Skip to main content
Top
Published in: Malaria Journal 1/2011

Open Access 01-12-2011 | Research

New highland distribution records of multiple Anopheles species in the Ecuadorian Andes

Authors: Lauren L Pinault, Fiona F Hunter

Published in: Malaria Journal | Issue 1/2011

Login to get access

Abstract

Background

Several recent climate change reviews have stressed the possibility of some malaria vectors occupying regions of higher altitudes than previously recorded. Indeed, highland malaria has been observed in several African nations, possibly attributable to changes in land use, vector control and local climate. This study attempts to expand the current knowledge of the distribution of common Anopheles species in Ecuador, with particular attention to highland regions (> 500 m) of the Andes.

Methods

Extensive field collections of larvae were undertaken in 2008, 2009 and 2010 throughout all regions of Ecuador (except the lower-altitude Amazonian plain) and compared to historical distribution maps reproduced from the 1940s. Larvae were identified using both a morphological key and sequencing of the 800 bp region of the CO1 mitochondrial gene. In addition, spatial statistics (Getis-Ord Hotspot Analysis: Gi*) were used to determine high and low-density clusters of each species in Ecuador.

Results

Distributions have been updated for five species of Anopheles in Ecuador: Anopheles albimanus, Anopheles pseudopunctipennis, Anopheles punctimacula, Anopheles eiseni and Anopheles oswaldoi s.l.. Historical maps indicate that An. pseudopunctipennis used to be widespread in highland Andean valleys, while other species were completely restricted to lowland areas. By comparison, updated maps for the other four collected species show higher maximum elevations and/or more widespread distributions in highland regions than previously recorded. Gi* analysis determined some highland hot spots for An. albimanus, but only cold spots for all other species.

Conclusions

This study documents the establishment of multiple anopheline species in high altitude regions of Ecuador, often in areas where malaria eradication programs are not focused.
Appendix
Available only for authorised users
Literature
1.
go back to reference Patz JA, Campbell-Lendrum D, Holloway T, Foley JA: Impact of regional climate change on human health. Nature. 2005, 438: 310-317. 10.1038/nature04188.CrossRefPubMed Patz JA, Campbell-Lendrum D, Holloway T, Foley JA: Impact of regional climate change on human health. Nature. 2005, 438: 310-317. 10.1038/nature04188.CrossRefPubMed
2.
go back to reference Minakawa N, Omukunda E, Zhou G, Githeko A, Yan G: Malaria vector productivity in relation to the highland environment in Kenya. Am J Trop Med Hyg. 2006, 75: 448-453.PubMed Minakawa N, Omukunda E, Zhou G, Githeko A, Yan G: Malaria vector productivity in relation to the highland environment in Kenya. Am J Trop Med Hyg. 2006, 75: 448-453.PubMed
3.
go back to reference Mouchet J, Manguin S, Sircoulon J, Laventure S, Faye O, Onapa AW, Carnevale P, Julvez J, Fonteneille D: Evolution of malaria in Africa for the past 40 years: Impact of climatic and human factors. J Am Mosquito Contr. 1998, 14: 121-130. Mouchet J, Manguin S, Sircoulon J, Laventure S, Faye O, Onapa AW, Carnevale P, Julvez J, Fonteneille D: Evolution of malaria in Africa for the past 40 years: Impact of climatic and human factors. J Am Mosquito Contr. 1998, 14: 121-130.
4.
go back to reference Reiter P: Climate change and mosquito-borne disease. Environ Health Persp. 2001, 109: 141-161.CrossRef Reiter P: Climate change and mosquito-borne disease. Environ Health Persp. 2001, 109: 141-161.CrossRef
5.
go back to reference Zell R: Global climate change and the emergence/re-emergence of infectious diseases. Int J Med Microbiol. 2004, 293: 16-26.PubMed Zell R: Global climate change and the emergence/re-emergence of infectious diseases. Int J Med Microbiol. 2004, 293: 16-26.PubMed
6.
go back to reference Lindsay SW, Martens WJ: Malaria in the African highlands: past, present and future. Bull World Health Organ. 1998, 76: 33-45.PubMedCentralPubMed Lindsay SW, Martens WJ: Malaria in the African highlands: past, present and future. Bull World Health Organ. 1998, 76: 33-45.PubMedCentralPubMed
7.
go back to reference Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G: Effects of microclimatic changes caused by deforestation on the survivorship and reproductive fitness of Anopheles gambiae in Western Kenya highlands. Am J Trop Med Hyg. 2006, 74: 772-778.PubMed Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G: Effects of microclimatic changes caused by deforestation on the survivorship and reproductive fitness of Anopheles gambiae in Western Kenya highlands. Am J Trop Med Hyg. 2006, 74: 772-778.PubMed
8.
go back to reference Moreno AR: Climate change and human health in Latin America: drivers, effects, and policies. Reg Environ Change. 2006, 6: 157-164. 10.1007/s10113-006-0015-z.CrossRef Moreno AR: Climate change and human health in Latin America: drivers, effects, and policies. Reg Environ Change. 2006, 6: 157-164. 10.1007/s10113-006-0015-z.CrossRef
9.
go back to reference Shope R: Global climate change and infectious diseases. Environ Health Persp. 1991, 96: 171-174.CrossRef Shope R: Global climate change and infectious diseases. Environ Health Persp. 1991, 96: 171-174.CrossRef
10.
go back to reference Epstein PR, Diaz HF, Elias S, Grabherr G, Graham NE, Martens WJM, Mosley-Thompson E, Susskind J: Biological and physical signs of climate change: Focus on mosquito-borne diseases. Bull Am Meteorol Soc. 1998, 79: 409-417. 10.1175/1520-0477(1998)079<0409:BAPSOC>2.0.CO;2.CrossRef Epstein PR, Diaz HF, Elias S, Grabherr G, Graham NE, Martens WJM, Mosley-Thompson E, Susskind J: Biological and physical signs of climate change: Focus on mosquito-borne diseases. Bull Am Meteorol Soc. 1998, 79: 409-417. 10.1175/1520-0477(1998)079<0409:BAPSOC>2.0.CO;2.CrossRef
11.
go back to reference Martens WJ, Niessen LW, Rotmans J, Jetten TH, McMichael AJ: Potential impact of global climate change on malaria risk. Environ Health Persp. 1995, 103: 458-464. 10.1289/ehp.95103458.CrossRef Martens WJ, Niessen LW, Rotmans J, Jetten TH, McMichael AJ: Potential impact of global climate change on malaria risk. Environ Health Persp. 1995, 103: 458-464. 10.1289/ehp.95103458.CrossRef
12.
go back to reference Rutar T, Baldomar-Salgueiro EJ, Maguire JH: Introduced Plasmodium vivax malaria in a Bolivian community at an elevation of 2,300 meters. Am J Trop Med Hyg. 2004, 70: 15-19.PubMed Rutar T, Baldomar-Salgueiro EJ, Maguire JH: Introduced Plasmodium vivax malaria in a Bolivian community at an elevation of 2,300 meters. Am J Trop Med Hyg. 2004, 70: 15-19.PubMed
13.
go back to reference Lindblade KA, Walker ED, Onapa AW, Katungu J, Wilson ML: Highland malaria in Uganda: prospective analysis of an epidemic associated with El Niño. Trans R Soc Trop Med Hyg. 1999, 93: 480-487. 10.1016/S0035-9203(99)90344-9.CrossRefPubMed Lindblade KA, Walker ED, Onapa AW, Katungu J, Wilson ML: Highland malaria in Uganda: prospective analysis of an epidemic associated with El Niño. Trans R Soc Trop Med Hyg. 1999, 93: 480-487. 10.1016/S0035-9203(99)90344-9.CrossRefPubMed
14.
go back to reference Loevinsohn ME: Climatic warming and increased malaria incidence in Rwanda. Lancet. 1994, 343: 714-718. 10.1016/S0140-6736(94)91586-5.CrossRefPubMed Loevinsohn ME: Climatic warming and increased malaria incidence in Rwanda. Lancet. 1994, 343: 714-718. 10.1016/S0140-6736(94)91586-5.CrossRefPubMed
15.
go back to reference Hay SI, Rogers DJ, Randolph SE, Stern SI, Cox J, Shanks D, Snow RW: Hot topic or hot air? Climate change and malaria resurgence in East African highlands. Trends Parasitol. 2002, 18: 530-534. 10.1016/S1471-4922(02)02374-7.PubMedCentralCrossRefPubMed Hay SI, Rogers DJ, Randolph SE, Stern SI, Cox J, Shanks D, Snow RW: Hot topic or hot air? Climate change and malaria resurgence in East African highlands. Trends Parasitol. 2002, 18: 530-534. 10.1016/S1471-4922(02)02374-7.PubMedCentralCrossRefPubMed
16.
go back to reference Levi-Castillo R: Los anophelinos de la Republica del Ecuador. Tomo Primero. 1945, Guayaquil, Artes Graficas Senliebeder C.A. Ltda Levi-Castillo R: Los anophelinos de la Republica del Ecuador. Tomo Primero. 1945, Guayaquil, Artes Graficas Senliebeder C.A. Ltda
17.
go back to reference Gorham JR, Stojanovich CJ, Scott HG: Illustrated key to the anopheline mosquitoes of western South America. Mosq Syst. 1973, 5: 97-155. Gorham JR, Stojanovich CJ, Scott HG: Illustrated key to the anopheline mosquitoes of western South America. Mosq Syst. 1973, 5: 97-155.
18.
go back to reference Rubio-Palis Y, Zimmerman RH: Ecoregional classification of malaria vectors in the neotropics. J Med Entomol. 1997, 34: 499-510.CrossRefPubMed Rubio-Palis Y, Zimmerman RH: Ecoregional classification of malaria vectors in the neotropics. J Med Entomol. 1997, 34: 499-510.CrossRefPubMed
19.
go back to reference Lounibos LP, Conn JE: Malaria vector heterogeneity in South America. Am Entomol. 2000, 46: 238-249.CrossRef Lounibos LP, Conn JE: Malaria vector heterogeneity in South America. Am Entomol. 2000, 46: 238-249.CrossRef
20.
go back to reference Marrelli MT, Floeter-Winter LM, Malafronte RS, Tadei WP, Lourenço-de-oliveira R, Flores-Mendoza C, Marinotti O: Amazonian malaria vector anopheline relationships interpreted from ITS2 rDNA sequences. Med Vet Entomol. 2005, 19: 208-218. 10.1111/j.0269-283X.2005.00558.x.CrossRefPubMed Marrelli MT, Floeter-Winter LM, Malafronte RS, Tadei WP, Lourenço-de-oliveira R, Flores-Mendoza C, Marinotti O: Amazonian malaria vector anopheline relationships interpreted from ITS2 rDNA sequences. Med Vet Entomol. 2005, 19: 208-218. 10.1111/j.0269-283X.2005.00558.x.CrossRefPubMed
21.
go back to reference Montalvan JA: Paludismo en Ecuador. 1948, Guayaquil, Dirección General de Sanidad, Instituto Nacional de Higiene "Leopoldo Izquieta Perez" Montalvan JA: Paludismo en Ecuador. 1948, Guayaquil, Dirección General de Sanidad, Instituto Nacional de Higiene "Leopoldo Izquieta Perez"
22.
go back to reference Rejmankova E, Roberts DR, Harbach RE, Pecor J, Peyton EL, Manguin S, Krieg R, Polanco J, Legters L: Environmental and regional determinants of Anopheles (Diptera: Culicidae) larval distribution in Belize, Central America. Environ Entomol. 1993, 22: 978-992.CrossRef Rejmankova E, Roberts DR, Harbach RE, Pecor J, Peyton EL, Manguin S, Krieg R, Polanco J, Legters L: Environmental and regional determinants of Anopheles (Diptera: Culicidae) larval distribution in Belize, Central America. Environ Entomol. 1993, 22: 978-992.CrossRef
23.
go back to reference Rodriguez AD, Rodriguez MH, Meza RA, Hernandez JE, Rejmankova E, Savage HM, Roberts DR, Pope KO, Legters L: Dynamics of population densities and vegetation associations of Anopheles albimanus larvae in a coastal area of southern Chiapas, Mexico. J Am Mosquito Contr. 1993, 9: 46-57. Rodriguez AD, Rodriguez MH, Meza RA, Hernandez JE, Rejmankova E, Savage HM, Roberts DR, Pope KO, Legters L: Dynamics of population densities and vegetation associations of Anopheles albimanus larvae in a coastal area of southern Chiapas, Mexico. J Am Mosquito Contr. 1993, 9: 46-57.
24.
go back to reference Rodriguez MH, Gonzalez-Ceron L, Hernandez JE, Nettel JA, Villarreal C, Kain KC, Wirtz RA: Different prevalences of Plasmodium vivax phenotypes VK210 and VK247 associated with the distribution of Anopheles albimanus and Anopheles pseudopunctipennis in Mexico. Am J Trop Med Hyg. 2000, 62: 122-127.PubMed Rodriguez MH, Gonzalez-Ceron L, Hernandez JE, Nettel JA, Villarreal C, Kain KC, Wirtz RA: Different prevalences of Plasmodium vivax phenotypes VK210 and VK247 associated with the distribution of Anopheles albimanus and Anopheles pseudopunctipennis in Mexico. Am J Trop Med Hyg. 2000, 62: 122-127.PubMed
25.
go back to reference Quiñones MLP, Suárez MFA, Fleming GA: Distribución y bionomía de los anofelinos de la Costa Pacífica de Colombia. Colomb Médica. 1987, 18: 19-24. Quiñones MLP, Suárez MFA, Fleming GA: Distribución y bionomía de los anofelinos de la Costa Pacífica de Colombia. Colomb Médica. 1987, 18: 19-24.
26.
go back to reference Narang SK, Seawright JA, Suarez MF: Genetic structure of natural populations of Anopheles albimanus in Colombia. J Am Mosquito Contr. 1991, 7: 437-445. Narang SK, Seawright JA, Suarez MF: Genetic structure of natural populations of Anopheles albimanus in Colombia. J Am Mosquito Contr. 1991, 7: 437-445.
27.
go back to reference Marten GG, Suárez MF, Astaeza R: An ecological survey of Anopheles albimanus larval habitats in Colombia. J Vector Ecol. 1996, 21: 122-131. Marten GG, Suárez MF, Astaeza R: An ecological survey of Anopheles albimanus larval habitats in Colombia. J Vector Ecol. 1996, 21: 122-131.
28.
go back to reference Poveda G, Rojas W, Quiñones ML, Vélez ID, Mantilla RI, Ruiz D, Zuluaga JS, Rua GL: Coupling between annual and ENSO timescales in the malaria - climate association in Colombia. Environ Health Persp. 2001, 109: 489-493. Poveda G, Rojas W, Quiñones ML, Vélez ID, Mantilla RI, Ruiz D, Zuluaga JS, Rua GL: Coupling between annual and ENSO timescales in the malaria - climate association in Colombia. Environ Health Persp. 2001, 109: 489-493.
29.
go back to reference Gutiérrez LA, Naranjo NJ, Cienfuegos AV, Muskus CE, Luckhart S, Conn JE, Correa MM: 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: 259-10.1186/1475-2875-8-259.PubMedCentralCrossRefPubMed Gutiérrez LA, Naranjo NJ, Cienfuegos AV, Muskus CE, Luckhart S, Conn JE, Correa MM: 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: 259-10.1186/1475-2875-8-259.PubMedCentralCrossRefPubMed
30.
go back to reference Morales-Ayala F: A list of the mosquitoes of Peru (Diptera, Culicidae). Mosq Syst. 1971, 3: 138-145. Morales-Ayala F: A list of the mosquitoes of Peru (Diptera, Culicidae). Mosq Syst. 1971, 3: 138-145.
31.
go back to reference Guthmann JP, Llanos-Cuentas A, Palacios A, Hall AJ: Environmental factors as determinants of malaria risk: A descriptive study on the northern coast of Peru. Trop Med Int Health. 2002, 7: 518-525. 10.1046/j.1365-3156.2002.00883.x.CrossRefPubMed Guthmann JP, Llanos-Cuentas A, Palacios A, Hall AJ: Environmental factors as determinants of malaria risk: A descriptive study on the northern coast of Peru. Trop Med Int Health. 2002, 7: 518-525. 10.1046/j.1365-3156.2002.00883.x.CrossRefPubMed
32.
go back to reference King WV: On the distribution of Anopheles albimanus and its occurrence in the United States. Southern Med J. 1937, 30: 943-946. 10.1097/00007611-193709000-00020.CrossRef King WV: On the distribution of Anopheles albimanus and its occurrence in the United States. Southern Med J. 1937, 30: 943-946. 10.1097/00007611-193709000-00020.CrossRef
33.
go back to reference Kumm HW, Komp WHW, Ruiz H: The mosquitoes of Costa Rica. Am J Trop Med Hyg. 1940, S1-20: 385-422. Kumm HW, Komp WHW, Ruiz H: The mosquitoes of Costa Rica. Am J Trop Med Hyg. 1940, S1-20: 385-422.
34.
go back to reference Vargas L, Casis GS, Earle WC: Anopheles pseudopunctipennis, Theobald, a vector of malaria in Mexico. Am J Trop Med Hyg. 1941, S1-21: 779-788. Vargas L, Casis GS, Earle WC: Anopheles pseudopunctipennis, Theobald, a vector of malaria in Mexico. Am J Trop Med Hyg. 1941, S1-21: 779-788.
35.
go back to reference Kumm HW, Zúniga H: The mosquitoes of El Salvador. Am J Trop Med Hyg. 1942, S1-22: 399-415. Kumm HW, Zúniga H: The mosquitoes of El Salvador. Am J Trop Med Hyg. 1942, S1-22: 399-415.
36.
go back to reference Meyer SL: Plants of importance in the breeding of Anopheles albimanus Wied. in Panama. B Torrey Bot Club. 1947, 74: 257-261. 10.2307/2482036.CrossRef Meyer SL: Plants of importance in the breeding of Anopheles albimanus Wied. in Panama. B Torrey Bot Club. 1947, 74: 257-261. 10.2307/2482036.CrossRef
37.
go back to reference Rozeboom LE: Distribution and ecology of the Anopheles mosquitoes of the Caribbean region. Am Assoc Adv Sci. 1941, 15: 98-107. Rozeboom LE: Distribution and ecology of the Anopheles mosquitoes of the Caribbean region. Am Assoc Adv Sci. 1941, 15: 98-107.
38.
go back to reference Loaiza JR, Scott ME, Bermingham E, Sanjur OI, Wilkerson R, Rovira J, Gutiérrez LA, Correa MM, Grijalva MJ, Birnberg L, Bickersmith S, Conn JE: Late Pleistocene environmental changes lead to unstable demography and population divergence of Anopheles albimanus in the northern Neotropics. Mol Phylogenet Evol. 2010, 57: 1341-1346. 10.1016/j.ympev.2010.09.016.PubMedCentralCrossRefPubMed Loaiza JR, Scott ME, Bermingham E, Sanjur OI, Wilkerson R, Rovira J, Gutiérrez LA, Correa MM, Grijalva MJ, Birnberg L, Bickersmith S, Conn JE: Late Pleistocene environmental changes lead to unstable demography and population divergence of Anopheles albimanus in the northern Neotropics. Mol Phylogenet Evol. 2010, 57: 1341-1346. 10.1016/j.ympev.2010.09.016.PubMedCentralCrossRefPubMed
39.
go back to reference Loaiza JR, Scott ME, Bermingham E, Rovira J, Conn JE: Evidence for Pleistocene population divergence and expansion of Anopheles albimanus in Southern Central America. Am J Trop Med Hyg. 2010, 82: 156-164. 10.4269/ajtmh.2010.09-0423.PubMedCentralCrossRefPubMed Loaiza JR, Scott ME, Bermingham E, Rovira J, Conn JE: Evidence for Pleistocene population divergence and expansion of Anopheles albimanus in Southern Central America. Am J Trop Med Hyg. 2010, 82: 156-164. 10.4269/ajtmh.2010.09-0423.PubMedCentralCrossRefPubMed
40.
go back to reference Levi-Castillo R: El complejo "pseudopunctipennis" en el Ecuador (Diptera - Culicidae). 1944, Guayaquil, Universidad de Guayaquil Imprenta Levi-Castillo R: El complejo "pseudopunctipennis" en el Ecuador (Diptera - Culicidae). 1944, Guayaquil, Universidad de Guayaquil Imprenta
41.
go back to reference Levi-Castillo R: Anopheles pseudopunctipennis in the Los Chillos valley of Ecuador. J Econ Entomol. 1945, 38: 385-388.CrossRef Levi-Castillo R: Anopheles pseudopunctipennis in the Los Chillos valley of Ecuador. J Econ Entomol. 1945, 38: 385-388.CrossRef
42.
go back to reference Lardeux F, Loayza P, Bouchité B, Chavez T: Host choice and human blood index of Anopheles pseudopunctipennis in a village of the Andean valleys of Bolivia. Malaria J. 2007, 6: 8-10.1186/1475-2875-6-8.CrossRef Lardeux F, Loayza P, Bouchité B, Chavez T: Host choice and human blood index of Anopheles pseudopunctipennis in a village of the Andean valleys of Bolivia. Malaria J. 2007, 6: 8-10.1186/1475-2875-6-8.CrossRef
43.
go back to reference Rueda LM, Peyton EL, Manguin S: Anopheles (Anopheles) pseudopunctipennis Theobald (Diptera: Culicidae): Neotype designation and description. J Med Entomol. 2004, 41: 12-22. 10.1603/0022-2585-41.1.12.CrossRefPubMed Rueda LM, Peyton EL, Manguin S: Anopheles (Anopheles) pseudopunctipennis Theobald (Diptera: Culicidae): Neotype designation and description. J Med Entomol. 2004, 41: 12-22. 10.1603/0022-2585-41.1.12.CrossRefPubMed
44.
go back to reference Loaiza JR, Bermingham E, Scott ME, Rovira JR, Conn JE: Species composition and distribution of adult Anopheles (Diptera: Culicidae) in Panama. J Med Entomol. 2008, 45: 841-851. 10.1603/0022-2585(2008)45[841:SCADOA]2.0.CO;2.PubMedCentralCrossRefPubMed Loaiza JR, Bermingham E, Scott ME, Rovira JR, Conn JE: Species composition and distribution of adult Anopheles (Diptera: Culicidae) in Panama. J Med Entomol. 2008, 45: 841-851. 10.1603/0022-2585(2008)45[841:SCADOA]2.0.CO;2.PubMedCentralCrossRefPubMed
45.
go back to reference Estrada-Franco JG, Lanzaro GC, Ma MC, Walker-Abbey A, Romans P, Galvan-Sanchez C, Cespedes JL, Vargas-Sagarnaga R, Laughinghouse A, Columbus I, Gwadz RW: 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: 735-745.PubMed Estrada-Franco JG, Lanzaro GC, Ma MC, Walker-Abbey A, Romans P, Galvan-Sanchez C, Cespedes JL, Vargas-Sagarnaga R, Laughinghouse A, Columbus I, Gwadz RW: 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: 735-745.PubMed
46.
go back to reference Manguin S, Roberts DR, Peyton EL, Fernandez-Salas I, Barreto M, Loayza RF, Elgueta Spinola R, Martinez Granaou R, Rodriguez MH: Biochemical systematics and population genetic structure of Anopheles pseudopunctipennis, vector of malaria in Central and South America. Am J Trop Med Hyg. 1995, 53: 362-377.PubMed Manguin S, Roberts DR, Peyton EL, Fernandez-Salas I, Barreto M, Loayza RF, Elgueta Spinola R, Martinez Granaou R, Rodriguez MH: Biochemical systematics and population genetic structure of Anopheles pseudopunctipennis, vector of malaria in Central and South America. Am J Trop Med Hyg. 1995, 53: 362-377.PubMed
47.
go back to reference Lardeux F, Chávez T, Rodríguez R, Torrez L: Anopheles of Bolivia: new records with an updated and annotated checklist. CR Biol. 2009, 332: 489-499. 10.1016/j.crvi.2008.11.001.CrossRef Lardeux F, Chávez T, Rodríguez R, Torrez L: Anopheles of Bolivia: new records with an updated and annotated checklist. CR Biol. 2009, 332: 489-499. 10.1016/j.crvi.2008.11.001.CrossRef
48.
go back to reference Villalobos EC, Valderrama Delgado A: El Anopheles punctimacula en el Peru. 1944, Lima, Publicaciones de la dirección general de salubridad, Servicio Nacional Antimalarico Villalobos EC, Valderrama Delgado A: El Anopheles punctimacula en el Peru. 1944, Lima, Publicaciones de la dirección general de salubridad, Servicio Nacional Antimalarico
49.
go back to reference Kumm HW, Novis O: Mosquito studies on the Ilha de Marajó, Pará, Brazil. Am J Epidemiol. 1938, 27: 498-515. Kumm HW, Novis O: Mosquito studies on the Ilha de Marajó, Pará, Brazil. Am J Epidemiol. 1938, 27: 498-515.
50.
go back to reference Wilkerson RC, Strickman D, Litwak TR: Illustrated key to the female anopheline mosquitoes of Central America and Mexico. J Am Mosquito Contr. 1990, 6: 7-34. Wilkerson RC, Strickman D, Litwak TR: Illustrated key to the female anopheline mosquitoes of Central America and Mexico. J Am Mosquito Contr. 1990, 6: 7-34.
51.
go back to reference Schoeler GB, Flores-Mendoza C, Fernández R, Davila JR, Zyzak M: Geographical distribution of Anopheles darlingi in the Amazon basin region of Peru. J Am Mosquito Contr. 2003, 19: 286-296. Schoeler GB, Flores-Mendoza C, Fernández R, Davila JR, Zyzak M: Geographical distribution of Anopheles darlingi in the Amazon basin region of Peru. J Am Mosquito Contr. 2003, 19: 286-296.
52.
go back to reference de Barros FSM, de Aguiar DB, Rosa-Freitas MG, Luitgards-Moura JF, daCosta Gurgel H, Alvez Honório N, de Arruda ME, Tsouris P, Vasconcelos SD: Distribution summaries of malaria vectors in the northern Brazilian Amazon. J Vector Ecol. 2007, 32: 161-167. 10.3376/1081-1710(2007)32[161:DSOMVI]2.0.CO;2.CrossRefPubMed de Barros FSM, de Aguiar DB, Rosa-Freitas MG, Luitgards-Moura JF, daCosta Gurgel H, Alvez Honório N, de Arruda ME, Tsouris P, Vasconcelos SD: Distribution summaries of malaria vectors in the northern Brazilian Amazon. J Vector Ecol. 2007, 32: 161-167. 10.3376/1081-1710(2007)32[161:DSOMVI]2.0.CO;2.CrossRefPubMed
53.
go back to reference Rodríguez M, Pérez L, Caicedo JC, Prieto G, Arroyo JA, Kaur H, Suárez-Mutis M, De La Hoz F, Lines J, Alexander N: Composition and biting activity of Anopheles (Diptera: Culicidae) in the Amazon region of Colombia. J Med Entomol. 2009, 46: 307-315. 10.1603/033.046.0215.PubMedCentralCrossRefPubMed Rodríguez M, Pérez L, Caicedo JC, Prieto G, Arroyo JA, Kaur H, Suárez-Mutis M, De La Hoz F, Lines J, Alexander N: Composition and biting activity of Anopheles (Diptera: Culicidae) in the Amazon region of Colombia. J Med Entomol. 2009, 46: 307-315. 10.1603/033.046.0215.PubMedCentralCrossRefPubMed
54.
go back to reference Quiñones ML, Ruiz F, Calle DA, Harbach RE, Erazo HF, 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: 617-624. 10.1590/S0074-02762006000600007.CrossRefPubMed Quiñones ML, Ruiz F, Calle DA, Harbach RE, Erazo HF, 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: 617-624. 10.1590/S0074-02762006000600007.CrossRefPubMed
55.
go back to reference Getis A, Ord JK: The analysis of spatial association by use of distance statistics. Geogr Anal. 1992, 24: 189-206.CrossRef Getis A, Ord JK: The analysis of spatial association by use of distance statistics. Geogr Anal. 1992, 24: 189-206.CrossRef
56.
go back to reference Faran ME: Anopheles (Nyssorhynchus) trinkae, a new species in the Albimanus section (Diptera: Culicidae). Mosq Syst. 1979, 11: 26-39. Faran ME: Anopheles (Nyssorhynchus) trinkae, a new species in the Albimanus section (Diptera: Culicidae). Mosq Syst. 1979, 11: 26-39.
57.
go back to reference Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P: Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am. 1994, 87: 651-701.CrossRef Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P: Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am. 1994, 87: 651-701.CrossRef
58.
go back to reference Lunt DH, Zhang DX, Szymura JM, Hewitt GM: The insect cytochrome oxidase 1 gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Mol Biol. 1996, 5: 153-165. 10.1111/j.1365-2583.1996.tb00049.x.CrossRefPubMed Lunt DH, Zhang DX, Szymura JM, Hewitt GM: The insect cytochrome oxidase 1 gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Mol Biol. 1996, 5: 153-165. 10.1111/j.1365-2583.1996.tb00049.x.CrossRefPubMed
60.
go back to reference Bødker R, Kisinza W, Malima R, Msangeni H, Lindsay S: Resurgence of malaria in the Usambara mountains, Tanzania, an epidemic of drug-resistant parasites. Glob Change Human Health. 2000, 1: 134-153. 10.1023/A:1010077105257.CrossRef Bødker R, Kisinza W, Malima R, Msangeni H, Lindsay S: Resurgence of malaria in the Usambara mountains, Tanzania, an epidemic of drug-resistant parasites. Glob Change Human Health. 2000, 1: 134-153. 10.1023/A:1010077105257.CrossRef
61.
go back to reference Balls MJ, Bødker R, Thomas CJ, Kisinza W, Msangeni HA, Lindsay SW: Effect of topography on the risk of malaria infection in the Usambara mountains, Tanzania. Trans R Soc Trop Med Hyg. 2004, 98: 400-408. 10.1016/j.trstmh.2003.11.005.CrossRefPubMed Balls MJ, Bødker R, Thomas CJ, Kisinza W, Msangeni HA, Lindsay SW: Effect of topography on the risk of malaria infection in the Usambara mountains, Tanzania. Trans R Soc Trop Med Hyg. 2004, 98: 400-408. 10.1016/j.trstmh.2003.11.005.CrossRefPubMed
62.
go back to reference Bødker R, Akida J, Shayo D, Kisinza W, Msangeni HA, Pedersen EM, Lindsay SW: Relationship between altitude and intensity of malaria transmission in the Usambara Mountains, Tanzania. Ann Entomol Soc Am. 2003, 40: 706-717. Bødker R, Akida J, Shayo D, Kisinza W, Msangeni HA, Pedersen EM, Lindsay SW: Relationship between altitude and intensity of malaria transmission in the Usambara Mountains, Tanzania. Ann Entomol Soc Am. 2003, 40: 706-717.
Metadata
Title
New highland distribution records of multiple Anopheles species in the Ecuadorian Andes
Authors
Lauren L Pinault
Fiona F Hunter
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2011
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-10-236

Other articles of this Issue 1/2011

Malaria Journal 1/2011 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.