• Sand fly;
  • Psychodopygus wellcomei;
  • Lutzomyia longipalpis;
  • abundance;
  • diversity;
  • agroforestry environment


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  7. Acknowledgments

Phlebotomine vectors transmit parasites and can cause visceral leishmaniasis (VL) or cutaneous leishmaniasis (TL). Phlebotomine females are hematophagous but need to ingest carbohydrates, possibly promoting the development of protozoan parasites in their digestive tract. The present study evaluated the species composition and abundance across several habitats in a metropolitan landscape, as well as associations among phlebotomines, plants, and local climatic parameters. Three consecutive monthly collections were carried out in an Atlantic Forest fragment, using CDC light traps in peridomestic areas and cashew, coconut, and mango tree. plantations. Eight species of phlebotomine were captured: Evandromyia evandroi, Lutzomyia longipalpis, Psathyromyia shannoni, Sciopemyia sordellii, Evandromyia walkeri, Psychodopygus wellcomei, Nyssomyia whitmani, and Nyssomyia intermedia, primarily from the forest environment. L. longipalpis was confirmed as a species adapted to anthropic environments, while P. wellcomei was shown to be predominately forest-dwelling. Phlebotomines exhibited diversified food consumption patterns in relation to carbohydrate sources. They fed on both native and exotic species of arboreal and shrubby vegetables and gramineous plants.


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  7. Acknowledgments

Phlebotomines (Diptera, Psychodidae, Phlebotominae), commonly known as sand flies, are small nocturnal or crepuscular insects found in rural or urban areas. They seek shelter in a variety of environments, including tree trunks and canopies, burrows, bushes, cracks in rocks, or even dog kennels and residences, where females can feed on the blood of animal hosts. Sand flies can be vectors of Leishmania parasites, which are subdivided into the subgenera Viannia and Leishmania, related to peripyloric and suprapyloric parasites (Aguiar et al. 1985, Alexander et al. 1992, Azevedo et al. 1993, Basimike et al. 1991, Comer and Brown 1993, Gomes et al. 1980, Memmott 1991), which may cause cutaneous leishmaniasis (TL) and visceral leishmaniasis (VL), both widely distributed worldwide. Given the diversity of Phlebotomine species, it is extremely important to control their abundance and distribution in order to reduce the incidence of these diseases (Chaves and Añez 2004, Calzada et al. 2013).

Carbohydrates are indispensable for sand fly activity. Turanose and melezitose, sugars secreted by homopterous insects belonging to the families Afidae and Coccidae, are an important component of the sand fly diet (Añez et al. 1994, Moore et al. 1987, Macvicker et al. 1990, Wallbanks et al. 1991), as well as the sap obtained directly from a number of vegetables (Schlein and Muller 1995, Schlein and Jacobson 1999). Sugar intake is also necessary for Leishmania parasite survival and multiplication inside the sand fly digestive tract (Jacobson et al. 2001).

Both TL and VL typically occur in areas of low socioeconomic status (Nascimento et al. 2005, Chaves et al. 2008). Environmental factors influence the geographic expansion of vectors and the transmission of leishmaniases (Patz et al. 2000). Deforestation may contribute to the increased number of cases in urban and periurban regions (Campbell-Lendrum et al. 2001, Bern et al. 2008).

In the state of Rio Grande do Norte, phlebotomine sand flies, vectors of Leshmania (Leishmania) infantum and Leishmania (Viannia) braziliensis, etiologic agents of VL and TL respectively, occur in both urban and rural areas of the state (Ximenes et al. 1991, Ximenes et al. 2007).

This study aimed to evaluate the species composition and abundance across several habitats in a metropolitan landscape, as well as associations between phlebotomines and plants and local climatic parameters.


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Study area

The insects were collected in six areas of the Rommel Mesquita de Faria Experimental Station (Figure 1), belonging to the Agricultural Research Enterprise of Rio Grande do Norte (EMPARN) in the city of Parnamirim, located on km 15 on the road between Natal and Jiqui. Parnamirim lies 53 m above sea level on the coast of Rio Grande do Norte in the metropolitan region of Natal, covering an area of 120 km². It has the third largest population in the state, with 202,456 inhabitants, and 100% of the residences were located in urban areas in 2010 (IBGE 2013).


Figure 1. Study area (Adapted from Google Earth). The large arrow indicates the forest area where the sand flies were collected.

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The 520-hectare collection area also includes an office, two laboratories, seven homes occupied by employees of the department (EMPARN), an area of Atlantic Forest, and experimental and commercial monoculture plantations of dwarf and giant Cocos nucifera L. (coconut trees) Anacardium occidentale L. (cashew trees), Mangifera indica L. (mature mango trees), Pennisetum pupureum Schumach, (grass), Musa paradisiacal L. (banana trees), Leucaena leucocephara Lam. (switchgrass), Mimosa caesalpiniifolia Benth. (sabiá), Acacia mangium Willd., (acácia), and Eucalyptus sp. L’Heritier (eucalyptus), as well as a number of isolated native and exotic trees (Figure 2).


Figure 2. Aerial image of the agroforest environment (Google Earth).

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Characteristics of collection spots

Six collection areas were selected: the Atlantic Forest, plantations of giant coconut trees, small coconut trees, cashew trees, mango trees, and the poultry yard of a residence. The Atlantic Forest, known as Jiqui Forest, has at least 59 tree species and a surface area of 79 hectares (Cestaro and Soares 2008). The giant coconut tree plantation consists of 15 hectares of C. nucifera (giant hybrid coconut trees), with secondary, predominantly herbaceous, vegetation (Figure 2). The cashew tree plantation has approximately three hectares of A. occidentale (cashew trees), including various small mature specimens (Figure 2), as well as a small amount of herbaceous vegetation. The small coconut tree plantation area consists of around 36 hectares of irrigated C. nucifera (small green coconut trees) and predominantly herbaceous vegetation, with scattered bushes (Figure 2). The mango tree plantation, located approximately 20 m from the shore of Lake Jiqui, has six large M. indica (mango trees) interspersed with two Syzygium cumini L. Skeels (jambolan trees) and rare herbaceous plants (Figure 2). The leaf litter also contains a substantial amount of fruit in various stages of decomposition during the fructification period. The house/poultry yard contains a family home near a small area where Gallus gallus Linnaeus, (chickens) are raised (Figure 2). This site is situated 1,140 m from the forest.

Phlebotomine collection procedure

A trap was installed at each collection site, on three consecutive days from January to December. CDC light traps (Hausherr's Machine Works, NJ, U.S.A.) were placed 1 m above the ground at approximately 17:00 and removed at 07:00 the following morning, resulting in approximately 14 h of exposure to each trap. The insects captured overnight were taken to the Entomology Laboratory of the Federal University of Rio Grande do Norte and placed in a freezer (−20° C) for 20 min. Next, males and females were stored separately at −20° C for subsequent analysis. Climate data were obtained from EMPARN (Agricultural Research Company of Rio Grande do Norte).

Search for aphids and coccids

Active monthly searches for aphids and coccids were carried out (Homoptera: Afidae and Coccidae) in the collection areas, followed by random sampling of 20 plants.


Phlebotomines were clarified in 10% potassium hydroxide, placed between a slide and cover slip and identified using an optic microscope. Identification was based on morphological traits and phylogenetic classification proposed by Galati (1995, 2003a, 2003b).

Analysis of monosaccharide intake

A sample of 726 male sand flies, collected in September in the forest area, was macerated for 15 min in 1 ml of TRIS-HCl 50µM buffer solution, pH 7.5, and centrifuged for 15 min to 12,000 g. The supernatant was homogenized and filtered, and 20 µl were injected into reverse phase Vidac C18 columns using high performance liquid chromatography (HPLC) to detect existing carbohydrates. Technical difficulties prevented identification of the insects and chromatography of the same sample of phlebotomines. Females were previously excluded from the sample in order to identify species.

Analysis of monosaccharides in plant samples

Samples of A. mangium (acacia), A. occidentale (cashew tree), Anadenanthera colubrina (Vell.) Brenan, Bauhinia forticata Link (pata de vaca), Coccoloba sp. P. Browne, C. nucifera (coconut tree), Eucalyptus sp. (eucalyptus), Gliricidia sepium (Jacq.) Steud (live vine stakes), Hancornia speciosa Gomes (mangaba tree), M. indica (mango tree), M. paradisiaca (banana tree), P. pupureum (elephant grass), Psidium guajava L. (guava tree), and Psychotria carrascoana Delpreteand E. B. Souza were obtained from the area and sap samples were extracted. For sap extraction young branches were soaked in distilled water and 1 ml of the liquid obtained was stored at −20° C for later analysis. The sample was then homogenized and filtered, and 20 µl was then injected into Vydac C18 reversed-phase columns using high performance liquid chromatography (HPLC) to identify existing carbohydrates.

Statistical analysis

Kruskal-Wallis analysis was used to test the hypothesis of equality among the different biotopes studied. This was followed by multiple comparisons and correlation tests between the species and climatic variables (temperature, relative humidity, rainfall, and wind speed).

Analysis of diversity between the environments was obtained using the Shannon-Wiener Diversity Index (H’) (Magurran 1988), and Ecological Methodology 5.2 software (Kenney and Krebs 2000).

The Index of Species Abundance (ISA) and Standardized Index of Species Abundance (SISA) (Roberts and Hsi 1979) were used to analyze the data obtained in the environments. The ISA values were determined and converted in SISA to values between 0–1 using Microsoft Office Excel 2007.


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  7. Acknowledgments

Sand flies

A total of 1,067 phlebotomines belonging to eight species was collected in the six biotypes surveyed. Evandromyia walkeri (Newstead) was the most abundant species, accounting for 69% of all captured species, followed by Evandromyia evandroi (Costa Lima & Antunes) with 12.46%, Lutzomyia longipalpis (Lutz & Neiva) with 7.12%, and Psychodopygus wellcomei (Fraiha, Shawn & Lainson) with 7.02%. The least occurring species were Nyssomyia whitmani (Antunes & Coutinho) with 1.4%, Sciopemyia sordellii (Shannon & Del Ponte) with 0.93%, and Nyssomyia intermedia (Lutz & Neiva) and Psathyromyia shannoni (Dyar) with only one specimen each (0.09%) (Table 1).

Table 1. Number of phlebotomines by species in different environments.
SpeciesForestGiant coconutHouse/poultry yardSmall coconutCashew treesMango treesTotal%
E. walkeri69937132474669.9%
E. evandroi52386305213312.5%
L. longipalpis7159180767.1%
P. wellcomei7310100757.0%
N. whitmani1220001151.4%
S. sordellii900100100.9%
N. intermedia10000010.1%
P. shannoni10000010.1%
Not identified811000100.9%

The Kruskal-Wallis test revealed uneven distribution of all phlebotomine sand fly species captured in the study area (p = 0.000). An analogous result was found when each species was considered separately. In other words, the Kruskal-Wallis test identified, for example, that the vector species P. wellcomei (p=0.000), L. longipalpis (p=0.000) and N. whitmani (p=0.003) are not uniformly distributed among the different environments surveyed.

According to the Shannon Diversity Index, the environments with the greatest diversity were plantations of cashew trees (H’ = 1.40), mangos (H’ = 1.37), and giant coconuts (H’ = 1.31), followed by bush (H’ = 1.02) and the dwarf coconut plantation (H’ = 0.95), while the lowest index was obtained in the peridomestic environment (H’ = 0.55) (Figure 3).


Figure 3. Standardized Index of Species Abundance (SISA) and Shannon Diversity Index of sand flies captured.

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The most abundant species were E. walkeri and E. evandroi, both with a SISA of 0.92, followed by L. longipalpis (SISA = 0.72). The least abundant species were P. wellcomei (SISA = 0.39), N. whitmani (SISA = 0.38), S. sordellii (SISA = 0.21), N. intermedia (SISA = 0.02), and P. shannoni (SISA = 0.02) (Figure 3).

Sand flies and climatic variables

Overall, there was an increase in phlebotomine sand fly abundance in February, October, and December, mainly in the forest area. The highest occurrence was observed during the dry months, with lower humidity and higher temperatures, and a significant decline was recorded at the beginning of the rainy season. However, it is important to underscore that P. wellcomei only occurs in months with higher rainfall and relative humidity and lower temperatures (Figure 4).


Figure 4. Total number of sand flies and mean monthly temperature (degrees Celsius), rainfall (mm), and relative air humidity (%) between January and December in the agroforest environment.

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The abundance of E. walkeri exhibited a significant positive correlation with temperature (r = 0.58; p = 0.047); that is, when temperature rises there is a tendency for increased abundance of this species. On the other hand, P. wellcomei showed a significant negative correlation with temperature (r = −0.78; p = 0.003) and a positive association with relative air humidity (r = 0.598; p = 0.040). In other words, with a rise in temperature there is a tendency for lower species abundance, and with an increase in relative air humidity the species tends to be more abundant at the site.

Atlantic Forest

The Atlantic Forest contained the greatest number of phlebotomines, accounting for 81% of the specimens, while those registering the lowest numbers were the cashew and mango tree areas, with 1.4% and 0.65%, respectively.

In the forest collection area, 862 phlebotomines from eight species were collected, (555 males and 307 females). E. walkeri was the most abundant species, corresponding to 81% of the sand flies collected, followed by P. wellcomei, and E. evandroi with 9% and 6%, respectively (Table 2).

Table 2. Number of male and female phlebotomines captured in the Jiqui forest.
L. longipalpis46133.5/15988%
E. evandroi422/169%
E. walkeri101/011.5%
Not identified010/111.5%

There was an overall predominance of males in this region (64.4%). However, it is important to highlight that P. wellcomei, E. evandroi, S. sordellii, and L. longipalpis females were more representative in the collections (Table 2).

A difference was observed in the occurrence of E. walkeri, P. wellcomei, E. evandroi, and N. whitmani in the forest over the year, with E. walkeri and P. wellcomei (Figure 5) exhibiting a five-month difference between abundance peaks.


Figure 5. Annual distribution of E. walkeri, E. evandroi, P. wellcomei and N. whitimani. The right vertical axis shows the species E. evandroi, P. wellcomei, and N. whitimani.

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Giant coconut tree plantation

With respect to the giant coconut tree plantation, 80 phlebotomines of five species were collected (45 males and 35 females). The most common species were E. evandroi and E. walkeri (48% and 46%, respectively). N. whitmani, P. wellcomei, and L. longipalpis were also observed in this area, though less abundant (3%, 1%, and 1%, respectively). Males accounted for 56.2% of specimens collected and females 43.8%. The hypothesis of E. evandroi equality between environments was rejected and multiple comparisons identified significant differences between the giant coconut tree environment and those containing cashew and mango trees.

Cashew tree plantation

The most common species in this area was L. longipalpis (54%), followed by E. evandroi (33%). Males predominated in both species (Table 1).

Mango trees

In the mango tree area, only seven phlebotomines were captured throughout the year, most of which were males. The most prevalent species was E. walkeri, followed by E. evandroi and N. whitmani (Table 1).

Small coconut tree plantation

Five species were recorded in the small coconut tree plantation situated further from the forest border, of which 58% were males and 42% females. The most common phlebotomines found were E. evandroi with 83%, followed by E. walkeri (8%), L. longipalpis, S. sordellii, and P. wellcomei with 3% each (Table 1).

House/poultry yard

A total of 67 phlebotomines were collected in the peridomestic environment. L. longipalpis was the most abundant species (88%), followed by E. evandroi and E. walkeri (9% and 1.5%, respectively). Males predominated in this environment (Table 3). Kruskal-Wallis multiple comparisons showed significant differences between the house/poultry yard sector and all other zones, indicating that L. longipalpis occurs predominantly in the peridomestic environment.

Table 3. Occurrence of species in the area of the house/poultry yard.
E. walkeri5251743/169981.1%
P. wellcomei11620.2/1738.5%
E. evandroi5470.1/1526.0%
N. whitmani12012/0121.4%
S. sordellii180.1291.0%
L. longipalpis070/770.8%
N. intermedia101/010.1%
P. shannoni010/110.1%
Not identified080/880.9%

Aphids and coccids

The monthly collections conducted in the phlebotomine capture environments found no aphids or coccids, suggesting either low occurrence or nonexistence of these insects in the study area.


The monosaccharides identified by HPLC in the sample of phlebotomines were xylose, arabinose, and mannose (Table 4). Captured females and males used in carbohydrate analysis belonged to the species E.walkeri (65%), P. wellcomei (23%), and E. evandroi (12%).

Table 4. Monosaccharides detected (+) in phlebotomine sand flies and in plants in the area detected by high performance liquid chromatography (HPLC).

Eight monosaccharides were identified in the plant samples: glucose, xylose, galactose, mannose, rhamnose, fucose, galactosamine, and arabinose (Table 4).

Xylose was one of the most common carbohydrates, detected in 71% of the plants analyzed, as well as among the sand flies collected (Table 4). Furthermore, it was the main monosaccharide found in A. colubrina, B. forticata, C. nucifera, G. sepium, and M. indica. As such, plants were considered a food source for phlebotomines.

Arabinose was also found among both plant and sand fly samples, and mannose was detected in phlebotomines and plant samples, such as Coccoloba sp., Eucalyptus sp., M. indica, P. pupureum, and P. carrascoana.

Glucose was found in three vegetables (A. mangium, G. sepium, and M. indica); however, sugar was not present in the phlebotomine sample. Galactose was not found in the phlebotomines, despite being present in four plants (A. colubrina, B. forticata, P. guajava, and P. carrascoana). Rhamnose was identified in six plants but was absent in phlebotomines, ruling it out as a food source. Fucose was detected in six plants but was absent in sand flies. Galactosamine was not found in phlebotomines but was recorded in five plant species (A. mangium, A. occidentale, C. nucifera, Eucaliptus sp., and P. pupureum). The banana tree was the only plant whose sugars were not present in phlebotomines, and it was eliminated as a source of monosaccharides for these insects.


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  7. Acknowledgments

Phlebotomines occurred primarily in the Atlantic Forest fragment, where more than 80% of the collections took place. The most abundant species was E. walkeri, which has not been definitively established as a vector of Leishmania, followed by E. evandroi. An association was observed between L. longipalpis, a vector of L. infantum, and the peridomestic areas, corroborating previous studies assessing the occurrence of this species in preserved and modified environments (Dias-Lima et al. 2003, Cameron et al. 1995).

Among the vector species captured, N. whitmani and N. intermedia are widely distributed in Brazil, being found in five regions of the country. L. longipalpis, also distributed in five regions, was recently recorded in southern Brazil; however, cases of VL occur mainly in northeast Brazil. P. wellcomei has been registered only in the north and northeast of the country (Aguiar and Medeiros 2003). Most of the TL cases have occurred in these two regions.

In the present study, N. whitmani, N. intermedia, and P. wellcomei demonstrated a preference for more preserved areas, either in the forest or nearby sites. These species have been identified as vectors of L. braziliensis in forest environments of the northeast (Ready et al. , Queiroz et al. 1994, Brandão-Filho et al. 1998, Rebêlo et al. 1999, Silva and Vasconcelos 2005).

These results suggest a geographic boundary between species vectors of L. infantum and L. braziliensis, likely defined by phytogeographic and biological factors. L. longipalpis occurs in peridomestic areas, while N. whitmani, P. wellcomei, and N. intermedia occur primarily in forest environments, with a predominance of P. wellcomei over N. whitmani and N. intermedia in the forest environment.

For most of the environments analyzed here, phlebotomine sand flies were predominant during the dry season; which occurs immediately after the rainy season. There was a significant decline in species abundance at the onset of the rainy season, with lower temperatures and higher relative humidity. After the forest area, the sites with the highest number of phlebotomines were the giant coconut tree plantation and the peridomestic environment. The presence of animals in the peridomestic area likely attracted L. longipalpis.

L. longipalpis was present in five of the six biotopes surveyed, confirming their diversified behavior and adaptation to degraded environments. Its presence in these areas was probably related to the canine and human VL cases notified in the city of Parnamirim, in the metropolitan region of Natal. The lack of significant correlations between L. longipalpis and local climate changes may be attributable to the short duration of the study, given that a long-term study identified wind speed as a limiting factor for this species, while humidity and temperature influenced males and females differently. According to this same study, male abundance was not correlated with rain or temperature, but rather to relative humidity and wind speed. However, the number of females was associated with all climatic changes. Wind speed was negatively correlated to the number of females. An increase in the number of females was observed approximately two weeks after the rise in relative humidity (Ximenes et al. 1991).

N. whitmani (Azevedo et al. 1990, Costa et al. 1990) and P. wellcomei (Queiroz et al. 1994) are epidemiologically significant as vectors of L. braziliensis in the northeastern region. Thus, the presence of both species in the study area suggests a risk of TL transmission in the Jiqui forest area and its surroundings, despite the fact that endemic TL for the state is historically in the hilly regions to the west. Epidemiologic surveillance agencies have reported cases of TL in the metropolitan region of Natal, although it is unknown whether these are autochthonous or not.

P. wellcomei and N. whitmani were predominantly forest-dwelling in the surveyed areas, accounting for 97% of collections for the former and 80% for the latter in the forest environment.

Although we conducted earlier systematic studies in all regions of Rio Grande do Norte (Ximenes et al. 2000, Ximenes et al. 2007), this is the first investigation that addresses bioecological aspects of P. wellcomei, a species whose occurrence in the state was recorded by our group in 2007.

The presence of P. wellcomei was clearly related to the rainy season, as occurs in the Brazilian Amazon Rainforest (Lainson and Shaw 1998). We cannot rule out the possibility of egg diapause during the dry season. Eggs from sylvan P. wellcomei females remained viable for about three months. Diapause has been reported in the larvae (Kumar and Kishore 1991, Killick-Kendrick and Killick-Kendrick 1987) and eggs of Old World phlebotomine sand flies (Trouillet and Vattier-Bernard 1979).

With respect to P. wellcomei, Fraiha et al. 1971 reported intense anthropophilia, even during the day. This evidence reinforces the need to monitor this species, since agroforestry requires the daily presence of employees and researchers, either inside or near the forest, due to the potential risk to several neighborhoods nearby.

Analyzing the distribution of phlebotomines in the study area was a complex process given that the dynamic established by rain, temperature, wind speed, and food availability determines their presence. However, analysis of the sugars ingested by phlebotomines and detected in certain plant species allows some inferences to be made.

The sand fly species present in the sample analyzed by liquid chromatography was likely E. walkeri, since it accounts for 81% of phlebotomines in the forest area, followed by P. wellcomei. Both species were predominant in September, the same month in which the phlebotomines used in the carbohydrate analysis were collected. The females identified in the sample also belonged to these species. New analyses are needed to determine whether distinct species require different carbohydrates.

The monosaccharides ingested by phlebotomines were xylose, mannose, and arabinose, naturally found in plants (Schädel et al. 2009, Poysti et al. 2007, Rodriguez et al. 2005), indicating that plant species in the forest area and its surroundings are used as a food source by these insects.

Among the plants assessed, the exotic species P. pupureum (grass) and Eucalyptus sp. (eucalyptus) were considered a possible food source, in that these were the only varieties that contained the three monosaccharides present in the phlebotomines analyzed (xylose, mannose, and arabinose). Grass and eucalyptus were found approximately 230 m and 110 m from the sand fly collection area, respectively. The former is widely used in rural areas of the state as animal feed, while the latter is found across extensive areas reforested for commercial purposes. Phlebotomus papatasi phlebotomines travel greater distances in search of preferred plant species for food (Schlein and Jacobson 1999).

Thus, the present study confirmed the diverse feeding behavior of phlebotomines in relation to carbohydrate sources. Feeding can occur in arboreal, shrubby, or grassy areas and on native or exotic species, such as grass, acacia, and eucalyptus. Studies aimed at analyzing the association between sand flies and plant or animal food sources could contribute to understanding the spread of leishmaniases in peri-urban areas.

P. wellcomei was not recorded in the areas closest to residences, indicating that this species is associated with forest environments. Another relevant aspect is the increasing urban expansion and presence of gated communities in areas surrounding the forest environment. This may result in vectors adapting to new environments and alternative food sources (Rebêlo et al. 2000, Bern et al. 2008).

The predominant species recorded in the giant coconut tree plantation were E. walkeri and E. evandroi, which are not considered vectors. However, E. walkeri, naturally infected by Leishmania Viannia spp., was found in a TL transmission area in Pernambuco, a state located about 380 km to the south of Rio Grande do Norte (Guimarães, unpublished data).

P. shannoni was only collected in the forest biotope. In the U.S.A., this species is considered a vector of the vesiculovirus, which causes vesicular stomatitis (Corn et al. 1990). Studies have found that that some species of Leishmania, including L. infantum, can develop in this phlebotomine (Ferro et al. 1998), a competent vector of Leishmania mexicana (Lawyer and Young 1987). It is also hypothesized that the presence of infected dogs in areas where P. shannoni occur might trigger epidemic outbreaks (Travi et al. 2002) of TL.

Finally, studies analyzing the bioecology of phlebotomine sand flies and their potential to adapt to new environments could contribute to the epidemiological surveillance of leishmaniases. The expansion and urbanization of leishmaniases in the country, considering the complex relationships between vertebrate, invertebrate, and protozoan hosts, are modulated or altered by the environmental degradation evident over time in the urban or periurban areas of small, medium-sized, and large Brazilian cities.


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  7. Acknowledgments

We thank EMPARN for authorizing this study, the CNPQ (Brazilian National Council of Technological and Scientific Development) and CAPES (Brazilian Federal Agency for the Support and Evaluation of Postgraduate Education) for financial support, Professor Maurício Sales (in memoriam), Professor Hugo Rocha, Nednaldo Dantas, and colleagues from the Entomology Lab who contributed to field activities.


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  7. Acknowledgments
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