Acta Biológica Colombiana
0120-548X
1900-1649
Universidad Nacional de Colombia, Facultad de Ciencias, Departamento de Biología
https://doi.org/10.15446/abc.v29n2.109004

Recibido: 19 de junio de 2023; Revision Received: 31 de agosto de 2023; Aceptado: 1 de febrero de 2024

FIRST RECORD OF Edentomya piauiensis (DIPTERA: PSYCHODIDAE) IN MARANHÃO STATE, BRAZIL

Primer registro de Edentomya piauiensis (Diptera: Psychodidae) en el Estado de Maranhão, Brasil

Maria José Alves de Passos BARBOSA, 1
Diogo Brunno e Silva BARBOSA, 2
Maria Regiane Araujo SOARES, 1*

Associate editor: Allan Henry Smith Pardo

Programa de Pós-graduação em Biodiversidade e Conservação, Campus Amílcar Ferreira Sobral, Universidade Federal do Piauí BR-343 KM 3,5 Floriano Piauí Brazil
Departamento de Biologia, Campus Ministro Petrônio Portella, Universidade Federal do Piauí Teresina Piauí Brazil

* For correspondence

ABSTRACT

We report the first record of Edentomya piauiensis in Maranhão State, Brazil in a cave, a similar ecotope where this species has been previously described in the literature. The specimens were captured in Toca do Inferno Cave, Barão de Grajaú, Maranhão, from September/2021, January, and May/2022. Twelve Hoover Pugedo (HP) light traps were installed at 1.5 m above the ground, uninterruptedly for 24h. We captured 1778 specimens of E. piauiensis. This finding expands knowledge of the geographical distribution of this species in Brazil.

Keywords

Biodiversity, Ecotope, Edentomya genus, Sandfly Fauna, Sandstone Cave.

RESUMEN

Edentomya piauiensis es reportada por primera vez en el estado de Maranhão, Brasil, en una cueva, en un ecotopo similar donde esta especie ha sido descrita previamente en la literatura. Las colectas de flebotomos se realizaron en la cueva Toca do Inferno, Barão de Grajaú, Maranhão, en septiembre de 2021, enero y mayo de 2022. Se instalaron doce trampas de luz modelo HP a 1,5 m del suelo por un período de 24 horas. Fueron recolectaron un total de 1778 ejemplares de E. piauiensis. Este hallazgo amplía el conocimiento sobre la distribución geográfica de esta especie de flebotominos en Brasil.

Palabras clave

Biodiversidad, Ecotopo, género Edentomya, Fauna flebotomínica, Cueva de arenisca.

Phlebotominae (Diptera: Psychodidae) are hematophagous insects with a wide spatial distribution, inhabiting the most varied ecotopes (Young and Duncan, 1994). This group of insects has a great ecological importance (Andrade-Filho et al., 2001), as it includes species with vectorial capacity for leishmaniasis transmission.

In Brazil, there have been few studies on cave environments and the sandfly fauna composition in this habitat is poorly known. Moreover, this lack of knowledge makes it difficult to record new species in many cave-dwelling (Carvalho et al., 2011; Carvalho et al., 2013). A systematic review of cave-dwelling reported 108 sandfly species, and this value represents about 40 % of the number of sandfly species recorded from Brazil (Dutra-Rêgo et al., 2022).

Edentomya piauiensis Galati, Andrade Filho, Silva & Falcão, 2003 is the only species of Edentomya genus. It was first described from specimens collected in a cave in Piauí State (Galati et al. 2003) and later in Pará State (Galati, 2021).

The bioecology of E. piauiensis is poorly known. According to ecological data of the Phlebotomini tribe, the genera inhabit humid places rich in organic matter, feeding on sugar solutions and only females are hematophagous because this is necessary for egg development (Maroli et al., 2013; Akhoundi et al., 2016). Sandflies have nocturnal habits (Killick-Kendrick, 1999), but in cave-dwelling by a permanent lack of light, in areas far from the entrance, this abiotic factor allows these insects to have different circadian schedules from those observed in epigean environments (Carvalho et al., 2012; Campos et al., 2017).

The literature shows that Maranhão State sandfly fauna consists of 98 species distributed in eight genera (Brumptomyia, Lutzomyia, Bichromomyia, Micropygomyia, Nyssomyia, Evandromyia, Psathyromyia and Psychodopygus), comprising 18 vector species for Leishmania spp. transmission (Rebelo et al., 2010; Silva et al., 2010; Moraes et al., 2015; Silva et al., 2015; Da Silva et al., 2019; Silva et al., 2019; Moraes et al., 2020).

In this paper, we reported the occurrence of E. piauiensis in sandfly fauna in Maranhão State, Brazil for the first time.

This study was conducted in the Toca do Inferno cave, located at Comunidade Faveirinha, rural area of Barão de Grajaú, Maranhão, Brazil, located at the coordinates 06°39′ S and 43°20′ W.

Sandflies were collected in September/2021, January and May/2022, once a month for 24 hours, inside and around the cave. Four HP light traps (Pugedo et al., 2005) were installed outside the cave and eight were placed inside the one, during three night of capture. The traps were installed at 1.5 m above the ground, at least 10 m of distance from each trap. The collection effort was 864 hours.

The captured sandfly were transported to the Laboratory of Natural History and Applied Biology at Federal University of Piauí, prepared in Berlese's fluid and mounted on slides for identification according to Vilela et al. (2003). We followed the taxonomic classification proposed by Galati (2021). All vouchers were deposited in Coleção de História Natural da Universidade Federal do Piauí (CHNUFPI) (catalog number CHNUFPI 1164 a CHNUFPI 1856).

The sandfly collection was authorized by Chico Mendes Institute for Biodiversity Conservation (ICMBio) under the license number 78923-1.

A total of 1778 of which were identified as E. piauiensis (461 females and 1317 males). Of the total, 169 E. piauiensis were collected outside the cave and 1609 inside the cave. Figure 1 shows the main characters used for specie identification.

The first record of E. piauiensis occurred in caves composed of limestone (Galati et al., 2003; Dutra-Rêgo et al., 2022), however, we reported the occurrence of this species in a sandstone cave. In these caves, bats and other mammals play an important role in providing organic matter, especially because they are permanently dry caves (Dutra-Rêgo et al., 2022).

Anatomical structures used in taxonomic determination of Edentomyia piauiensis. a: Male. b: Genital characters. c: Female head with cibarium. d: Genital fork and spermatheca

Figure 1.: Anatomical structures used in taxonomic determination of Edentomyia piauiensis. a: Male. b: Genital characters. c: Female head with cibarium. d: Genital fork and spermatheca

In this study, sandflies were collected both inside and around the cave, which suggests the maintenance of a flow with the internal and external environment (Carvalho et al., 2013), distinctly from Deanemya maruaga a cave-dwelling species adapted to live in aphotic zone, being its immature stages depending on organic matter from this environment (Alves et al., 2011).

We suggest that E. piauiensis has habits strongly linked to the interior of the cave, since the light traps installed within the cave collected an expressive number of sandflies. However, the occurrence of specimens around the cave may show a certain dependence on the external environment of the cave, probably because of a greater availability of food resources or light sources have attracted them.

With this new record of E. piauiensis for Maranhão, the list of phlebotomine sandfly in this state is expanded to 99 species. Until the present date of the submission of this manuscript, this is the only species belonging to the genus Edentomya (Galati et al., 2003, Galati, 2021).

The expansion of knowledge about this species is important in order to understand the evolution of phlebotomine sandflies, especially in cave environments, which can pressure the retention of primitive morphological characters such as the absence of cibarium teeth as in E. piauiensis (Dutra-Rego et al., 2022, Galati et al., 2003).

The results contribute to the knowledge of wild sandfly fauna in Maranhão State. In addition, this study expands the distribution of this species in a cave formation other than the one originally described.

ACKNOWLEDGMENTS

We thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for financial support / for funding this research; to Mr. José Nazareno for making the access to the cave possible; to Valdir Peres da Silva Lima, the technician of the Secretaria Municipal de Saúde de Barão de Grajaú, for their assistance in field activities and to Dr. José Dilermando Andrade Filho of the Fundação Oswaldo Cruz, State of Minas Gerais for confirming this species. Competing interests: The authors have declared that no competing interests exist.

REFERENCES

  1. Akhoundi, M., Kuhls, K., Cannet, A., Votýpka, J., Marty, P., Delaunay, P. and Sereno, D. (2016). A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLOS Neglected Tropical Diseases, 10(3): e0004349. https://doi.org/10.1371/journal.pntd.0004349 [DOI] 🠔
  2. Alves, V. R., Freitas, R. A. D., Santos, F. L. and Barrett, T. V. (2011). Diversity of sandflies (Psychodidae: Phlebotominae) captured in sandstone caves from Central Amazonia, Brazil. Memórias do Instituto Oswaldo Cruz, 106(3):353–359. https://doi.org/10.1590/S0074-02762011000300016 [DOI] 🠔
  3. Andrade-Filho, J. D., Valente, M. B., Andrade, W. A. D., Brazil, R. P. and Falcão, A. L. (2001). Flebotomíneos do estado de Tocantins, Brasil (Diptera: Psychodidae). Revista da Sociedade Brasileira de Medicina Tropical, 34(4):323–329. https://doi.org/10.1590/S0037-86822001000400003 [DOI] 🠔
  4. Campos, A. M., Dos Santos, C. L. C., Stumpp, R., Da Silva, L. H. D., Maia, R. A., Paglia, A. P. and Andrade Filho, J. D. (2017). Photoperiod differences in sand fly (Diptera: Psychodidae) species richness and abundance in caves in Minas Gerais State, Brazil. Journal of Medical Entomology, 54(1):100–105. https://doi.org/10.1093/jme/tjw135 [DOI] 🠔
  5. Carvalho, G. M. L., Brazil, R. P., Sanguinette, C. C. and Andrade Filho, J. D. (2011). Description of evandromyia spelunca, a new phlebotomine species of the cortelezii complex, from a cave in Minas Gerais State, Brazil (Diptera: Psychodidae: Phlebotominae). Parasites & Vectors, 4(1):158. https://doi.org/10.1186/1756-3305-4-158 [DOI] 🠔
  6. Carvalho, G. M. L., Brazil, R. P., Saraiva, L., Quaresma, P. F., Botelho, H. A., Ramos, M. C. D. N. F., de Almeida Zenóbio, A. P. L., E Meira, P. C. L. S., De Castilho Sanguinette, C. and Andrade Filho, J. D. (2012). Hourly activity and natural infection of sandflies (Diptera: Psychodidae) captured from the aphtoic zone of a cave, Minas Gerais State, Brazil. PLoS ONE, 7(12):e52254. https://doi.org/10.1371/journal.pone.0052254 [DOI] 🠔
  7. Carvalho, G. M. D. L., Brazil, R. P., Ramos, M. C. D. N. F., Serra E Meira, P. C. L., Zenóbio, A. P. L. D. A., Botelho, H. A., Sanguinette, C. D. C., Saraiva, L. and Andrade Filho, J. D. (2013). Ecological aspects of phlebotomine sandflies (Diptera: Psychodidae) from a cave of the speleological province of Bambuí, Brazil. PLoS ONE, 8(10):e77158. https://doi.org/10.1371/journal.pone.0077158 [DOI] 🠔
  8. Da Silva, A. A., Rebêlo, J. M. M., Carneiro, B. F., Castro, M. P. P., De Sousa De Almeida, M., Ponte, I. S., Aguiar, J. V. C. and Silva, F. S. (2019). Exploiting the synergistic effect of kairomones and light-emitting diodes on the attraction of phlebotomine sand flies to light traps in Brazil. Journal of Medical Entomology, 56(5):1441–1445. https://doi.org/10.1093/jme/tjz073 [DOI] 🠔
  9. Dutra-Rêgo, F., Freire, M. L., Carvalho, G. M. D. L. and Andrade-Filho, J. D. (2022). Revisiting the cave-dwelling sand flies (Diptera, Psychodidae, Phlebotominae) from Brazil: Diversity and potential role in the transmission of Leishmania Ross, 1903 (Kinetoplastida: Trypanosomatidae). Medical and Veterinary Entomology, 36(4):408–423. https://doi.org/10.1111/mve.12578 [DOI] 🠔
  10. Galati, E. A. B., Andrade-Filho, J. D., Silva, A. C. L. D. and Falcão, A. L. (2003). Description of a new genus and new species of New World Phlebotominae (Diptera, Psychodidae). Revista Brasileira de Entomologia, 47(1):63–70. https://doi.org/10.1590/S0085-56262003000100010 [DOI] 🠔
  11. Galati, E. A. B. (2021). Morfologia e terminologia de Phlebotominae (Diptera: Psychodidae). Classificação e identificação de táxons das Américas. Vol I. Apostila da Disciplina Bioecologia e Identificação de Phlebotominae do Programa de Pós-Graduação em Saúde Pública. Faculdade de Saúde Pública da Universidade de São Paulo, São Paulo. https://www.fsp.usp.br/egalati [URL] 🠔
  12. Killick-Kendrick, R. (1999). The biology and control of Phlebotomine sand flies. Clinics in Dermatology, 17(3):279–289. https://doi.org/10.1016/S0738-081X(99)00046-2 [DOI] 🠔
  13. Maroli, M., Feliciangeli, M. D., Bichaud, L., Charrel, R. N. and Gradoni, L. (2013). Phlebotomine sandflies and the spreading of leishmaniasis and other diseases of public health concern. Medical and Veterinary Entomology, 27(2):123–147. https://doi.org/10.1111/j.1365-2915.2012.01034.x [DOI] 🠔
  14. Moraes, J. L. P., Santos, C. L. C., Bastos, V. J. C., Pereira, A. C. N., Moraes, L. S., Moraes, J. R. L., Costa, M. C. and Rebêlo, J. M. M. (2015). Espécies de flebotomíneos (Diptera, Psychodidae) em matas ciliares na transição entre a Amazônia úmida e o Nordeste semi-árido do Brasil. Entomotopica, 30(3):20–29. 🠔
  15. Moraes, J. L. P., Santana, H. T. M., Bandeira, M. C. A., and Rebêlo, J. M. M. (2020). Effects of forest degradation on the sand fly communities of northeast Brazil. Journal of Vector Ecology, 45(1):89–99. https://doi.org/10.1111/jvec.12376 [DOI] 🠔
  16. Pugedo H., Barata, R. A., França-Silva, J. C., Silva, J. C. and Dias, E. S. (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 [DOI] 🠔
  17. Rebêlo, J. M. M., Rocha, R. V. D., Moraes, J. L. P., Silva, C. R. M. D., Leonardo, F. S. and Alves, G. A. (2010). The fauna of phlebotomines (Diptera, Psychodidae) in different phytogeographic regions of the state of Maranhão, Brazil. Revista Brasileira de Entomologia, 54(3):494–500. https://doi.org/10.1590/S0085-56262010000300022 [DOI] 🠔
  18. Silva, F. S., Carvalho, L. P. C. D., Cardozo, F. P., Moraes, J. L. P. and Rebêlo, J. M. M. (2010). Sand flies (Diptera: Psychodidae) in a cerrado area of the Maranhão state, Brazil. Neotropical Entomology, 39(6):1032–1038. https://doi.org/10.1590/S1519-566X2010000600028 [DOI] 🠔
  19. Silva, F. S., Brito, J. M., Costa Neta, B. M. and Lobo, S. E. P. D. (2015). Evaluation of light-emitting diodes as attractant for sandflies (Diptera: Psychodidae: Phlebotominae) in northeastern Brazil. Memórias do Instituto Oswaldo Cruz, 110(6):801–803. https://doi.org/10.1590/0074-02760150132 [DOI] 🠔
  20. Silva, R. C. R., Guimarães E Silva, A. S., Da Silva Sousa, S. S., Bezerra, J. M. T., Macário Rebêlo, J. M. and Pinheiro, V. C. S. (2019). Occurrence of phlebotominae (Diptera: Psychodidae) in urban leishmaniasis transmission foci in North-Eastern Brazil. Journal of Medical Entomology, 56(1):247–253. https://doi.org/10.1093/jme/tjy182 [DOI] 🠔
  21. Vilela, M. L., Rangel, E. F. and Lainson, R. (2003). Métodos de coleta e preservação de flebotomíneos. In: Rangel, E. F. Lainson, R. (org): Flebotomíneos no Brasil. Rio de Janeiro: Editora Fiocruz. Cap 8, p. 353–367. 🠔
  22. Young, D. G. and Duncan, M. A. (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. n. 54(1):1–881. 🠔
All the authors declare that there is no conflict of interest.
Maria Regiane A. Soares designed research; Maria Jose A. P. Barbosa, Maria Regiane A. Soares, Diogo B. S. Barbosa collected and analysed the data; Maria Jose A. P. Barbosa, Maria Regiane A. Soares, Diogo B. S. Barbosa led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Barbosa, M. J. A. P., Barbosa, D. B. S., Soares, M. R. A. S (2024). First Record of Edentomyiapiauiensis (Diptera: Psychodidae) in Maranhão State, Brazil. Acta Biol Colomb, 29(2), 178-181 https://doi.org/10.15446/abc.v29n2.109004