**3.** *Lutzomyia* **(***Nyssomyia***)** *flaviscutellata* **(Mangabeira 1942)**

This species was also observed in Atlantic Forest protected areas and inside houses near the forest in Rio de Janeiro state [33]. In the same state, studies performed in rural areas of ACL transmission showed the co-occurrence of *L. (N.) intermedia* and *L. (N.) whitmani* biting humans. In peridomestic areas, *L. (N). intermedia* was predominant, while *L. (N.) whitmani* was more frequent in the nearest forest. With this spatial separation, the authors suggested that both species would be sharing *Leishmania (V.) braziliensis* transmission on the same focus, through‐ out the year. *Lutzomyia (N.) whitmani* was captured during all year, but was more frequent in

Also in Southeast region, besides São Paulo and Rio de Janeiro states, *L. (N.) whitmani* was associated with *Leishmania (Viannia) braziliensis* transmission in Caratinga (Minas Gerais state)

In South Brazil, *L. (N.) whitmani* is probably associated to ACL transmission in Paraná state. Studies performed in the north of this state detected it as predominant sand fly species and

*Leishmania (V.) braziliensis* in Northeast region is also probably transmitted by *L. (N.) whitma‐ ni*. In Bahia and Ceará states this vector shows similar habits to the Southeast region popula‐ tions: high anthropophily and presence in domestic areas [38-40]. In Ceará state, *L. (N.) whitmani* was found naturally infected by *Leishmania* of *Viannia* subgenus [41]. Afterwards, new infections were detected and the parasite characterization confirmed to be *Leishmania (V.) braziliensis* [42]. Other evidences of this vector's role in ACL transmission in the region were

In Bahia state, *L. (N.) whitmani* was found naturally infected by *Leishmania (V.) braziliensis* in Três Braços [43]. This finding, associated with the high frequency of this sand fly in perido‐ mestic and domestic areas allowed the hypothesis of occurrence of a domestic transmission cycle in this area [44]. In Ilhéus municipality, *L. (N.) whitmani* was suggested as ACL vector, considering its almost absolute predominance over other sand fly species (99.7%), its high anthropophily and its occurrence on every sand fly capture point, most of them coincident

In the Mid-West Region, in Corguinho municipality (Mato Grosso do Sul state), *Leishmania (V.) braziliensis* was isolated from every tested ACL patient by monoclonal antibodies. *Lutzomyia (N.) whitmani* was suggested as vector because it was observed in high abundances and anthropophilic [45]. Furthermore, its predominance over other sand flies was observed in eight of ten ecotopes studied in the locality. *Lutzomyia (N.) whitmani* was present both in ground level and in the forest canopy, suggesting its eclectic feeding habits on mammals and birds. Although in this locality the species is not very common in peridomestic areas, its high abundance and anthropophily are strong evidences of its role in ACL transmission [46].

The behavior of *L. (N.) whitmani* in North region seems to be different from other regions. In these areas, the species was considered mainly sylvatic, being captured on tree trunks and canopies, besides showing low attractiveness for humans [47]. Afterwards, novel studies confirmed such observations and suggested that, if the species were to be anthropophilic, it would be only in some situations [48, 49]. In 1989, in Pará state, a parasite was isolated from

and in a mountainous region of Afonso Cláudio (Espírito Santo state) [35, 36].

naturally infected by *Leishmania (V.) braziliensis* parasites [37].

its high abundance and anthropophily [40, 42].

with areas of ACL human cases [40].

months with lower temperatures [34].

10 Leishmaniasis - Trends in Epidemiology, Diagnosis and Treatment

*Lutzomyia (N.) flaviscutellata* was described by Mangabeira [51] as *Flebotomus flaviscutellatus*, based on two male specimens captured in Belém (Pará state). Later, Sherlock & Carneiro [52] described a female collected in Salvador (Bahia state), although its identification has been questioned by several authors [18, 27, 53]. At the same time, the species *Phlebotomus apicalis* was described by Floch & Abonnenc [54] in French Guiana. Three years later, after a review of the specimens, *P. apicalis* was considered synonym of *L. (N.) flaviscutellata* [55].

In the following years, descriptions of *L. (N.) olmeca* [56], *L. (N.) olmeca bicolor* [53] and *L. (N.) olmeca nociva* [57], all of them morphologically similar to *L. (N.) flaviscutellata*, led some authors to consider these four species as the "*L. flaviscutellata* complex" [58]. However, they are all currently considered valid species, with more recent taxonomic reviews supporting their status [18, 59].

*Lutzomyia (N.) flaviscutellata* is currently widely distributed across Latin America, occurring in Bolivia, Brazil, Colombia, Ecuador, French Guiana, Peru, Suriname, Trinidad and Venezuela [7, 18].

This sand fly species is associated with *Leishmania (Leishmania) amazonensis* transmission in Brazil. This parasite, when infecting humans, can cause localized cutaneous lesions and eventually develop a more severe clinical form, diffuse cutaneous leishmaniasis (DCL). This clinical form is rare, with chronic development, where the immunodepressed patient shows frequent relapses and insufficient responses to available therapies [60].

The first observation of this sand fly's role in ACL transmission cycle was from a study in the Utinga forest, an Amazon area in Belém municipality (Pará state) [61]. In this area, wild rodents of *Proechimys* and *Oryzomys* genus were captured with cutaneous lesions on tails and feet, from where *Leishmania* parasites were isolated. These rodents were then used as baits and 98% of captured sand flies were *L. (N.) flaviscutellata*. Captured sand flies were dissected and flagel‐ lates were isolated from eight females.

Studies of the feeding habits of *L. (N.) flaviscutellata* showed higher preference for small sylvatic rodents (*Proechimys* sp., *Oryzomys* sp.), agoutis (*Dasyprocta* sp.) and porcupines (*Coendou* sp.), having the species also fed on opossums (*Philander* sp.), monkeys (*Saimiri* sp.) and chickens (*Gallus gallus*). Few females fed on humans, so the authors considered the species as having low anthropophily [62]. This preference for biting small rodents indicates that captures of this species tend to be more efficient when using animal baited traps, such as the Disney trap [63].

Despite its strong zoophilic habits and low anthropophily, *Lutzomyia (N.) flaviscutellata* has recently been captured in peridomestic areas, suggesting its dispersion to human dwellings [64-67]. This hypothesis is plausible, since the species also occurs in secondary forests in the Amazon. In a study performed in the late 1980s in Pará state, *L. (N.) flaviscutellata* was the predominant sand fly species in an area where the primary forest was replaced with exotic trees (*Pinus* and *Gmelina*), with occasional captures in peridomestic areas of houses near the forest [68]. In a review of the Amazonian ACL transmission cycles, *L. (N.) flaviscutellata* was considered one of the few vector species that could adapt to deforestation and become peridomestic [69].

In Brazil, *L. (N.) flaviscutellata* was detected in 131 municipalities, mostly in North and Mid-West regions, with occurrences also in Southwest and Northeast regions (Figure 5).

*Lutzomya (N.) flaviscutellata* is considered mainly an Amazonian species, although it can also be found in Cerrado and some few occurrences were recorded in Atlantic Forest, Caatinga and Pantanal (Figure 6).

In the Amazon, *L. (N.) flaviscutellata* is more commonly found in seasonally flooded areas of "igapó forests", when compared with non-flooded areas of "terra-firme forests" [70]. Its vertical distribution was also studied in the Amazon. The species has a very low flight, with 26 times more specimens captured 0.2 meters above ground than at 1.2 meters. This observa‐ tion reinforces its association with small rodents and the fact that human cutaneous lesions caused by *Leishmania (L.) amazonensis* are mainly located in the lowest parts of the body [71].

The species was also captured in peridomestic areas of Manaus (Amazonas state) [72], Ilha de Marajó (Pará state) [73] and Santarém (Pará state) [74]. Other examples of surveyed Amazon forest areas of the North region with records of *L. (N.) flaviscutellata* include the states: Acre [75, 76], Amazonas [13, 76-79], Amapá [80], Pará [61, 62, 68, 70, 81], Rondônia [82, 83] and Roraima [84, 85].

Also in the North region, Tocantins state has most of its area covered by Cerrado. It was in this biome that *L. (N.) flaviscutellata* was captured during a four-year sand fly fauna monitoring in the ACL endemic areas of Porto Nacional and Guaraí municipalities. This vector species was found in peridomestic captures in rural settlements and periurban areas [66, 67] and was suggested as *Leishmania (L.) amazonensis* vector in Porto Nacional [66]. In municipalities of the south of the same state, *L. (N.) flaviscutellata* was captured near houses in areas directly and indirectly impacted by a hydroelectric power plant construction in Tocantins River [86].

In Bela Vista municipality (Mato Grosso do Sul State, Mid-West region), an ACL outbreak associated with *Leishmania (L.) amazonensis* in a military training unit led to a sand fly fauna monitoring during years 2004 to 2006. Using light traps, few specimens of *L. (N.) flaviscutella‐ ta* were caught [87]. When a modified Disney trap baited with hamsters (*Mesocricetus auratus*) was used, *L. (N.) flaviscutellata* was the species with the highest female abundance [88]. Despite its capture with these methodologies, some females were also captured in white and black Shannon traps [89], suggesting that the species can also feed on humans, and therefore be a possible *Leishmania (L.) amazonensis* vector in this locality [87].

The sand fly fauna of an ecotourism area in Bonito (Mato Grosso do Sul state) was studied. In Cerrado areas, *L. (N.) flaviscutellata* was caught with light traps mainly inside the forest, but it was also found in yards and kennels of houses [64].

Environmental Changes and the Geographic Spreading of American Cutaneous Leishmaniasis in Brazil http://dx.doi.org/10.5772/57207 13

Amazon. In a study performed in the late 1980s in Pará state, *L. (N.) flaviscutellata* was the predominant sand fly species in an area where the primary forest was replaced with exotic trees (*Pinus* and *Gmelina*), with occasional captures in peridomestic areas of houses near the forest [68]. In a review of the Amazonian ACL transmission cycles, *L. (N.) flaviscutellata* was considered one of the few vector species that could adapt to deforestation and become

In Brazil, *L. (N.) flaviscutellata* was detected in 131 municipalities, mostly in North and Mid-

*Lutzomya (N.) flaviscutellata* is considered mainly an Amazonian species, although it can also be found in Cerrado and some few occurrences were recorded in Atlantic Forest, Caatinga and

In the Amazon, *L. (N.) flaviscutellata* is more commonly found in seasonally flooded areas of "igapó forests", when compared with non-flooded areas of "terra-firme forests" [70]. Its vertical distribution was also studied in the Amazon. The species has a very low flight, with 26 times more specimens captured 0.2 meters above ground than at 1.2 meters. This observa‐ tion reinforces its association with small rodents and the fact that human cutaneous lesions caused by *Leishmania (L.) amazonensis* are mainly located in the lowest parts of the body [71].

The species was also captured in peridomestic areas of Manaus (Amazonas state) [72], Ilha de Marajó (Pará state) [73] and Santarém (Pará state) [74]. Other examples of surveyed Amazon forest areas of the North region with records of *L. (N.) flaviscutellata* include the states: Acre [75, 76], Amazonas [13, 76-79], Amapá [80], Pará [61, 62, 68, 70, 81], Rondônia [82, 83] and Roraima

Also in the North region, Tocantins state has most of its area covered by Cerrado. It was in this biome that *L. (N.) flaviscutellata* was captured during a four-year sand fly fauna monitoring in the ACL endemic areas of Porto Nacional and Guaraí municipalities. This vector species was found in peridomestic captures in rural settlements and periurban areas [66, 67] and was suggested as *Leishmania (L.) amazonensis* vector in Porto Nacional [66]. In municipalities of the south of the same state, *L. (N.) flaviscutellata* was captured near houses in areas directly and indirectly impacted by a hydroelectric power plant construction in Tocantins River [86].

In Bela Vista municipality (Mato Grosso do Sul State, Mid-West region), an ACL outbreak associated with *Leishmania (L.) amazonensis* in a military training unit led to a sand fly fauna monitoring during years 2004 to 2006. Using light traps, few specimens of *L. (N.) flaviscutella‐ ta* were caught [87]. When a modified Disney trap baited with hamsters (*Mesocricetus auratus*) was used, *L. (N.) flaviscutellata* was the species with the highest female abundance [88]. Despite its capture with these methodologies, some females were also captured in white and black Shannon traps [89], suggesting that the species can also feed on humans, and therefore be a

The sand fly fauna of an ecotourism area in Bonito (Mato Grosso do Sul state) was studied. In Cerrado areas, *L. (N.) flaviscutellata* was caught with light traps mainly inside the forest, but it

possible *Leishmania (L.) amazonensis* vector in this locality [87].

was also found in yards and kennels of houses [64].

West regions, with occurrences also in Southwest and Northeast regions (Figure 5).

peridomestic [69].

12 Leishmaniasis - Trends in Epidemiology, Diagnosis and Treatment

Pantanal (Figure 6).

[84, 85].

**Figure 5.** Brazilian municipalities with *Lutzomyia (Nyssomyia) flaviscutellata* occurrence

**Figure 6.** Brazilian municipalities with *Lutzomyia (Nyssomyia) flaviscutellata* occurrence and biomes

In Southeast region, another ecotourism area was surveyed, in Rio de Janeiro state, Atlantic Forest biome. In Angra dos Reis municipality, the state's biggest continental island - Ilha Grande - has records of sporadic ACL cases since the first outbreak in the decade of 1970. At the time of the ACL outbreak, the sand fly fauna was monitored and *L. (N.) flaviscutellata* was captured inside the forest with Disney traps, baited with *Proechimys* rodents [90]. Over three decades later, the same localities were surveyed, and *L. (N.) flaviscutellata* was captured inside the forest and in peridomestic areas of several fisherman villages in Ilha Grande [65]. Even though there are no recorded human cases of *Leishmania (L.) amazonensis* infection in Ilha Grande, one DCL case was recorded in 2007 in Paraty, a municipality neighbor to Angra dos Reis [91].