Research Article |
Corresponding author: Ricardo Andrade Barata ( ricbarata@hotmail.com ) Academic editor: Oana Teodora Moldovan
© 2021 Layane Meira Teodoro, Gustavo Mayr de Lima Carvalho, Aldenise Martins Campos, Roberta Fernanda Ventura Cerqueira, Marconi Souza-Silva, Rodrigo Lopes Ferreira, Ricardo Andrade Barata.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Teodoro LM, Carvalho GML, Campos AM, Cerqueira RFV, Souza-Silva M, Ferreira RL, Barata RA (2021) Phlebotomine sand flies (Diptera, Psychodidae) from iron ore caves in the State of Pará, Brazil. Subterranean Biology 37: 27-42. https://doi.org/10.3897/subtbiol.37.57534
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The present study aimed to evaluate the distribution of sand fly species in iron ore caves in the State of Pará, Brazil and to associate the richness and abundance of these insects with the capacity of leishmaniasis transmission. Entomological captures were carried out in the years 2010, 2013, 2014 and 2015, throughout active samples with brushes, along the entire caves’ extension, in dry and rainy periods. A total of 9,807 sand flies were counted during the 532 samplings events, being 4,340 in the dry period and 5,467 in the rainy period. A random sample of 802 morphologically identified specimens consisted of 8 genera and 17 species, being 369 males (46%) and 433 females (54%). The predominant species was Sciopemyia sordellii with 60.6% of the total of sand flies collected. Differences in composition and richness were observed between caves located inside of forest and anthropized areas. The mean richness and abundance were different between the wet and rainy periods, with a greater abundance of these insects in the rainy period. The phlebotomine fauna proved to be rich and abundant in the sampled caves, however, environmental degradation seems to be the main factor determining changes in the composition and richness, reinforces the importance of these places as a shelter for sand flies in degraded areas.
Leishmaniasis, Phlebotominae, Vector ecology
Phlebotomines (Diptera, Psychodidae, Phlebotominae) are insects with medical importance because include vector species of Leishmania sp., Bartonella bacilliformis and arbovirus (
Caves are favorable environments for the occurrence of these insects due to the stable conditions of temperature and humidity (
In Brazil, the data regarding the phlebotomine fauna in caves are incomplete (
In the Serra do Carajás, located in the state of Pará, the mining potential of the Curionópolis and Parauapebas municipalities has attracted enterprises that, despite contributing to the economic development of the region, have caused major environmental changes, with direct impacts on biodiversity and public health (
Serra de Carajás has a large number of caves with economic and biological potential, but it is also considered an endemic area for cutaneous leishmaniasis (
The study was carried out in iron ore caves located in the regions of Morro I, Morro II (Serra Norte), within the Flona de Carajás and Serra Leste, outside a conservation unit, in the municipalities of Parauapebas and Curionópolis (Figure
Ferruginous geosystem of Carajás, Pará, Brazil (limited by red lines), with iron ore caves (yellow dots) in the regions of Morro I, Morro II (Carajás National Forest) and Serra Leste. Limits of the ferruginous geosystem and the coordinates of the caves, available in https://institutopristino.org.br/atlas
It has the largest iron ore mineral province on the planet, Serra dos Carajás, which has the highest concentration of ferruginous caves in Brazil, with approximately 20% of all caves registered in the country (
Both municipalities have a semi-humid tropical climate (Aw/As), with annual temperatures around 26 °C and high relative humidity; the rainy season occurs, from November to May, and the dry season, from June to October, with the rainfall index being around 2,000 mm annually (
Entomological captures were carried out in the years 2010, 2013, 2014 and 2015, through active samples with brushes, along the entire caves’ extension, in dry and rainy periods from speleological activities carried out by independent consulting companies, in the years, but using similar collection methods (
The collected specimens were sent to the Parasitology Laboratory of the Department of Biological Sciences at the Federal University of Jequitinhonha and Mucuri Valleys. The sandflies were prepared and assembled between a slide and coverslip, according to the Langeron technique (1949), modified, using Berlese’s liquid to mount both sexes. The identification of the specimens was carried out according to the classification proposed by
The qualitative similarity was obtained by the Jaccard index and contrasted in a metric multidimensional scaling (MDS) with resampling using the Bootstrap method. Furthermore, the significant separation of species groups between the different sampling areas (Morro I, Morro II and Serra Leste) was evaluated by similarity analysis – ANOSIM (
Differences in mean richness and abundance between areas and between dry and rainy periods were assessed using the Kruskal-Wallis test (
In total, 306 iron ore caves (44 caves in Morro I, 115 in Morro II and 147 in Serra Leste) were inspected, and the phlebotomine fauna captured in 276 of these caves in 532 samplings (dry and rainy seasons) consisted of 8 genera and 17 species, namely: Evandromyia carmelinoi (Ryan, Fraiha, Lainson & Shaw, 1986), Evandromyia monstruosa (Floch & Abonnenc, 1944), Evandromyia saulensis (Floch & Abonnenc, 1944), Evandromyia termitophila (Martins, Falcão & Silva, 1964), Lutzomyia longipalpis (Lutz & Neiva, 1912), Micropygomyia goiana (Martins, Falcão & Silva), Micropygomyia oswaldoi (Mangabeira, 1942), Micropygomyia peresi (Mangabeira, 1942), Micropygomyia pilosa (Damasceno & Causey, 1944), Nyssomyia umbratilis (Ward & Fraiha, 1977), Pintomyia série chagasi, Pintomyia gruta (Ryan, 1986), Pintomyia serrana (Damasceno & Arouck, 1949), Psathyromyia lutziana (Costa Lima, 1932), Sciopemyia sordellii (Shannon & Del Ponte, 1927), Trichophoromyia brachipyga (Mangabeira, 1942), Trichopygomyia dasypodogeton (Castro, 1939) and Micropygomyia spp., totaling 802 specimens, being 369 males (46%) and 433 females (54%). The predominant species was Sciopemyia sordellii with 60.6% of the total of sand flies identified (Table
Distribution of sand flies collected in iron ore caves in the State of Pará, Brazil, in the years 2010, 2013, 2014 and 2015.
Species | Curionópolis | Parauapebas | N | % | ||
---|---|---|---|---|---|---|
♂ | ♀ | ♂ | ♀ | |||
Evandromyia carmelinoi | 2 | 1 | 0 | 0 | 3 | 0.38 |
Ev. monstruosa | 0 | 1 | 0 | 1 | 2 | 0.24 |
Ev. saulensis | 0 | 1 | 13 | 10 | 24 | 3.00 |
Ev. termitophila | 0 | 2 | 0 | 0 | 2 | 0.24 |
Lutzomyia longipalpis | 13 | 13 | 1 | 2 | 29 | 3.62 |
Micropygomyia goiana | 0 | 0 | 0 | 3 | 3 | 0.38 |
Mi. oswaldoi | 0 | 3 | 0 | 0 | 3 | 0.38 |
Mi. peresi | 11 | 2 | 2 | 2 | 17 | 2.12 |
Mi. pilosa | 2 | 1 | 1 | 1 | 5 | 0.63 |
Micropygomyia spp. | 17 | 0 | 11 | 3 | 31 | 3.87 |
Nyssomyia umbratilis | 0 | 0 | 1 | 1 | 2 | 0.24 |
Pintomyia série chagasi | 0 | 0 | 0 | 6 | 6 | 0.75 |
Pi. gruta | 7 | 9 | 25 | 22 | 63 | 7.86 |
Pi. serrana | 0 | 0 | 0 | 1 | 1 | 0.12 |
Psathyromyia lutziana | 0 | 0 | 0 | 1 | 1 | 0.12 |
Sciopemyia sordellii | 46 | 64 | 184 | 192 | 486 | 60.60 |
Trichophoromyia brachipyga | 0 | 0 | 1 | 0 | 1 | 0.12 |
Trichopygomyia dasypodogeton | 0 | 0 | 1 | 0 | 1 | 0.12 |
Not identified | 2 | 8 | 29 | 83 | 122 | 15.21 |
Sub-total | 100 | 105 | 269 | 328 | 802 | 100 |
Total | 205 (25.5%) | 597 (74.5%) |
Similarity analysis (ANOSIM) showed a significant difference between the species composition of the Parauapebas and Curionópolis caves (R = 0.06 and P <0.05) (Figure
The mean dissimilarity between the caves of Parauapebas and Curionópolis corresponded to 72.29, and the species responsible for the dissimilarity were Sciopemyia sordellii (77.26% contribution), Pintomyia gruta (12.01% contribution) and Lutzomyia longipalpis (7.92% contribution).
The mean richness was different between the two sampled areas (KW-H (1; 206) = 20.34; p <0.01), with a higher mean richness in the Parauapebas caves (mean = 2 spp., sd = 1) in relation to Curionópolis (mean = 1.44 spp., sd = 0.7). The mean richness was different between the regions of Morro II and Serra Leste (KW-H (2; 206) = 20.36; p <0.01), with a higher mean richness in the Morro I caves (mean = 2 spp., sd = 1.1) in relation to Morro II (mean = 1.98 spp., sd = 0.94) and Serra Leste (mean = 1.44 spp., sd = 0.7). The richness did not show any significant relation with the linear extension of the caves.
A total of 9,807 individuals were counted during the 532 samplings, 4,340 in the dry period and 5,467 in the rainy period. In the Morro I and II caves, 6,791 specimens (295 samples) were counted and 3,016 in Serra Leste (238 samples) (Suppl. material
The mean abundance was different between the two sampled areas (KW-H (1; 532) = 28.37; p <0.01), with a higher mean abundance in the caves of Parauapebas (mean = 23.10 individuals, sd = 31.73) in relation to Curionópolis (mean = 13.60 individuals, sd = 29.40) (Figure
Considering all areas, the mean abundance was different between the dry and rainy periods (KW-H (1; 532) = 4.14; p <0.01), with a higher mean abundance in the rainy season (mean = 21 individuals, sd = 33.83) in relation to the dry (mean = 16 individuals, sd = 27.70) (Figure
Distribution of abundance of sand flies counted in caves of Parauapebas and Curionópolis (A), in the regions of Morro I, Morro II and Serra Leste (B) in the dry and rainy periods of the year (C, D), Morro (MI), Morro II (MII) and Serra Leste (SL). Negative values do not represent negative abundance but the mean value subtracted from the standard deviation.
Despite their restrictive traits, such as the scarcity of food resources, which could preclude the establishment of epigean species, caves can present a diverse and peculiar fauna. In this sense, inventories carried out in caves, particularly of sand flies, are extremely important, as they can contribute to the knowledge of the fauna of these insects, generating data of taxonomic, ecological and epidemiological importance (
The use of light traps has been widely used in studies of sand flies in caves (
Sciopemyia sordellii was predominant (60.6% of the total number of specimens captured) and had a higher number of occurrences in the caves. Other authors have also recorded this species in caves (
Pintomyia gruta represented 7.86% of the collected sand flies. This species is endemic to the Northeastern part of the country, and until a few years ago, its occurrence was restricted to the caves of Serra dos Carajás (
Among the most important findings of this work, the first records of Pi. serrana, Tr. brachipyga, Tr. dasypodogeton and Ev. saulensis in Brazilian caves must be highlighted. Despite the latter not be considered vector species of Leishmania,
Females of the Mi. peresi species, as well as Ev. saulensis, feed on ectothermic animals, such as reptiles and amphibians. Possibly, the registration of these species in caves is associated with the presence of reptiles and amphibians, which use this environment as a shelter (
The species Micropygomyia spp. collected in the caves of the municipalities of Curionópolis and Parauapebas did not have their identification confirmed. It is important to highlight that it is probably a new species, which needs to be further studied. For this, new collections should be carried out in these places in search of new specimens for a future description of this species.
Two specimens of Evandromyia termitophila were reported in captures in ferruginous caves in Pará.
Considering the epidemiological importance of some species, we call attention to the record of Ny. umbratilis, which had also been recorded in caves in the State of Amazonas and Rondônia (
Lutzomyia longipalpis species must be highlighted because it is the most important species in the epidemiological cycle of visceral leishmaniasis in Latin America (
The differences in composition and the lower richness and abundance found for the Serra Leste caves (Curionópolis), despite being weak may be related to the effect of environmental degradation observed in this region. Studies carried out outside cave environments have shown a reduction ratio of sand flies in areas with capoeira vegetation, rural and urban areas concerning to forested areas (
In Brazil, a greater number of sand flies has been associated with the rainiest periods of the year (
The phlebotomine fauna was shown to be rich and abundant in the sampled caves, however, environmental degradation seems to be the main factor in producing changes in composition and richness, especially in the Serra Leste region. In addition, the large number of species in the caves of Morro I and II, in comparison to Serra Leste, reinforces the importance of these places as a shelter for sand flies in degraded areas.
We are grateful to the independent consultants who carried out samples in the field and to the consulting companies. We are also grateful to the members of the Coleção de Invertebrados Subterrâneos de Lavras (ISLA). The authors are also grateful to the editors and reviewers for theirs valuable suggestions. RLF is grateful to the National Council of Technological and Scientific Development (CNPq) for the research grant No 308334/2018-3.
Table S1
Data type: occurrence data