Skip to main content
Top
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Spatial distributions of Anopheles species in relation to malaria incidence at 70 localities in the highly endemic Northwest and South Pacific coast regions of Colombia

Authors: Martha L. Ahumada, Lorena I. Orjuela, Paula X. Pareja, Marcela Conde, Diana M. Cabarcas, Eliana F. G. Cubillos, Jorge A. Lopez, John C. Beier, Sócrates Herrera, Martha L. Quiñones

Published in: Malaria Journal | Issue 1/2016

Login to get access

Abstract

Background

A proper identification of malaria vectors is essential for any attempt to control this disease. Between 40 and 47 Anopheles species have been recorded in Colombia, and eight species complexes have been identified in the last decade. An update of Anopheles species distribution and its relationship with malaria is required, particularly for newly identified members of species complexes.

Methods

A cross-sectional entomological study was conducted at 70 localities in the highest malaria transmission areas in Colombia. In each locality, immature and adult mosquitoes were collected. All specimens were determined using morphological characters and confirmed used restriction profiles of Internal Transcribed Spacer 2 (PCR–RFLP-ITS2), and Cytochrome c Oxidase I (COI) sequence gene. To detect natural Plasmodium infections, enzyme-linked immunosorbent assay and nested PCR analysis were used. Distribution of Anopheles species was spatially associated with malaria incidence.

Results

A total of 1736 larvae and 12,052 adult mosquitoes were determined in the 70 localities. Thirteen Anopheles species were identified. COI sequence analysis suggested 4 new lineages for Colombia: for Anopheles albimanus (An. albimanus B), Anopheles pseudopunctipennis s.l., Anopheles neivai (An. neivai nr. neivai 4), and Anopheles apicimacula. Two members of species complexes were identified, as: Anopheles nuneztovari C, and Anopheles albitarsis I. Another seven species were confirmed. Four mosquitoes were infected with Plasmodium species, An. albimanus B and An. nuneztovari C. In Northwest of Colombia, An. nuneztovari C, An. albimanus, and Anopheles darlingi were present in the municipalities with highest annual parasitic index (API) (>35 cases/1000 inhabitants). In the north of South Pacific coast, with a similar API, An. nuneztovari C were widely distributed inland, and the main species in coastal regions were An. albimanus B and An. neivai s.l. In the South Pacific coast bordering with Ecuador, 3 Anopheles species were found in municipalities with high API (15–88 cases/1000 inhabitants): An. albimanus B, Anopheles calderoni and An. neivai s.l.

Conclusions

In the highest malaria areas of Colombia, 13 Anopheles species and four new lineages were found, which highlights the need for updating the species distribution. A DNA barcode analysis allowed the taxonomic identification to be refined, particularly for species complexes, and to improve the further understanding of their relation with malaria transmission.
Appendix
Available only for authorised users
Literature
2.
go back to reference Padilla JC, Álvarez G, Montoya R, Chaparro P, Herrera S. Epidemiology and control of malaria in Colombia. Mem Inst Oswaldo Cruz. 2011;106(Suppl 1):114–22. Padilla JC, Álvarez G, Montoya R, Chaparro P, Herrera S. Epidemiology and control of malaria in Colombia. Mem Inst Oswaldo Cruz. 2011;106(Suppl 1):114–22.
4.
go back to reference Montoya-Lerma J, Solarte YA, Giraldo-Calderón GI, Quiñones ML, Ruiz-López F, González R. Malaria vector species in Colombia-a review. Mem Inst Oswaldo Cruz. 2011;106(Suppl 1):223–38.CrossRefPubMedPubMedCentral Montoya-Lerma J, Solarte YA, Giraldo-Calderón GI, Quiñones ML, Ruiz-López F, González R. Malaria vector species in Colombia-a review. Mem Inst Oswaldo Cruz. 2011;106(Suppl 1):223–38.CrossRefPubMedPubMedCentral
5.
go back to reference Norris DE. Genetic markers for study of the anopheline vectors of human malaria. Int J Parasitol. 2002;32:1607–15.CrossRefPubMed Norris DE. Genetic markers for study of the anopheline vectors of human malaria. Int J Parasitol. 2002;32:1607–15.CrossRefPubMed
6.
go back to reference Ruiz-Lopez F, Wilkerson RC, Conn JE, McKeon SN, Levin DM, Quiñones ML, et al. DNA barcoding reveals both known and novel taxa in the Albitarsis Group (Anopheles: Nyssorhynchus) of Neotropical malaria vectors. Parasit Vectors. 2012;5:44.CrossRefPubMedPubMedCentral Ruiz-Lopez F, Wilkerson RC, Conn JE, McKeon SN, Levin DM, Quiñones ML, et al. DNA barcoding reveals both known and novel taxa in the Albitarsis Group (Anopheles: Nyssorhynchus) of Neotropical malaria vectors. Parasit Vectors. 2012;5:44.CrossRefPubMedPubMedCentral
7.
go back to reference Ruiz-Lopez F, Wilkerson RC, Ponsonby DJ, Herrera M, Sallum MAM, Velez ID, et al. Systematics of the oswaldoi complex (Anopheles, Nyssorhynchus) in South America. Parasit Vectors. 2013;6:324.CrossRefPubMedPubMedCentral Ruiz-Lopez F, Wilkerson RC, Ponsonby DJ, Herrera M, Sallum MAM, Velez ID, et al. Systematics of the oswaldoi complex (Anopheles, Nyssorhynchus) in South America. Parasit Vectors. 2013;6:324.CrossRefPubMedPubMedCentral
8.
go back to reference Brochero H, Quiñones ML. Retos de la entomología médica para la vigilancia en salud pública en Colombia: reflexión para el caso de malaria. Biomédica. 2008;28:18–24.CrossRefPubMed Brochero H, Quiñones ML. Retos de la entomología médica para la vigilancia en salud pública en Colombia: reflexión para el caso de malaria. Biomédica. 2008;28:18–24.CrossRefPubMed
9.
go back to reference Olano VA, Brochero HL, Sáenz R, Quiñones ML, Molina JA. Mapas preliminares de la distribución de especies de Anopheles vectores de malaria en Colombia. Biomédica. 2001;21:402–8. Olano VA, Brochero HL, Sáenz R, Quiñones ML, Molina JA. Mapas preliminares de la distribución de especies de Anopheles vectores de malaria en Colombia. Biomédica. 2001;21:402–8.
10.
go back to reference Quiñones ML, Suarez MF, Rodríguez A, Fleming GA, Galvis LE. Comportamiento de Anopheles (Kerteszia) lepidotus Zavortink, 1973, y su incriminación como posible vector de malaria en el departamento del Tolima, Colombia. Biomédica. 1984;4:5–13.CrossRef Quiñones ML, Suarez MF, Rodríguez A, Fleming GA, Galvis LE. Comportamiento de Anopheles (Kerteszia) lepidotus Zavortink, 1973, y su incriminación como posible vector de malaria en el departamento del Tolima, Colombia. Biomédica. 1984;4:5–13.CrossRef
11.
go back to reference Quiñones ML, Ruiz F, Calle DA, Harbach RE, Linton YM. Incrimination of Anopheles (Nyssorhynchus) rangeli and An. (Nys.) oswaldoi as natural vectors of Plasmodium vivax in Southern Colombia. Mem Inst Oswaldo Cruz. 2006;101:617–23.CrossRefPubMed Quiñones ML, Ruiz F, Calle DA, Harbach RE, Linton YM. Incrimination of Anopheles (Nyssorhynchus) rangeli and An. (Nys.) oswaldoi as natural vectors of Plasmodium vivax in Southern Colombia. Mem Inst Oswaldo Cruz. 2006;101:617–23.CrossRefPubMed
12.
go back to reference Orjuela LI, Herrera M, Erazo H, Quiñones ML. Especies de Anopheles presentes en el departamento del Putumayo y su infección natural con Plasmodium. Biomédica. 2013;33:42–52.PubMed Orjuela LI, Herrera M, Erazo H, Quiñones ML. Especies de Anopheles presentes en el departamento del Putumayo y su infección natural con Plasmodium. Biomédica. 2013;33:42–52.PubMed
13.
go back to reference Escovar JE, González R, Quiñones ML, Wilkerson RC, Ruiz F, Harrison BA. Morphology of the larvae, male genitalia and DNA sequences of Anopheles (Kerteszia) pholidotus (Diptera: Culicidae) from Colombia. Mem Inst Oswaldo Cruz. 2014;109:473–9.CrossRefPubMedPubMedCentral Escovar JE, González R, Quiñones ML, Wilkerson RC, Ruiz F, Harrison BA. Morphology of the larvae, male genitalia and DNA sequences of Anopheles (Kerteszia) pholidotus (Diptera: Culicidae) from Colombia. Mem Inst Oswaldo Cruz. 2014;109:473–9.CrossRefPubMedPubMedCentral
14.
go back to reference Orjuela LI, Ahumada ML, Avila I, Herrera S, Beier JC, Quiñones ML. Human biting activity, spatial-temporal distribution and malaria vector role of Anopheles calderoni in the southwest of Colombia. Malar J. 2015;14:256.CrossRefPubMedPubMedCentral Orjuela LI, Ahumada ML, Avila I, Herrera S, Beier JC, Quiñones ML. Human biting activity, spatial-temporal distribution and malaria vector role of Anopheles calderoni in the southwest of Colombia. Malar J. 2015;14:256.CrossRefPubMedPubMedCentral
15.
go back to reference Conde M, Pareja PX, Orjuela LI, Ahumada ML, Durán S, Jara JA, et al. Larval habitat characteristics of the main malaria vectors in the most endemic regions of Colombia: potential implications for larval control. Malar J. 2015;14:476.CrossRefPubMedPubMedCentral Conde M, Pareja PX, Orjuela LI, Ahumada ML, Durán S, Jara JA, et al. Larval habitat characteristics of the main malaria vectors in the most endemic regions of Colombia: potential implications for larval control. Malar J. 2015;14:476.CrossRefPubMedPubMedCentral
16.
go back to reference González R, Carrejo N. Introducción al estudio taxonómico de Anopheles de Colombia claves y notas de distribución. 2nd ed. Cali: Programa Editorial de la Universidad del Valle; 2009. González R, Carrejo N. Introducción al estudio taxonómico de Anopheles de Colombia claves y notas de distribución. 2nd ed. Cali: Programa Editorial de la Universidad del Valle; 2009.
17.
go back to reference Service MW. Mosquito ecology: field sampling methods. Chapman and Hall. 2nd ed. Essex: Elsevier Science Publishers; 1993. Service MW. Mosquito ecology: field sampling methods. Chapman and Hall. 2nd ed. Essex: Elsevier Science Publishers; 1993.
18.
go back to reference Collins FH, Paskewitz SM. A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Mol Biol. 1996;5:1–9.CrossRefPubMed Collins FH, Paskewitz SM. A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Mol Biol. 1996;5:1–9.CrossRefPubMed
19.
go back to reference Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294–9.PubMed Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294–9.PubMed
20.
go back to reference Ruiz F, Linton YM, Ponsonby DJ, Conn JE, Herrera M, Quiñones ML, et al. Molecular comparison of topotypic specimens confirms Anopheles (Nyssorhynchus) dunhami Causey (Diptera: Culicidae) in the Colombian Amazon. Mem Inst Oswaldo Cruz. 2010;105:899–903.PubMedPubMedCentral Ruiz F, Linton YM, Ponsonby DJ, Conn JE, Herrera M, Quiñones ML, et al. Molecular comparison of topotypic specimens confirms Anopheles (Nyssorhynchus) dunhami Causey (Diptera: Culicidae) in the Colombian Amazon. Mem Inst Oswaldo Cruz. 2010;105:899–903.PubMedPubMedCentral
21.
go back to reference Foley DH, Harrison G, Murphy JR, Dowler M, Rueda LM, Wilkerson RC. Mosquito bisection as a variable in estimates of PCR-derived malaria sporozoite rates. Malar J. 2012;11:145.CrossRefPubMedPubMedCentral Foley DH, Harrison G, Murphy JR, Dowler M, Rueda LM, Wilkerson RC. Mosquito bisection as a variable in estimates of PCR-derived malaria sporozoite rates. Malar J. 2012;11:145.CrossRefPubMedPubMedCentral
22.
go back to reference Beier JC, Asiago CM, Onyango FK, Koros JK. ELISA absorbance cut-off method affects malaria sporozoite rate determination in wild Afrotropical Anopheles. Med Vet Entomol. 1988;2:259–64.CrossRefPubMed Beier JC, Asiago CM, Onyango FK, Koros JK. ELISA absorbance cut-off method affects malaria sporozoite rate determination in wild Afrotropical Anopheles. Med Vet Entomol. 1988;2:259–64.CrossRefPubMed
23.
go back to reference Snounou GS, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;61:315–20.CrossRefPubMed Snounou GS, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;61:315–20.CrossRefPubMed
26.
go back to reference Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol. 1992;9:678–87.PubMed Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol. 1992;9:678–87.PubMed
27.
go back to reference Huelsenbeck JP, Ronquist F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–5.CrossRefPubMed Huelsenbeck JP, Ronquist F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–5.CrossRefPubMed
28.
go back to reference Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.CrossRefPubMed Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.CrossRefPubMed
29.
go back to reference Panday RS. Anopheles nuneztovari and malaria transmission in Surinam. Mosq News. 1977;37:728–37. Panday RS. Anopheles nuneztovari and malaria transmission in Surinam. Mosq News. 1977;37:728–37.
30.
go back to reference Brochero H, Rey G, Buitrago LS, Olano VA. Biting activity and breeding sites of Anopheles species in the municipality Villavicencio, Meta, Colombia. J Am Mosq Control. 2005;21:182–6.CrossRef Brochero H, Rey G, Buitrago LS, Olano VA. Biting activity and breeding sites of Anopheles species in the municipality Villavicencio, Meta, Colombia. J Am Mosq Control. 2005;21:182–6.CrossRef
31.
go back to reference Brochero H, Pareja PX, Ortiz G, Olano VA. Sitios de cría y actividad de picadura de especies de Anopheles en el municipio de Cimitarra, Santander, Colombia. Biomédica. 2006;26:269–77.CrossRefPubMed Brochero H, Pareja PX, Ortiz G, Olano VA. Sitios de cría y actividad de picadura de especies de Anopheles en el municipio de Cimitarra, Santander, Colombia. Biomédica. 2006;26:269–77.CrossRefPubMed
32.
go back to reference Harris AF, Matias-Arnez A, Hill N. Biting time of Anopheles darlingi in the Bolivian Amazon and implications for control of malaria. Trans R Soc Trop Med Hyg. 2006;100:45–7.CrossRefPubMed Harris AF, Matias-Arnez A, Hill N. Biting time of Anopheles darlingi in the Bolivian Amazon and implications for control of malaria. Trans R Soc Trop Med Hyg. 2006;100:45–7.CrossRefPubMed
33.
go back to reference Parra-Henao G, Alarcón EP. Observaciones sobre la bionomía de Anopheles spp. (Diptera: Culicidae) en el municipio Valencia, departamento Córdoba, Colombia. Bol Mal Salud Amb. 2008;48:95–8. Parra-Henao G, Alarcón EP. Observaciones sobre la bionomía de Anopheles spp. (Diptera: Culicidae) en el municipio Valencia, departamento Córdoba, Colombia. Bol Mal Salud Amb. 2008;48:95–8.
34.
go back to reference Gutiérrez LA, González JJ, Gómez GF, Castro MI, Rosero DA, Luckhart S, et al. Species composition and natural infectivity of anthropophilic Anopheles (Diptera: Culicidae) in the states of Cordoba and Antioquia, Northwestern Colombia. Mem Inst Oswaldo Cruz. 2009;104:1117–24.PubMedPubMedCentral Gutiérrez LA, González JJ, Gómez GF, Castro MI, Rosero DA, Luckhart S, et al. Species composition and natural infectivity of anthropophilic Anopheles (Diptera: Culicidae) in the states of Cordoba and Antioquia, Northwestern Colombia. Mem Inst Oswaldo Cruz. 2009;104:1117–24.PubMedPubMedCentral
35.
go back to reference Zimmerman RH, Lounibos LP, Nishimura N, Galardo AKR, Galardo CD, Arruda ME. Nightly biting cycles of malaria vectors in a heterogeneous transmission area of eastern Amazonian Brazil. Malar J. 2013;12:262.CrossRefPubMedPubMedCentral Zimmerman RH, Lounibos LP, Nishimura N, Galardo AKR, Galardo CD, Arruda ME. Nightly biting cycles of malaria vectors in a heterogeneous transmission area of eastern Amazonian Brazil. Malar J. 2013;12:262.CrossRefPubMedPubMedCentral
36.
go back to reference Schiemann DJ, Quiñones ML, Hankeln T. Anthropophilic Anopheles species composition and malaria in Tierradentro, Cordoba, Colombia. Mem Inst Oswaldo Cruz. 2014;109:384–7.CrossRefPubMedCentral Schiemann DJ, Quiñones ML, Hankeln T. Anthropophilic Anopheles species composition and malaria in Tierradentro, Cordoba, Colombia. Mem Inst Oswaldo Cruz. 2014;109:384–7.CrossRefPubMedCentral
37.
go back to reference Moreno M, Saavedra MP, Bickersmith SA, Lainhart W, Tong C, Alava F, et al. Implications for changes in Anopheles darlingi biting behaviour in three communities in the peri-Iquitos region of Amazonian Peru. Malar J. 2015;14:290.CrossRefPubMedPubMedCentral Moreno M, Saavedra MP, Bickersmith SA, Lainhart W, Tong C, Alava F, et al. Implications for changes in Anopheles darlingi biting behaviour in three communities in the peri-Iquitos region of Amazonian Peru. Malar J. 2015;14:290.CrossRefPubMedPubMedCentral
38.
go back to reference Ahumada ML, Pareja PX, Buitrago LS, Quiñones ML. Comportamiento de picadura de Anopheles darlingi Root, 1926 (Diptera: Culicidae) y su asociación con la transmisión de malaria en Villavicencio (Colombia). Biomédica. 2013;33:241–50.PubMed Ahumada ML, Pareja PX, Buitrago LS, Quiñones ML. Comportamiento de picadura de Anopheles darlingi Root, 1926 (Diptera: Culicidae) y su asociación con la transmisión de malaria en Villavicencio (Colombia). Biomédica. 2013;33:241–50.PubMed
39.
go back to reference Rubio-Palis. Anopheles (Nyssorhynchus) de Venezuela. Taxonomía, bionomía, ecología e importancia médica. Esc. Mal. San. Amb.“Dr. Arnoldo Gabaldon”, Maracay; 2000. Rubio-Palis. Anopheles (Nyssorhynchus) de Venezuela. Taxonomía, bionomía, ecología e importancia médica. Esc. Mal. San. Amb.“Dr. Arnoldo Gabaldon”, Maracay; 2000.
40.
go back to reference Silva-do-Nascimento TF, Rona LD, Peixoto AA, Lourenço-de-Oliveira R. Molecular divergence in the timeless and cpr genes among three sympatric cryptic species of the Anopheles triannulatus complex. Mem Inst Oswaldo Cruz. 2011;106(Suppl 1):218–22.CrossRefPubMed Silva-do-Nascimento TF, Rona LD, Peixoto AA, Lourenço-de-Oliveira R. Molecular divergence in the timeless and cpr genes among three sympatric cryptic species of the Anopheles triannulatus complex. Mem Inst Oswaldo Cruz. 2011;106(Suppl 1):218–22.CrossRefPubMed
41.
go back to reference Herrera-Varela M, Orjuela LI, Peñalver C, Conn JE, Quiñones ML. Anopheles species composition explains differences in Plasmodium transmission in La Guajira, northern Colombia. Mem Inst Oswaldo Cruz. 2014;109:955–9.CrossRefPubMed Herrera-Varela M, Orjuela LI, Peñalver C, Conn JE, Quiñones ML. Anopheles species composition explains differences in Plasmodium transmission in La Guajira, northern Colombia. Mem Inst Oswaldo Cruz. 2014;109:955–9.CrossRefPubMed
42.
go back to reference Gutiérrez LA, Orrego LM, Gómez GF, López A, Luckhart S, Conn JE, et al. A new mtDNA COI gene lineage near An. janconnae of the Albitarsis complex from Caribbean Colombia. Mem Inst Oswaldo Cruz. 2010;105:1019–25.CrossRefPubMedPubMedCentral Gutiérrez LA, Orrego LM, Gómez GF, López A, Luckhart S, Conn JE, et al. A new mtDNA COI gene lineage near An. janconnae of the Albitarsis complex from Caribbean Colombia. Mem Inst Oswaldo Cruz. 2010;105:1019–25.CrossRefPubMedPubMedCentral
43.
go back to reference Naranjo-Díaz N, Rosero DA, Rúa-Uribe G, Luckhart S, Correa MM. Abundance, behavior and entomological inoculation rates of anthropophilic anophelines from a primary Colombian malaria endemic area. Parasit Vectors. 2013;6:61.CrossRefPubMedPubMedCentral Naranjo-Díaz N, Rosero DA, Rúa-Uribe G, Luckhart S, Correa MM. Abundance, behavior and entomological inoculation rates of anthropophilic anophelines from a primary Colombian malaria endemic area. Parasit Vectors. 2013;6:61.CrossRefPubMedPubMedCentral
44.
go back to reference Naranjo-Díaz N, Altamiranda M, Luckhart S, Conn JE, Correa MM. Malaria vectors in ecologically heterogeneous localities of the Colombian Pacific region. PLoS One. 2014;9:e103769.CrossRefPubMedPubMedCentral Naranjo-Díaz N, Altamiranda M, Luckhart S, Conn JE, Correa MM. Malaria vectors in ecologically heterogeneous localities of the Colombian Pacific region. PLoS One. 2014;9:e103769.CrossRefPubMedPubMedCentral
45.
go back to reference González-Cerón M, Rodríguez MH, Nettel JC, Villarreal C, Kain KC, Hernández JE. Differential susceptibilities of Anopheles albimanus and Anopheles pseudopunctipennis to infections with coindigenous Plasmodium vivax variants VK210 and VK247 in Southern Mexico. Infect Immun. 1999;67:410–2.PubMedPubMedCentral González-Cerón M, Rodríguez MH, Nettel JC, Villarreal C, Kain KC, Hernández JE. Differential susceptibilities of Anopheles albimanus and Anopheles pseudopunctipennis to infections with coindigenous Plasmodium vivax variants VK210 and VK247 in Southern Mexico. Infect Immun. 1999;67:410–2.PubMedPubMedCentral
46.
go back to reference Fleming G. Biology and ecology of malaria vectors in the Americas. Washington: Pan American Health Organization; 1986. PNSP/86–72. Fleming G. Biology and ecology of malaria vectors in the Americas. Washington: Pan American Health Organization; 1986. PNSP/86–72.
47.
go back to reference Moreno JE, Rubio-Palis Y, Páez E, Pérez A, Sánchez V, Vaccari E. Anopheles (Anopheles) neomaculipalpus: a new malaria vector in the Amazon basin? Med Vet Entomol. 2005;19:329–32.CrossRefPubMed Moreno JE, Rubio-Palis Y, Páez E, Pérez A, Sánchez V, Vaccari E. Anopheles (Anopheles) neomaculipalpus: a new malaria vector in the Amazon basin? Med Vet Entomol. 2005;19:329–32.CrossRefPubMed
48.
go back to reference Astaiza R, Murillo C, Fajardo P. Biología de Anopheles (Kerteszia) neivai H., D. & K., 1913 (Diptera: Culicidae) en la costa Pacífica de Colombia II. Fluctuación de la población adulta. Rev Saúde Pública. 1988;22:101–8.CrossRefPubMed Astaiza R, Murillo C, Fajardo P. Biología de Anopheles (Kerteszia) neivai H., D. & K., 1913 (Diptera: Culicidae) en la costa Pacífica de Colombia II. Fluctuación de la población adulta. Rev Saúde Pública. 1988;22:101–8.CrossRefPubMed
49.
go back to reference Solarte Y, Hurtado C, Gonzalez R, Alexander B. Man-biting activity of Anopheles (Nyssorhynchus) albimanus and An. (Kerteszia) neivai (Diptera: Culicidae) in the Pacific lowlands of Colombia. Mem Inst Oswaldo Cruz. 1996;91:141–6.CrossRefPubMed Solarte Y, Hurtado C, Gonzalez R, Alexander B. Man-biting activity of Anopheles (Nyssorhynchus) albimanus and An. (Kerteszia) neivai (Diptera: Culicidae) in the Pacific lowlands of Colombia. Mem Inst Oswaldo Cruz. 1996;91:141–6.CrossRefPubMed
50.
go back to reference Murillo C, Astaiza R, Fajardo P. Biología de Anopheles (Kerteszia) neivai H., D. & K., 1913 (Diptera: Culicidae) en la Costa Pacífica de Colombia. I. Fluctuación de la población larval y características de sus criaderos. Rev Saúde Pública. 1988;22:94–100.CrossRefPubMed Murillo C, Astaiza R, Fajardo P. Biología de Anopheles (Kerteszia) neivai H., D. & K., 1913 (Diptera: Culicidae) en la Costa Pacífica de Colombia. I. Fluctuación de la población larval y características de sus criaderos. Rev Saúde Pública. 1988;22:94–100.CrossRefPubMed
51.
go back to reference Marrelli MT, Malafronte RS, Sallum MAM, Natal D. Kerteszia subgenus of Anopheles associated with the Brazilian Atlantic rainforest: current knowledge and future challenges. Malar J. 2007;6:127.CrossRefPubMedPubMedCentral Marrelli MT, Malafronte RS, Sallum MAM, Natal D. Kerteszia subgenus of Anopheles associated with the Brazilian Atlantic rainforest: current knowledge and future challenges. Malar J. 2007;6:127.CrossRefPubMedPubMedCentral
52.
go back to reference Gutiérrez LA, Naranjo N, Jaramillo LM, Muskus C, Luckhart S, Conn JE, et al. Natural infectivity of Anopheles species from the Pacific and Atlantic regions of Colombia. Acta Trop. 2008;107:99–105.CrossRefPubMed Gutiérrez LA, Naranjo N, Jaramillo LM, Muskus C, Luckhart S, Conn JE, et al. Natural infectivity of Anopheles species from the Pacific and Atlantic regions of Colombia. Acta Trop. 2008;107:99–105.CrossRefPubMed
53.
go back to reference Escovar JE, González R, Quiñones ML. Anthropophilic biting behaviour of Anopheles (Kerteszia) neivai Howard, Dyar & Knab associated with Fishermen’s activities in a malaria-endemic area in the Colombian Pacific. Mem Inst Oswaldo Cruz. 2013;108:1057–64.CrossRefPubMedPubMedCentral Escovar JE, González R, Quiñones ML. Anthropophilic biting behaviour of Anopheles (Kerteszia) neivai Howard, Dyar & Knab associated with Fishermen’s activities in a malaria-endemic area in the Colombian Pacific. Mem Inst Oswaldo Cruz. 2013;108:1057–64.CrossRefPubMedPubMedCentral
54.
go back to reference Fajardo P, Alzate A. Anopheles nuneztovari como vector de malaria en el Bajo Calima, Buenaventura. Colombia Médica. 1987;18:14–8. Fajardo P, Alzate A. Anopheles nuneztovari como vector de malaria en el Bajo Calima, Buenaventura. Colombia Médica. 1987;18:14–8.
55.
go back to reference Quiñones ML, Suarez MF, Fleming G. Distribución y bionomía de los anofelinos de la costa pacífica de Colombia. Colombia Médica. 1987;18:19–24. Quiñones ML, Suarez MF, Fleming G. Distribución y bionomía de los anofelinos de la costa pacífica de Colombia. Colombia Médica. 1987;18:19–24.
56.
go back to reference Narang SK, Seawright JA, Suarez MF. Genetic structure of natural populations of Anopheles albimanus in Colombia. J Am Mosquito Control Assoc. 1991;7:437–45. Narang SK, Seawright JA, Suarez MF. Genetic structure of natural populations of Anopheles albimanus in Colombia. J Am Mosquito Control Assoc. 1991;7:437–45.
57.
go back to reference Gutiérrez LA, Naranjo NJ, Cienfuegos AV, Muskus CE, Luckhart S, Conn JE, et al. Population structure analyses and demographic history of the malaria vector Anopheles albimanus from the Caribbean and the Pacific regions of Colombia. Malar J. 2009;8:259.CrossRefPubMedPubMedCentral Gutiérrez LA, Naranjo NJ, Cienfuegos AV, Muskus CE, Luckhart S, Conn JE, et al. Population structure analyses and demographic history of the malaria vector Anopheles albimanus from the Caribbean and the Pacific regions of Colombia. Malar J. 2009;8:259.CrossRefPubMedPubMedCentral
58.
go back to reference Estrada-Franco JG, Lanzaro GC, Ma MC, Walker-Abbey A, Romans P, Galvan-Sanchez C, et al. Characterization of Anopheles pseudopunctipennis sensu lato from three countries of neotropical America from variation in allozymes and ribosomal DNA. Am J Trop Med Hyg. 1993;49:735–45.PubMed Estrada-Franco JG, Lanzaro GC, Ma MC, Walker-Abbey A, Romans P, Galvan-Sanchez C, et al. Characterization of Anopheles pseudopunctipennis sensu lato from three countries of neotropical America from variation in allozymes and ribosomal DNA. Am J Trop Med Hyg. 1993;49:735–45.PubMed
59.
go back to reference Coetzee M, Estrada-Franco JG, Wunderlich CA, Hunt RH. Cytogenetic evidence for a species complex within Anopheles pseudopunctipennis theobald (Diptera: Culicidae). Am J Trop Med Hyg. 1999;60:649–53.PubMed Coetzee M, Estrada-Franco JG, Wunderlich CA, Hunt RH. Cytogenetic evidence for a species complex within Anopheles pseudopunctipennis theobald (Diptera: Culicidae). Am J Trop Med Hyg. 1999;60:649–53.PubMed
60.
go back to reference Manguin S, Robert DR, Peyton EL, Fernandez-Salas I, Barreto M, Fernandez R, et al. Biochemical systematics and population genetic structure of Anopheles pseudopunctipennis, vector of malaria in Central and South America. Am J Trop Med Hyg. 1995;53:362–77.PubMed Manguin S, Robert DR, Peyton EL, Fernandez-Salas I, Barreto M, Fernandez R, et al. Biochemical systematics and population genetic structure of Anopheles pseudopunctipennis, vector of malaria in Central and South America. Am J Trop Med Hyg. 1995;53:362–77.PubMed
61.
go back to reference Gomez GF, Bickersmith SA, Gonzalez R, Conn JE, Correa MM. Molecular taxonomy provides new insights into Anopheles species of the neotropical Arribalzagia series. PLoS One. 2015;10:e0119488.CrossRefPubMedPubMedCentral Gomez GF, Bickersmith SA, Gonzalez R, Conn JE, Correa MM. Molecular taxonomy provides new insights into Anopheles species of the neotropical Arribalzagia series. PLoS One. 2015;10:e0119488.CrossRefPubMedPubMedCentral
Metadata
Title
Spatial distributions of Anopheles species in relation to malaria incidence at 70 localities in the highly endemic Northwest and South Pacific coast regions of Colombia
Authors
Martha L. Ahumada
Lorena I. Orjuela
Paula X. Pareja
Marcela Conde
Diana M. Cabarcas
Eliana F. G. Cubillos
Jorge A. Lopez
John C. Beier
Sócrates Herrera
Martha L. Quiñones
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1421-4

Other articles of this Issue 1/2016

Malaria Journal 1/2016 Go to the issue