Ecological Aspects of Phlebotomines (Diptera: Psychodidae) - BioOne

SAMPLING, DISTRIBUTION, DISPERSAL

Ecological Aspects of Phlebotomines (Diptera: Psychodidae) in Endemic Area of Visceral Leishmaniasis, Campo Grande, State of Mato Grosso do Sul, Brazil ALESSANDRA GUTIERREZ OLIVEIRA,1,2 EUNICE APARECIDA BIANCHI GALATI,3 CARLOS EURICO FERNANDES,1 MARIA ELIZABETH CAVALHEIROS DORVAL,1 AND REGINALDO PEC ¸ ANHA BRAZIL4

J. Med. Entomol. 49(1): 43Ð50 (2012); DOI: http://dx.doi.org/10.1603/ME11082

ABSTRACT Aspects of phlebotomine behavior were investigated in the city of Campo Grande, Mato Grosso do Sul state. The insects were captured weekly during December 2003 to November 2005, with Centers for Disease Control light traps at seven different sites including forests and residential areas. In total, 11,024 specimens (7,805 males and 3,219 females) were collected, from which 9,963 (90.38%) were identiÞed as Lutzomyia longipalpis, the proven vector of American visceral leishmaniasis agent. The remaining 9.62% comprised 21 species. L . longipalpis was the most frequent species in all sampled sites, and the Þrst in the ranking of standardized species abundance index. In residential areas this species clearly predominated in the peridomicile (90.96%), in contrast to the intradomicile (9.04%); in animal shelters, it was more numerous in hen houses and prevailed at ground level, inside, and at forest edge around the residences; this aspect is worrying because this insect may remain sheltered in forested environments during the use of insecticides in homes. In the forest environment, other probable or proven vector of cutaneous leishmaniasis agents were also captured such as Lutzomyia whitmani (⫽Nyssomyia whitmani, sensu Galati), Lutzomyia antunesi (⫽Nyssomyia antunesi, sensu Galati), and Lutzomyia flaviscutellata (⫽Bichromomyia flaviscutellata, sensu Galati). KEY WORDS phlebotomine, Lutzomyia longipalpis, Mato Grosso do Sul, urban environment

In Mato Grosso do Sul state American cutaneous leishmaniasis (ACL) occurs in almost all its territory and visceral leishmaniasis (VL) has been expanding through the municipalities, including Campo Grande, the state capital. These infections affecting both urban and rural population, with records in 2005 for the state of 264 cases of VL and 143 of ACL, of which 184 and 10, respectively, in Campo Grande (Mato Grosso do Sul 2006). Studies on the phlebotomine fauna in the urban area of Campo Grande showed species incriminated as vectors of both ACL and VL (Oliveira et al. 2003, 2006), with Lutzomyia longipalpis (Lutz & Neiva) and Lutzomyia. cruzi occurring in sympatry (Oliveira et al. 2000). The latter has been incriminated as vector of VL in Corumba´, a city located in the western region of Mato Grosso do Sul, which borders Bolivia (Galati et al. 1997, Santos et al. 1998, Pita-Pereira et al. 2008). 1 Departamento de Patologia/Universidade Federal de Mato Grosso do Sul, Cidade Universita´ria s/n, 79070-900, Campo Grande, MS, Brazil. 2 Corresponding author, e-mail: [email protected]. 3 Departamento de Epidemiologia, Faculdade de Sau ´ de Pu´ blica, Universidade de Saõ Paulo, Av. Drive Arnaldo 715, 01246-904, Saõ Paulo, SP, Brazil. 4 Laborato ´ rio de Bioquõ´mica de Insetos, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, 21040-360, Rio de Janeiro, RJ, Brazil.

The lack of knowledge about the behavior of phlebotomine populations, especially in Campo Grande, raised the need for research on the ecology of this group of insects. This study aims at presenting distribution, diversity, and abundance of species, related to forested, intra and peridomiciliary environments, in different areas of the city and contribute to the control of the vector and, consequently, of leishmaniases. Materials and Methods Area of Study. Campo Grande (20⬚26⬘34⬙S and 54⬚38⬘47⬙W), comprising an area of 8,118.4 km2 in Mato Grosso do Sul, Brazil, is geographically located in the central part of the state, occupying 2.27% of its total area (Fig. 1). According to the estimate of the Instituto Brasileiro de GeograÞa e Estatõ´stica (IBGE), its urban population in 2010 was 787,204 inhabitants. The predominant climate of Campo Grande, according to Ko¨ ppenÕs ClassiÞcation, is a tropical rainy type of savanna, AW subtype, characterized by a poor distribution of annual rainfall, with well-deÞned occurrence of a dry period during the coldest months of the year and a rainy period in the summertime (Oliveira et al. 2008a). Sand Fly Collections. Captures were performed in three regions of the city with traps installed in seven

0022-2585/12/0043Ð0050$04.00/0 䉷 2012 Entomological Society of America

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Fig. 1. Location of the urban area of Campo Grande, Mato Grosso do Sul, Brazil.

sites; the selection criteria were based on density and diversity of phlebotomines obtained in a previous study (Oliveira et al. 2003). All capture sites are described in Oliveira et al. (2008b). Western region: “Vila do Ze´ Pereira,” where “Ze´ Pereira Forest” and residences one and two are located; Southern region: “Jardim Monte Alegre,” where “Chaćara das Palmeiras” and “Chaćara Wood” are found; and Central region: “Vila Bandeirantes,” with residences three and 4. At each selected Þxed site, automatic Centers for Disease Control (CDC) light traps (Natal et al. 1991) (Horst armadilhas) were installed simultaneously: three in forested areas (inside the forest at ground level (1 m), canopy level (5 m), and on the ground in the forest edge); and two in anthropic environments, one in the intradomicile, and another in the peridomicile (cultivation areas, hen house, pigsty, kennel, goat, and sheep pen). The collections were performed on a weekly basis, from 1800 until 0600 hours, irrespective of summer time, in the period from December 2003 to November 2005. The captured specimens were transported to the Laboratory of Parasitology of the Federal University of Mato Grosso do Sul (UFMS) for assemblage, identiÞcation, and other observations. Terminology of the species were used in accordance with Young and Dun-

can (1994) and terminology and abbreviations in parentheses by Galati (2003) and Marcondes (2007), respectively. For the evaluation of the most abundant species as well as its spatial distribution, the Index of Species Abundance (ISA) was converted into a zero-to-one scale, through the Standardized Index of Species Abundance (SISA). In this index, value one corresponds to the most abundant species (Roberts and Hsi 1979). For the analysis of diversity and evenness of species in their respective ecotopes, ShannonÕs (H) and PielouÕs (J) indexes were used (Hayek and Buzas 1997). The comparison of the frequencies among the phlebotomine populations, for the different urban regions and traps, was drawn by the chi-squared test (␹2, revised by the Yates correction) for the contingency and absolute frequency tables. Results The 208 weekly captures yielded 11,024 specimens of phlebotomines, 7,805 males (70.8%) and 3,219 females (29.2%); the fauna was composed of 22 species. Table 1 shows the total number of insects captured in all areas as well as the diversity index of Shannon (H) and the evenness of Pielou (J). The most abundant species was L. longipalpis (⫽Lu. longipalpis, sensu; Galati 2003) both in forested

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OLIVEIRA ET AL.: ECOLOGICAL ASPECTS OF PHLEBOTOMINES

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Table 1. Total number of phlebotomines captured in urban areas of Campo Grande, Mato Grosso do Sul state, from Dec. 2003 to Nov. 2005 and respective indexes of diversity (H) and evenness (J) Forested areas Ze´ Pereira L. flaviscutellata (⫽Bi. flaviscutellata) Brumptomyia. avellari Brumptomyia brumpti Brumptomyia sp. L. bourrouli (⫽Ev. bourrouli) L. cortelezzii (⫽Ev. cortelezzii) L. lenti (⫽Ev. lenti) L. teratodes (⫽Ev. teratodes) L. termitophila (⫽Ev. termitophila) Lutzomyia sp. (⫽Evandromyia sp.) Lutzomyia sp. (⫽Lu.(Castromyia) sp.) L. longipalpis (⫽Lu. longipalpis) L. longipennis (⫽Mi. longipennis) L. quinquefer (⫽Mi. quinquefer) L .antunesi (⫽Ny. antunesi) L. whitmani (⫽Ny. whitmani) L. christenseni (⫽Pi. christenseni) L. damascenoi (⫽Pi. damascenoi) L. aragaoi (⫽Pa. aragaoi) L. campograndensis (⫽Pa. campograndensis) L. hermanlenti (⫽Pa. hermanlenti) L. punctigeniculata (⫽Pa. punctigeniculata) L. shannoni (⫽Pa. shannoni) L. claustrei (⫽Ps. claustrei) L. sordellii (⫽Sc. sordellii) Total Index of diversity (H) Index of evenness (J)

2 18 1 3 1 15 7 Ñ 2 Ñ 2 431 2 29 71 53 8 1 65 16 114 1

Chać. Wood Ñ 1 Ñ Ñ Ñ 3 54 1 17 Ñ 1 260 Ñ Ñ Ñ 4 28 2 Ñ 2 2 Ñ

24 31 132 Ñ 4 Ñ 1002 406 1.9804 1.2714 0.6316 0.4956

Residential areas Chać. das Palmeiras Ñ 2 Ñ Ñ Ñ 1 85 Ñ 110 1 Ñ 433 Ñ Ñ Ñ 10 8 Ñ Ñ Ñ 1 1 107 Ñ 3 762 1.2969 0.5219

Res. 1

Res. 2

Res. 3

Res. 4

Total

%

Ñ Ñ Ñ Ñ Ñ 2 1 Ñ Ñ Ñ Ñ 381 Ñ 1 Ñ 2 Ñ Ñ Ñ Ñ

Ñ 1 Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ 267 1 Ñ Ñ Ñ Ñ Ñ Ñ Ñ

Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ 1 Ñ Ñ 7394 Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ

Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ 797 Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ

2 22 1 3 1 21 147 1 130 1 3 9963 3 30 71 69 44 3 65 18

0.02 0.20 0.01 0.03 0.01 0.19 1.33 0.01 1.18 0.01 0.03 90.38 0.03 0.027 0.64 0.63 0.40 0.03 0.59 0.16

Ñ Ñ

2 Ñ

Ñ Ñ

Ñ Ñ

119 2

1.07 0.02

Ñ

3 Ñ Ñ 165 1.50 Ñ Ñ 1 133 1.20 Ñ Ñ Ñ Ñ 7 0.06 387 274 7395 798 11024 100.00 0.1007 0.1503 0.001 0.0092 0.5447 0.0626 0.0933 0.0014 0.0132 0.1692

Chać, grange; Res, residence; Bi, Bichromomyia, Ev, Evandromyia; Lu, Lutzomyia; Mi, Micropygomyia; Ny, Nyssomyia; Pi, Pintomyia; Pa, Psathyromyia; Ps, Psychodopygus; Sc, Sciopemyia. The name of the species in brackets is in accordance with Galati (2003), and abbreviation, sensu Marcondes (2007).

(SISA ⫽ 1) and residential areas (SISA ⫽ 1), values that indicate maximum abundance conferring it the Þrst place in the ranking for both environments. It also represented 90.38% of the total of insects captured. L. shannoni (⫽Psathyromyia shannoni, sensu; Galati 2003) was the second most frequently found species (1.5%) and came second in both environments, forested (SISA ⫽ 0.79) and residential (SISA ⫽ 0.35) areas. Although L. lenti (⫽Evandromyia lenti, sensu; Galati 2003) had presented frequency of 1.33%, higher than that shown by L. whitmani (⫽Nyssomyia whitmani; in accordance with Galati 2003) (0.63%), it was less abundant in the anthropic (SISA ⫽ 0.25) and forested (SISA ⫽ 0.70) environments when compared with L. whitmani (SISA ⫽ 0.27 and 0.77) (Table 2). The other potential vector species of ACL agents, L. claustrei (⫽Psychodopygus claustrei, sensu; Galati 2003) and L. antunesi (⫽Nyssomyia antunesi, sensu; Galati 2003) and the proven vector of Leishmania (Leishmania) amazonensis, Lutzomyia flaviscutellata (⫽Bichromomyia flaviscutellata, sensu; Galati 2003) were found only in forested areas, with low frequency, 1.2, 0.64, and 0.02%, respectively. The male/female ratio for L. longipalpis in residential areas was 5.52 in “Chaćara das Palmeiras”; 2.93 in

residence 1; 2.81 in residence 2; 3.05 in residence 3; and 1.30 in residence 4; totaling 2.95 males for one female. Overall, L. longipalpis was less frequently captured in intra than in the peridomicile of the residences, a signiÞcant difference (P ⬍ 0001; Table 3), with exception of residence 1, where it was predominant in the intradomicile. In forested areas, the yield from the traps placed inside (ground and canopy) and at the border were compared, observing that in “Ze´ Pereira Forest” there was predominance of insects inside (ground) and in “Chaćara Wood,” at the border (P ⬍ 0001). However, on canopies, more ßies were captured in “Mata do Ze´ Pereira” than in “Chaćara Wood,” also with a signiÞcant difference (P ⬍ 0001). In residential areas, L. longipalpis prevailed at all sites. In “Chaćara das Palmeiras” the three shelters were compared, and the hen house was the ecotope with seven species and 79% of the specimens. The pigsty came second, with Þve species and 19.3% of specimens. The goat and sheep pen shown to be less attractive for phlebotomines, with only seven specimens collected. In both hen house and pigsty, the most frequently found species, in addition to L. longipalpis, was L. shannoni, mainly males. L. lenti was the third most abundant in the pigsty and the fourth in the hen house. L. whitmani and L. termitophila (⫽Evandro-

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Table 2. Standardized index of species abundance (SISA) for phlebotomines captured in forested and residential areas. Campo Grande, Mato Grosso do Sul state, Dec. 2003 through Nov. 2005 Forested areas Ze´ Pereira

Chać. Wood

SISA

2 18 1 3 1 15 7 Ñ 2 Ñ 2 431 2 29 71 53 8 1 65 16

Ñ 1 Ñ Ñ Ñ 3 54 1 17 Ñ 1 260 Ñ Ñ Ñ 4 28 2 Ñ 2

114 1 24 132 4

L. flaviscutellata (⫽Bi. flaviscutellata) Brumptomyia. avellari Brumptomyia brumpti Brumptomyia sp. L. bourrouli (⫽Ev. bourrouli) L. cortelezzii (⫽Ev. cortelezzii) L. lenti (⫽Ev. lenti) L. teratodes (⫽Ev. teratodes) L. termitophila (⫽Ev. termitophila) Lutzomyia sp. (⫽Evandromyia sp.) Lutzomyia sp. (⫽ Lu. (Castromyia) sp) L. longipalpis (⫽Lu. longipalpis) L. longipennis (⫽Mi. longipennis) L. quinquefer (⫽Mi. quinquefer) L. antunesi (⫽Ny. antunesi) L. whitmani (⫽Ny. whitmani) L. christenseni (⫽Pi. christenseni) L. damascenoi (⫽Pi. damascenoi) L. aragaoi (⫽Pa. aragaoi) L. campograndensis (⫽Pa. campograndensis) L. hermanlenti (⫽Pa. hermanlenti) L. punctigeniculata (⫽Pa. punctigeniculata) L. shannoni (⫽Pa. shannoni) L. claustrei (⫽Ps. claustrei) L. sordellii (⫽Sc. sordellii)

Residential areas Rank

Chać. das Palmeiras

Res. 1

Res. 2

Res. 3

Res. 4

SISA

Rank

0.14 0.56 0.02 0.17 0.02 0.63 0.70 0.25 0.55 Ñ 0.37 1.00 0.14 0.36 0.43 0.77 0.67 0.33 0.41 0.60

19th 8th 20th 18th 20th 6th 4th 16th 9th Ñ 13th 1st 19th 14th 11th 3rd 5th 15th 12th 7th

Ñ Ñ Ñ Ñ Ñ 1 55 Ñ 72 1 Ñ 352 Ñ Ñ Ñ 7 3 Ñ Ñ Ñ

Ñ Ñ Ñ Ñ Ñ 2 1 Ñ Ñ Ñ Ñ 381 Ñ 1 Ñ 2 Ñ Ñ Ñ Ñ

Ñ 1 Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ 267 1 Ñ Ñ Ñ Ñ Ñ Ñ Ñ

Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ 1 Ñ Ñ 7394 Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ

Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ 434 Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ

Ñ 0.12 Ñ Ñ Ñ 0.27 0.25 Ñ 0.33 0.02 Ñ 1.00 0.12 0.12 Ñ 0.27 0.08 Ñ Ñ Ñ

Ñ 7th Ñ Ñ Ñ 4th 5th Ñ 3rd 10th Ñ 1st 7th 7th Ñ 4th 8th Ñ Ñ Ñ

2 Ñ

0.77 0.02

3rd 20th

1 Ñ

Ñ Ñ

2 Ñ

Ñ Ñ

Ñ Ñ

0.17 Ñ

6th Ñ

31 Ñ Ñ

0.79 0.48 0.19

2nd 10th 17th

85 Ñ 2

Ñ Ñ Ñ

3 Ñ Ñ

Ñ Ñ Ñ

Ñ Ñ Ñ

0.35 Ñ 0.06

2nd Ñ 9th

Chać, grange; Res, residence; Bi, Bichromomyia; Ev, Evandromyia; Lu, Lutzomyia; Mi, Micropygomyia; Ny, Nyssomyia; Pi, Pintomyia; Pa, Psathyromyia; Ps, Psychodopygus; Sc, Sciopemyia. The name of the species in brackets is in accordance with Galati (2003), and abbreviation, sensu Marcondes (2007).

myia termitophila, sensu; Galati 2003) were only seen in the pens (Table 4). Table 5 presents a comparison between the yield of the hen house at residence 3 and the kennel at residence 4, as the two areas are ⬇50 m distant from each other. It was observed that the birds (95.2%) are much more attractive than the dogs (4.8%). The performances of the two hen houses were also analyzed; and the one belonging to residence 3 was more productive in relation to the total number of specimens. However, it presented only one species, L. longipalpis, in contrast to the hen house of “Chaćara das Palmeiras,” peripheral area, which, despite a lower number of insects, presented higher diversity (Table 6). In all the shelters the differences obtained were statistically signiÞcant (P ⬍ 0.001 and P ⬍ 0.05).

Discussion The presence of 22 Lutzomyia spp. found in Campo Grande conÞrms the great diversity of fauna described in a previous study (28 species) (Oliveira et al. 2003). The sand ßy composition was similar, with exception of some species typical of forested environments that were seen in the Þrst work but not in the present report. Such fact is mainly because of the selection of the sites, because currently more residential areas were chosen, although a forest site (Ze´ Pereira) was maintained. The captures with light traps have shown to be very efÞcient for the capture of insects with nocturnal habits and were used to study the phlebotomine fauna in the forested (Arias and Freitas 1982, Aguiar et al.

Table 3. Frequency of Lutzomyia longipalpis captured in intra and peridomicile environments, in the urban area of Campo Grande, Mato Grosso do Sul state, in the period Dec. 2003 through Nov. 2005 Environment Site Residence 1 Residence 2 Residence 3 Residence 4 “Chaćara das Palmeiras”

Month (␹2) 65.4* 46.2* 117.9* 56.7* 31.5*

␹2 test for absolute frequencies; GL ⫽ 1. * P ⬍ 0.001, related to traps in the same residence.

Intra

Peri

n

%

n

%

287 101 225 150 35

75.32 37.82 3.04 34.56 9.94

94 166 7169 284 317

24.67 62.17 97.08 65.43 90.05

Total

(␹2)

381 267 7394 434 352

97.76* 15.82* 6521.38* 41.37* 225.92*

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Table 4. Number of phlebotomines captured at different animal shelters in “Chaćara das Palmeiras”, urban area of Campo Grande, Mato Grosso do Sul state, in the period Dec. 2003 through Nov. 2005

Species Brumptomyia avellari L. lenti (⫽Ev. lenti) L. termitophila (⫽Ev. termitophila) L. longipalpis (⫽Lu. longipalpis) L. whitmani (⫽Ny. whitmani) L. shannoni (⫽Pa. shannoni) L. sordellii (⫽Sc. sordellii) L. cortelezzii (⫽Ev. cortelezzii) Total

Goat and sheep pen

Hen house

Pigsty

么

乆

么

乆

么

乆

1 Ñ Ñ 3 Ñ Ñ Ñ Ñ 4

Ñ Ñ 1 4 2 Ñ Ñ Ñ 7

Ñ 32 19 282 4 80 2 1 420

Ñ 12 45 35 3 5 Ñ Ñ 100

1 13 Ñ 49 Ñ 22 1 Ñ 86

Ñ 16 Ñ 25 Ñ Ñ Ñ Ñ 41

Total

␹2

2 73 65 398 9 107 3 1 658

1.0 41.1* 124.9* 401.1* 8.7** 109.1* 2.0 1.0 648.9**

␹2 test of adhesion, GL ⫽ 2. The name of the species in brackets is in accordance with Galati (2003), and abbreviation, sensu Marcondes (2007). * P ⬍ 0.001, ** P ⬍ 0.05.

1985, Galati et al. 2006), peri and intradomiciliary areas of rural settings (Ryan and Brazil 1984, Dourado et al. 1989, dos Santos et al. 2003, Brazil et al. 2006, Michalsky et al. 2009). However, in urban areas, the catches may suffer interference of luminosity that inßuences aspects of the behavior of these dipterans (Shaw and Lainson 1972). The data obtained in Campo Grande, where residential areas presented a greater yield than forested areas (an average of 18.48 and 6.7 phlebotomines/capture, respectively) do not comply with the opinion of the authors above cited. The greatest diversity (Table 1) occurred in “Ze´ Pereira Forest” (H ⫽ 1.9804) with 22 species, followed by “Chaćara das Palmeiras” (H ⫽ 1.2969), which, despite being located in an urban area, shows characteristics of a rural setting, such as breeding of chickens, pigs, goats, and sheep, besides being located near the forest of “Chaćara Wood” that obtained the third highest value (H ⫽ 1.2714). Similar results were previously described in Campo Grande (Oliveira et al. 2003). The same tendency was observed for the evenness index, which remained high in sites with greater diversity of species but very low in residential areas (residence 3 ⫽ 0.0014), where L. longipalpis presented absolute predominance, inßuencing the low values of this index. There was a coincidence between the two most abundant species for forested and residential environments, L. longipalpis and L. shannoni. However, the abundance of the latter is because of its higher frequency in shelters of domestic animals near forested areas.

L. longipalpis, a proven vector of the VL agent in Neotropical Region, presented the highest density in all studied ecotopes in the urban area, both in forested and in totally residential areas. This species is widely distributed and frequently occurs in forested areas, mainly on the slopes (Galati et al. 1996, 2006; Andrade Filho et al. 1998), savannas (Lainson and Rangel 2005) and peridomiciles (Andrade Filho et al. 2001, Galati et al. 2003, Oliveira et al. 2003). The male/female ratio of L. longipalpis was 2.95, a result similar to those previously found for this species in Campo Grande (Oliveira et al. 2003), Porteirinha (Barata et al. 2004), and Janauba, MG (Michalsky et al. 2009), but lower than those found by Margonari et al. (2004) and Resende et al. (2006), in Belo Horizonte, MG. According to Barretto (1943) and Aguiar et al. (1985), captures with light traps can attract more male than female specimens. The possibility of traps being located near the breeding sites is considered. Also observed is the attractiveness of males to the traps when following females with the purpose to form clusters for mating (Feliciangeli 1987). In the two forested areas where L. longipalpis predominated, a statistically signiÞcant difference (P ⬍ 0001) was observed between the two ecotopes, mainly in relation to the quantity of insects captured inside and at the border (both installed close to the ground). In “Ze´ Pereira Forest,” the trap installed inside the forest captured a larger greater number of specimens than the one at the border, probably because of the multiplicity of shelters, the microhabitats rich in or-

Table 5. Frequency of phlebotomines captured at hen houses and kennels of two residences in the central area of Campo Grande, Mato Grosso do Sul state, in the period Dec. 2003 through Nov. 2005 Residence 3 Species L. longipalpis (⫽Lu. longipalpis) L. claustrei (⫽Ps. claustrei) Total

Residence 4

Hen house

Kennel

么

乆

么

乆

5,432 Ñ 5,432

1,737 Ñ 1,737

251 1 252

113 Ñ 113

Total

␹2

7,533 1 7,534

6147.0* 1.0 6147.0*

␹2 test of absolute frequencies, GL ⫽ 1. The name of the species in brackets is in accordance with Galati (2003), and abbreviation, sensu Marcondes (2007). * P ⬍ 0.001.

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Table 6. Frequency of phlebotomines captured at hen houses of two residences in the urban area of Campo Grande, Mato grosso do Sul state, in the period Dec. 2003 through Nov. 2005

L. lenti (⫽Ev. lenti) L. termitophila (⫽Ev. termitophila) L. longipalpis (⫽Lu. longipalpis) L. whitmani (⫽Ny. whitmani) L. shannoni (⫽Pa. shannoni) L. sordellii (⫽Sc. sordellii) L. cortelezzii (⫽Ev. cortelezzii) Total

Chaćara das Palmeiras

Residence 3

Species 么

乆

么

乆s

Ñ Ñ 5,432 Ñ Ñ Ñ Ñ 5,432

Ñ Ñ 1,737 Ñ Ñ Ñ Ñ 1,737

32 19 282 4 80 2 1 420

12 45 35 3 5 Ñ Ñ 100

Total

␹2

44 64 7,486 7 85 2 1 7,689

44.0* 64.0* 6,271.7* 7.0* 85.0* 2.0 1.0 5,549.6*

␹2 test of absolute frequencies, GL ⫽ 1. The name of the species in brackets is in accordance with Galati (2003), and abbreviation, sensu Marcondes (2007). * P ⬍ 0.001.

ganic matter and the large quantity of animals for blood meal. However, in “Chaćara Wood,” the trap at the border captured many more than that in the interior, possibly on account of the proximity of shelters of domestic animals on the nearby land, providing food and shelters, as observed in Serra da Bodoquena by Galati et al. (2003). With regard to residential areas (Table 3), in all sites of capture, except residence 1, the peridomicile was the most attractive site to L. longipalpis, due mainly to the presence of domestic animals as well as the adaptation to urban microhabitats, leading to the development of these insects surrounding the houses. This tendency was observed in Montes Claros (Monteiro et al. 2005), Janauba (Michalsky et al. 2009), and Belo Horizonte, all in Minas Gerais state (Margonari et al. 2004, Resende et al. 2006), in Teresina and other municipal districts of Piauõ´ state (Costa et al. 1990, Andrade Filho et al. 2001). Still in reference to the peridomiciliary environment, the observed high density of vectors increases the possibility of transmitting leishmaniasis in these places (Deane and Deane 1962, Sherlock and Guitton 1969, Brazil et al. 1991, Andrade Filho et al. 2001, Souza et al. 2002, Margonari et al. 2004). The presence of shelters for domestic animals and the poor hygiene conditions also contribute to the high density of L. longipalpis (Ximenes et al. 1999). In “Chaćara das Palmeiras,” among the three studied shelters, the hen house yielded best, with 79% of captured specimens; and the pigsty came second in yield and diversity. L. longipalpis prevailed in all ecotopes and, in view of the quantity of males in relation to females, these environments may be said to be the breeding sites of this species, reinforcing the hypothesis of Galati et al. (2003) concerning the importance of the pigsty as a place for breeding and maintenance of the high density of specimens captured at Guaicurus settlement in Bonito, Mato Grosso do Sul state. Otherwise, the goat and sheep pen showed to be poorly attractive, conÞrming the observations of Galati et al. (2003) during captures by aspiration in sheep in contrast to Deane (1956), in Ceara´ state, and Ximenes et al. (1999), in Rio Grande do Norte state,

who reported the phlebotomine preference for large animals (equines and bovines). In the two residences located in the central area, two peridomiciles were compared, one with a kennel and another with a hen house. In the former 20 times more sand ßies were captured than in the latter, demonstrating the strong attraction that birds exert on sand ßies (Table 5). This fact corroborates the data obtained by Lainson et al. (1983) and Oliveira et al. (2008b) about the preference of these insects for birds, especially in view of the proximity of the two sites. Furthermore, the hen house was responsible for 67.1% of the total of specimens captured and 74.2% of the specimens of L. longipalpis, which demonstrates the role of birds as responsible for the high density of these species of phlebotomines. When analyzing the location of the house, some peculiarities of the residential quarter were observed, which may also be associated with high density, such as: the terrainÕs dimensions (20 ⫻ 60 m), larger than the local pattern (12 ⫻ 30 m), enabling land owners to grow fruit trees, vegetables, and breed animals; and the large amount of organic matter in decomposition on the soil because of the deÞciency of environmental education. This could be evidenced by the abrupt decrease in number of specimens after the deactivation of the hen house by the land ownersÔ initiative in December 2005. The presence of shelters for domestic animals, especially hen houses, seems to be a risk factor for the maintenance of the elevated density of the species. With this observed dominance and density there seem to be no doubts about the vector role of L. longipalpis in Campo Grande. Such characteristics derive from its high degree of adaptation to the artiÞcial environment, conferring it the ability to survive in adverse conditions when compared with those of their natural habitat. The presence of forests near residences can work as a stock place for the repopulation of the houses when submitted to the action of insecticides. Besides L. longipalpis, the most prominent in this study, there are other species captured in lower density in the urban area of Campo Grande which also require special attention because of their implication

January 2012


in the transmission of ACL agents: L. whitmani, one of the main vector of Leishmania (Viannia) braziliensis, L. antunesi, a suspect vector of Leishmania (Viannia) lindenbergi in Para´ state and L. flaviscutellata, the main vector of Leishmania (L.) amazonensis with wide distribution in Brazilian areas, including in Mato Grosso do Sul (Lainson & Shaw 2005, Dorval et al. 2010). Acknowledgments To Orcy de Oliveira, for assistance on Þeld activities, laboratory and equipment maintenance. To the local residents, who assisted us in a patient and courteous way. To the staff of the Laboratory of ParasitologyÐUFMS, for their collaboration; and to UCDB administration staff, for their logistical support. We thank FUNDECT 498/02, DECIT/ FUNDECT- 41/100208/2003, FIOCRUZ, FAPERJ, for Þnancial support.

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