Publicado

2021-05-28

GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL

Diversidad genética de Lutzomyia (Nyssomyia) intermedia en un área endémica de leishmaniasis cutánea americana del estado de Paraná, Brasil

DOI:

https://doi.org/10.15446/abc.v26n3.84619

Palabras clave:

intraspecific variation, molecular epidemiology, phenetic analysis, Phlebotominae (en)
análisis fenético, epidemiología molecular, Phlebotominae, variación intraespecífica (es)

Descargas

Autores/as

Lutzomyia intermedia (Diptera: Psychodidae) features as one of the main vectors that are involved in the transmission of American cutaneous leishmaniasis (ACL) in the Neotropical region. However, genetic studies involving this taxon are still incipient and important for understanding the level of variability of different populations, their role, and implications as vectors. The aim of this study was to determine the level of genetic diversity of L. intermedia present in the Ribeira River Valley, an area of ACL transmission in the state of Paraná, Brazil, through the Random amplified polymorphic DNA (RAPD). Two municipalities were chosen to collect sand flies: Cerro Azul (new transmission area of the ACL) and Adrianópolis (endemic area of the ACL). The insects were captured in the house, in the peridomicile and in the wild (forest). Two of the used markers made it possible to estimate the polymorphism of the studied populations, resulting in 40 genotypes, most of them from peridomicile. The dendrogram generated by the analysis with the primer A10 showed different degrees of similarity, suggesting that there may be gene flow in the studied populations. The Principal Coordinate Analysis (PCO) with the A2 primer, was useful in grouping L. intermedia according to its ecological and geographical origin. There was no distinction between the lineages composing the L. intermedia complex. The results of this study, with the record of great genotypic diversity in L. intermedia, may contribute to explain the maintenance of the life cycle of Leishmania braziliensis (Kinetoplastida: Trypanosomatidae) in the region.

Lutzomyia intermedia (Diptera: Psychodidae) es uno de los principales vectores que participan en la transmisión de leishmaniasis cutánea americana (LCA) en la región Neotropical. A pesar de que aún los estudios genéticos que involucran a este taxón son incipientes, tienen una gran importancia para comprender el nivel de variabilidad de las diferentes poblaciones y sus implicaciones en su papel vectorial. El objetivo de este estudio fue determinar el nivel de diversidad genética de L. intermedia presente en el Valle del Río Ribeira, área de transmisión de LCA en el estado de Paraná, Brasil, mediante RAPD (ADN polimórfico amplificado aleatoriamente). Los flebótomos fueron recolectados en los municipios Cerro Azul (nueva área de transmisión de LCA) y Adrianópolis (área endémica de LCA), donde fueron capturados en ambientes residenciales, en el peridomicilio y en el bosque. Dos de los marcadores utilizados permitieron estimar el polimorfismo en las poblaciones estudiadas con la obtención de 40 genotipos, la mayoría de ellos en el peridomicilio. El dendrograma generado por el análisis con el cebador A10 mostró diferentes grados de similitud, lo que sugiere que puede haber flujo génico en las poblaciones. El Análisis de Coordenadas Principales (PCO) con el cebador A2 fue útil para agrupar L. intermedia según su origen ecológico y geográfico. No hubo distinción entre los linajes que componen el complejo L. intermedia. Los resultados de este estudio, con el registro de gran diversidad genotípica en L. intermedia, pueden contribuir a explicar el mantenimiento del ciclo biológico de Leishmania braziliensis (Kinetoplastida: Trypanosomatidae) en la región.

Referencias

Adamson RE, Ward RD, Feliciangeli MD, Maingon R. The application of random amplified polymorphic DNA for sandfly species identification. Med Vet Entomol. 1993;7(3):203-207. Doi: https://doi.org/10.1111/j.1365-2915.1993.tb00677.x DOI: https://doi.org/10.1111/j.1365-2915.1993.tb00677.x

Almazán MC, Copa GN, Lauthier JJ, Gil JF, Quiroga IL, Hoyos CL, et al. Sand fly typing: a simple and morphologically-supported method based on polymorphism of 18S rRNA gene in a Leishmaniasis endemic area of Argentina. Acta Trop. 2020;211:105609. Doi: https://doi.org/10.1016/j.actatropica.2020.105609 DOI: https://doi.org/10.1016/j.actatropica.2020.105609

Andrade Filho JD, Galati EAB, Falcão AL. Nyssomyia intermedia (Lutz & Neiva, 1912) and Nyssomyia neivai (Pinto, 1926) (Diptera: Psychodidae: Phlebotominae) geographical distribution and epidemiological importance. Mem Inst Oswaldo Cruz. 2007;102(4):481-487. Doi: https://doi.org/10.1590/S0074-02762007005000035 DOI: https://doi.org/10.1590/S0074-02762007005000035

Azevedo ACR, Monteiro FA, Cabello PH, Souza NA, Rosa-Freitas MG, Rangel EF. Studies on Populations of Lutzomyia longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) in Brazil. Mem Inst Oswaldo Cruz. 2000;95(3):305-322. Doi: https://doi.org/10.1590/S0074-02762000000300005 DOI: https://doi.org/10.1590/S0074-02762000000300005

Balbino V, Coutinho-Abreu IV, Sonoda IV, Melo MA, de Andrade PP, de Castro JA, et al. Genetic structure of natural populations of the sand fly Lutzomyia longipalpis (Diptera: Psychodidae) from the Brazilian northeastern region. Acta Trop. 2006;98(1):15-24. Doi: https://doi.org/10.1016/j.actatropica.2006.01.007 DOI: https://doi.org/10.1016/j.actatropica.2006.01.007

Bejarano EE, Rojas W, Uribe S, Vélez ID, Porter, CH. Genetic analysis of a recently detected urban population of Lutzomyia evansi (Diptera: Psychodidae) in Colombia. Rev Soc Entomol Argent. 2009;68(1-2):135-141.

Burkett-Cadena ND, Vittor AY. Deforestation and vector-borne disease: Forest conversion favors important mosquito vectors of human pathogens. Basic Appl Ecol. 2018;26:101-110. Doi: https://doi.org/10.1016/j.baae.2017.09.012 DOI: https://doi.org/10.1016/j.baae.2017.09.012

Castro EA, Luz E, Telles FQ, Pandey A, Biseto A, Dinaiski M, et al. Eco-epidemiological survey of Leishmania (Viannia) braziliensis American cutaneous and mucocutaneous leishmaniasis in Ribeira Valley River, Paraná State, Brazil. Acta Trop. 2005;93(2):141-149. Doi: https://doi.org/10.1016/j.actatropica.2004.10.004 DOI: https://doi.org/10.1016/j.actatropica.2004.10.004

Chan-Chable RJ, Martínez-Arce A, Mis-Avila PC, Ortega-Morales AI. DNA barcodes and evidence of cryptic diversity of anthropophagous mosquitoes in Quintana Roo, Mexico. Ecol Evol. 2019;9(8):4692-4705. Doi: https://doi.org/10.1002/ece3.5073 DOI: https://doi.org/10.1002/ece3.5073

Coelho ASG. Bood: Avaliação de dendrogramas baseados em estimativas de distâncias/similaridades genéticas através do procedimento de bootstrap [computer program]. Version 3.03. Goiânia: Universidade Federal de Goiás; 2005. p.

Dvorak V, Aytekin AM, Alten B, Skarupova S, Votypka J, Volf P. A comparison of the intraspecific variability of Phlebotomus sergenti Parrot, 1917 (Diptera: Psychodidae). J Vector Ecol. 2006;31(2):229-238. Doi: https://doi.org/10.3376/1081-1710(2006)31[229:ACOTIV]2.0.CO;2 DOI: https://doi.org/10.3376/1081-1710(2006)31[229:ACOTIV]2.0.CO;2

Forattini OP, Rabello EX, Serra OP, Cotrim MD, Galati EAB, Barata JM. Observações sobre a transmissão da Leishmaniose Tegumentar no Estado de São Paulo, Brasil. Rev Saude Publica. 1976;10(1):31-43. Doi: https://doi.org/10.1590/S0034-89101976000100003 DOI: https://doi.org/10.1590/S0034-89101976000100003

Fraga J, Rodriguez J, Fuentes O, Hernández Y, Castex M, Gonzalez R, et al. Genetic variability of Triatoma flavida and Triatoma bruneri (Hemiptera: Reduviidae) by RAPD-PCR technique. Rev Inst Med Trop Sao Paulo. 2011;53(1):19-24. Doi: https://doi.org/10.1590/S0036-46652011000100004 DOI: https://doi.org/10.1590/S0036-46652011000100004

Freitas MTS, Costa Jr CRL, Silva LG, Leal-Balbino TC, Brazil RP, Balbino VQ. Genetic Structure of Sympatric Populations of Female Lutzomyia longipalpis (Diptera: Psychodidae) In Sobral and Caririaçu, Ceará State, Brazil. Vector Biol J. 2018;3(1):1-5. Doi: https://doi.org/10.4172/2473-4810.1000125 DOI: https://doi.org/10.4172/2473-4810.1000125

Galati EAB, Fonseca MB, Marassá AM, Bueno EFM. Dispersal and survival of Nyssomyia intermedia and Nyssomyia neivai (Diptera: Psychodidae: Phlebotominae) in a cutaneous leishmaniasis endemic area of the speleological province of the Ribeira Valley, state of São Paulo, Brazil. Mem Inst Oswaldo Cruz. 2009;104:1148-1158. Doi: https://doi.org/10.1590/S0074-02762009000800012 DOI: https://doi.org/10.1590/S0074-02762009000800012

Golczer G, Arrivillaga J. Use and trends of molecular markers in sandflies (Diptera: Psychodidae). Bol Mal Salud Amb. 2015;55(1):19-40.

Gomes AC, Santos JLF, Galati EAB. Ecological aspects of American cutaneous leishmaniasis: 4. Observations on the endophilic behavior of the sandfly and the vectorial role of Psychodopygus intermedius in the Ribeira Valley region of the S. Paulo State, Brazil. Rev de Saude Publica. 1986;20(4):280-287. Doi: https://doi.org/10.1590/S0034-89101986000400003 DOI: https://doi.org/10.1590/S0034-89101986000400003

Gonçalves AL, Ennio LE, Castro EA, Klisiowicz DR, Gazda TL, Melo ALA, et al. Abundance and diversity of vectors (Diptera: Psychodidae) in an old transmission area of cutaneous leishmaniasis in the new world after Bolivia-Brazil gas pipeline construction. Mem Inst Investig Cienc Salud. 2019;17(2):16-23. Doi: https://doi.org/10.18004/mem.iics/1812-9528/2019.017.02.16-023 DOI: https://doi.org/10.18004/mem.iics/1812-9528/2019.017.02.16-023

González R, Wilkerson R, Suárez MF, García F, Gallego G, Cárdenas H, et al. A population genetics study of Anopheles darlingi (Diptera: Culicidae) from Colombia based on random amplified polymorphic DNA-polymerase chain reaction and amplified fragment lenght polymorphism markers. Mem Inst Oswaldo Cruz. 2007;102(3):255-262. Doi: https://doi.org/10.1590/S0074-02762007005000037 DOI: https://doi.org/10.1590/S0074-02762007005000037

Hiragi C, Simões K, Martins E, Queiroz P, Lima L, Monnerat R. Variabilidade Genética em Populações de Aedes aegypti (L.) (Diptera: Culicidae) Utilizando Marcadores de RAPD. Neotrop Entomol. 2009;38(4):542-547. Doi: https://doi.org/10.1590/S1519-566X2009000400018 DOI: https://doi.org/10.1590/S1519-566X2009000400018

Ipardes (Instituto Paranaense de Desenvolvimento Econômico e Social). Cadernos municipais. Curitiba; 2020. Available in: http://www.ipardes.pr.gov.br/Pagina/Cadernos-municipais Cited: 03 ene 2020.

Jaccard P. Nouvelles recherches sur la distribution florale. Bull Soc Vaudoise Sci Nat. 1908;44:223-270.

Lima Costa CR, Freitas MTS, Figueirêdo Jr CAS, Aragão NS, Silva LG, Marcondes CB, et al. Genetic structuring and fixed polymorphisms in the gene period among natural populations of Lutzomyia longipalpis in Brazil. Parasit Vectors 2015;8:193. Doi: https://doi.org/10.1186/s13071-015-0785-6 DOI: https://doi.org/10.1186/s13071-015-0785-6

Loxdale HD, Lushai G. Molecular markers in entomology. Bull Entomol Res. 1998;88(6):577-600. Doi: https://doi.org/10.1017/S0007485300054250 DOI: https://doi.org/10.1017/S0007485300054250

Lozano-Sardaneta YN, Paternina LE, Sánchez-Montes S, Quintero A, Ibáñez-Bernal S, Sánchez-Cordero V, et al. DNA barcoding and fauna of phlebotomine sand flies (Diptera: Psychodidae: Phlebotominae) from Los Tuxtlas, Veracruz, Mexico. Acta Trop. 2020;201:105220. Doi: https://doi.org/10.1016/j.actatropica.2019.105220 DOI: https://doi.org/10.1016/j.actatropica.2019.105220

Mantel N. The Detection of Disease Clustering and a Generalized Regression Approach. Cancer Res. 1967;27(2):209-220.

Marcondes CB. A Redescription of Lutzomyia (Nyssomyia) intermedia (Lutz & Neiva, 1912), and Ressurrection of L. neivai (Pinto, 1926) (Diptera, Psychodidae, Phlebotominae). Mem Inst Oswaldo Cruz 1996;91(4):457-462. Doi: https://doi.org/10.1590/S0074-02761996000400012 DOI: https://doi.org/10.1590/S0074-02761996000400012

Marcondes CB. Morfometria e DNA mitocondrial de populações sul americanas de Lutzomyia (Nyssomyia) intermedia (Lutz & Neiva, 1912) (Diptera, Psychodidae, Phlebotominae). Rev Soc Bras Med Trop. 1997;30(6):533-534. DOI: https://doi.org/10.1590/S0037-86821997000600017

Mathis A, Depaquit J, Dvořák V, Tuten H, Bañuls AL, Halada P, et al. Identification of phlebotomine sand flies using one MALDI-TOF MS reference database and two mass spectrometer systems. Parasit Vectors. 2015;8:266. Doi: https://doi.org/10.1186/s13071-015-0878-2 DOI: https://doi.org/10.1186/s13071-015-0878-2

Meneses CR, Cupolillo E, Monteiro F, Rangel EF. Micro-geographical variation among male populations of the sandfly, Lutzomyia (Nyssomyia) intermedia, from an endemic area of American cutaneous leishmaniasis in the state of Rio de Janeiro, Brazil. Med Vet Entomol. 2005;19(1):38-47. Doi: https://doi.org/10.1111/j.0269-283X.2005.00535.x DOI: https://doi.org/10.1111/j.0269-283X.2005.00535.x

Mukhopadhyay J, Ghosh K, Braig HR. Identification of cutaneous Leishmaniasis vectors, Phlebotomus papatasi and P. duboscqi using random amplified polymorphic DNA. Acta Trop. 2000;76(3):277-283. Doi: https://doi.org/10.1016/S0001-706X(00)00130-3 DOI: https://doi.org/10.1016/S0001-706X(00)00130-3

Pinedo-Cancino V, Sheen P, Tarazona-Santos E, Oswald WE, Jeri C, Vittor AY, et al. Limited diversity of Anopheles darlingi in the Peruvian Amazon region of Iquitos. Am J Trop Med Hyg. 2006;75(2)238-245. Doi: https://doi.org/10.4269/ajtmh.2006.75.238 DOI: https://doi.org/10.4269/ajtmh.2006.75.238

Posso CA, González R, Cárdenas H, Gallego G, Duque MC, Suarez MF. Random Amplified Polymorphic DNA Analysis of Anopheles nuneztovari (Diptera: Culicidae) from Western and Northeastern Colombia. Mem Inst Oswaldo Cruz. 2003;98(4):469-476. Doi: https://doi.org/10.1590/S0074-02762003000400007 DOI: https://doi.org/10.1590/S0074-02762003000400007

Rocha LS, Falqueto A, Santos CB, Grimaldi Jr G, Cupolillo E. Genetic structure of Lutzomyia (Nyssomyia) intermedia populations from two ecologic regions in Brazil where transmission of Leishmania (Viannia) braziliensis reflects distinct eco-epidemiologic features. Am J Trop Med Hyg. 2007;76(3):559-65. Doi: https://doi.org/10.4269/ajtmh.2007.76.559 DOI: https://doi.org/10.4269/ajtmh.2007.76.559

Rohlf FJ. NTSYS-pc: Numerical taxonomy and multivariate analysis system [computer program]. Version 2.1. New York: Exeter Software; 2000.

Salomón OD, Mastrángelo AV, Santini MS, Liotta DJ, Yadón ZE. Retrospective eco-epidemiology as a tool for the surveillance of leishmaniasis in Misiones, Argentina, 1920-2014. Rev Panam Salud Publica. 2016;40(1):29-39.

Saraiva L, Carvalho GM, Sanguinette CC, Carvalho DAA, Andrade Filho JD. Biogeographical aspects of the occurrence of Nyssomyia neivai and Nyssomyia intermedia (Diptera: Psychodidae) in a sympatric area of the Brazilian savannah. Mem Inst Oswaldo Cruz. 2012;107(7):867-872. Doi: https://doi.org/10.1590/S0074-02762012000700005 DOI: https://doi.org/10.1590/S0074-02762012000700005

Savoia D. Recent updates and perspectives on leishmaniasis. J Infect Dev Ctries. 2015;9(6):588-596. Doi: https://doi.org/10.3855/jidc.6833 DOI: https://doi.org/10.3855/jidc.6833

Seblova V, Volfova V, Dvorak V, Pruzinova K, Votypka J, Kassahun A, et al. Phlebotomus orientalis sand flies from two geographically distant Ethiopian localities: biology, genetic analyses and susceptibility to Leishmania donovani. PLoS Negl Trop Dis. 2013;7(4):e2187. Doi: https://doi.org/10.1371/journal.pntd.0002187 DOI: https://doi.org/10.1371/journal.pntd.0002187

Sharma A, Kumar S, Tripathi P. Assessment of Achyranthes aspera induced toxicity and molecular analysis of RAPD-PCR profiles of larval genomic DNA of Aedes aegypti L. (Diptera: Culicidae). J Parasit Dis. 2017;41(4):1066-1073. Doi: https://doi.org/10.1007/s12639-017-0935-1 DOI: https://doi.org/10.1007/s12639-017-0935-1

Silva MH, Nascimento MD, Leonardo FS, Rebêlo JM, Pereira SR. Genetic Differentiation in Natural Populations of Lutzomyia longipalpis (Lutz & Neiva) (Diptera: Psychodidae) with Different Phenotypic Spot Patterns on Tergites in Males. Neotrop Entomol. 2011;40(4):501-506. Doi: https://doi.org/10.1590/S1519-566X2011000400015 DOI: https://doi.org/10.1590/S1519-566X2011000400015

Sneath P, Sokal RR. Numerical taxonomy: the principles and practice of numerical classification. San Francisco: W. H. Freeman.; 1973. 573 p.

Souza CM, Fortes-Dias CL, Linardi PM, Dias ES. Phenetic studies on randomly amplified polymorphic DNA-polymerase chain reaction-variability of four geographical populations of Lutzomyia whitmani (Diptera: Psychodidae) in Brazil. Rev Soc Bras Med Trop. 2004a;37(2):148-153. Doi: https://doi.org/10.1590/S0037-86822004000200007 DOI: https://doi.org/10.1590/S0037-86822004000200007

Souza NA, Brazil RP, Araki AS. The current status of the Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) species complex. Mem Inst Oswaldo Cruz. 2017;112(3):161-174. Doi: https://doi.org/10.1603/0022-2585-41.5.906 DOI: https://doi.org/10.1590/0074-02760160463

Souza NA, Vigoder FM, Araki AS, Ward RD, Kyriacou CP, Peixoto AA. Analysis of the Copulatory Courtship Songs of Lutzomyia longipalpis in Six Populations from Brazil. J Med Entomol. 2004b;41(5):906-913. Doi: https://doi.org/10.1603/0022-2585-41.5.906 DOI: https://doi.org/10.1603/0022-2585-41.5.906

Sudia WD, Chamberlain RW. Battery-operated light trap, an improved model. Mosq News. 1962;22:126-129.

Suesdek L. Microevolution of medically important mosquitoes - A review. Acta Trop. 2019;191:162-171. Doi: https://doi.org/10.1016/j.actatropica.2018.12.013 DOI: https://doi.org/10.1016/j.actatropica.2018.12.013

Tibayrenc M, Neubauer K, Barnabé C, Guerrini F, Skarecky D, Ayala FJ. Genetic characterization of six parasitic protozoa: parity between random-primer DNA typing and multilocus enzyme electrophoresis. Proc Natl Acad Sci USA. 1993;90(4):1335-1339. Doi: https://doi.org/10.1073/pnas.90.4.1335 DOI: https://doi.org/10.1073/pnas.90.4.1335

Vigoder FM, Souza NA, Brazil RP, Bruno RV, Costa PL, Ritchie MG, et al. Phenotypic differentiation in love song traits among sibling species of the Lutzomyia longipalpis complex in Brazil. Parasit Vectors 2015;8:290. Doi: https://doi.org/10.1186/s13071-015-0900-8 DOI: https://doi.org/10.1186/s13071-015-0900-8

Young DG, Duran MA. Guide to the identification and geographic distribution of Lutzomyia sand flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae). Mem Am Entomol Inst. 1994;54:1-881. DOI: https://doi.org/10.21236/ADA285737

Cómo citar

APA

Gonçalves, A. L., Castro, E. A. de, Luz, E., Fendrich, R. C., Souza, N. A. de y Thomaz-Soccol, V. (2021). GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL. Acta Biológica Colombiana, 26(3), 365–373. https://doi.org/10.15446/abc.v26n3.84619

ACM

[1]
Gonçalves, A.L., Castro, E.A. de, Luz, E., Fendrich, R.C., Souza, N.A. de y Thomaz-Soccol, V. 2021. GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL. Acta Biológica Colombiana. 26, 3 (may 2021), 365–373. DOI:https://doi.org/10.15446/abc.v26n3.84619.

ACS

(1)
Gonçalves, A. L.; Castro, E. A. de; Luz, E.; Fendrich, R. C.; Souza, N. A. de; Thomaz-Soccol, V. GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL. Acta biol. Colomb. 2021, 26, 365-373.

ABNT

GONÇALVES, A. L.; CASTRO, E. A. de; LUZ, E.; FENDRICH, R. C.; SOUZA, N. A. de; THOMAZ-SOCCOL, V. GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL. Acta Biológica Colombiana, [S. l.], v. 26, n. 3, p. 365–373, 2021. DOI: 10.15446/abc.v26n3.84619. Disponível em: https://revistas.unal.edu.co/index.php/actabiol/article/view/84619. Acesso em: 11 jul. 2024.

Chicago

Gonçalves, André Luiz, Edilene Alcântara de Castro, Ennio Luz, Ricardo Cancio Fendrich, Nataly Araújo de Souza, y Vanete Thomaz-Soccol. 2021. «GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL». Acta Biológica Colombiana 26 (3):365-73. https://doi.org/10.15446/abc.v26n3.84619.

Harvard

Gonçalves, A. L., Castro, E. A. de, Luz, E., Fendrich, R. C., Souza, N. A. de y Thomaz-Soccol, V. (2021) «GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL», Acta Biológica Colombiana, 26(3), pp. 365–373. doi: 10.15446/abc.v26n3.84619.

IEEE

[1]
A. L. Gonçalves, E. A. de Castro, E. Luz, R. C. Fendrich, N. A. de Souza, y V. Thomaz-Soccol, «GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL», Acta biol. Colomb., vol. 26, n.º 3, pp. 365–373, may 2021.

MLA

Gonçalves, A. L., E. A. de Castro, E. Luz, R. C. Fendrich, N. A. de Souza, y V. Thomaz-Soccol. «GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL». Acta Biológica Colombiana, vol. 26, n.º 3, mayo de 2021, pp. 365-73, doi:10.15446/abc.v26n3.84619.

Turabian

Gonçalves, André Luiz, Edilene Alcântara de Castro, Ennio Luz, Ricardo Cancio Fendrich, Nataly Araújo de Souza, y Vanete Thomaz-Soccol. «GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL». Acta Biológica Colombiana 26, no. 3 (mayo 28, 2021): 365–373. Accedido julio 11, 2024. https://revistas.unal.edu.co/index.php/actabiol/article/view/84619.

Vancouver

1.
Gonçalves AL, Castro EA de, Luz E, Fendrich RC, Souza NA de, Thomaz-Soccol V. GENETIC DIVERSITY OF Lutzomyia (Nyssomyia) intermedia IN AN ENDEMIC AREA OF AMERICAN CUTANEOUS LEISHMANIASIS, STATE OF PARANÁ, BRAZIL. Acta biol. Colomb. [Internet]. 28 de mayo de 2021 [citado 11 de julio de 2024];26(3):365-73. Disponible en: https://revistas.unal.edu.co/index.php/actabiol/article/view/84619

Descargar cita

CrossRef Cited-by

CrossRef citations0

Dimensions

PlumX

Visitas a la página del resumen del artículo

502

Descargas

Los datos de descargas todavía no están disponibles.