Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence

Abstract Background Understanding wildlife disease ecology is becoming an urgent need due to the continuous emergence and spread of several wildlife zoonotic diseases. West Nile Virus (WNV) is the most widespread arthropod-borne virus in the world, and in recent decades there has been an increase bo...

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Main Authors: Annapaola Rizzoli, Luca Bolzoni, Elizabeth A Chadwick, Gioia Capelli, Fabrizio Montarsi, Michela Grisenti, Josue Martínez de la Puente, Joaquin Muñoz, Jordi Figuerola, Ramon Soriguer, Gianfranco Anfora, Marco Di Luca, Roberto Rosà
Format: Article
Language:English
Published: BMC 2015-04-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-015-0831-4
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author Annapaola Rizzoli
Luca Bolzoni
Elizabeth A Chadwick
Gioia Capelli
Fabrizio Montarsi
Michela Grisenti
Josue Martínez de la Puente
Joaquin Muñoz
Jordi Figuerola
Ramon Soriguer
Gianfranco Anfora
Marco Di Luca
Roberto Rosà
author_facet Annapaola Rizzoli
Luca Bolzoni
Elizabeth A Chadwick
Gioia Capelli
Fabrizio Montarsi
Michela Grisenti
Josue Martínez de la Puente
Joaquin Muñoz
Jordi Figuerola
Ramon Soriguer
Gianfranco Anfora
Marco Di Luca
Roberto Rosà
author_sort Annapaola Rizzoli
collection DOAJ
description Abstract Background Understanding wildlife disease ecology is becoming an urgent need due to the continuous emergence and spread of several wildlife zoonotic diseases. West Nile Virus (WNV) is the most widespread arthropod-borne virus in the world, and in recent decades there has been an increase both in geographic range, and in the frequency of symptomatic infections in humans and wildlife. The principal vector for WNV in Europe is the common house Culex pipiens mosquito, which feeds on a wide variety of vertebrate host species. Variation in mosquito feeding preference has been described as one of the most influential parameters driving intensity and timing of WNV infection in the United States, but feeding preferences for this species have been little studied in Europe. Methods Here, we estimated feeding preference for wild Cx. pipiens in northern Italy, using molecular analysis to identify the origin of blood meals, and avian census to control host abundance variations. Additionally, we used host bird odour extracts to test experimentally mosquito preferences in the absence of environmental variations. Results For the first time, we demonstrate a clear feeding preference for the common blackbird (Turdus merula), both for wild collected specimens and in the lab, suggesting a potential important role for this species in the WNV epidemiology in Europe. A seasonal decrease in abundance of blackbirds is associated with increased feeding on Eurasian magpies (Pica pica), and this may be linked to seasonal emergence of WNV in humans. Feeding preferences on blackbirds are more marked in rural areas, while preference for magpies is higher in peridomestic areas. Other species, such as the house sparrow (Passer domesticus) appear to be selected by mosquitoes opportunistically in relation to its abundance. Conclusions Our findings provide new insights into the ecology of Cx. pipiens in Europe and may give useful indications in terms of implementing targeted WNV surveillance plans. However, a clearer understanding of spatio-temporal variations of Cx. pipiens feeding preferences, and targeted studies on reservoir competence for WNV for these species are therefore now urgently needed as this is essential to describe disease dynamics and quantify virus transmission risk.
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spelling doaj.art-2004382b63a744df8efa5c3deb84b4932023-06-04T11:10:07ZengBMCParasites & Vectors1756-33052015-04-018111310.1186/s13071-015-0831-4Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergenceAnnapaola Rizzoli0Luca Bolzoni1Elizabeth A Chadwick2Gioia Capelli3Fabrizio Montarsi4Michela Grisenti5Josue Martínez de la Puente6Joaquin Muñoz7Jordi Figuerola8Ramon Soriguer9Gianfranco Anfora10Marco Di Luca11Roberto Rosà12Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach. 1Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach. 1Cardiff University, School of Biosciences, Biomedical Science BuildingLaboratory of Parasitology - Istituto Zooprofilattico Sperimentale delle VenezieLaboratory of Parasitology - Istituto Zooprofilattico Sperimentale delle VenezieDepartment of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach. 1Department of Wetland Ecology Estación Biológica Doñana, Consejo Superior de Investigaciones CientificasDepartment of Wetland Ecology Estación Biológica Doñana, Consejo Superior de Investigaciones CientificasDepartment of Wetland Ecology Estación Biológica Doñana, Consejo Superior de Investigaciones CientificasDepartment of Wetland Ecology Estación Biológica Doñana, Consejo Superior de Investigaciones CientificasDepartment of Sustainable Ecosystems and Bioresources, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach. 1Department of Infectious, Parasitic and Immune-Mediated DiseasesDepartment of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach. 1Abstract Background Understanding wildlife disease ecology is becoming an urgent need due to the continuous emergence and spread of several wildlife zoonotic diseases. West Nile Virus (WNV) is the most widespread arthropod-borne virus in the world, and in recent decades there has been an increase both in geographic range, and in the frequency of symptomatic infections in humans and wildlife. The principal vector for WNV in Europe is the common house Culex pipiens mosquito, which feeds on a wide variety of vertebrate host species. Variation in mosquito feeding preference has been described as one of the most influential parameters driving intensity and timing of WNV infection in the United States, but feeding preferences for this species have been little studied in Europe. Methods Here, we estimated feeding preference for wild Cx. pipiens in northern Italy, using molecular analysis to identify the origin of blood meals, and avian census to control host abundance variations. Additionally, we used host bird odour extracts to test experimentally mosquito preferences in the absence of environmental variations. Results For the first time, we demonstrate a clear feeding preference for the common blackbird (Turdus merula), both for wild collected specimens and in the lab, suggesting a potential important role for this species in the WNV epidemiology in Europe. A seasonal decrease in abundance of blackbirds is associated with increased feeding on Eurasian magpies (Pica pica), and this may be linked to seasonal emergence of WNV in humans. Feeding preferences on blackbirds are more marked in rural areas, while preference for magpies is higher in peridomestic areas. Other species, such as the house sparrow (Passer domesticus) appear to be selected by mosquitoes opportunistically in relation to its abundance. Conclusions Our findings provide new insights into the ecology of Cx. pipiens in Europe and may give useful indications in terms of implementing targeted WNV surveillance plans. However, a clearer understanding of spatio-temporal variations of Cx. pipiens feeding preferences, and targeted studies on reservoir competence for WNV for these species are therefore now urgently needed as this is essential to describe disease dynamics and quantify virus transmission risk.https://doi.org/10.1186/s13071-015-0831-4Culex pipiensFeeding preferenceMosquito host selectionBlood meal analysisMultinomial simulationsBehavioural bioassay
spellingShingle Annapaola Rizzoli
Luca Bolzoni
Elizabeth A Chadwick
Gioia Capelli
Fabrizio Montarsi
Michela Grisenti
Josue Martínez de la Puente
Joaquin Muñoz
Jordi Figuerola
Ramon Soriguer
Gianfranco Anfora
Marco Di Luca
Roberto Rosà
Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence
Parasites & Vectors
Culex pipiens
Feeding preference
Mosquito host selection
Blood meal analysis
Multinomial simulations
Behavioural bioassay
title Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence
title_full Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence
title_fullStr Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence
title_full_unstemmed Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence
title_short Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence
title_sort understanding west nile virus ecology in europe culex pipiens host feeding preference in a hotspot of virus emergence
topic Culex pipiens
Feeding preference
Mosquito host selection
Blood meal analysis
Multinomial simulations
Behavioural bioassay
url https://doi.org/10.1186/s13071-015-0831-4
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