Ecology of sand flies near São Manoel hydroelectric plant, southern Brazilian Amazon, including a new species of Trichophoromyia (Diptera: Psychodidae: Phlebotominae)

ABSTRACT

A sand fly survey was carried out as part of the environmental risk assessment surrounding the construction of a hydroelectric power plant at the Teles Pires River, at the boundary between the Brazilian states of Mato Grosso and Pará. In order to evaluate the diversity and similarity of the sand fly communities in sylvatic forest and domestic environments, sand flies were collected every three months for two years (January 2015 to July 2017). A total of 1,682 sand flies distributed in 14 genera and 59 species were collected. In the forest, 1,364 individuals distributed in 14 genera and 54 species were collected; the most abundant species were Psychodopygus davisi (Root, 1934) (16%) followed by Trichophoromyia sp. (12%) and Nyssomyia antunesi (Coutinho, 1939) (9%). In domestic environments, 318 individuals were collected from 10 genera and 29 species, with Evandromyia termitophila (Martins, Falcão & Silva, 1964) (37%) being the most abundant species, followed by Nyssomyia delsionatali Galati & Galvis, 2012 (8%) and Evandromyia walkeri (Newstead, 1914) (8%). Non-metric multidimensional scaling and non-parametric permutational multivariate analysis of variance of sand fly relative abundance and species occurrence indicated significant differences in the sand fly fauna between sylvatic forest and human-associated environments. New state-level occurrence records for eight species are also reported and Trichophoromyia dilermandoi sp. nov. is described. This new species can be distinguished from similar species by the rectangular shape of the paramere, the presence of 10-12 setae in the gonocoxite and the aedeagal ducts/sperm pump ratio of 5.7.

KEYWORDS:
Environmental risk assessment; new records; taxonomy; vector

INTRODUCTION

Hydroelectric power plants are construction projects are important for economic and social development in Brazil. However, such projects typically disrupt natural habitats. In the Amazon region, they result in the destruction of large areas of forest, with many negative impacts on the environment, its biodiversity and indigenous communities (Forattini 1973, Gomes and Galati 1987, Castello and Macedo 2016, Moreno et al. 2018). The study of the impacts of hydroelectric power plant construction on biodiversity is paramount for the preservation of species and ecosystem functions, since it makes it possible to collect data on the adaptive capacity or vulnerability that environmental changes can trigger. With these studies, it is possible to monitor population susceptibility and evaluate the impact of specific interventions (Gomes 2002). In addition, novel human incursion into, and disruption of, sylvatic forested areas is often associated with altered and/or increased infectious disease transmission, especially of zoonotic vector-borne diseases (Moreno et al. 2018, Vilela et al. 2011).

Studies on the faunal composition of sand fly communities in disturbed habitats are necessary to evaluate the impact of human-made changes in the landscape will have on the health of the population. Changes related to climatic variations and environmental modifications such as the impacts caused by the construction of hydroelectric dams represent a risk for the expansion of species of medical importance from previously preserved forest areas into environments with human occupation (Walsh et al. 1993, Campbell-Lendrum et al. 2001, Shaw 2007, Vilela et al. 2011).

In Brazil, the Amazon region has a very high diversity of sand flies species (Shimabukuro et al. 2017), which are small dipterans, and in the Amazon region many of their species are vectors of protozoa of the genus Leishmania Ross, 1903, the etiological agent of leishmaniases (Lainson et al. 1994, WHO 2010), as well various phleboviruses and bacteria (Herrer and Christensen 1975).

The objective of this study was to evaluate the diversity and similarity of sand flies in different forest and domestic environments in the region surrounding the construction of the São Manoel Hydroelectric Power Plant, on both banks of the Teles Pires River in the municipalities of Paranaíta, in the state of Mato Grosso, and Jacareacanga, in the state of Pará.

MATERIAL AND METHODS

Study area

The study was carried out in Paranaíta, located in the central northern region of the state of Mato Grosso, with approximately 11,000 inhabitants (IBGE 2017), and in Jacareacanga, located in the southwest region of the state of Pará, and it has about 41,000 inhabitants and the largest indigenous population of Pará, with approximately 10,000 indigenous people (Fig. 1) (IBGE 2017). The climate of the region, according to the classification of Köppen (Alvares et al. 2013) can be characterized as Tropical Monsoon Climate (Am). This climate is characterized by average temperatures above 26 °C throughout the year. Some months are very dry, with an average of less than 60 mm of precipitation, and about 2,800-3,100 mm of total annual precipitation (Alvares et al. 2013).

Figure 1
Study area in the municipalities of Paranaíta, Mato Grosso, and Jacareacanga, Pará. (F) Forest, (D) domicile. Gray line depicts border between the two states. Map data ©2019 Google.

The site for the implementation of the São Manoel Hydroelectric Power Plant is located in the region of the middle Teles Pires River, approximately 330 km from the junction with the Juruena River, where the Tapajós River forms. In addition to the environmental impact of the implementation of the São Manoel Hydroelectric Power Plant, the region still suffers from the impacts of agriculture and livestock husbandry. The main type of vegetation at and around the power plant site is Amazon rainforest.

Collection and identification of sand flies

Samples of sand flies were collected between October 2015 to April 2017, at three-month intervals using HP light traps (Pugedo et al. 2005), which were operated from 5:00 pm to 6:00 am of the following day. The HP traps were installed 1.5 m above the ground. Sand flies were collected in both forest and domiciliary environments. In all sites in which the domiciliary environment was sampled, a total of 12 traps were used: six houses were selected, and one trap was installed inside of each house, and another trap was installed outside each house, inside or nearby hen houses. The selected houses were located along the road that gives access to the power plant near the construction site, and in the surroundings of the quarters of the power plant workers. In the forest environment, a total of 12 traps were used: 12 sites were selected, and a single trap was installed at each site, with six traps placed on the banks of the Teles Pires River, and six traps placed in forest fragments remaining after recent deforestation associated with the power plant construction (Table 1).

Table 1
Details of the collection sites sampled in forest environments and domestic environments in Paranaíta, in the state of Mato Grosso, and Jacareacanga, in the state of Pará, between October 2015 and April 2017.

State	Municipality	Location	Collections	Coordinates
Pará	Jacareacanga	Forest 1	8	9°13’6.23”S, 56°57’34.96”W
Pará	Jacareacanga	Forest 2	6	9°13’35.01”S, 56°52’19.98”W
Pará	Jacareacanga	Forest 3	3	9°18’23.89”S, 56°46’41.72”W
Mato Grosso	Paranaíta	Forest 4	5	9°13’41.20”S, 56°57’39.17”W
Mato Grosso	Paranaíta	Forest 5	8	9°14’56.30”S, 56°52’15.71”W
Mato Grosso	Paranaíta	Forest 6	3	9°18’39.40”S, 56°48’0.20”W
Pará	Jacareacanga	Forest 7	3	9°’11’7.00”S, 57°0’42.00”W
Pará	Jacareacanga	Forest 8	4	9°11’24.00”S, 57°2’23.00”W
Mato Grosso	Paranaíta	Forest 9	1	9°14’16.00”S, 57°0’14.00”W
Pará	Jacareacanga	Forest 10	3	9°7’49.60”S, 56°51’16.80”W
Pará	Jacareacanga	Forest 11	4	9°9’49.18”S, 56°44’35.92”W
Mato Grosso	Paranaíta	Forest 12	4	9°18’8.28”S, 56°59’40.61”W
Mato Grosso	Paranaíta	Domicile 1	4	9°27’11.70”S, 56°29’28.90”W
Mato Grosso	Paranaíta	Domicile 2	8	9°19’10.00”S, 6°58’53.23”W
Pará	Jacareacanga	Domicile 3	5	9°15’14.10”S, 56°35’23.70”W
Pará	Jacareacanga	Domicile 4	5	9°9’58.20”S, 56°44’28.50”W
Pará	Jacareacanga	Domicile 5	6	9°7’45.10”S, 56°53’55.65”W
Mato Grosso	Paranaíta	Domicile 6	7	9°26’7.03”S, 56°45’29.41”W

In the field, sand flies collected in each trap were screened and stored in 1.5 ml microtubes submerged in 80% ethanol and transported to the laboratory. The insects were prepared according to Langeron (1949) and identified following the key and classification proposed by Galati (2003, 2018). The abbreviation of generic names was made according to Marcondes (2007). The specimens have been deposited in the Coleção de Flebotomíneos (FIOCRUZ/COLFLEB) of the Instituto René Rachou, Fiocruz Minas.

Sand flies were collected under the state of Tocantins permit number 586/2015 and the SISBIO license #12433-3 of the Ministry of the Environment of Brazil.

Data analysis

The similarity of the sand fly species community composition was compared using non-metric multidimensional scaling (NMDS), with the data categorized according to the three collection environments: forest, and inside and outside of houses (i.e., intra- and peridomestic, respectively). For the relative abundance of sand flies, the dissimilarity matrix was calculated using the Bray-Curtis index, while for species presence-absence the Jaccard index was used. A non-parametric permutational multivariate analysis of variance (npPERMANOVA) was also used with 999 replications of the distance matrices (Anderson 2001) to statistically test differences between the collection environments in the relative abundance and occurrence of sand flies. All analyzes were performed using the vegan package (Oksanen 2010) of the software R version 3.2.4 (R Core Team 2010). Due to variation in the number of collections made in each environment (Table 1), for both NMDS and npPERMANOVA, the abundance data were first standardized by dividing the number of individuals of each species of sand fly collected by the number of samples collected in each environment.

The final dataset was mapped and formatted to Darwin Core Standard (Wieczorek et al. 2012) and publish in the Global Biodiversity Information Facility as an occurrence dataset (Lopes et al. 2024).

Description of the new species

During the entomological surveys reported here, a new species was discovered. For description of the new species, a LEICA M205-C model stereomicroscope was used for measurements that are given in micrometers (µm). The arithmetic means and standard deviation of the type specimens are given between brackets. The drawings were made with the aid of a camera lucinda using an Olympus CBX microscope, and subsequently edited in the GIMP software (GIMP 2019). The description of the new species and the name of the terminology are in accordance with Galati et al. (Galati et al. 2017) and Cumming and Wood (Cumming and Wood 2009).

RESULTS

A total of 1,682 sand flies belonging to 14 genera and 59 species were collected, comprising 865 (51.4%) males and 817 (48.6%) females (Appendix 1).

The collected sand flies conformed to the classic pattern of species abundance distributions, with relatively few highly abundant species, and many relatively rare species of increasingly lower abundance. In addition, in general, the abundance and occurrence of different sand fly species tended to be patchy, especially occurrence for less abundant species, which were typically collected in only one or a small number of sites.

The most abundant genera collected during the study were: Psychodopygus Mangabeira, 1941 (n = 541; 32%), Nyssomyia Barretto, 1962 (n = 329; 20%) and Trichophoromyia (n = 322; 19%). The most abundant species were Psychodopygus davisi (Root, 1934) (n = 222; 13%) and Nyssomyia antunesi (Coutinho, 1939) (n = 128; 8%). A relatively large number of Trichophoromyia females were also collected (n = 162; 10%), but given their morphological similarity, their species identity could not be determined. In addition, a new species of Trichophoromyia was collected in the forest environment only, which was relatively abundant in comparison to most other sand fly species (n = 63; 3.7%), and is described below.

Some female specimens (n = 298; 17.7%) were identified only to the genus-level due to morphological similarities of important structures for identification at species-level, such as the spermatheca and cibarium. Such specimens were the genera Evandromyia Mangabeira, 1941, and Trychopygomyia Barretto, 1962, as well as the Trichophoromyia and Psychodopygus mentioned above. Also, some other specimens (n = 20; 1.2%) had damaged structures that could not be observed for species-level identification. Such specimens were from Migonemyia Galati, 2003, Nyssomyia, Psathyromyia Barretto, 1962, and Sciopemyia Barretto, 1962.

In the forest environment, 1,364 (81.1%) individuals were collected from 14 genera and 54 species, of which 655 (48%) were males and 709 (52%) were females (Appendix 1). The most abundant species were Ps. davisi (n = 222; 16%) and Ny. antunesi (n = 128; 9%). Again, undetermined specimens of Trichophoromyia sp. (n = 160; 12%) were abundant in the forest environment. In the forest environment, 719 individuals were recorded from a single site (Forest 4; F4), which corresponds to 53% of the total collected in this environment. Thirty-two (52%) of the sand flies species collected in forest were found only in this environment.

In the domiciliary environments, 318 (18.9%) individuals were collected from 10 genera and 30 species, of which 137 (43%) were males and 181 (57%) females (Appendix 1). In the intradomicilary sites, a total of 63 specimens distributed in 14 species and 6 genera were collected, and in the peridomestic sites, a total of 255 specimens were collected and they were distributed in 27 species. Overall, in both intra and peridomestic sites, the most abundant species were Evandromyia termitophila (Martins, Falcão & Silva, 1964) (n = 118; 37%), Nyssomyia delsionatali Galati & Galvis, 2012 (n = 26; 8%) and Evandromyia walkeri (n = 24; 8%). Of the domiciliary environments, one household (Peri6) was highlighted by the largest number of sand flies collected, 86 (27%) individuals. Two sand flies species, Pa. campograndensis and Ps. wellcomei collected in this environment were found only in the domiciliary environment.

The following species of medical interest were recorded in both anthropic and forest environments: Bi. flaviscutellata, Mg. migonei, Ny. antunesi, Ny. delsionatali and Ny. whitmani. Exclusive to the forest environment were: Ny. anduzei, Ny. umbratilis, Ps. ayrozai and Ps. davisi and Ps. wellcomei was only sampled from the intradomicialiar environment.

Overall, our entomological surveys included nine new state-level occurrence records, as follows. The species Micropygomyia acanthopharynx (Martins et al., 1962), Ny. delsionatali, Psathyromyia hermanlenti (Martins et al., 1970), Psathyromyia runoides (Faichild & Hertig, 1953) and Trichopygomyia rondoniensis (Martins et al., 1965) were recorded for the first time in the state of Pará. The species Evandromyia georgii (Freitas & Barrett, 2002) and Trichopygomyia trichopyga (Floch & Abonnenc, 1945) were recorded for the first time in the state of Mato Grosso and Psathyromyia campograndensis (Oliveira et al., 2001) recorded for the first time in both states.

The NMDS calculated with the data of relative abundance of sand fly species and species presence-absence data between forest and domestic environments (both intra and peridomestic sites), explained 62% and 60% of the data variation in the two axes, respectively. Permutation tests showed that both the relative abundance and occurrence of sand fly species differed significiantly between the forest and domiciliary environments, although “environment” only accounted for a relatvely small amount of variation (~16%) in sand fly diversity PERMANOVA: Df= 1; F = 5.11; R² = 0.19; p = 9,999e-05*** and Df = 1; F = 3.51; R² = 0.14; p = 9,999e-05***, respectively (Fig. 2).

Figure 2
Comparison of sand fly diversity in domestic and sylvatic sites using non-metric multidimensional scaling (NMDS). The dissimilarity matrices used for NMDS were calculated using either the Bray-Curtis (A) or Jaccard (B) indices derived, respectively, from the relative abundance or presence-absence (i.e., occurrence) of sand fly species at each collection site. Collection sites: Domestic environments and sylvatic. The numbers of the collection sites indicate different sites, corresponding to those shown in Fig. 1 and listed in Table 1 and Appendix 1.

TAXONOMY

Trichophoromyia dilermandoi Lopes & Shimabukuro, sp. nov.

Figs 3-8

https://zoobank.org/2D2B519D-D4E9-40C7-94ED-2568647A26BB

Diagnosis. Paramere rectangular and without a fringe of long setae on the dorsal lobe. Presence of 10-12 setae in the gonocoxite and the aedeagal ducts/sperm pump ratio of 5.7.

Type material: Holotype male (slide number 91566), BRAZIL: Pará state, Jacareacanga; 9°13’6.23”S, 56°57’34.96”W; 201; Lopes et al. leg.; collected in the right margin of the Teles Pires River, Aragão site, forest, HP light trap. Paratypes males (slide numbers provided between brackets): right margin of the Teles Pires River, Aragão site, Jacareacanga, Pará state; 9°13’6.23”S, 56°57’34.96”W; vii.2016 (91601, 91620), x.2016 (91561, 91560, 91567, 91568, 91569, 91570, 91571), 15-19.i.2017 (91572, 91573, 91593, 91619, 91616, 91585). In addition, we have identified and deposited 57 slides from the same localities under numbers 91562-91565, 91574-91584, 91586-91592, 91594-91600, 91602-91615, 91617-91618 and 91621-91622. All slides have been deposited in Coleção de Flebotomíneos (FIOCRUZ/COLFLEB) of Instituto René Rachou, Belo Horizonte, Brazil.

Description. Male. Head. (Fig. 3) Length 344 (323 ± 105; n = 10), width 316 (321 ± 22; n = 8). Eyes: length 185 (191 ± 12; n = 8), width 120 (108 ± 10; n = 6) (front view). Interocular distance 114 (113 ± 11; n = 7). Clypeus: length 97 (105 ± 9; n = 11), width 60 (66 ± 12; n = 11) Flagellomeres (Fig. 4) Length of the flagellomeres: FI 216 (206 ± 11; n = 10), FII 123 (119 ± 5; n = 10), FIII 125 (120 ± 5; n = 10), FXII 63 (63 ± 3; n = 9) e FXIII 47 (51 ± 2; n = 9). Ascoids without posterior prolongation in all segments, Posterior extension of the long ascoid in F1, F2 and F3, reaching the next segment. Antennal formula AIII 2, AXIV-AXIV 2, AXV-AXVI 0. Palpi (Fig. 5): Length of the palpi: PI 25 (23 ± 3; n = 12), PII 87 (85 ± 5; n = 11), PIII 120 (105 ± 31; n = 9), PIV 40 (48 ± 6; n = 7), PV 161 (136 ± 30; n = 6). Newstead’s sensilla concentrated in the middle portion of PIII and two sensilla are also found in the pre-apical portion of PII. Cervix. Ventro-cervial sensillae absent.

Figures 3-5
Trichophoromyia dilermandoi sp. nov., adult male holotype: (3) head; (4) antenna and palpi: (A-C) flagellomeres: (A) I, (B) II, (C) III, (D) XII, (E) XIII, (F) XIV; (G-I) palpi: (G) segments I and II, (H) segment III, (I) segment IV; (5) wing. Scale bars: 3 = 100 µm, 4-5 = 50 µm.

Thorax. Mesonotum and metanotum dark brown, pronotum, mesopleuron, metapleuron and coxae brown. Mesonotum 472 (497 ± 19; n = 12) long. Pleura with four proepimeral setae (3-7; n = 11) and 12 upper anepisternal setae (8-12; n = 11) and metaepisternal and metapimeral setae absent. Wing (Fig. 6): Length 1,969 (1,983 ± 60; n = 12), width 502 (528 ± 29; n = 12). Alpha 459 (540 ± 47; n = 12), beta 275 (278 ± 23, n = 12), gamma 227 (225 ± 20; n = 12), delta 275 (311 ± 38, n = 11), pi 124 (127 ± 13, n = 11), R5 = 1,134 (1,199 ± 50, n = 12). Legs. Some measurements were based on paratypes 4 and 10 because they were lost (or broken) in the holotype: Femur length: anterior 810 (809 ± 51; n = 6), middle 690 (727 ± 33; n = 3), posterior 853 (paratype 10) (842 ± 15; n = 2). Length of tibia: anterior broken in the holotype (1,060 ± 314; n = 5), middle (paratype 10) 1,063 (1.168 ± 148; n = 2), posterior 1,522 (paratype 10) (1,512 ± 14; n = 2). Length T1: anterior 662 (661 ± 149; n = 4), middle (paratype 10) 780 (774 ± 9; n = 2) posterior (paratype 4) 818 (n = 1). Extension T2 +: anterior 773 (744 ± 95; n = 3).

Abdomen: Length 1,678 (1,516 ± 108; n = 12).

Figure 6
Terminalia of the adult male holotype of Trichophoromyia dilermandoi with details of the paramere. Scale bar = 50 µm.

Terminalia (Fig. 7): gonostylus 212 (213 ± 8; n = 12) long, with four spines; the spines having the following arrangement: an apical, the upper external inserted on the apical third and the lower external between the external upper and internal spines, the internal is located before the middle section of the gonostylus. Gonocoxite: Length 321 (348 ± 29; n = 12), width 110 (116 ± 20; n = 12), with a median tuft with 9-12 strong, thick setae (n = 6) and 2-3 thin basal setae (n = 60). Short paramere with a square lobe in the basal half of the dorsal margin, the dorsal margin of this lobe is covered by setae of different widths and at the edge of the square, there are two setae pointing toward the tip of the epandrial lobe (Fig. 8). Paramere length: dorsal margin 111 (172 ± 58; n = 12), ventral margin 117 (112 ± 8; n = 12). Parameral sheath: length of the dorsal margin of the ventral branch 46 (57 ± 11; n = 11) and length of the ventral margin of the ventral branch 47 (38 ± 9; n = 11). Epandrial lobe: 390 (402 ± 24; n = 12) long, 30 (31 ± 2; n = 12) wide. Cercus 113 (n = 1) (from paratype 5). Sperm pump (Fig. 8): 159 (170 ± 12; n = 12) long. Ejaculatory apodeme (piston) 125 (133 ± 8; n = 12) long; Sperm sac: 45 (46 ± 4; n = 12) long. Aedeagal ducts (Fig. 8) 917 (917 ± 4; n = 11) long. Aedeagal ducts/sperm pump ratio 5.7.

Figure 7
Photo of the terminalia and paramere of the adult male holotype of Trichophoromyia dilermandoi. Scale bar = 100 µm.

Figure 8
Sperm ducts and pump of the adult male holotype of Trichophoromyia dilermandoi. Scale bar = 50 µm.

Female: Unknown.

Distribution: Brazil, Pará state.

Etymology. This species is named after Dr. José Dilermando Andrade Filho, a researcher and colleague at the Instituto René Rachou, FIOCRUZ/MG, for his considerable contribution to the study of sand flies.

Remarks. Trichophoromyia is currently comprised of 47 species (Galati 2018). This genus is identified by the following characters: dark body colour, the fourth palpus segment shorter than the second, and the presence of Newstead’s sensilla in the second palpus segment of both sexes. The males present the gonostylus with four well developed spines, and the apical spine is shorter than the length of the gonostylus; the size of the genitalia is equal to the length of the thorax. The females present two longitudinal rows of external teeth in the lacinia of the maxilla. In females, the spermathecae presents 25 or more rings, the apical being three or more times larger than the pre-apical (Galati 2018). However, in this genus, the great majority of females are isomorphic, which makes it impossible to differentiate them, such that the identification of most species is only possible for male specimens (Galati 2018, Young and Duncan 1994). There are six Trichophoromyia species in which the aedeagal ducts are four times longer than the sperm pump, the paramere presents a dorsal lobe, and the gonocoxite is three times longer than it is width: Th. castanheirai (Damasceno et al., 1945), Th. napoensis (Young & Rogers, 1984), Th. beniensis (Le Pont & Desjeux, 1987), Th. howardi (Young, 1979), Th. readyi (Ryan, 1986) and Th. sp. 1 de Araracuara (Morales & Minter, 1981) (unavailable name according to article 11.4 of the ICZN). Compared to these species, Th. dilermandoi sp. nov. can be differentiated from Th. napoensis and Th. beniensis based on the shape of the dorsal lobe of the paramere, which is triangular in these species and rectangular in Th. dilermandoi. In addition, both of the former species have more than 15 setae in the gonocoxite, while Th. dilermandoi presents 10-12 setae. Trichophoromyia howardi, Th. readyi and Th. sp. 1 de Araracuara can be differentiated by the shape of the dorsal lobe of the paramere, which is rounded, while Th. castanheirai can be distinguished from our new species based on the length of the digitiform region of the paramere, which is six times longer than it is wide in Th. castanheirai species and two times longer than it is wide in Th. dilermandoi. The presence of a fringe of long setae on the dorsal lobe of the paramere also differentiates Th. castanheirai, which are short and sparse in the new species.

DISCUSSION

Our results showed a rich and abundant fauna of sand flies in forest and domiciliary environments around the São Manoel hydroelectric power plant. The high richness and abundance of species recorded in these environments were expected, since it is part of the Amazon region (Shimabukuro et al. 2017, Young and Duncan 1994). This region contains the largest number of sand fly species worldwide, due to its humid climate, habitat diversity and wide variety of shelters, food sources and other resources (Lainson 1988).

The sand fly fauna differed between forest and house environments for relative abundance data and species occurrence. The difference found for occurrence of sand fly species among the environments sampled is due to the large number of exclusive species among them, which suggests that many species are not dispersing between anthropogenic and sylvatic environments. With regard to the difference found for the relative abundance of sand fly species between forest and anthropogenic environments, it was possible to observe that the most abundant species in house environments were not the most abundant species in forest environment and vice versa, and this explains the dissimilarity found between anthropogenic and sylvatic environments.

Ecological studies have already shown that the variation of sand fly fauna composition can occur according to local availability of resting and breeding sites, their adaptation to the niche, food sources, soil and anthropic action (Chagas et al. 2018, Pereira Junior et al. 2019, Rebelo et al. 2019).

The dissimilarity found for the fauna of sand flies between forest and domiciliary environments has been reported in different areas of the Brazilian Amazon, and can be on account of anthropic changes, such as deforestation, at different scales (small human settlements, dam and road construction, agribusiness, etc.), which can affect sand fly fauna significantly by reducing vertebrate host availability and altering the microclimatic conditions that are appropriate for sand fly development (Campos et al. 2013, Rebelo et al. 2019). On the other hand, some sand fly species can adapt to peridomestic environment, because domestic animals and animal shelters provide sources of food and breeding sites, respectively (Feitosa and Castellón 2006, Ramos et al. 2014).

The three most abundant taxa (Ps. davisi, Trichophoromyia sp. and Ny. antunesi/urbinatti) in the forest environment accounted for 36% of the total number of sand flies collected in that environment. The high abundance of Ps. davisi and Ny. antunesi/urbinatti (the females of these two species are indistinguishable) are consistent with findings in similar environments of the Amazon (Gil et al. 2009, Silva et al. 2014, Galardo et al. 2015, Pereira Junior et al. 2019). There was also a high abundance of Trichophoromyia females, which could not be identified to species-level because most females in this genus are isomorphic. Among the three Trichophoromyia species collected, only the female of Th. ubiquitalis can be differentiated. Therefore, it is likely the high numbers of unidentified females belong to one or both of the other two species collected in our study-either Th. octavioi or Th. dilermandoi, whose male is described here.

Both Ps. davisi and Ny. antunesi have been associated with Le. sp. transmission, and are anthropophilic species (Grimaldi Jr et al. 1991, Silveira et al. 2002, Gil et al. 2003). Contrary to our findings, Ps. davisi has been recorded in peridomestic areas of the Amazon (Silva et al. 2021) and it has been reported as a sucpected vector of Le. naiffi in Rondônia (Gil et al. 2003), while Ny. antunesi has been reported as a suspected vector in Colombia (Vásquez-Trujillo et al. 2021), it has also been found with DNA from Le. naiffi in areas of Rondônia state (Silva et al. 2021) and Le. sp. in Mato Grosso and Pará states (Ryan et al. 1984, Thies et al. 2013).

Species of medical interest such as Bi. flaviscutellata, Mg. migonei, Ny. antunesi, Ny. delsionatali and Ny. whitmani were recorded in both anthropic and forest environment. These five species have been found in both environments in areas of Porto Velho, Rondônia state (Silva et al. 2021), also Bi. flaviscutellata has been recorded in both peridomestic and forest areas of Pará and Maranhão states (Carvalho et al. 2018, Rebelo et al. 2019).

In the domicilary environment Ev. termitophila, Ny. delsionatali and Ev. walkeri accounted for 53% of the total of sand flies collected in that environment. Both Ev. termitophila and Ev. walkeri have been previously found in peridomiciliary areas, as well as in forested areas (Alves et al. 2012, Machado et al. 2012, Silva et al. 2014), these species could play a role in the transmission of Leishmania among wild animals (Rego et al. 2015, Fonteles et al. 2018, Lopes et al. 2021). Nyssomyia delsionatali has been found from remnant forests near the banks of the Teles Pires River, in the state of Mato Grosso, mainly in chicken coops located between forest fragment and houses (Galati and Ovallos 2012). It is possible that the high abundance of these species in the domiciliary region is related to the proximity of the households to the forest and these species are attracted to domestic animals (Ramos et al. 2014, Resadore et al. 2017, Pereira Junior et al. 2019). This suggests that sand flies are adaptable to human-modified environments which can lead to increased contact between humans and sand flies increasing the risk of leishmaniases transmission (Ramos et al. 2014). In this regard, it is particularly noteworthy that we found Ny. whitmani at a relatively low abundance in both intra- and peridomestic locations, as this important sand fly vector species is generally regarded as not being anthrophilic or capable of adapting to human-associated environments within the Amazon region (Lainson 1988, Rangel and Lainson 2009).

The importance of Pa. campograndensis in the transmission of Leishmania to humans is unknown to date, there are few records of anthropophily in species of Psathyromyia (Gomes and Galati 1987, Moschin et al. 2013), and Ps. wellcomei is an incriminated vector of Le. braziliensis (Ward et al. 1973, Ryan et al. 1987).

Here, we present new records for Mi. acanthopharynx, Ny. delsionatali, Pa. hermanlenti, Pa. runoides and Ty. rondoniensis recorded for the first time in the state of Pará, Pa. campograndensis is recorded for the first time in both Pará and Mato Grosso, increasing the number of species recorded for Pará from 118 (Shimabukuro et al. 2019) to 124. The new records for Mato Grosso include also Evandromyia georgii (Freitas & Barrett, 2002) and Trichopygomyia trichopyga (Floch & Abonnenc, 1945) increasing the number of species from 111 to 114 (Shimabukuro et al. 2019). The collections were carried out in areas of both preserved and deforested Amazon forest located in the border between the states of Pará and Mato Grosso, so it is not surprising that species with well-known Amazonian distribution already recorded in one or the other (i.e., Ev. georgii, Ty. rondoniensis, Ty. trichopyga, Pa. campograndensis and Ny. delsionatali) are found in our study. The records of Mi. acanthopharynx and Pa. hermanlenti expand the occurrence of these species which are found in savannah-like environments (cerrado) and the Amazon forest. The record of Pa. runoides in Pará is interesting because it fills in a gap in the known distribution of these species, which has has been recorded in other states comprising the Brazilian Amazon (with the exception of Amapá and Maranhão), as well as in the cerrado areas of Minas Gerais in the southeast of Brazil. This species has been described from Panama and presents a trans-Andean distribution (Galati 2018), which might suggest it is a species complex, or even a not closely-related species, and further investigation on the taxonomic status of this taxon is needed.

This study contributes to the knowledge of the fauna of sand flies in an area under environmental impact resulting from the construction of a large hydroelectrical powerplant in the Amazon forest. The fauna of sand flies was diverse and abundant, and the composition and relative abundance of the species was different between forest and domiciliary environments. In addition, incriminated Leishmania vector species were recorded in all sampled environments. This fact draws attention to both the risk of humans entering sylvatic areas with their native fauna, as well as the dispersal of species of sand flies from forest environments into places where there are human dwellings and large numbers of workers in the vast region impacted by the hydroelectric construction project. New occurrence records are provided, and a new species is described suggesting that there may be others not yet known in the region, because of its rich and abundant sand fly fauna.

ACKNOWLEDGEMENTS

We would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior for the scholarship to TAL (Finance Code 001), and the company BIOLEX Consultoria Ambiental for providing logistical support and funding for the fieldwork. PHFS would like to thank additional financial support given by the Fundação de Amparo à Pesquisa de Minas Gerais (process PPM-00676-18). We also thank Luke Baton for editing the English and for providing comments on draft versions of this manuscript.

LITERATURE CITED

• Alvares CAPC, Stape JLM, Sentelhas JLM, Gonçalves JL, Parovek G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728. https://doi.org/10.1127/0941-2948/2013/0507
  » https://doi.org/10.1127/0941-2948/2013/0507
• Alves GB, Oshiro ET, da Cruz Leite M, Melão AV, Ribeiro LM, et al. (2012) Phlebotomine sandflies fauna (Diptera: Psychodidae) at rural settlements in the municipality of Caceres, State of Mato Grosso, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 45: 437-443. https://doi.org/10.1590/S0037-86822012005000010
  » https://doi.org/10.1590/S0037-86822012005000010
• Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Australian Ecology 26: 46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
  » https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
• Campbell-Lendrum D, Dujardin JP, Martinez E, Feliciangeli MD, Perez JE, Silans LN, Desjeux P (2001) Domestic and peridomestic transmission of American cutaneous leishmaniasis: changing epidemiological patterns present new control opportunities. Memórias do Instituto Oswaldo Cruz 96: 159-162. https://doi.org/10.1590/S0074-02762001000200004
  » https://doi.org/10.1590/S0074-02762001000200004
• Campos AM, Matavelli R, Santos CL, Moraes LS, Rebelo JM (2013) Ecology of phlebotomines (Diptera: Psychodidae) in a transitional area between the Amazon and the Cerrado in the State of Maranhão, Brazil. Journal of Medical Entomology 50(1): 52-58. https://doi.org/10.1603/ME12074
  » https://doi.org/10.1603/ME12074
• Carvalho BM, dos Santos TV, Barata I, Lima JAN, Vale MM, Ready PD, Rangel EF (2018) Entomological surveys of Lutzomyia flaviscutellata and other vectors of cutaneous leishmaniasis in municipalities with records of Leishmania amazonensis within the Bragança region of Pará State, Brazil. Journal of Vector Ecology 43: 168-178. https://doi.org/10.1111/jvec.12296
  » https://doi.org/10.1111/jvec.12296
• Castello L, Macedo MN (2016) Large-scale degradation of Amazonian freshwater ecosystems. Globlal Change Biology 22: 990-1007. https://doi.org/10.1111/gcb.13173
  » https://doi.org/10.1111/gcb.13173
• Chagas ECDS, Silva AS, Fe NF, Ferreira LS, Sampaio VS, Terrazas WCM, et al. (2018) Composition of sand fly fauna (Diptera: Psychodidae) and detection of Leishmania DNA (Kinetoplastida: Trypanosomatidae) in different ecotopes from a rural settlement in the central Amazon, Brazil. Parasites & Vectors 11: 180. https://doi.org/10.1186/s13071-018-2743-6
  » https://doi.org/10.1186/s13071-018-2743-6
• Cumming JM, Wood DM (2009) Adult morphology and terminology. In: Brown BV, Borkent A, Cumming JM, Wood DM, Woodley NE, Zumbado MA (Eds) Manual of Central American Diptera. National Research Council Press, Ottawa, 9-50.
• Feitosa MAC, Castellón EG (2006) Fauna de flebotomíneos (Diptera: Psychodidae) em fragmentos de floresta ao redor de conjuntos habitacionais na cidade de Manaus, Amazonas, Brasil. I. Estratificação Vertical. Acta Amazônica 36: 539-548.
• Fonteles RS, Pereira Filho AA, Moraes JLP, Pereira SRF, Rodrigues BL, Rebelo JMM (2018) Detection of Leishmania DNA and Blood Meal Identification in Sand Flies (Diptera: Psychodidae) From Lençois Maranhenses National Park Region, Brazil. Journal of Medical Entomology 28: 445-451. https://doi.org/10.1093/jme/tjx230
  » https://doi.org/10.1093/jme/tjx230
• Forattini OP (1973) Entomologia Médica. Editora Edgar Blucher, São Paulo, vol. 4, 658 pp.
• Galardo AK, Galardo CD, Silveira GA, Ribeiro KA, Hijjar AV, Oliveira LL, Santos TV (2015) Phlebotominae sand flies (Diptera: Psychodidae): potential vectors of American cutaneous leishmaniasis agents in the area associated with the Santo Antonio Hydroelectric System in Western Amazonian Brazil. Revista da Sociedade Brasileira de Medicina Tropical 48: 265-271. https://doi.org/10.1590/0037-8682-0088-2015
  » https://doi.org/10.1590/0037-8682-0088-2015
• Galati EAB (2003) Morfologia e taxonomia: classificação de Phlebotominae. In: Rangel EF, Lainson R (Eds) Flebotomíneos do Brasil. Editora Fiocruz, Rio de Janeiro, 23-51.
• Galati EAB (2018) Phlebotominae (Diptera, Psychodidae): classification, morphology and terminology of adults and identification of American taxa. In: Rangel EF, Shaw JJ (Eds) Brazilian Sand Flies: Biology, taxonomy, medical importance and control. Springer, 9-212.
• Galati EAB, Galvis-Ovallos F, Lawyer P, Leger N, Depaquit J (2017) An illustrated guide for characters and terminology used in descriptions of Phlebotominae (Diptera, Psychodidae). Parasite 24: 26. https://doi.org/10.1051/parasite/2017027
  » https://doi.org/10.1051/parasite/2017027
• Galati EAB, Ovallos FG (2012) Description of two new sand fly species related to Nyssomyia antunesi (Diptera, Psychodidae, Phlebotominae). Journal of Medical Entomology 49: 238-252. https://doi.org/10.1603/me11118
  » https://doi.org/10.1603/me11118
• Gil LH, Araujo MS, Villalobos JM, Camargo LM, Ozaki LS, Fontes CJ, et al. (2009) Species structure of sand fly (Diptera: Psychodidae) fauna in the Brazilian western Amazon. Memórias do Instituto Oswaldo Cruz 104: 955-959. https://doi.org/10.1590/s0074-02762009000700002
  » https://doi.org/10.1590/s0074-02762009000700002
• Gil LH, Basano SA, Souza AA, Silva MG, Barata I, Ishikawa EA, et al. (2003) Recent observations on the sand fly (Diptera: Psychodidae) fauna of the state of Rondonia, Western Amazonia, Brazil: the importance of Psychdopygus davisi as a vector of zoonotic cutaneous leishmaniasis. Memórias do Instituto Oswaldo Cruz 98: 751-755. https://doi.org/10.1590/s0074-02762003000600007
  » https://doi.org/10.1590/s0074-02762003000600007
• GIMP (2019) GNU Image Manipulation Program. GIMP Development Team, https://www.gimp.org
  » https://www.gimp.org
• Gomes AC (2002) Vigilância entomológica. Informativo Epidemiológico do SUS 11: 79-90.
• Gomes AC, Galati EAB (1987) Aspectos ecológicos da leishmaniose tegumentar americana. Estratificação da atividade espacial e estacional de Phlebotominae (Diptera, Psychodidae) em áreas de cultura agricola da região do Vale do Ribeira, Estado de São Paulo, Brasil. Memórias do Instituto Oswaldo Cruz 82: 467-473. https://doi.org/10.1590/s0074-02761987000400004
  » https://doi.org/10.1590/s0074-02761987000400004
• Grimaldi Jr G, Momen H, Naiff RD, McMahon-Pratt D, Barrett TV (1991) Characterization and classification of leishmanial parasites from humans, wild mammals, and sand flies in the Amazon region of Brazil. American Journal of Tropical Medicine and Hygiene 44: 645-661. https://doi.org/10.4269/ajtmh.1991.44.645
  » https://doi.org/10.4269/ajtmh.1991.44.645
• Herrer A, Christensen HA (1975) Implication of Phlebotomus sand flies as vectors of bartonellosis and leishmaniasis as early as 1764. Science 190: 154-155. https://doi.org/10.1126/science.1101379
  » https://doi.org/10.1126/science.1101379
• IBGE (2017) PAS - Pesquisa Anual de Serviços. Instituto Brasileiro de Geografia e Estatística, Brasília. https://cidades.ibge.gov.br/brasil
  » https://cidades.ibge.gov.br/brasil
• Lainson R (1988) Ecological interactions in the transmission of the leishmaniases. Philosophical Transactions of the Royal Society of London, B series Biological Sciences 321: 389-404. https://doi.org/10.1098/rstb.1988.0099
  » https://doi.org/10.1098/rstb.1988.0099
• Lainson R, Shaw JJ, Silveira FT, de Souza AAA, Braga RR, Ishikawa EAY (1994) The dermal leishmaniases of Brazil, with special reference to the eco-epidemiology of the disease in Amazonia. Memórias do Instituto Oswaldo Cruz 89: 435-443. https://doi.org/10.1590/s0074-02761994000300027
  » https://doi.org/10.1590/s0074-02761994000300027
• Langeron M (1949) Précis de microscopie. Masson, Paris, 7^th ed., 1430 pp.
• Lopes JV, EM Monteiro, Pereira NCL, Paula AJV, Silva FL, Lana RS, et al. (2021) Entomological studies in Itaúna, Brazil, an area with visceral leishmaniasis transmission: fauna survey, natural leishmania infection, and molecular characterization of the species circulating in Phlebotomine sand flies (Diptera: Psychodidae). Journal of Medical Entomology 56: 1368-1376. https://doi.org/10.1093/jme/tjz061
  » https://doi.org/10.1093/jme/tjz061
• Lopes TA, Campos AM, Capucci DC, Bragança MAL, Shimabukuro PHF (2024) Ecological study of phlebotomine sand flies (Diptera: Psychodidae) collected in the region of the São Manoel hydroelectric power plant. FIOCRUZ, Oswaldo Cruz Foundation, Occurrence Dataset, v. 1.5. https://ipt.sibbr.gov.br/sibbr/resource?r=fiocruz_sf_hydroelectric_amz [Accessed: 12/10/2023 ] br/sibbr/resource?r=fiocruz_sf_hydroelectric_amz [Accessed: 12/10/2023 ] https://doi.org/10.15468/8fcs5p
  » https://ipt.sibbr.gov.br/sibbr/resource?r=fiocruz_sf_hydroelectric_amz» https://doi.org/10.15468/8fcs5p
• Machado TO, Bragança MAL, Carvalho ML, Andrade Filho JD (2012) Species diversity of sandflies (Diptera: Psychodidae) during different seasons and in different environments in the district of Taquaruçú, state of Tocantins, Brazil. Memórias do Instituto Oswaldo Cruz 107: 955-959. https://doi.org/10.1590/s0074-02762012000700021
  » https://doi.org/10.1590/s0074-02762012000700021
• Marcondes CB (2007) A proposal of generic and subgeneric abbreviations for phlebotomine sand flies (Diptera: Psychodidae: Phlebotominae) of the world. Entomological News 118: 351-356. https://doi.org/10.1093/jme/tjy197
  » https://doi.org/10.1093/jme/tjy197
• Moreno ES, Oliveira JC, Shimabukuro PHF, Carvalho L (2018) Licenciamento ambiental de grandes empreendimentos: quais os limites para avaliação de impactos diretos e indiretos em saúde? Estudo de caso na Terra Indígena Wajãpi, Amapá. Boletim do Museu Paraense Emílio Goeldi, Ciências Humanas 13: 519-540.
• Moschin JC, Ovallos FG, Sei IA, Galati EA (2013) Ecological aspects of phlebotomine fauna (Diptera, Psychodidae) of Serra da Cantareira, Greater São Paulo Metropolitan region, state of São Paulo, Brazil. Revista Brasileira de Epidemiologia 16(1): 190-201.
• Oksanen J (2010) Multivariate Analysis of Ecological Communities in R: vegan tutorial. http://cc.oulu.fi/~jarioksa/opetus/metodi/vegantutor.pdf
  » http://cc.oulu.fi/~jarioksa/opetus/metodi/vegantutor.pdf
• Pereira Junior AM, Souza ABN, Castro TS, da Silva MS, de Paulo PFM, Ferreira GEM, de Medeiros JF (2019) Diversity, natural infection and blood meal sources of phlebotomine sandflies (Diptera, Psychodidae) in the western Brazilian Amazon. Memórias do Instituto Oswaldo Cruz 114: e190170. https://doi.org/10.1590/0074-02760190170
  » https://doi.org/10.1590/0074-02760190170
• Pugedo H, Barata RA, Franca-Silva JC, Silva JC, Dias ES (2005) HP: um modelo aprimorado de armadilha luminosa de sucção para a captura de pequenos insetos. Revista da Sociedade Brasileira de Medicina Tropical 38(1): 70-72. https://doi.org/10.1590/S0037-86822005000100017
  » https://doi.org/10.1590/S0037-86822005000100017
• R Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
  » http://www.R-project.org
• Ramos WR, Medeiros JF, Julião GR, Rios-Velásquez CM, Marialva EF, Desmouliére SJM, et al. (2014) Anthropic effects on sand fly (Diptera: Psychodidae) abundance and diversity in an Amazonian rural settlement, Brazil. Acta Tropica 139: 44-52. https://doi.org/10.1016/j.actatropica.2014.06.017
  » https://doi.org/10.1016/j.actatropica.2014.06.017
• Rangel EF, Lainson R (2009) Proven and putative vectors of American cutaneous leishmaniasis in Brazil: aspects of their biology and vectorial competence. Memórias do Instituto Oswaldo Cruz 104: 937-954. https://doi.org/10.1590/s0074-02762009000700001
  » https://doi.org/10.1590/s0074-02762009000700001
• Rebelo JMM, Moraes JLP, Cruz GBV, Andrade-Silva J, Bandeira MDCA, Oliveira Pereira YN, Santos CLCD (2019) Influence of deforestation on the community structure of sand flies (Diptera: Psychodidae) in Eastern Amazonia. Journal of Medical Entomology 56: 1004-1012. https://doi.org/10.1093/jme/tjz014
  » https://doi.org/10.1093/jme/tjz014
• Rego FD, Rugani JM, Shimabukur PHF, Tonelli GB, Quaresma PF, Gontijo CMF (2015) Molecular detection of Leishmania in phlebotomine sand flies (Diptera: Psychodidae) from a cutaneous leishmaniasis focus at Xakriabá Indigenous Reserve, Brazil. Plos One 10: e0122038. https://doi.org/10.1371/journal.pone.0122038
  » https://doi.org/10.1371/journal.pone.0122038
• Resadore F, Pereira Junior AM, Carvalho LPC, dos Santos APA, Teles CBG, Medeiros JF (2017) phlebotomine sand fly composition (Diptera: Psychodidae) and putative vectors of American Cutaneous Leishmaniasis in Porto Velho municipality, Western Amazon, Brazil. Journal of Medical Entomology 54: 798-803. https://doi.org/10.1093/jme/tjw233
  » https://doi.org/10.1093/jme/tjw233
• Ryan L, Lainson R, Shaw JJ (1987) Leishmaniasis in Brazil. XXIV. Natural flagellate infections of sandflies (Diptera: Psychodidae) in Pará State, with particular reference to the rôle of Psychodopygus wellcomei as the vector of Leishmania braziliensis braziliensis in the Serra dos Carajás. Transactions of the Royal Society of Tropical Medicine and Hygiene 81(3): 353-359. https://doi.org/10.1016/0035-9203(87)90133-7
  » https://doi.org/10.1016/0035-9203(87)90133-7
• Shaw J (2007) The leishmaniases - survival and expansion in a changing world. A mini-review. Memórias do Instituto Oswaldo Cruz 102: 541-547. https://doi.org/10.1590/s0074-02762007000500001
  » https://doi.org/10.1590/s0074-02762007000500001
• Shimabukuro PHF, Andrade AJ, Galati EAB (2017) Checklist of American sand flies (Diptera, Psychodidae, Phlebotominae): genera, species, and their distribution. Zookeys 660: 67-106. https://doi.org/10.3897/zookeys.660.10508
  » https://doi.org/10.3897/zookeys.660.10508
• Shimabukuro PHF, Andrade AJ, Galati EAB (2019) Phlebotominae. In: Catálogo Taxonômico da Fauna do Brasil. PNUD, PNUD, http://fauna.jbrj.gov.br/fauna/faunadobrasil/3297 [Accessed: 22/07/2024]
  » http://fauna.jbrj.gov.br/fauna/faunadobrasil/3297
• Silva ANR, Pereira Júnior AM, de Paulo PFM, da Silva MS, Costa GDS, Freitas MTS, et al. (2021) Detection of Leishmania species (Kinetoplastida, Trypanosomatidae) in phlebotomine sand flies (Diptera, Psychodidae) from Porto Velho, Northern Brazil. Acta Tropica 213: 105757. https://doi.org/10.1016/j.actatropica.2020.105757
  » https://doi.org/10.1016/j.actatropica.2020.105757
• Silva TRR, Assis MDG, Freire MP, Rego FD, Gontijo CMF, Shimabukuro PHF (2014) Molecular detection of Leishmania in sand flies (Diptera: Psychodidae: Phlebotominae) collected in the Caititu Indigenous Reserve of the municipality of Labrea, state of Amazonas, Brazil. Journal of Medical Entomology 51: 1276-1282. https://doi.org/10.1603/me14025
  » https://doi.org/10.1603/me14025
• Silveira FT, Ishikawa EAY, de Souza AAA, Lainson R (2002) An outbreak of cutaneous leishmaniasis among soldiers in Belém, Pará State, Brazil, caused by Leishmania (Viannia) lindenbergi n. sp. A new leishmanial parasite of man in the Amazon region. Parasite 9: 43-50. https://doi.org/10.1051/parasite/200209143
  » https://doi.org/10.1051/parasite/200209143
• Thies SF, Ribeiro ALM, Michalsky ÉM, Miyazaki RD, Fortes-Dias CL, Fontes CJF, Dias ES (2013) Phlebotomine sandfly fauna and natural Leishmania infection rates in a rural area of Cerrado (tropical savannah) in Nova Mutum, State of Mato Grosso in Brazil. Revista da Sociedade Brasileira de Medicina Tropical 46: 293-298. https://doi.org/10.1590/0037-8682-0031-2013
  » https://doi.org/10.1590/0037-8682-0031-2013
• Vásquez-Trujillo A, Santamaría-Herreño E, González-Reina AE, Buitrago-Alvarez LS, Góngora-Orjuela A, Cabrera-Quintero OL (2021) Lutzomyia antunesi, probable vector de leishmaniasis cutánea en el area rural de Villavicencio. Revista de Salud Publica (Bogota) 10: 625-632.
• Vilela ML, Azevedo CG, Carvalho BM, Rangel EF (2011) Phlebotomine fauna (Diptera: Psychodidae) and putative vectors of leishmaniases in impacted area by hydroelectric plant, State of Tocantins, Brazil. Plos One 6: e27721. https://doi.org/10.1371/journal.pone.0027721
  » https://doi.org/10.1371/journal.pone.0027721
• Walsh JF, Molyneux DH, Birley MH (1993) Deforestation: effects on vector-borne disease. Parasitology 106(Suppl. 1): S55-S75. https://doi.org/10.1017/S0031182000086121
  » https://doi.org/10.1017/S0031182000086121
• Ward RD, Shaw JJ, Lainson R, Fraiha H (1973) Leishmaniasis in Brazil: VIII. Observations on the phlebotomine fauna of an area highly endemic for cutaneous leishmaniasis, in the Serra dos Carajas, Pará State. Transactions of the Royal Society of Tropical Medicine and Hygiene 67(2):174-83. https://doi.org/10.1016/0035-9203(73)90142-9
  » https://doi.org/10.1016/0035-9203(73)90142-9
• WHO (2010) Control of the leishmaniases. World Health Organization, Geneva, Technical Report Series #949, 186 pp. https://www.who.int/publications/i/item/WHO-TRS-949
  » https://www.who.int/publications/i/item/WHO-TRS-949
• Wieczorek J, Bloom D, Guralnick R, Blum S, Döring M, Giovanni R, et al. (2012) Darwin Core: an evolving community-developed biodiversity data standard. Plos One 7(1): e29715. https://doi.org/10.1371/journal.pone.0029715
  » https://doi.org/10.1371/journal.pone.0029715
• Young DG, Duncan MA (1994) Guide to the Identification and Geographic Distribution of Lutzomyia Sand Flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae). Memoirs of the American Entomological Institute 54: 1-881.

ADDITIONAL NOTES

• Funding
  Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (001) Fundação de Amparo à Pesquisa de Minas Gerais (PPM-00676-18). We would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior for the scholarship to TAL (Finance Code 001), and the company BIOLEX Consultoria Ambiental for providing logistical support and funding for the fieldwork. PHFS would like to thank additional financial support given by the Fundação de Amparo à Pesquisa de Minas Gerais (process PPM-00676-18).
• Data Availability
  Lopes TA, Campos AM, Capucci DC, Bragança MAL, Shimabukuro PHF (2024) Ecological study of phlebotomine sand flies (Diptera: Psychodidae) collected in the region of the São Manoel hydroelectric power plant. FIOCRUZ, Oswaldo Cruz Foundation, Occurrence Dataset, v. 1.5. https://ipt.sibbr.gov.br/sibbr/resource?r=fiocruz_sf_hydroelectric_amz. https://doi.org/10.15468/8fcs5p
• ZooBank register
  https://zoobank.org/8A03DFB3-F9A2-43AE-94D5-B417DA8890A4
• How to cite this article
  Campos AM, Lopes TA, Capucci DC, Rodrigues BL, Bragança MAL, Shimabukuro PHF (2025) Ecology of sand flies near São Manoel hydroelectric plant, southern Brazilian Amazon, including a new species of Trichophoromyia (Diptera: Psychodidae: Phlebotominae). Zoologia 42: e24052. https://doi.org/10.1590/S1984-4689.v42.e24052
• Published by
  Sociedade Brasileira de Zoologia at Scientific Electronic Library Online - https://www.scielo.br/zool

APPENDIX

Appendix 1
Sand flies (Diptera: Psychodidae) collected in the Amazon region, in the municipality of Paranaíta, Mato Grosso and Jacareacanga, Parárazil in an area under the influence of the construction of the hydroelectric power plant, São Manoel.

Species	Domestic environments												T	Sylvatic environments												T	Overall total
	I1	P1	I2	P2	I3	P3	I4	P4	I5	P5	I6	P6		F1	F2	F3	F 4	F 5	F 6	F 7	F 8	F 9	F 10	F 11	F 12
Bi. flaviscutellata	-	-	-	1	-	-	-	-	-	-	-	-	1	2	-	-	2	-	-	-	-	-	-	2	2	8	9
Br. avellari	-	1	-	-	-	9	-	1	-	-	-	-	11	-	-	-	2	5	1	-	-	-	-	-	-	8	19
Br. brumpti	-	-	-	-	-	-	-	6	-	-	-	-	6	-	-	-	-	-	-	-	-	-	-	-	-	0	6
Br. pintoi	-	-	-	-	-	-	-	-	-	1	-	-	1	-	-	-	2	-	-	-	-	-	-	-	-	2	3
Ev. bacula	-	-	-	1	-	-	-	-	-	-	-	-	1	1	-	-	-	-	-	-	-	-	-	-	1	2	3
Ev. begonae	-	-	-	-	-	-	-	-	-	-	-	-	0	3	1	-	-	-	-	-	-	-	-	-	-	4	4
Ev. carmelinoi	-	-	-	-	-	-	-	-	-	2	-	-	2	-	-	-	-	-	-	-	-	-	-	-	-	0	2
Ev. evandroi	-	-	-	-	-	-	-	-	1	2	-	1	4	-	-	-	-	-	1	-	-	-	-	-	-	1	5
Ev. georgii	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	-	-	1	-	-	-	-	-	-	1	1
Ev. lenti	-	-	1	1	-	-	-	-	6	-	-	5	13	-	-	-	-	-	-	-	-	-	-	-	-	0	13
Ev. monstruosa	-	-	-	-	-	-	-	-	-	-	-	-	0	1	-	-	2	-	-	-	1	-	-	-	1	5	5
Ev. saulensis	-	-	-	-	-	-	-	-	-	-	-	-	0	2	-	-	4	3	-	-	-	-	-	-	-	9	9
Ev. sp.	-	-	-	1	-	-	-	-	-	-	-	-	1	-	-	-	-	-	-	-	-	-	-	-	-	0	1
Ev. termitophila	-	-	1	2	3	15	-	-	11	9	3	74	118	-	-	-	-	-	-	1	-	-	-	-	-	1	119
Ev. walkeri	1	3	-	-	4	5	1	-	2	8	-	-	24	-	2	-	44	2	-	-	1	-	-	1	-	50	74
Lu. evangelistai	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	-	-	-	-	-	1	-	-	-	1	1
Mi. acanthopharynx	-	-	-	-	-	-	-	-	-	-	-	-	0	1	-	-	-	-	-	-	-	-	-	-	-	1	1
Mi. micropyga	-	-	-	-	-	-	-	-	-	-	-	-	0	1	-	-	1	-	-	-	-	-	-	-	-	2	2
Mi. sp.	-	-	-	-	-	1	-	-	-	-	-	-	1	-	-	-	-	-	-	-	-	-	-	-	-	0	1
Mg. migonei	-	-	-	1	2	1	-	-	1	-	-	-	5	-	-	1	1	-	-	-	-	-	-	-	-	2	7
Ny. anduzei	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	-	-	-	-	-	-	-	-	1	1	1
Ny. antunesi	2	9	-	2	1	-	1	1	-	-	1	-	17	5	1	-	47	47	1	-	-	-	-	2	8	111	128
Ny. delsionatali	-	-	-	-	-	1	5	15	2	3	-	-	26	-	-	-	2	-	-	2	-	-	-	2	-	6	32
Ny. fraihai	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	1	-	-	-	-	-	-	1	-	2	2
Ny. richardwardi	-	-	-	-	-	1	-	-	-	-	-	-	1	2	-	-	4	-	-	-	-	-	-	-	-	6	7
Ny. shawi	-	-	-	1	-	-	-	-	-	-	-	-	1	-	9	-	28	-	-	-	-	-	-	-	1	38	39
Ny. sp.	-	-	-	-	-	1	-	2	-	-	-	-	3	-	-	1	8	1	-	-	-	-	-	-	-	10	13
Ny. umbratilis	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	2	-	-	-	-	-	-	-	-	2	2
Ny. urbinattii	-	1	-	-	-	-	-	5	-	2	-	-	8	-	-	-	-	2	-	-	-	-	-	-	-	2	10
Ny. whitmani	-	-	-	1	1	11	-	-	2	2	-	1	18	1	1	-	71	2	-	-	-	-	-	-	2	77	95
Pi. serrana	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	1	-	-	-	-	-	-	-	-	1	1
Pa. dendrophyla	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	-	-	-	-	-	1	-	-	1	2	2
Pa. aragaoi	-	-	-	-	-	-	-	-	-	-	-	-	0	1	-	-	3	-	1	1	-	-	1	-	-	7	7
Pa. barrettoi barrettoi	-	-	-	-	-	-	-	-	-	-	-	-	0	-	1	-	-	-	-	-	-	-	-	-	-	1	1
Pa. campograndensis	-	-	-	-	-	-	-	-	1	-	-	-	1	-	-	-	-	-	-	-	-	-	-	-	-	0	1
Pa. hermanlenti	-	-	-	-	-	1	-	-	-	1	-	-	2	1	-	-	-	-	-	1	1	-	-	-	2	5	7
Pa. inflata	-	-	-	-	-	-	-	-	-	-	-	-	0	-	2	2	-	-	8	-	-	-	-	-	-	12	12
Pa. lutziana	-	-	-	-	-	-	-	-	-	-	-	-	0	1	1	-	6	-	-	-	1	-	-	0	2	11	11
Pa. runoides	-	-	-	-	-	1	-	1	-	3	-	-	5	1	1	-	1	-	-	-	-	-	-	-	-	3	8
Pa. Shannoni series	-	-	-	-	-	1	-	-	-	-	-	-	1	-	-	-	-	-	1	-	-	-	-	-	-	1	2
Pa. sp.	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	2	1	-	-	-	-	2	-	-	5	5
Ps. amazonensis	-	-	-	-	-	-	-	-	-	-	-	-	0	1	-	-	1	-	-	-	-	-	-	-	-	2	2
Ps. ayrozai	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	1	-	-	-	-	-	-	-	-	1	1
Ps. carrerai	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	2	28	-	-	-	-	-	-	-	8	38	38
Ps. chagasi	-	-	-	-	-	2	1	-	-	-	-	-	3	-	1	-	-	-	-	-	-	-	-	-	1	2	5
Ps. claustrei	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	1	13	-	-	1	-	-	1	1	1	18	18
Ps. complexus	-	-	-	-	-	-	-	-	-	1	-	-	1	9	1	8	15	-	2	-	-	2	-	1	52	90	91
Ps. davisi	-	-	-	-	-	-	-	-	-	-	-	-	0	-	22	6	157	-	-	2	-	-	1	3	31	222	222
Ps. hirsutus	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	2	36	-	-	1	-	-	-	1	2	42	42
Ps. lainsoni	-	-	1	-	-	1	-	-	-	-	-	-	2	1	-	-	-	-	-	-	1	-	-	1	-	3	5
Ps. llanosmartinsi	-	-	-	-	-	-	-	-	-	1	-	-	1	2	1	-	-	1	-	-	-	-	-	-	-	4	5
Ps. paraensis	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	3	6	-	2	-	-	-	-	-	-	11	11
Ps. sp.	-	-	-	-	2	-	-	1	-	-	-	-	3	2	6	-	67	2	-	1	-	1	3	1	13	96	99
Ps. Chagasi series	-	-	-	-	-	1	-	-	-	-	-	-	1	-	-	-	-	-	-	-	-	-	-	-	-	0	1
Ps. wellcomei	-	-	-	-	-	-	-	-	1	-	-	-	1	-	-	-	-	-	-	-	-	-	-	-	-	0	1
Sc. servulolimai	-	-	-	2	-	-	-	-	1	-	-	1	4	-	1	-	2	-	-	2	-	-	1	-	1	7	11
Sc. sordellii	-	-	1	5	1	-	-	-	1	1	-	4	13	8	2	-	9	-	7	1	2	-	2	-	7	38	51
Sc. sp.	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	1	-	-	-	-	-	-	-	-	1	1
Th. octavioi	-	-	-	-	-	-	-	-	-	-	-	-	0	1	4	1	6	1	-	-	-	-	-	-	-	62	62
Th. sp.	-	-	1	1	-	-	-	-	-	-	-	-	2	3	8	1	51	6	7	-	1	1	-	-	82	160	162
Th. dilermandoi	-	-	-	-	-	-	-	-	-	-	-	-	0	5	-	1	31	5	-	-	-	1	-	2	18	63	63
Th. ubiquitalis	-	-	-	-	-	-	-	14	-	-	-	-	14	4	-	-	6	-	-	-	-	-	-	4	7	21	35
Ty. longispina	-	-	-	-	-	-	-	1	-	-	-	-	1	-	-	-	-	-	-	-	1	-	-	-	-	1	2
Ty. trichopyga	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	1	-	-	-	-	-	-	-	-	1	1
Ty. dasypodogeton	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	35	1	1	-	-	-	-	-	-	37	37
Ty. rondoniensis	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	1	-	-	-	1	-	-	1	-	3	3
Ty. sp.	-	-	-	-	-	1	-	-	-	-	-	-	1	4	-	-	16	1	6	1	4	-	-	-	3	35	36
Vi. furcata	-	-	-	-	-	-	-	-	-	-	-	-	0	1	-	-	1	-	-	-	-	-	-	-	1	3	3
Vi. tuberculata	-	-	-	-	-	-	-	-	-	-	-	-	0	-	-	-	1	-	-	-	-	-	1	-	1	3	3
Total number of individuals	3	14	5	19	14	53	8	47	29	36	4	86	318	64	65	29	719	80	39	14	14	7	12	23	249%	1364	1.682

• I = intradomicile, P = peridomicile, F = forest, and numbers refer to different sites, T = Total number of individuals collected.

Edited by

• Editorial responsibility
  Ricardo Moratelli

Data availability

Lopes TA, Campos AM, Capucci DC, Bragança MAL, Shimabukuro PHF (2024) Ecological study of phlebotomine sand flies (Diptera: Psychodidae) collected in the region of the São Manoel hydroelectric power plant. FIOCRUZ, Oswaldo Cruz Foundation, Occurrence Dataset, v. 1.5. https://ipt.sibbr.gov.br/sibbr/resource?r=fiocruz_sf_hydroelectric_amz. https://doi.org/10.15468/8fcs5p

Data citations

Shimabukuro PHF, Andrade AJ, Galati EAB (2019) Phlebotominae. In: Catálogo Taxonômico da Fauna do Brasil. PNUD, PNUD, http://fauna.jbrj.gov.br/fauna/faunadobrasil/3297 [Accessed: 22/07/2024]

Publication Dates

• Publication in this collection
  26 May 2025
• Date of issue
  2025

History

• Received
  10 Aug 2024
• Accepted
  26 Feb 2025