Distribution of Lutzomyia Whitmani in Phytoregions of the State of Maranhão, Northeastern Brazil

The study had the aim of characterizing the geographical distribution of Lutzomyia whitmani s.9% females) were caught in the rural and urban zones of 35 municipalities in regions consisting of forests, savanna and mixed vegetation with coconut plantations, sandbanks and heath. Greater abundance was observed in areas surrounding dwellings (91.6%) than inside the dwellings (8.4%). The presence of the vector in different phytoregions and in rural and urban areas favors the transmission of tegumentary leishmaniasis in these environments. This taxon may constitute a complex of species in Maranhão, which can be confirmed by molecular biology studies. 2 Lutzomyia whitmani in Maranhão state, Brazil Rebêlo JMM et al Lutzomyia (Nyssomyia) whitmani sensu lato is an important element of the South American phlebotomine fauna and there are records of its distribution in French Guiana, Argentina, Paraguay and Peru. In Brazil, this taxon occurs in all geographical regions, 1 although there are no records from the states of Amapá, Amazonas, Roraima and Santa Catarina. In the Amazon region, this taxon may be essentially of wild type and zoophilic in forested areas. In the northeastern region, it is associated with anthropo-genic areas and may exhibit both anthropophilic and zoophilic behavior. This variation in behavior has led to the hypothesis that this taxon consists of a complex of cryptic species 2,4 or different phylogenetic lineages that inhabit the bioclimatic zones of the Amazon forest, savanna (cerrado region) and Atlantic forest. 5 In the state of Maranhão, L. whitmani s.l. exhibits characteristics that are intermediate between the Amazon and extra-Amazon populations, and it can be found both in wild environments and in rural and urban peridomestic environments. However, the populations distributed in the different geographical and vegetation regions of Maranhão have not yet been studied with regard to the lineages that belong to these regions, except for the population found in forest and perido-mestic environments in the municipality of Buriticupu, in the west of the state, which belongs to the Amazon lineage. 5 Definition of the lineages may clarify the distribution pattern of this taxon and its association with Leishmania species in Maranhão. The aim of the present study was to characterize the distribution of L. whitmani s.l. in foci of leishmaniasis in different phytoregions. MeTHoDS The study was conducted between 1992 and 2005 in 43 municipalities located in the northeast and southwest of Maranhão, Northeastern Brazil, covering three tropical climatic zones (hot and moist, semi-moist …

Lutzomyia (Nyssomyia) whitmani sensu lato is an important element of the South American phlebotomine fauna and there are records of its distribution in French Guiana, Argentina, Paraguay and Peru.In Brazil, this taxon occurs in all geographical regions, 1 although there are no records from the states of Amapá, Amazonas, Roraima and Santa Catarina.
In the Amazon region, this taxon may be essentially of wild type and zoophilic in forested areas.In the northeastern region, it is associated with anthropogenic areas and may exhibit both anthropophilic and zoophilic behavior.This variation in behavior has led to the hypothesis that this taxon consists of a complex of cryptic species 2,4 or different phylogenetic lineages that inhabit the bioclimatic zones of the Amazon forest, savanna (cerrado region) and Atlantic forest. 5 the state of Maranhão, L. whitmani s.l.exhibits characteristics that are intermediate between the Amazon and extra-Amazon populations, and it can be found both in wild environments and in rural and urban peridomestic environments.However, the populations distributed in the different geographical and vegetation regions of Maranhão have not yet been studied with regard to the lineages that belong to these regions, except for the population found in forest and peridomestic environments in the municipality of Buriticupu, in the west of the state, which belongs to the Amazon lineage. 5Definition of the lineages may clarify the distribution pattern of this taxon and its association with Leishmania species in Maranhão.
The aim of the present study was to characterize the distribution of L. whitmani s.l. in foci of leishmaniasis in different phytoregions.

MeTHoDS
The study was conducted between 1992 and 2005 in 43 municipalities located in the northeast and southwest of Maranhão, Northeastern Brazil, covering three tropical climatic zones (hot and moist, semi-moist and semi-arid) and the following phytoregions: open evergreen seasonal forest, dense evergreen seasonal forest, ombrophilous forest, savanna (cerrado), sandbank, palm forest and scrub heath (caatinga).The specimens were caught using illuminated traps of CDC type, which were installed inside homes and in shelters for domestic animals, in the rural zone and urban periphery, between the hours of 6:00 pm and 6:00 am.The number of traps used varied from two to 20 and the number of hours worked varied from 120 to 1,440, according to the municipality: Paço do Lumiar,

INTRoDUCTIoN
a The map showing species occurrence can be consulted in the online version of this paper.

ReSULTS
Lutzomyia whitmani s.l. was found in 35 municipalities that had cases of tegumentary leishmaniasis (TL).a It was distributed between all of the phytogeographical zones of the state, from the dense and moist forest of Amazon origin to the more xeric areas (semi-moist and semiarid), including mixed areas of these vegetation types.
In total, 9,600 specimens of L. whitmani s.l. were caught, with greater frequency in areas surrounding homes (91.6%) than inside homes (8.4%) (Table ).Male specimens predominated, both inside homes (64.5%) and in areas surrounding them (65.2%).This taxon was not found predominantly in any particular phytogeographical zone.However, within each zone, there were some municipalities with very low frequencies of specimens and others with high frequencies (Table ).The mean number of specimens caught per trap/hour was greatest in the municipalities of Buriticupu (7), Dom Pedro (6.8), Barreirinhas (5.8), Imperatriz (4.7), Senador La Roque (4.3), Timon (3), Governador Edson Lobão (1.5), São Luís (1.4), Porto Franco (1.2), Santo Amaro (1.2) and Grajaú (1.1).Despite the differences in structure and physical appearance of the vegetation and in climatic types in the state, L. whitmani s.l. was found indiscriminately in the peridomestic environment in all of the municipalities.However, this taxon was recorded inside homes in only 12 municipalities (Table ).It was also caught within the urban area of ten municipalities: Amarante, Barreirinhas, Carolina, Caxias, Coelho Neto, Dom Pedro, Formosa Serra Negra, Imperatriz, Lageado Novo and Timon, which are located in different geographical areas that are ecologically distinct.

DISCUSSIoN
Previous studies have shown that in the Amazon phytogeographical region of Maranhão, L. whitmani s.l.To be continued inhabits both wild environments and rural peridomestic areas, and it has been found to be naturally infected with Leishmania. 3 A similar behavioral pattern is observed in the northeastern part of the state.It is therefore pertinent to investigate whether the distribution pattern of this taxon has modified the epidemiological profile of TL transmission in Maranhão.Hence, it is possible that this vector may be transmitting L. shawi in the Amazon region of the state and L. braziliensis in the northeastern region of the state, as observed in the states of Pará 6 and Ceará, 7 respectively.
The open evergreen seasonal forest of Amazon origin formerly extended further east and mixed with the palm forest and savanna in the areas between the Itapecuru and Parnaíba rivers, where the climate is more xeric.Before the intensive process of deforestation, the original forest may have served as a corridor for dispersion of vector populations from west to east.In this case, the possibility that L. (N.) whitmani s.l.might also have transmitted L. shawi in the northeastern region of the state, bordering Piauí, would not be ruled out.Subsequently, the populations of this insect in the open areas (caatinga scrub heath, savanna and palm forest) would have had the opportunity to make the journey in reverse, from east to west, favored by the progressive increase in deforestation of the Amazon forest type, which has been replaced by palm forests and rough pasture.This latter possibility sustains the hypothesis of Ready et al 5 that the peridomestic habit of the vector in Buriticupu (in the Amazon area) resulted from the gene flow of extra-Amazon lineage.In this case, it can be suggested that the L. whitmani population of the Amazon region of Maranhão may also transmit L. braziliensis.
In summary, the results from the present study show that L. whitmani s.l.occurs in all regions of the state in which entomological surveys have been conducted.However, because of the large area covered by the state of Maranhão, many municipalities have still not been studied in this respect, particularly in the northwest and southeast of the state, where the phlebotomine fauna remains unknown.Nevertheless, three points reinforce the hypothesis that this taxon consists of a complex of species in Maranhão: 1) its occurrence in different phytogeographical and climatic regions; 2) its frequent presence in wild and rural environments and its dispersion in the main settlements of some smallsized municipalities, independent of the region; and 3) its proliferation in the urban areas of medium-sized municipalities (with more than 100,000 inhabitants) in the northeast of the state.This hypothesis may be confirmed through future molecular biology studies.

Table .
Specimens of Lutzomyia whitmani sensu lato caught in peridomestic environments and inside homes, according to phytoregion.State of Maranhão, Northern Brazil, 1992 to 2005.