Revisiting the cave-dwelling sand flies (Diptera, Psychodidae, Phlebotominae) from Brazil: Diversity and potential role in the transmission of Leishmania Ross, 1903 (Kinetoplastida: Trypanosomatidae).
Brazil
Leishmania
Phlebotominae
cave
sand fly
Journal
Medical and veterinary entomology
ISSN: 1365-2915
Titre abrégé: Med Vet Entomol
Pays: England
ID NLM: 8708682
Informations de publication
Date de publication:
12 2022
12 2022
Historique:
received:
11
01
2022
accepted:
24
04
2022
pubmed:
19
5
2022
medline:
9
11
2022
entrez:
18
5
2022
Statut:
ppublish
Résumé
Brazilian caves, one of the many tourist attractions of the country, may act as a shelter for insects, such as sand flies (Diptera: Psychodidae), natural hosts of various microorganisms including parasites of the genus Leishmania Ross, 1903. In the last decades, with the increasing global need for sustainable development, ecotourism has emerged as one of the major activities in Brazil. However, the constant monitoring in environmentally protected areas is not often carried out, endangering visitors and professionals, especially due to the occurrence of zoonoses. Several sand fly species have already been recorded in Brazilian caves, drawing attention to the possibility of Leishmania transmission at this ecotope. Indeed, this current systematic review summarizes the fauna of cave-dwelling sand flies in Brazil, focusing on their biological behaviour and the occurrence of potential vectors of Leishmania parasites.
Types de publication
Journal Article
Review
Systematic Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
408-423Informations de copyright
© 2022 Royal Entomological Society.
Références
Akhoundi, M., Kuhls, K., Cannet, A., Votýpka, J., Marty, P., Delaunay, P. et al. (2016) A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Neglected Tropical Diseases, 10, e0004349.
Alves, V.R., de Freitas, R.A. & Barrett, T. (2008) Lutzomyia maruaga (Diptera: Psychodidae), a new bat-cave sand fly from Amazonas, Brazil. Memórias do Instituto Oswaldo Cruz, 103, 251-253. https://doi.org/10.1590/S0074-02762008005000012
Alves, V.R., de Freitas, R.A., Santos, F.L. & Barrett, T.V. (2011) Diversity of sandflies (Psychodidae: Phlebotominae) captured in sandstone caves from Central Amazonia, Brazil. Memórias do Instituto Oswaldo Cruz, 106, 253-259. https://doi.org/10.1590/s0074-02762011000300016
Andrade-Filho, J.D., Galati, E.A.B. & Falcão, A.L. (2007) Nyssomyia intermedia (Lutz & Neiva, 1912) and Nyssomyia neivai (Pinto, 1926) (Diptera: Psychodidae: Phlebotominae) geographical distribution and epidemiological importance. Memórias do Instituto Oswaldo Cruz, 102, 481-487.
Andrade-Filho, J.D., Lima da Silva, A.C. & Falcão, A.L. (2001) Phlebotomine sand flies in the State of Piauí, Brazil (Diptera: Psychodidae: Phlebotominae). Memórias do Instituto Oswaldo Cruz, 96, 1085-1087.
Andrade-Filho, J.D., Machado, T.O., Almeida, L.D.G.A., Carvalho, G.M.L., de Castilho Sanguinette, C., Brazil, R.P., 2008. Phlebotomine (Diptera:Psychodidae) sandflies collected in a cave in Palmas, Tocantins state, Brazil, in: International Symposium on Phlebotomine Sandflies - ISOPS VI. p. OP-06.
Andrade-Filho, J.D., Scholte, R.G.C., Amaral, A.L.G., Shimabukuro, P.H.F., Carvalho, O.S. & Caldeira, R.L. (2017) Occurrence and probability maps of Lutzomyia longipalpis and Lutzomyia cruzi (Diptera: Psychodidae: Phlebotominae) in Brazil. Journal of Medical Entomology, 54, 1430-1434. https://doi.org/10.1093/JME/TJX094
Arias, J.R. & de Freitas, R.A. (1978) Sobre os vetores de leishmaniose cutânea na Amazônia central do Brasil. 2: incidência de flagelados em flebótomos selváticos. Acta Amazonica, 8, 387-396. https://doi.org/10.1590/1809-43921978083387
Arias, J.R., Naiff, R.D., Miles, M.A. & De Souza, A.A. (1981) The opossum, Didelphis marsupialis (Marsupialia: Didelphidae), as a reservoir host of Leishmania braziliensis guyanensis in the Amazon Basin of Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene, 75, 537-541. https://doi.org/10.1016/0035-9203(81)90194-2
Auler, A.S. & Piló, L.B. (2015) Caves and Mining in Brazil: the dilemma of cave preservation within a mining context. Environment and Earth Science, 1, 487-496. https://doi.org/10.1007/978-3-642-17435-3_55
Balbino, V.Q., Marcondes, C.B., Alexander, B., Luna, L.K.S., Lucena, M.M.M., Mendes, A.C.S. et al. (2001) First report of Lutzomyia (Nyssomyia) umbratilis Ward & Frahia, 1977 outside of Amazonian region, in Recife, state of Pernambuco, Brazil (Diptera: Psychodidae: Phlebotominae). Memórias do Instituto Oswaldo Cruz, 96, 315-317. https://doi.org/10.1590/S0074-02762001000300005
Barata, R.A., Antonini, Y., Gonçalves, C.M., Costa, D.C. & Dias, E.S. (2008) Flebotomíneos do Parque Nacional Cavernas do Peruaçu, MG. Neotropical Entomology, 37, 226-228. https://doi.org/10.1590/S1519-566X2008000200018
Barata, R.A. & Apolinário, E.C. (2012) Sandflies (Diptera: Psychodidae) from caves of the quartzite Espinhaço range, Minas Gerais, Brazil. Memórias do Instituto Oswaldo Cruz, 107, 1016-1020. https://doi.org/10.1590/S0074-02762012000800009
Barata, R.A., Serra e Meira, P.C.L. & Carvalho, G.M.L. (2012) Lutzomyia diamantinensis sp. nov., a new phlebotomine species (Diptera: Psychodidae) from a quartzite cave in Diamantina, state of Minas Gerais, Brazil. Memórias do Instituto Oswaldo Cruz, 107, 1006-1010. https://doi.org/10.1590/S0074-02762012000800007
Barr, T.C. (1968) Cave ecology and the evolution of troglobites. In: Evolutionary biology. Boston, MA: Springer, pp. 35-102. https://doi.org/10.1007/978-1-4684-8094-8_2
Barral, A., Pedral-Sampaio, D. & Grimaldi, G. (1991) Leishmaniasis in Bahia, Brazil: evidence that Leishmania amazonensis produces a wide spectrum of clinical disease. The American Journal of Tropical Medicine and Hygiene, 44, 536-546.
Brazil, R.P., Passos, W.L., Brazil, B.G., Temeljkovitch, M. & Andrade-Filho, J.D. (2010) Diptera, Psychodidae, Phlebotominae Rondani,1840: range extension and new records from lowland Bolivia. Check List, 6, 587-588. https://doi.org/10.15560/6.4.587
Brazil, R.P., Rodrigues, A.A.F. & Andrade-Filho, J.D. (2015) Sand fly vectors of Leishmania in the Americas - a mini review. Entomology, Ornithology & Herpetology, 4, 1000144.
Brilhante, A.F., Nunes, V.L.B., Kohatsu, K.A., Galati, E.A.B., Rocca, M.E.G. & Ishikawa, E.A.Y. (2015) Natural infection of phlebotomines (Diptera: Psychodidae) by Leishmania (Leishmania) amazonensis in an area of ecotourism in Central-Western Brazil. Journal of Venemous Animals and Toxins Including Tropical Diseases, 21, 39.
Cameron, M.M., Milligan, P.J.M., Llanos-Cuentas, A. & Davies, C.R. (1995) An association between phlebotomine sandflies and aphids in the Peruvian Andes. Medical and Veterinary Entomology, 9, 127-132. https://doi.org/10.1111/J.1365-2915.1995.TB00168.X
Campos, A.M., Dos Santos, C.L.C., Stumpp, R., Da Silva, L.H.D., Maia, R.A., Paglia, A.P. et al. (2017) Photoperiod differences in sand fly (Diptera: Psychodidae) species richness and abundance in caves in Minas Gerais state, Brazil. Journal of Medical Entomology, 54, 100-105. https://doi.org/10.1093/jme/tjw135
Campos, A.M., Maia, R.A., Capucci, D., Paglia, A.P. & Andrade-Filho, J.D. (2020) Species composition of sand flies (Diptera: Psychodidae) in caves of Quadrilátero Ferrífero, state of Minas Gerais, Brazil. PLoS One, 15, e0220268. https://doi.org/10.1371/journal.pone.0220268
Cantanhêde, L.M., Mattos, C.B., De Souza Ronconi, C., Filgueira, C.P.B., Da Silva Júnior, R.F., Limeira, C. et al. (2019) First report of Leishmania (Viannia) lindenbergi causing tegumentary leishmaniasis in the Brazilian western Amazon region. Parasite, 26, 30. https://doi.org/10.1051/PARASITE/2019030
Carvalho, G.M.L., Brazil, R.P., das Neves Farah Ramos, M.C., Serra e Meira, P.C.L., de Almeida Zenóbio, A.P.L., Botelho, H.A. et al. (2013) Ecological aspects of phlebotomine sandflies (Diptera: Psychodidae) from a cave of the speleological province of Bambuí, Brazil. PLoS One, 8, e77158. https://doi.org/10.1371/journal.pone.0077158
Carvalho, G.M.L., Brazil, R.P., Rêgo, F.D., Ramos, M.C.N.F., Zenóbio, A.P.L.A. & Andrade-Filho, J.D. (2017a) Molecular detection of Leishmania DNA in wild-caught phlebotomine sand flies (Diptera: Psychodidae) from a cave in the state of Minas Gerais, Brazil. Journal of Medical Entomology, 54, 196-203. https://doi.org/10.1093/jme/tjw137
Carvalho, G.M.L., Brazil, R.P., Sanguinette, C.C. & Andrade-Filho, J.D. (2010) Description of a new phlebotomine species, Martinsmyia reginae sp. nov. (Diptera: Psychodidae: Phlebotominae) from a cave in the state of Tocantins Brazil. Memórias do Instituto Oswaldo Cruz, 105, 336-340.
Carvalho, G.M.L., Brazil, R.P., Sanguinette, C.C. & Andrade-Filho, J.D. (2011a) Description of evandromyia spelunca, a new phlebotomine species of the cortelezzii complex, from a cave in Minas Gerais state, Brazil (Diptera: Psychodidae: Phlebotominae). Parasites and Vectors, 4, 158.
Carvalho, G.M.L., Brazil, R.P., Saraiva, L., Quaresma, P.F., Botelho, H.A., Ramos, M.C.N.F. et al. (2012) Hourly activity and natural infection of sandflies (Diptera: Psychodidae) captured from the aphotic zone of a cave, Minas Gerais State, Brazil. PLoS One, 7, e52254. https://doi.org/10.1371/JOURNAL.PONE.0052254
Carvalho, G.M.L., de Vasconcelos, F.B., da Silva, D.G., Botelho, H.A. & Andrade-Filho, J.D. (2011b) Diversity of phlebotomine sand flies (Diptera: Psychodidae) in Ibitipoca State Park, Minas Gerais, Brazil. Journal of Medical Entomology, 48, 764-769. https://doi.org/10.1603/ME10258
Carvalho, G.M.L., Rêgo, F.D., Tanure, A., Silva, A.C.P., Dias, T.A., Paz, G.F. et al. (2017b) Bloodmeal identification in field-collected sand flies from Casa Branca, Brazil, using the cytochrome b PCR method. Journal of Medical Entomology, 54, 1049-1054. https://doi.org/10.1093/JME/TJX051
Córdoba-Lanús, E., De-Grosso, M.L., Piñero, J.E., Valladares, B. & Salomón, O.D. (2006) Natural infection of Lutzomyia neivai with Leishmania spp. in northwestern Argentina. Acta Tropica, 98, 1-5. https://doi.org/10.1016/J.ACTATROPICA.2005.11.010
Costa, J.C.R., Marchi, G.H., Santos, C.S., Andrade, M.C.M., Chaves Junior, S.P., Silva, M.A.N. et al. (2021) First molecular evidence of frogs as a food source for sand flies (Diptera: Phlebotominae) in Brazilian caves. Parasitology Research, 120, 1571-1582. https://doi.org/10.1007/s00436-021-07154-3
Cruz, J.B., Neto, J.F.C. 2019 Anuário estatístico do patrimônio espeleológico brasileiro 2019. Brasília.
Deane, L.M. & Deane, M.P. (1957) Observações sobre abrigos e criadouros de flebótomos no noroeste do Estado do Ceará. Revista Brasileira de Malariologia e Doenças Tropicais, 9, 225-246.
Decu, V. (1986) Some considerations on the bat guano synusia. Emile Racovitza, 25, 41-51.
de Aguiar, G.M. & de Medeiros, W.M. (2003) Distribuição regional e habitats das espécies de flebotomíneos do Brasil. In: Rangel, E.F. & Lainson, R. (Eds.) Flebotomíneos no Brasil. Rio de Janeiro: FIOCRUZ, pp. 207-255.
de Almeida, P.S., de Paula, M.B., Brilhante, A.F., Medeiros-Sousa, A.R., Neitzke-Abreu, H.C., de Souza Carrijo, C.J. et al. (2019) Phlebotomine (Diptera: Psychodidae) fauna in a cavern containing cave paintings and its surrounding environment, central-West Brazil. Acta Tropica, 199, 105151.
de Andrade, A.R.O., Nunes, V.L.B., Galati, E.A.B., De Arruda, C.C.P., Santos, M.F.D.C., Rocca, M.E.G. et al. (2009) Epidemiological study on leishmaniasis in an area of environmental tourism and ecotourism, state of Mato Grosso do Sul, 2006-2007. Revista da Sociedade Brasileira de Medicina Tropical, 42, 488-493.
de Carvalho, M.R., Valença, H.F., Silva, F.J., de Pita-Pereira, D., Araújo-Pereira, T., Britto, C. et al. (2010) Natural Leishmania infantum infection in Migonemyia migonei (França, 1920) (Diptera:Psychodidae:Phlebotominae) the putative vector of visceral leishmaniasis in Pernambuco State, Brazil. Acta Tropica, 116, 108-110. https://doi.org/10.1016/J.ACTATROPICA.2010.03.009
de Pita-Pereira, D., Alves, C.R., Souza, M.B., Brazil, R.P., Bertho, Á.L., de Figueiredo Barbosa, A. et al. (2005) Identification of naturally infected Lutzomyia intermedia and Lutzomyia migonei with Leishmania (Viannia) braziliensis in Rio de Janeiro (Brazil) revealed by a PCR multiplex non-isotopic hybridisation assay. Transactions of the Royal Society of Tropical Medicine and Hygiene, 99, 905-913.
Dorval, M.E.C., Alves, T.P., Cristaldo, G., da Rocha, H.C., Alves, M.A., Oshiro, E.T. et al. (2010) Sand fly captures with Disney traps in area of occurrence of Leishmania (Leishmania) amazonensis in the state of Mato Grosso do Sul, mid-western Brazil. Revista da Sociedade Brasileira de Medicina Tropical, 43, 491-495.
dos Santos, S.O., Arias, J., Ribeiro, A.A., de Paiva Hoffmann, M., Freitas, R.A. & Malacco, M.A.F. (1998) Incrimination of Lutzomyia cruzi as a vector of American visceral leishmaniasis. Medical and Veterinary Entomology, 12, 315-317.
Forattini, O.P. (1973) In: Blücher, E. (Ed.) Entomologia Médica: Psychodidae. Phlebotominae. Leishmanioses. Bartonelose. São Paulo: Univ. São Paulo.
Galati, E.A.B. (2018) Phlebotominae (Diptera, Psychodidae): classification, morphology and terminology of adults and identification of American taxa. In: Rangel, E. & Shaw, J. (Eds.) Brazilian sand flies: biology, taxonomy, medical importance and control. Cham: Springer International Publishing, pp. 9-212.
Galati, E.A.B., Andrade-Filho, J.D., da Silva, A.C.L. & Falcão, A.L. (2003a) Description of a new genus and new species of Phlebotominae. Revista Brasileira de Entomologia, 47, 63-70.
Galati, E.A.B., Gonçalves-Andrade, R.M., Consales, C.A. & Bueno, E.F.M. (2010a) Phlebotomines (Diptera, Psychodidae) in the speleological province of the Ribeira Valley: 2. Parque Estadual do alto Ribeira (PETAR), São Paulo State, Brazil. Revista Brasileira de Entomologia, 54, 477-487.
Galati, E.A.B., Marassá, A.M., Gonçalves-Andrade, R.M., Consales, C.A. & Bueno, E.F.M. (2010b) Phlebotomines (Diptera, Psychodidae) in the Ribeira Valley Speleological Province - 1. Parque Estadual Intervales, state of São Paulo, Brazil. Revista Brasileira de Entomologia, 54, 311-321.
Galati, E.A.B., Nunes, V.L.B., Boggiani, P.C., Dorval, M.E.C., Cristaldo, G., da Rocha, H.C. et al. (2003b) Phlebotomines (Diptera, Psychodidae) in caves of the Serra da Bodoquena, Mato Grosso do Sul state, Brazil. Revista Brasileira de Entomologia, 47, 283-296.
Galati, E.A.B., Nunes, V.L.B. & Cristaldo, G. (2003c) Ecology of phlebotomines (Diptera: Psychodidae) in a visceral and cutaneous leishmaniosis focus in the Serra da Bodoquena and in an adjacent area of the state of Mato Grosso do Sul, Brazil. Revista de Patologia Tropical, 32, 235-261.
Galati, E.A.B., Nunes, V.L.B., de Almeida Rego, F., Jr., Oshiro, E.T. & Rodrigues Chang, M. (1997) Estudo de flebotomíneos (Diptera: Psychodidae) em foco de leishmaniose visceral no Estado de Mato Grosso do Sul, Brasil. Revista de Saúde Pública, 31, 378-390.
Galati, E.A.B., Nunes, V.L.B., Oshiro, E.T. & Rego-Jr, F.A. (1989) Nova espécie de Phlebotominae, Lutzomyia corumbaensis, sp. n. (Diptera, Psychodidae) do complexo Lutzomyia cortelezzii. Revista Brasileira de Entomologia, 33, 3-4.
Gomes, F.T., Ferreira, R.L. & Jacobi, C.M. (2001) Comunidade de artrópodes de uma caverna calcária em área de mineração: composição e estrutura. Revista Brasileira de Zoociências, 3, 77-96.
Guernaoui, S., Boussaa, S., Pesson, B. & Boumezzough, A. (2006) Nocturnal activity of phlebotomine sandflies (Diptera: Psychodidae) in a cutaneous leishmaniasis focus in Chichaoua, Morocco. Parasitology Research, 98, 184-188. https://doi.org/10.1007/S00436-005-0032-8/FIGURES/6
Guimarães, V.C.F.V., Pruzinova, K., Sadlova, J., Volfova, V., Myskova, J., Brandão-Filho, S.P. et al. (2016) Lutzomyia migonei is a permissive vector competent for Leishmania infantum. Parasites and Vectors, 9, 159.
Hagen, H.A. (1881) On the color and the pattern of insects. Proceedings of the American Academy of Arts and Sciences, 17, 234-267. https://doi.org/10.2307/25138651
Killick-Kendrick, R. (1990) Phlebotomine vectors of the leishmaniases: a review. Medical and Veterinary Entomology, 4, 1-24. https://doi.org/10.1111/J.1365-2915.1990.TB00255.X
Lainson, R. & Shaw, J.J. (1968) Leishmaniasis in Brazil: I. observations on enzootic rodent leishmaniasis-incrimination of Lutzomyia flaviscutellata (mangabeira) as the vector in the lower amazonian basin. Transactions of the Royal Society of Tropical Medicine and Hygiene, 62, 385-395. https://doi.org/10.1016/0035-9203(68)90090-4
Lainson, R., Shaw, J.J., Ready, P.D., Miles, M.A. & Povoa, M. (1981) Leishmaniasis in Brazil: XVI. Isolation and identification of, Leishmania species from sandflies, wild mammals and man in North Pará State, with particular reference to L. braziliensis guyanensis causative agent of “pian-bois”. Transactions of the Royal Society of Tropical Medicine and Hygiene, 75, 530-536. https://doi.org/10.1016/0035-9203(81)90192-9
Lainson, R., Shaw, J.J., Ward, R.D., Ready, P.D. & Naiff, R.D. (1979) Leishmaniasis in Brazil: XIII. Isolation of Leishmania from armadillos (Dasypus novemcinctus), and observations on the epidemiology of cutaneous leishmaniasis in North Pará State. Transactions of the Royal Society of Tropical Medicine and Hygiene, 73, 239-242.
Lampo, M., Feliciangeli, M.D., Márquez, L.M., Bastidas, C. & Lau, P. (2000) A possible role of bats as a blood source for the Leishmania vector Lutzomyia longipalpis (Diptera: Psychodidae). The American Journal of Tropical Medicine and Hygiene, 62, 718-719. https://doi.org/10.4269/AJTMH.2000.62.718
Le Pont, F. & Pajot, F.X. (1980) Leishmaniasis in French Guiana. I. Studies on the ecology and natural infection rate of the vector Lutzomyia umbratilis 1977 during the dry season. Epidemiological considerations. Cahiers ORSTOM, Serie Entomologie Medicale et Parasitologie, 18, 359-382.
Leão, P.D.O., Pereira-Júnior, A.M., De Paulo, P.F.M., Carvalho, L.P.C., Souza, A.B.N., Da Silva, M.S. et al. (2020) Vertical stratification of sand fly diversity in relation to natural infections of Leishmania sp. and blood-meal sources in Jamari National Forest, Rondônia State, Brazil. Parasites and Vectors, 13, 422. https://doi.org/10.1186/S13071-020-04295-9/TABLES/4
Lewis, D.J. (1975) Functional morphology of the mouth parts in New World phlebotomine sandflies (Diptera: Psychodidae). Transactions of the Royal Entomological Society of London, 126, 497-532.
Lewis, D.J. & Domoney, C.R. (1966) Sugar meals in Phlebotominae and Simuliidae (Diptera). Proceedings of the Royal Entomological Society of London. Series A, General Entomology, 41, 175-179. https://doi.org/10.1111/J.1365-3032.1966.TB00340.X
Lino, C.F. (2001) Cavernas: o fascinante Brasil subterrâneo, 2nd edition. São Paulo: Gaia.
Lorenzetti, D.L. & Ghali, W.A. (2013) Reference management software for systematic reviews and meta-analyses: an exploration of usage and usability. BMC Medical Research Methodology, 13, 141. https://doi.org/10.1186/1471-2288-13-141/TABLES/2
Marcondes, C.B. (2007) A proposal of generic and subgeneric abbreviations for phlebtomine sandflies (Diptera: Psychodidae: Phelbotomina) of the world. Entomological News, 118, 351-356.
Martins, A.V., Falcão, A.L. & Silva, J.E. (1957) Estudos sôbre os Flébotomos do Estado de Minas Gerais - I. Phlebotomus renei n. sp. (Diptera, Psychodidae). Revista Brasileira de Malariologia e Doenças Tropicais, 9, 321-325.
Martins, A.V., Falcão, A.L. & Silva, J.E. (1962) Note on the Phlebotomus of the state of Goiás, with a description of two new species and the female of P. longipennis and redescription of the male of P. evandroi. Revista Brasileira de Malariologia e Doenças Tropicais, 14, 379-394.
Martins, A.V., Souza, M.A. & Silva, J.E. (1961) Estudo sôbre os flebótomos do Estado de Minas Gerais: II - Descrição do macho e redescrição da fêmea de “Lutzomyia cavernicola” (Costa Lima, 1932) (Diptera, Psychodidae). Revista Brasileira de Biologia, 21, 225-232.
Missawa, N.A., Veloso, M.A.E., Maciel, G.B.M.L., Michalsky, É.M. & Dias, E.S. (2011) Evidence of transmission of visceral leishmaniasis by Lutzomyia cruzi in the municipality of Jaciara, State of Mato Grosso, Brazil. Revista da Sociedade Brasileira de Medicina Tropical, 44, 76-78.
Mitchell, R.W. (1969) A comparison of temperate and tropical cave communities. The Southwestern Naturalist, 14, 73-88. https://doi.org/10.2307/3669249
Ogawa, G.M., Pereira-Júnior, A.M., Resadore, F., de Godoi Mattos Ferreira, R., Medeiros, J.F. & Camargo, L.M.A. (2016) Sandfly fauna (Diptera: Psychodidae) from caves in the state of Rondônia, Brazil. Revista Brasileira de Parasitologia Veterinária, 25, 61-68. https://doi.org/10.1590/S1984-29612016017
Ouzzani, M., Hammady, H., Fedorowicz, Z. & Elmagarmid, A. (2016) Rayyan-a web and mobile app for systematic reviews. Systematic Reviews, 5, 210. https://doi.org/10.1186/S13643-016-0384-4/FIGURES/6
PAHO. 2020 Leishmaniases. Epidemiological Report of the Americas, December 2020.
Pajot, F.X., Le Pont, F., Gentile, B. & Besnard, R. (1982) Epidemiology of leishmaniasis in French Guiana. Transactions of the Royal Society of Tropical Medicine and Hygiene, 76, 112-113. https://doi.org/10.1016/0035-9203(82)90033-5
Pereira-Júnior, A.M., Souza, A.B.N., Castro, T.S., da Silva, M.S., de Paulo, P.F.M., Ferreira, G.E.M. et al. (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
Polseela, R., Vitta, A., Nateeworanart, S. & Apiwathnasorn, C. (2011) Distribution of cave-dwelling phlebotomine sand flies and their nocturnal and diurnal activity in Phitsanulok Province, Thailand. Southeast Asian Journal of Tropical Medicine and Public Health, 42, 1395-1404.
Poulson, T.L. & White, W.B. (1969) The cave environment. Science, 165, 971-981.
Rangel, E.F. & 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
Ready, P.D., Lainson, R., Shaw, J.J. & Ward, R.D. (1986) The ecology of lutzomyia umbratilis Ward & Fraiha (Diptera: Psychodidae), the major vector to man of Leishmania braziliensis guyanensis in north-eastern Amazonian Brazil. Bulletin of Entomological Research, 76, 21-40. https://doi.org/10.1017/S0007485300015248
Rebêlo, J.M.M., Assunção, A.N., Silva, O. & Moraes, J.L.P. (2010) Ocorrência de flebotomíneos (Diptera, Psychodidae) em focos de leishmanioses, em área de ecoturismo do entorno do Parque Nacional dos Lençóis Maranhenses, Brasil. Cadernos de Saúde Pública, 26, 195-198. https://doi.org/10.1590/S0102-311X2010000100020
Rêgo, F.D. & Soares, R.P.P. (2021) Lutzomyia longipalpis: an update on this sand fly vector. Anais da Academia Brasileira de Ciências, 93, e20200254. https://doi.org/10.1590/0001-37652021xxxx
Resadore, F., Pereira-Júnior, A.M., Carvalho, L.P.C., De Azevedo Dos Santos, A.P., Teles, C.B.G. & Medeiros, J.F. (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
Rethlefsen, M.L., Kirtley, S., Waffenschmidt, S., Ayala, A.P., Moher, D., Page, M.J. et al. (2021) PRISMA-S: an extension to the PRISMA statement for reporting literature searches in systematic reviews. Systematic Reviews, 10, 39. https://doi.org/10.1186/S13643-020-01542-Z/TABLES/1
Rodrigues, A.C.M., Melo, L.M., Magalhães, R.D., Moraes, N.B., Souza-Júnior, A.D. & Bevilaqua, C.M.L. (2016) Molecular identification of Lutzomyia migonei (Diptera: Psychodidae) as a potential vector for Leishmania infantum (Kinetoplastida: Trypanosomatidae). Veterinary Parasitology, 220, 28-32. https://doi.org/10.1016/J.VETPAR.2016.02.018
Rotureau, B. (2006) Ecology of the Leishmania species in the Guianan ecoregion complex. The American Journal of Tropical Medicine and Hygiene, 74, 81-96. https://doi.org/10.4269/AJTMH.2006.74.81
Ryan, L. 1986 Flebótomos do Estado do Pará, Brasil: Diptera, Psychodidae, Phlebotominae. Belém.
Ryan, L., Lainson, R., Shaw, J.J., Braga, R.R. & Ishikawa, E.A.Y. (1987) Leishmaniasis in Brazil. XXV. Sandfly vectors of Leishmania in Pará State, Brazil. Medical and Veterinary Entomology, 1, 383-395. https://doi.org/10.1111/J.1365-2915.1987.TB00369.X
Savani, E.S.M.M., Nunes, V.L.B., Galati, E.A.B., Castilho, T.M. & Floeter-Winter, L.M. (2009) The finding of Lutzomyia almerioi and Lutzomyia longipalpis naturally infected by Leishmania spp. in a cutaneous and canine visceral leishmaniases focus in Serra da Bodoquena, Brazil. Veterinary Parasitology, 160, 18-24.
Serra e Meira, P.C.L., Abreu, B.L., de Almeida Zenóbio, A.P.L., de Castilho Sanguinette, C., Rêgo, F.D., de Lima Carvalho, G.M. et al. (2022) Phlebotominae Fauna (Diptera: Psychodidae) and molecular detection of Leishmania (Kinetoplastida: Trypanosomatidae) in urban caves of Belo Horizonte, Minas Gerais, Brazil. Journal of Medical Entomology, 59, 257-266. https://doi.org/10.1093/jme/tjab156
Sherlock, I. (1957) Sobre o “Phlebotomus renei” Martins, Falcão & Silva, 1956 (Diptera, Psychodidae). Revista Brasileira de Biologia, 17, 547-556.
Shimabukuro, P.H.F., de Lima Carvalho, G.M., Gontijo, C.M.F. & Rêgo, F.D. (2016) Description of the female of Martinsmyia minasensis (Diptera, Psychodidae, Phlebotominae), with distribution records and a key to female identification. Journal of Medical Entomology, 53, 533-540. https://doi.org/10.1093/JME/TJV254
Shimabukuro, P.H.F., Marassá, A.M. & Galati, E.A.B. (2007) Brumptomyia carvalheiroi sp. nov. (Diptera: Psychodidae: Phlebotominae) from Atlantic forest domain, São Paulo State, Brazil. Zootaxa, 1637, 47-54.
Silveira, F.T., Ishikawa, E.A.Y., De Souza, A.A.A. & 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
Silveira, F.T., Souza, A.A., Lainson, R., Shaw, J.J., Braga, R.R. & Ishikawa, E.E.A. (1991) Cutaneous leishmaniasis in the Amazon region: natural infection of the sandfly Lutzomyia ubiquitalis (Psychodidae: Phlebotominae) by Leishmania (Viannia) lainsoni in Pará state, Brazil. Memórias do Instituto Oswaldo Cruz, 86, 127-130. https://doi.org/10.1590/S0074-02761991000100021
Teodoro, L.M., de Lima Carvalho, G.M., Campos, A.M., Cerqueira, R.F.V., Souza-Silva, M., Ferreira, R.L. et al. (2021) Phlebotomine sand flies (Diptera, Psychodidae) from iron ore caves in the State of Pará, Brazil. Subterranean Biology, 37, 27-42.
Tesh, R.B., Guzman, H. & Wilson, M.L. (1992) Trans-beta-farnesene as a feeding stimulant for the sand fly Lutzomyia longipalpis (Diptera: Psychodidae). Journal of Medical Entomology, 29, 226-231. https://doi.org/10.1093/JMEDENT/29.2.226
Tonelli, G.B., Tanure, A., Rêgo, F.D., de Lima Carvalho, G.M., Simões, T.C. & Andrade-Filho, J.D. (2017) Aspects of the ecology of phlebotomine sand flies (Diptera: Psychodidae) in the Private Natural Heritage Reserve Sanctuary Caraça. PLoS One, 12, e0178628. https://doi.org/10.1371/journal.pone.0178628
Vandel, A. (2013) Biospeleology: the biology of cavernicolous animals. Oxford: Pergamon Press.
Vasconcelos dos Santos, T. & Silveira, F.T. (2020) Increasing putative vector importance of Trichophoromyia phlebotomines (Diptera: Psychodidae). Memórias do Instituto Oswaldo Cruz, 115, e190284. https://doi.org/10.1590/0074-02760190284
Vilela, M.L., Azevedo, A.C.R. & Godoy, R.E. (2015) Description of a new phlebotomine species of the Brazilian Cerrado from sandstone caves in Tocantins state, Brazil: Lutzomyia (Lutzomyia) elizabethrangelae sp. nov. (Diptera: Psychodidae). Journal of Medical Entomology, 52, 596-603. https://doi.org/10.1093/JME/TJV036
Williams, P. (1970) Phlebotomine sandflies and leishmaniasis in British Honduras (Belize). Transactions of the Royal Society of Tropical Medicine and Hygiene, 64, 317-363. https://doi.org/10.1016/0035-9203(70)90171-9