão-Filho et al. 1998) were actually L. complexa (Andrade 2004). Although it is intriguing that Silva & Vasconcelos (2005) recorded L. wellcomei in the Charles Darwin Reserve, they did not justify their identification by stating that it was based on the morphology of male flies. If both species occur in the eastern region of Pernambuco, the identification of female sand flies of these species will be more difficult. Trypanosoma freitasi Rego, Magalhães & Siqueira and an undescribed Leishmania sp. were isolated from L. claustrei in Amazonia (Naiff et al. 1989, Ryan et al. 1987). This Leishmania species later was described as L. naiffi (Lainson & Shaw 1989). This parasite, although rare in humans, is widespread throughout South America (Pratlong et al. 2002). It also was isolated from L. hirsuta (Mangabeira) and L. davisi (Root), which also belong to the subgenus Psychodopygus, in the State of Rondonia (Gil et al. 2003). Lutzomyia claustrei and L. flaviscutellata are strongly attracted to armadillos (Dasypus novemcinctus (Linnaeus)) and guinea pigs (Cavia porcellus (Linnaeus)) in French Guyana (Le Pont
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1990), but there is no information on the attraction of L. claustrei to humans. The finding of natural infections and the susceptibility of these Recife insects to Leishmania require investigation. Although no reports of autochthonous human cases of dermal leishmaniasis were verified in the area of Recife, the possible circulation of leishmanial parasites in the semi-preserved forested areas of this municipality is possible. The phlebotomine sand fly fauna of the relics of the Atlantic rain forest in northeastern Brazil includes potentially important vector species. These species are the remnants of a rich sand fly fauna that was present in this habitat before it was devastated by humans. Its similarity to the phlebotomine fauna of the eastern Amazon region suggests that at some time there was a link between the two forests. Lutzomyia whitmani has flourished in the modified environment created by humans, as has L. intermedia in similar types of habitats in southern Brazil; both species are important vectors of L. (V.) braziliensis (Shaw 2002). With the addition of the two species recorded for the first time in the present paper (L. claustrei and L. flaviscutellata), there is now an impressive list of potential leishmanial vectors (L. ayrozai, L. umbratilis, L. complexa, L. furcata) in Pernambuco. In areas where the Atlantic rain forest is better preserved, the fauna includes species previously found to be infected with Leishmania in the Amazon Basin. Among these species are L. ayrozai (Barretto & Coutinho), L. yuilli (Young & Porter), and L. flaviscutellata in southern Bahia (Vexenat et al. 1986). Lutzomyia ayrozai also has been collected in São Paulo (Gomes et al. 1989), Pernambuco (Brandão-Filho et al. 1998), Paraná (Marcondes et al. 2001), Rio de Janeiro (Souza et al. 2001, Meneses et al. 2002), and Santa Catarina (Marcondes et al. 2005). Comparative studies of sand flies from different regions might reveal biological dissimilarities (e.g., in life cycle, fecundity, fertility, adult longevity, and emergence), as observed in L. umbratilis from two areas in the State of Amazonas separated by the Negro River (Justiniano et al. 2004). Studies of morphology, cuticular hydrocarbons, chromosomes, isoenzymes, and molecular markers, as well as susceptibility to parasites and cross-mating experiments of the populations of these species should reveal greater levels of heterogeneity.
References Andrade, M.S., Valença, H.F., Silva, A.L., Almeida, F.A., Almeida, E. L., Brito M.E.F & Brandão-Filho, S.P. (2005) Sand fly fauna in military training area endemic for American tegumentary leishmaniasis in Atlantic rain forest region of Pernambuco, Brazil. Cadernos de Saúde Pública, 21, 109–118. Arias, J.R., & Freitas, R.A. (1978) Sobre os vetores de leishmaniose cutânea na Amazônia central do Brasil. 2. Incidência de flagelados em flebótomos selváticos. Acta Amazonica, 8, 387–396. Balbino, V.Q., Marcondes, C.B., Alexander, B., Luna, L.K., Lucena, M.M., Mendes, A.C. & Andrade, P.P. (2001) First report of Lutzomyia (Nyssomyia) umbratilis Ward & Frahia, 1977 outside of Amazonian Region, in Recife, State of Pernambuco, Brazil (Diptera: Psychodidae: Phlebotominae). Memórias do Instituto Oswaldo Cruz, 96, 315–317.
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Brandão-Filho, S.P., Brito, M.E.F., Martins, C.A.P., Sommer, I.B., Valença, H.F., Almeida F. A. & Gomes, J. (1998) Leishmaniose tegumentar americana em centro de treinamento militar localizado na Zona da Mata de Pernambuco, Brasil. Revista da Sociedade Brasileira de Medicina Tropical, 31, 575–578. Brandão-Filho, S.P., Campbell-Lendrum, D.H., Brito, M.E.F., Shaw, J.J. & Davies, C.R. (1999) Epidemiological surveys confirm an increasing burden of cutaneous leishmaniasis in north-east Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene, 93, 488–494. Brandão-Filho, S.P., Brito, M.E.F., Carvalho, F.G., Ishikawa, E.A., Floeter-Winter, L.M. & Shaw, J.J. (2003) Wild and synanthropic hosts of Leishmania (Viannia) braziliensis in the endemic cutaneous leishmaniasis locality of Amaraji, Pernambuco State, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene, 97, 291–296. Campbell-Lendrum, D.H., Pinto, M.C., Brandão-Filho, S.P., Souza, A.A., Ready, P.D. & Davies, C.R. (1999) Experimental comparison of anthropophily between geographically dispersed populations of Lutzomyia whitmani (Diptera: Psychodidae). Medical and Veterinary Entomology, 13, 299–309. Dégallier, N., Le Pont, F. & Claustre, J. (1983) Description of an animal-baited mosquito trap used in French Guiana. Cahiers ORSTOM Séries Entomologie Médicale et Parasitologie, 21, 103–110. Disney, R.H.L. (1966) A trap for phlebotomine sand flies attracted to rats. Bulletin of Entomological Research, 56, 445–451. Gil, L.H., Basano, S.A., Souza, A.A., Silva, M.G., Barata, I., Ishikawa, E.A., Camargo, L.M. & Shaw, J.J. (2003) Recent observations on the sand fly (Diptera: Psychodidae) fauna of the State of Rondonia, Western Amazonia, Brazil: the importance of Psychodopygus davisi as a vector of zoonotic cutaneous leishmaniasis. Memórias do Instituto Oswaldo Cruz, 98, 751–755. Gomes, A.C., Barata, J.M., Rocha e Silva, E.O. & Galati, E.A. (1989). Aspectos ecológicos da leishmaniose tegumentar americana. 6. Fauna flebotomínea antropófila de matas residuais situadas na região centronordeste do Estado de São Paulo- Brasil. Revista do Instituto de Medicina Tropical de São Paulo, 31, 32–39. Justiniano, S.C., Chagas, A.C., Pessoa, F.A. & Queiroz, R.G. (2004). Comparative biology of two populations of Lutzomyia umbratilis (Diptera: Psychodidae) of Central Amazonia, Brazil, under laboratory conditions. Brazilian Journal of Biology, 64, 227–235. Kamhawi, S., Ramalho-Ortigão, M., Pham, V.M., Kumar, S., Lawyer, P.G., Turco, S.J., Barillas-Mury, C., Sacks, D.L. & Valenzuela, J.G. (2004) A role for insect galectins in parasite survival. Cell, 119, 329–341. Lainson, R. & Shaw, J.J. (1968) Leishmaniasis in Brazil: I – Observations on enzootic rodent leishmaniasis – incrimination of Lutzomyia flaviscutellata (Mangabeira) as the vector in the lower Amazonian basin. Transactions of the Royal Society of Tropical Medicine and Hygiene, 63, 385–395. Lainson, R. & Shaw, J. J. (1989) Leishmania (Viannia) naiffi sp. n. a parasite of the armadillo, Dasypus novencinctus (L.), in Amazonian Brazil. Annales de Parasitologie Humaine et Comparée, 64, 3–9. Lane, R.P. & Ready, P.D. (1985) Multivariate discrimination between Lutzomyia wellcomei, a vector of mucocutaneous leishmaniasis, and L. complexus (Diptera: Phlebotominae). Annals of Tropical Medicine and Parasitology, 79, 469–472. Le Pont, F. (1990) Attractivité du tatou (Dasypus novemcinctus L.) et des cobayes pour les phlébotomes en Guyane Française. Bulletin de la Societé de Pathologie Exotique, 83, 671–676. Lucena, D.T. (1950) Flebótomos do nordeste. Contribuição para o conhecimento de sua distribuição geográfica. Boletim da Secretaria de Agricultura Indústria Comércio, 17, 184–191. Marcondes, C.B. (2001) Entomologia Médica e Veterinária. Editora Atheneu, São Paulo, Brazil, 432 pp. Marcondes, C.B., Conceição, M.B.E., Portes, M.G.E. & Simão, B.P. (2005) Phlebotomine sandflies in a focus of dermal leishmaniasis in the eastern region of the Brazilian State of Santa Catarina – preliminary results. Revista da Sociedade Brasileira de Medicina Tropical, 38, 353–355. Marcondes, C.B., Santos-Neto, L.G. & Lozovei, A.L. (2001) Ecology of Phlebotomine sandflies (Diptera, Psychodidae) in Brazilian Atlantic Forest. Revista da Sociedade Brasileira de Medicina Tropical, 34, 255–260. Meneses, C.R., Azevedo, A.C., Costa, S.M., Costa, W.A. & Rangel, E.F. (2002) Journal of Vector Ecology, 27, 207–214.
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