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      Dispersal of Adult Culex Mosquitoes in an Urban West Nile Virus Hotspot: A Mark-Capture Study Incorporating Stable Isotope Enrichment of Natural Larval Habitats

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          Abstract

          Dispersal is a critical life history behavior for mosquitoes and is important for the spread of mosquito-borne disease. We implemented the first stable isotope mark-capture study to measure mosquito dispersal, focusing on Culex pipiens in southwest suburban Chicago, Illinois, a hotspot of West Nile virus (WNV) transmission. We enriched nine catch basins in 2010 and 2011 with 15N-potassium nitrate and detected dispersal of enriched adult females emerging from these catch basins using CDC light and gravid traps to distances as far as 3 km. We detected 12 isotopically enriched pools of mosquitoes out of 2,442 tested during the two years and calculated a mean dispersal distance of 1.15 km and maximum flight range of 2.48 km. According to a logistic distribution function, 90% of the female Culex mosquitoes stayed within 3 km of their larval habitat, which corresponds with the distance-limited genetic variation of WNV observed in this study region. This study provides new insights on the dispersal of the most important vector of WNV in the eastern United States and demonstrates the utility of stable isotope enrichment for studying the biology of mosquitoes in other disease systems.

          Author Summary

          The distance and direction of adult mosquitoes movement on the landscape are important processes in the spread of mosquito-borne diseases, and are critical to understand to the development of effective intervention programs. Here we present a novel approach to study adult mosquito dispersal by using stable isotope enrichment of natural larval habitats. We apply this technique in a focal hotspot of West Nile virus (WNV) transmission in suburban, Chicago, USA to measure dispersal of Culex spp. mosquitoes. We enriched larval mosquitoes in residential catch basins using 15N-potassium nitrate and captured adult mosquitoes in traps surrounding these catch basins. Of 10,817 adult female Culex mosquitoes trapped and tested for stable isotopes, 12 individuals were enriched with 15N, indicating they originated from the catch basins receiving stable isotope amendments. The mean dispersal distance was 1.15 km and maximum flight range was 2.48 km. Ninety percent of the female Culex mosquitoes stayed within 3 km of their larval habitat, which corresponds with the distance-limited genetic variation of WNV observed in this study region. This study provides new insights on the dispersal of the most important vector of WNV in the eastern United States and demonstrates the utility of stable isotope enrichment for studying the biology of mosquitoes in other disease systems.

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          Most cited references28

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          Dispersal of the dengue vector Aedes aegypti within and between rural communities.

          Knowledge of mosquito dispersal is critical for vector-borne disease control and prevention strategies and for understanding population structure and pathogen dissemination. We determined Aedes aegypti flight range and dispersal patterns from 21 mark-release-recapture experiments conducted over 11 years (1991-2002) in Puerto Rico and Thailand. Dispersal was compared by release location, sex, age, season, and village. For all experiments, the majority of mosquitoes were collected from their release house or adjacent house. Inter-village movement was detected rarely, with a few mosquitoes moving a maximum of 512 meters from one Thai village to the next. Average dispersal distances were similar for males and females and females released indoors versus outdoors. The movement of Ae. aegypti was not influenced by season or age, but differed by village. Results demonstrate that adult Ae. aegypti disperse relatively short distances, suggesting that people rather than mosquitoes are the primary mode of dengue virus dissemination within and among communities.
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            Beyond insecticides: new thinking on an ancient problem.

            Vector-borne disease is one of the greatest contributors to human mortality and morbidity throughout the tropics. Mosquito-transmitted diseases such as malaria, dengue, yellow fever and filariasis are the main contributors to this burden. Although insecticides have historically been used to try to control vector populations, over the past 15 years, substantial progress has been made in developing alternative vector control strategies ranging from biocontrol methods through to genetic modification of wild insect populations. Here, we review recent advances concerning these strategies and consider the potential impediments to their deployment, including the challenges of obtaining regulatory approval and community acceptance.
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              Culex pipiens (Diptera: Culicidae): a bridge vector of West Nile virus to humans.

              Host-feeding patterns of Culex pipiens L. collected in southwest suburban Chicago in 2005 were studied using polymerase chain reaction (PCR) and DNA sequencing techniques. Culex spp. mosquitoes, most identified to Cx. pipiens and the remainder to Cx. restuans by PCR, had fed on 18 avian species, most commonly American robin (Turdus migratorious), house sparrow (Passer domesticus), and mourning dove (Zenaida macroura). Additional blood meals were derived from four mammal species, primarily humans and raccoons (Procyon lotor). During a West Nile virus (WNV) epidemic in 2005, West Nile virus (WNV) RNA was detected in heads and thoraces of five Cx. pipiens (n = 335, 1.5%) using quantitative PCR. The hosts of these virus-infected, blood-fed mosquitoes included two American robins, one house sparrow, and one human. This is the first report of a WNV-infected Cx. pipiens mosquito collected during an epidemic of WNV that was found to have bitten a human. These results fulfill a criterion for incrimination of Cx. pipiens as a bridge vector.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                March 2014
                27 March 2014
                : 8
                : 3
                : e2768
                Affiliations
                [1 ]Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, United States of America
                [2 ]Department of Entomology, Texas A&M University, College Station, Texas, United States of America
                [3 ]Department of Biology, Georgia Southern University, Statesboro, Georgia, United States of America
                [4 ]Department of Entomology, Michigan State University, East Lansing, Michigan, United States of America
                [5 ]Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, Illinois, United States of America
                [6 ]Department of Entomology, University of Illinois, Urbana, Illinois, United States of America
                [7 ]College of Veterinary Medicine, University of Illinois, Urbana, Illinois, United States of America
                [8 ]Department of Environmental Studies, Emory University, Atlanta, Georgia, United States of America
                [9 ]Department of Pathobiological Sciences, University of Wisconsin, Madison, Wisconsin, United States of America
                Mahidol University, Thailand
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GLH JDB MOR UDK TLG EDW. Performed the experiments: GLH TKA DJD BLK AMG WMB CMN. Analyzed the data: GLH. Contributed reagents/materials/analysis tools: GLH TKA WMB. Wrote the paper: GLH TKA JDB MOR UDK TLG EDW.

                Article
                PNTD-D-13-01478
                10.1371/journal.pntd.0002768
                3967984
                24676212
                d34c6ceb-4ee5-453d-8357-2dfce617471c
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 26 September 2013
                : 18 February 2014
                Page count
                Pages: 7
                Funding
                This project was supported by the National Science Foundation and National Institutes of Health Ecology of Infectious Disease program under Award No. 084040, NIAID grant R37AI21884, and the Michigan Agricultural Experiment Station and the Agricultural Research Service, multistate project NE-507. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Urban Ecology
                Veterinary Science
                Veterinary Diseases
                Veterinary Virology
                Zoology
                Entomology
                Ecology and Environmental Sciences

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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