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Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Research

Implications for changes in Anopheles darlingi biting behaviour in three communities in the peri-Iquitos region of Amazonian Peru

Authors: Marta Moreno, Marlon P Saavedra, Sara A Bickersmith, William Lainhart, Carlos Tong, Freddy Alava, Joseph M Vinetz, Jan E Conn

Published in: Malaria Journal | Issue 1/2015

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Abstract

Background

Malaria transmission in the peri-Iquitos region of Amazonian Peru has been designated as seasonal and hypo-endemic with recently described hyper-endemic hotspots. Despite relatively recent distribution of long-lasting insecticidal bed nets (LLINs), malaria in Amazonian Peru persists and increased substantially in 2014 compared to previous years. Anopheles darlingi, identified as the main malaria vector, is known for its variable behaviour depending on locality and environment.

Methods

To evaluate vector biology metrics in relation to seasonality and malaria transmission, mosquito collections were carried out in three localities in the peri-Iquitos region, Loreto, Peru in 2011–2012. Human landing catch (HLC) collection method, Shannon (SHA) and CDC trap types were compared for effectiveness in a neotropical setting. Abundance, human biting rate and entomological inoculation rate (EIR) were measured to provide an updated view of transmission patterns post-LLIN distribution.

Results

HLC collected significantly more anopheline mosquitoes than SHA and CDC light traps. Anopheles darlingi was the most prevalent species in all three villages (84% overall). Biting patterns varied depending on trap type, season and village. EIR varied temporally (monthly) and spatially and the highest (2.52) occurred during the 2012 malaria outbreak in Cahuide. Unexpectedly there was a high infection rate (1.47 and 1.75) outside the normal malaria transmission season, coincident with a second local outbreak in Cahuide. The first identification of Anopheles dunhami and Anopheles oswaldoi C in Peru, using molecular markers, is also reported in this study.

Conclusion

These data underscore the importance of HLC as the most meaningful collection method for measuring vector biology indices in this region. The highest monthly EIR provides additional evidence of seasonal transmission in riverine localities correlated with high river levels, and An. darlingi as the only contributor to transmission. The trend of an increase in outdoor-biting together with early-evening infected mosquitoes may undermine the effectiveness of LLINs as a primary malaria intervention.
Literature
1.
go back to reference Kleinschmidt I, Sharp BL, Clarke GP, Curtis B, Fraser C (2001) Use of generalized linear mixed models in the spatial analysis of small-area malaria incidence rates in Kwazulu Natal, South Africa. Am J Epidemiol 153:1213–1221CrossRefPubMed Kleinschmidt I, Sharp BL, Clarke GP, Curtis B, Fraser C (2001) Use of generalized linear mixed models in the spatial analysis of small-area malaria incidence rates in Kwazulu Natal, South Africa. Am J Epidemiol 153:1213–1221CrossRefPubMed
2.
go back to reference Hirzel AH, Hausser J, Chessel D, Perrin N (2002) Ecological-niche factor analysis: how to compute habitat-suitability maps without absence data? Ecology 83:2027–2036CrossRef Hirzel AH, Hausser J, Chessel D, Perrin N (2002) Ecological-niche factor analysis: how to compute habitat-suitability maps without absence data? Ecology 83:2027–2036CrossRef
3.
go back to reference da Silva-Nunes M, Moreno M, Conn JE, Gamboa D, Abeles S, Vinetz JM et al (2012) Amazonian malaria: asymptomatic human reservoirs, diagnostic challenges, environmentally driven changes in mosquito vector populations, and the mandate for sustainable control strategies. Acta Trop 12:281–291CrossRef da Silva-Nunes M, Moreno M, Conn JE, Gamboa D, Abeles S, Vinetz JM et al (2012) Amazonian malaria: asymptomatic human reservoirs, diagnostic challenges, environmentally driven changes in mosquito vector populations, and the mandate for sustainable control strategies. Acta Trop 12:281–291CrossRef
4.
go back to reference Parker BS, Paredes Olortegui M, Penataro Yori P, Escobedo K et al (2013) Hyperendemic malaria transmission in areas of occupation-related travel in the Peruvian Amazon. Malar J 12:178PubMedCentralCrossRefPubMed Parker BS, Paredes Olortegui M, Penataro Yori P, Escobedo K et al (2013) Hyperendemic malaria transmission in areas of occupation-related travel in the Peruvian Amazon. Malar J 12:178PubMedCentralCrossRefPubMed
5.
go back to reference Chowell G, Munayco CV, Escalante AA, McKenzie FE (2009) The spatial and temporal patterns of falciparum and vivax malaria in Peru: 1994–2006. Malar J 8:142PubMedCentralCrossRefPubMed Chowell G, Munayco CV, Escalante AA, McKenzie FE (2009) The spatial and temporal patterns of falciparum and vivax malaria in Peru: 1994–2006. Malar J 8:142PubMedCentralCrossRefPubMed
6.
go back to reference MINSA (2014) Ministerio de Salud del Perú: Sala de Situación de Salud MINSA (2014) Ministerio de Salud del Perú: Sala de Situación de Salud
7.
go back to reference Flores-Mendoza C, Fernandez R, Escobedo-Vargas KS, Vela-Perez Q, Schoeler GB (2004) Natural Plasmodium infections in Anopheles darlingi and Anopheles benarrochi (Diptera: Culicidae) from eastern Peru. J Med Entomol 41:489–494CrossRefPubMed Flores-Mendoza C, Fernandez R, Escobedo-Vargas KS, Vela-Perez Q, Schoeler GB (2004) Natural Plasmodium infections in Anopheles darlingi and Anopheles benarrochi (Diptera: Culicidae) from eastern Peru. J Med Entomol 41:489–494CrossRefPubMed
8.
go back to reference Conn JE, Moreno M, Saavedra M, Bickersmith SA, Knoll E, Fernandez R et al (2013) Molecular taxonomy of Anopheles (Nyssorhynchus) benarrochi (Diptera: Culicidae) and malaria epidemiology in southern Amazonian Peru. Am J Trop Med Hyg 88:319–324PubMedCentralCrossRefPubMed Conn JE, Moreno M, Saavedra M, Bickersmith SA, Knoll E, Fernandez R et al (2013) Molecular taxonomy of Anopheles (Nyssorhynchus) benarrochi (Diptera: Culicidae) and malaria epidemiology in southern Amazonian Peru. Am J Trop Med Hyg 88:319–324PubMedCentralCrossRefPubMed
9.
go back to reference Reinbold-Wasson DD, Sardelis MR, Jones JW, Watts DM, Fernandez R, Carbajal F et al (2012) Determinants of Anopheles seasonal distribution patterns across a forest to periurban gradient near Iquitos. Peru. Am J Trop Med Hyg 86:459–463CrossRefPubMed Reinbold-Wasson DD, Sardelis MR, Jones JW, Watts DM, Fernandez R, Carbajal F et al (2012) Determinants of Anopheles seasonal distribution patterns across a forest to periurban gradient near Iquitos. Peru. Am J Trop Med Hyg 86:459–463CrossRefPubMed
10.
go back to reference Angella AF, Salgueiro P, Gil LH, Vicente JL, Pinto J, Ribolla PE (2014) Seasonal genetic partitioning in the neotropical malaria vector, Anopheles darlingi. Malar J 13:203PubMedCentralCrossRefPubMed Angella AF, Salgueiro P, Gil LH, Vicente JL, Pinto J, Ribolla PE (2014) Seasonal genetic partitioning in the neotropical malaria vector, Anopheles darlingi. Malar J 13:203PubMedCentralCrossRefPubMed
11.
go back to reference Zimmerman RH, Galardo AK, Lounibos LP, Arruda M, Wirtz R (2006) Bloodmeal hosts of Anopheles species (Diptera: Culicidae) in a malaria-endemic area of the Brazilian Amazon. J Med Entomol 43:947–956CrossRefPubMed Zimmerman RH, Galardo AK, Lounibos LP, Arruda M, Wirtz R (2006) Bloodmeal hosts of Anopheles species (Diptera: Culicidae) in a malaria-endemic area of the Brazilian Amazon. J Med Entomol 43:947–956CrossRefPubMed
13.
go back to reference Gil LH, Alves FP, Zieler H, Salcedo JM, Durlacher RR, Cunha RP et al (2003) Seasonal malaria transmission and variation of anopheline density in two distinct endemic areas in Brazilian Amazonia. J Med Entomol 40:636–641CrossRefPubMed Gil LH, Alves FP, Zieler H, Salcedo JM, Durlacher RR, Cunha RP et al (2003) Seasonal malaria transmission and variation of anopheline density in two distinct endemic areas in Brazilian Amazonia. J Med Entomol 40:636–641CrossRefPubMed
14.
go back to reference Moreno JE, Rubio-Palis Y, Paez E, Perez E, Sanchez V (2007) Abundance, biting behaviour and parous rate of anopheline mosquito species in relation to malaria incidence in gold-mining areas of southern Venezuela. Med Vet Entomol 21:339–349CrossRefPubMed Moreno JE, Rubio-Palis Y, Paez E, Perez E, Sanchez V (2007) Abundance, biting behaviour and parous rate of anopheline mosquito species in relation to malaria incidence in gold-mining areas of southern Venezuela. Med Vet Entomol 21:339–349CrossRefPubMed
15.
go back to reference Rodriguez M, Perez L, Caicedo JC, Prieto G, Arroyo JA, Kaur H et al (2009) Composition and biting activity of Anopheles (Diptera: Culicidae) in the Amazon region of Colombia. J Med Entomol 46:307–315PubMedCentralCrossRefPubMed Rodriguez M, Perez L, Caicedo JC, Prieto G, Arroyo JA, Kaur H et al (2009) Composition and biting activity of Anopheles (Diptera: Culicidae) in the Amazon region of Colombia. J Med Entomol 46:307–315PubMedCentralCrossRefPubMed
16.
go back to reference Martins-Campos KM, Pinheiro WD, Vitor-Silva S, Siqueira AM, Melo GC, Rodrigues IC et al (2012) Integrated vector management targeting Anopheles darlingi populations decreases malaria incidence in an unstable transmission area, in the rural Brazilian Amazon. Malar J 11:351PubMedCentralCrossRefPubMed Martins-Campos KM, Pinheiro WD, Vitor-Silva S, Siqueira AM, Melo GC, Rodrigues IC et al (2012) Integrated vector management targeting Anopheles darlingi populations decreases malaria incidence in an unstable transmission area, in the rural Brazilian Amazon. Malar J 11:351PubMedCentralCrossRefPubMed
17.
go back to reference Athrey G, Hodges TK, Reddy MR, Overgaard HJ, Matias A, Ridl FC et al (2012) The effective population size of malaria mosquitoes: large impact of vector control. PLoS Genet 8:e1003097PubMedCentralCrossRefPubMed Athrey G, Hodges TK, Reddy MR, Overgaard HJ, Matias A, Ridl FC et al (2012) The effective population size of malaria mosquitoes: large impact of vector control. PLoS Genet 8:e1003097PubMedCentralCrossRefPubMed
18.
go back to reference Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I et al (1987) Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ 65:39–45PubMedCentralPubMed Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I et al (1987) Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ 65:39–45PubMedCentralPubMed
19.
go back to reference Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE et al (1993) High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 61:315–320CrossRefPubMed Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE et al (1993) High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 61:315–320CrossRefPubMed
20.
go back to reference Hasan AU, Suguri S, Sattabongkot J, Fujimoto C, Amakawa M, Harada M et al (2009) Implementation of a novel PCR based method for detecting malaria parasites from naturally infected mosquitoes in Papua New Guinea. Malar J 8:182PubMedCentralCrossRefPubMed Hasan AU, Suguri S, Sattabongkot J, Fujimoto C, Amakawa M, Harada M et al (2009) Implementation of a novel PCR based method for detecting malaria parasites from naturally infected mosquitoes in Papua New Guinea. Malar J 8:182PubMedCentralCrossRefPubMed
21.
go back to reference Povoa MM, Machado RL, Segura MN, Vianna GM, Vasconcelos AS, Conn JE (2000) Infectivity of malaria vector mosquitoes: correlation of positivity between ELISA and PCR-ELISA tests. Trans R Soc Trop Med Hyg 94:106–107CrossRefPubMed Povoa MM, Machado RL, Segura MN, Vianna GM, Vasconcelos AS, Conn JE (2000) Infectivity of malaria vector mosquitoes: correlation of positivity between ELISA and PCR-ELISA tests. Trans R Soc Trop Med Hyg 94:106–107CrossRefPubMed
22.
go back to reference Manguin S, Wilkerson RC, Conn JE, Rubio-Palis Y, Danoff-Burg JA, Roberts DR (1999) Population structure of the primary malaria vector in South America, Anopheles darlingi, using isozyme, random amplified polymorphic DNA, internal transcribed spacer 2, and morphologic markers. Am J Trop Med Hyg 60:364–376PubMed Manguin S, Wilkerson RC, Conn JE, Rubio-Palis Y, Danoff-Burg JA, Roberts DR (1999) Population structure of the primary malaria vector in South America, Anopheles darlingi, using isozyme, random amplified polymorphic DNA, internal transcribed spacer 2, and morphologic markers. Am J Trop Med Hyg 60:364–376PubMed
23.
go back to reference Santos LM, Gama RA, Eiras AE, Fonseca CG (2010) Genetic differences based on AFLP markers in the mosquito species Anopheles darlingi collected in versus near houses in the region of Porto Velho, RO, Brazil. Genet Mol Res 9:2254–2262CrossRefPubMed Santos LM, Gama RA, Eiras AE, Fonseca CG (2010) Genetic differences based on AFLP markers in the mosquito species Anopheles darlingi collected in versus near houses in the region of Porto Velho, RO, Brazil. Genet Mol Res 9:2254–2262CrossRefPubMed
24.
go back to reference Mirabello L, Conn JE (2006) Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity (Edinb) 96:311–321CrossRef Mirabello L, Conn JE (2006) Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity (Edinb) 96:311–321CrossRef
25.
go back to reference Pinedo-Cancino V, Sheen P, Tarazona-Santos E, Oswald WE, Jeri C, Vittor AY et al (2006) Limited diversity of Anopheles darlingi in the Peruvian Amazon region of Iquitos. Am J Trop Med Hyg 75:238–245PubMedCentralPubMed Pinedo-Cancino V, Sheen P, Tarazona-Santos E, Oswald WE, Jeri C, Vittor AY et al (2006) Limited diversity of Anopheles darlingi in the Peruvian Amazon region of Iquitos. Am J Trop Med Hyg 75:238–245PubMedCentralPubMed
26.
go back to reference Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Sanches Lozano W et al (2006) The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg 74:3–11PubMed Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Sanches Lozano W et al (2006) The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg 74:3–11PubMed
27.
go back to reference Rosas-Aguirre A, Guzman-Guzman M, Moreno-Gutierrez D, Rodriguez-Ferrucci H, Vargas-Pacherrez D, Acuna-Gonzalez Y (2011) Long-lasting insecticide—treated bednet ownership, retention and usage 1 year after their distribution in Loreto, Peru. Rev Peru Med Exp Salud Publica 28:228–236 (in Spanish) CrossRefPubMed Rosas-Aguirre A, Guzman-Guzman M, Moreno-Gutierrez D, Rodriguez-Ferrucci H, Vargas-Pacherrez D, Acuna-Gonzalez Y (2011) Long-lasting insecticide—treated bednet ownership, retention and usage 1 year after their distribution in Loreto, Peru. Rev Peru Med Exp Salud Publica 28:228–236 (in Spanish) CrossRefPubMed
29.
go back to reference Knols BG, de Jong R, Takken W (1995) Differential attractiveness of isolated humans to mosquitoes in Tanzania. Trans R Soc Trop Med Hyg 89:604–606CrossRefPubMed Knols BG, de Jong R, Takken W (1995) Differential attractiveness of isolated humans to mosquitoes in Tanzania. Trans R Soc Trop Med Hyg 89:604–606CrossRefPubMed
30.
go back to reference Forattini OP (1962) Entomologia Medica, vol 1. Faculdade de Higiene e Sáude Publica, São Paulo Forattini OP (1962) Entomologia Medica, vol 1. Faculdade de Higiene e Sáude Publica, São Paulo
31.
go back to reference Faran ME, Linthicum KJ (1981) A handbook of the Amazonian species of Anopheles (Nyssorhynchus) (Diptera: Culicidae). Mosquito System 13:1–81 Faran ME, Linthicum KJ (1981) A handbook of the Amazonian species of Anopheles (Nyssorhynchus) (Diptera: Culicidae). Mosquito System 13:1–81
32.
go back to reference Consoli RA, Lourenco-de-Oliveira R (1994) Principais mosquitos de importância sanitária no Brasil. Editora Fiocruz, Fundação Oswaldo Cruz Consoli RA, Lourenco-de-Oliveira R (1994) Principais mosquitos de importância sanitária no Brasil. Editora Fiocruz, Fundação Oswaldo Cruz
33.
go back to reference Zapata MA, Cienfuegos AV, Quiros OI, Quinones ML, Luckhart S, Correa MM (2007) Discrimination of seven Anopheles species from San Pedro de Uraba, Antioquia, Colombia, by polymerase chain reaction-restriction fragment length polymorphism analysis of its sequences. Am J Trop Med Hyg 77:67–72PubMed Zapata MA, Cienfuegos AV, Quiros OI, Quinones ML, Luckhart S, Correa MM (2007) Discrimination of seven Anopheles species from San Pedro de Uraba, Antioquia, Colombia, by polymerase chain reaction-restriction fragment length polymorphism analysis of its sequences. Am J Trop Med Hyg 77:67–72PubMed
34.
go back to reference Matson R, Rios CT, Chavez CB, Gilman RH, Florin D, Sifuentes VL et al (2008) Improved molecular technique for the differentiation of neotropical anopheline species. Am J Trop Med Hyg 78:492–498PubMedCentralPubMed Matson R, Rios CT, Chavez CB, Gilman RH, Florin D, Sifuentes VL et al (2008) Improved molecular technique for the differentiation of neotropical anopheline species. Am J Trop Med Hyg 78:492–498PubMedCentralPubMed
35.
go back to reference Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMed Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMed
36.
go back to reference Foster PG, Bergo ES, Bourke BP, Oliveira TM, Nagaki SS, Sant’Ana DC et al (2013) Phylogenetic analysis and DNA-based species confirmation in Anopheles (Nyssorhynchus). PLoS One 8:e54063PubMedCentralCrossRefPubMed Foster PG, Bergo ES, Bourke BP, Oliveira TM, Nagaki SS, Sant’Ana DC et al (2013) Phylogenetic analysis and DNA-based species confirmation in Anopheles (Nyssorhynchus). PLoS One 8:e54063PubMedCentralCrossRefPubMed
37.
go back to reference Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMed Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMed
38.
go back to reference Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMed Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMed
39.
go back to reference Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMed Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMed
40.
go back to reference Ruiz F, Linton YM, Ponsonby DJ, Conn JE, Herrera M, Quinones ML et al (2010) Molecular comparison of topotypic specimens confirms Anopheles (Nyssorhynchus) dunhami Causey (Diptera: Culicidae) in the Colombian Amazon. Mem Inst Oswaldo Cruz 105:899–903PubMedCentralPubMed Ruiz F, Linton YM, Ponsonby DJ, Conn JE, Herrera M, Quinones ML et al (2010) Molecular comparison of topotypic specimens confirms Anopheles (Nyssorhynchus) dunhami Causey (Diptera: Culicidae) in the Colombian Amazon. Mem Inst Oswaldo Cruz 105:899–903PubMedCentralPubMed
41.
go back to reference Galardo AK, Arruda M, D’Almeida Couto AA, Wirtz R, Lounibos LP, Zimmerman RH (2007) Malaria vector incrimination in three rural riverine villages in the Brazilian Amazon. Am J Trop Med Hyg 76:461–469PubMed Galardo AK, Arruda M, D’Almeida Couto AA, Wirtz R, Lounibos LP, Zimmerman RH (2007) Malaria vector incrimination in three rural riverine villages in the Brazilian Amazon. Am J Trop Med Hyg 76:461–469PubMed
42.
go back to reference Girod R, Gaborit P, Carinci R, Issaly J, Fouque F (2008) Anopheles darlingi bionomics and transmission of Plasmodium falciparum, Plasmodium vivax and Plasmodium malariae in Amerindian villages of the Upper-Maroni Amazonian forest, French Guiana. Mem Inst Oswaldo Cruz 103:702–710CrossRefPubMed Girod R, Gaborit P, Carinci R, Issaly J, Fouque F (2008) Anopheles darlingi bionomics and transmission of Plasmodium falciparum, Plasmodium vivax and Plasmodium malariae in Amerindian villages of the Upper-Maroni Amazonian forest, French Guiana. Mem Inst Oswaldo Cruz 103:702–710CrossRefPubMed
43.
go back to reference Rubio-Palis Y, Bevilacqua M, Medina DA, Moreno JE, Cardenas L, Sanchez V et al (2013) Malaria entomological risk factors in relation to land cover in the Lower Caura River Basin, Venezuela. Mem Inst Oswaldo Cruz 108:220–228PubMedCentralCrossRefPubMed Rubio-Palis Y, Bevilacqua M, Medina DA, Moreno JE, Cardenas L, Sanchez V et al (2013) Malaria entomological risk factors in relation to land cover in the Lower Caura River Basin, Venezuela. Mem Inst Oswaldo Cruz 108:220–228PubMedCentralCrossRefPubMed
44.
go back to reference Naranjo-Diaz N, Rosero DA, Rua-Uribe G, Luckhart S, Correa MM (2013) Abundance, behavior and entomological inoculation rates of anthropophilic anophelines from a primary Colombian malaria endemic area. Parasit Vectors 6:61PubMedCentralCrossRefPubMed Naranjo-Diaz N, Rosero DA, Rua-Uribe G, Luckhart S, Correa MM (2013) Abundance, behavior and entomological inoculation rates of anthropophilic anophelines from a primary Colombian malaria endemic area. Parasit Vectors 6:61PubMedCentralCrossRefPubMed
45.
go back to reference Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M et al (2014) Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J 13:125PubMedCentralCrossRefPubMed Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M et al (2014) Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J 13:125PubMedCentralCrossRefPubMed
46.
go back to reference Bugoro H, Iro’ofa C, Mackenzie DO, Apairamo A, Hevalao W, Corcoran S et al (2011) Changes in vector species composition and current vector biology and behaviour will favour malaria elimination in Santa Isabel Province, Solomon Islands. Malar J 10:287PubMedCentralCrossRefPubMed Bugoro H, Iro’ofa C, Mackenzie DO, Apairamo A, Hevalao W, Corcoran S et al (2011) Changes in vector species composition and current vector biology and behaviour will favour malaria elimination in Santa Isabel Province, Solomon Islands. Malar J 10:287PubMedCentralCrossRefPubMed
47.
go back to reference Schoeler GB, Flores-Mendoza C, Fernandez R, Davila JR, Zyzak M (2003) Geographical distribution of Anopheles darlingi in the Amazon Basin region of Peru. J Am Mosq Control Assoc 19:286–296PubMed Schoeler GB, Flores-Mendoza C, Fernandez R, Davila JR, Zyzak M (2003) Geographical distribution of Anopheles darlingi in the Amazon Basin region of Peru. J Am Mosq Control Assoc 19:286–296PubMed
48.
go back to reference Moutinho PR, Gil LH, Cruz RB, Ribolla PE (2011) Population dynamics, structure and behavior of Anopheles darlingi in a rural settlement in the Amazon rainforest of Acre, Brazil. Malar J 10:174PubMedCentralCrossRefPubMed Moutinho PR, Gil LH, Cruz RB, Ribolla PE (2011) Population dynamics, structure and behavior of Anopheles darlingi in a rural settlement in the Amazon rainforest of Acre, Brazil. Malar J 10:174PubMedCentralCrossRefPubMed
49.
go back to reference Hayes J, Calderon G, Falcon R, Zambrano V (1987) Newly incriminated anopheline vectors of human malaria parasites in Junin Department, Peru. J Am Mosq Control Assoc 3:418–422PubMed Hayes J, Calderon G, Falcon R, Zambrano V (1987) Newly incriminated anopheline vectors of human malaria parasites in Junin Department, Peru. J Am Mosq Control Assoc 3:418–422PubMed
50.
go back to reference Lima JB, Rosa-Freitas MG, Rodovalho CM, Santos F, Lourenco-de-Oliveira R (2014) Is there an efficient trap or collection method for sampling Anopheles darlingi and other malaria vectors that can describe the essential parameters affecting transmission dynamics as effectively as human landing catches? A review. Mem Inst Oswaldo Cruz 109:685–705PubMedCentralCrossRefPubMed Lima JB, Rosa-Freitas MG, Rodovalho CM, Santos F, Lourenco-de-Oliveira R (2014) Is there an efficient trap or collection method for sampling Anopheles darlingi and other malaria vectors that can describe the essential parameters affecting transmission dynamics as effectively as human landing catches? A review. Mem Inst Oswaldo Cruz 109:685–705PubMedCentralCrossRefPubMed
51.
go back to reference Hiwat H, De Rijk M, Andriessen R, Koenraadt CJ, Takken W (2011) Evaluation of methods for sampling the malaria vector Anopheles darlingi (Diptera, Culicidae) in Suriname and the relation with its biting behavior. J Med Entomol 48:1039–1046CrossRefPubMed Hiwat H, De Rijk M, Andriessen R, Koenraadt CJ, Takken W (2011) Evaluation of methods for sampling the malaria vector Anopheles darlingi (Diptera, Culicidae) in Suriname and the relation with its biting behavior. J Med Entomol 48:1039–1046CrossRefPubMed
52.
go back to reference Rubio-Palis Y, Moreno JE, Sanchez V, Estrada Y, Anaya W, Bevilacqua M et al (2012) Can mosquito magnet(R) substitute for human-landing catches to sample anopheline populations? Mem Inst Oswaldo Cruz 107:546–549CrossRefPubMed Rubio-Palis Y, Moreno JE, Sanchez V, Estrada Y, Anaya W, Bevilacqua M et al (2012) Can mosquito magnet(R) substitute for human-landing catches to sample anopheline populations? Mem Inst Oswaldo Cruz 107:546–549CrossRefPubMed
53.
go back to reference Gama RA, Silva IM, Geier M, Eiras AE (2013) Development of the BG-Malaria trap as an alternative to human-landing catches for the capture of Anopheles darlingi. Mem Inst Oswaldo Cruz 108:763–771PubMedCentralCrossRefPubMed Gama RA, Silva IM, Geier M, Eiras AE (2013) Development of the BG-Malaria trap as an alternative to human-landing catches for the capture of Anopheles darlingi. Mem Inst Oswaldo Cruz 108:763–771PubMedCentralCrossRefPubMed
54.
go back to reference Burkot TR, Russell TL, Reimer LJ, Bugoro H, Beebe NW, Cooper RD, Sukawati S, Collins FH, Lobo NF (2013) Barrier screens: a method to sample blood-fed and host-seeking exophilic mosquitoes. Malar J 12:49PubMedCentralCrossRefPubMed Burkot TR, Russell TL, Reimer LJ, Bugoro H, Beebe NW, Cooper RD, Sukawati S, Collins FH, Lobo NF (2013) Barrier screens: a method to sample blood-fed and host-seeking exophilic mosquitoes. Malar J 12:49PubMedCentralCrossRefPubMed
Metadata
Title
Implications for changes in Anopheles darlingi biting behaviour in three communities in the peri-Iquitos region of Amazonian Peru
Authors
Marta Moreno
Marlon P Saavedra
Sara A Bickersmith
William Lainhart
Carlos Tong
Freddy Alava
Joseph M Vinetz
Jan E Conn
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-015-0804-2

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