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      Urbanization Increases Aedes albopictus Larval Habitats and Accelerates Mosquito Development and Survivorship

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          Abstract

          Introduction

          Aedes albopictus is a very invasive and aggressive insect vector that causes outbreaks of dengue fever, chikungunya disease, and yellow fever in many countries. Vector ecology and disease epidemiology are strongly affected by environmental changes. Urbanization is a worldwide trend and is one of the most ecologically modifying phenomena. The purpose of this study is to determine how environmental changes due to urbanization affect the ecology of Aedes albopictus.

          Methods

          Aquatic habitats and Aedes albopictus larval population surveys were conducted from May to November 2013 in three areas representing rural, suburban, and urban settings in Guangzhou, China. Ae. albopictus adults were collected monthly using BG-Sentinel traps. Ae. albopictus larva and adult life-table experiments were conducted with 20 replicates in each of the three study areas.

          Results

          The urban area had the highest and the rural area had the lowest number of aquatic habitats that tested positive for Ae. albopictus larvae. Densities in the larval stages varied among the areas, but the urban area had almost two-fold higher densities in pupae and three-fold higher in adult populations compared with the suburban and rural areas. Larvae developed faster and the adult emergence rate was higher in the urban area than in suburban and rural areas. The survival time of adult mosquitoes was also longer in the urban area than it was in suburban and rural areas. Study regions, surface area, water depth, water clearance, surface type, and canopy coverage were important factors associated with the presence of Ae. albopictus larvae.

          Conclusions

          Urbanization substantially increased the density, larval development rate, and adult survival time of Ae. albopictus, which in turn potentially increased the vector capacity, and therefore, disease transmissibility. Mosquito ecology and its correlation with dengue virus transmission should be compared in different environmental settings.

          Author Summary

          Aedes albopictus has expanded its ecological habitat range throughout the world. Although Ae. albopictus was previously considered a rural vector, this species has adapted well to suburban and urban environments, and it has become the most important and sometimes the sole vector of dengue virus transmission in urban areas. Dengue is a vector-borne disease that has become a severe global public health problem during the last decade. We explored the effect of ecology in different ecological settings (urban, suburban, and rural) on Ae. albopictus larval habitat and mosquito development in Guangzhou, where recently dengue has caused serious public health concerns. The environmental changes caused by urbanization had a significant impact on the ecology of Ae. albopictus. Compared with rural and suburban areas, urban areas had more Ae. albopictus larval habitats, shorter larval development time, higher adult emergence rate, and longer lifespan. These results imply that urbanization significantly increases the potential for dengue outbreaks. Because urbanization is a global trend resulting from economic development, the elucidation of Ae. albopictus adaptation to different environments in China also reveals the potential for this important vector to colonize other parts of the world.

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          Most cited references34

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          Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus.

          Aedes albopictus, commonly known as the Asian tiger mosquito, is currently the most invasive mosquito in the world. It is of medical importance due to its aggressive daytime human-biting behavior and ability to vector many viruses, including dengue, LaCrosse, and West Nile. Invasions into new areas of its potential range are often initiated through the transportation of eggs via the international trade in used tires. We use a genetic algorithm, Genetic Algorithm for Rule Set Production (GARP), to determine the ecological niche of Ae. albopictus and predict a global ecological risk map for the continued spread of the species. We combine this analysis with risk due to importation of tires from infested countries and their proximity to countries that have already been invaded to develop a list of countries most at risk for future introductions and establishments. Methods used here have potential for predicting risks of future invasions of vectors or pathogens.
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            Seroprevalence of Chikungunya virus (CHIKV) infection on Lamu Island, Kenya, October 2004.

            An outbreak of Chikungunya virus (CHIKV) disease associated with high fever and severe protracted arthralgias was detected in Lamu, Kenya, peaking in July 2004. At least 1,300 cases were documented. We conducted a seroprevalence study to define the magnitude of transmission on Lamu Island. We conducted a systematic cross-sectional survey. We administered questionnaires and tested 288 sera from Lamu residents for IgM and IgG antibodies to CHIKV. Chikungunya virus infection (seropositivity) was defined as a person with IgG and/or IgM antibodies to CHIKV. IgM antibodies to CHIKV were detected in 18% (53/288) and IgG antibodies in 72% (206/288); IgM and/or IgG antibodies were present in 75% (215/288). The seroprevalence findings suggested that the outbreak was widespread, affecting 75% of the Lamu population; extrapolating the findings to the entire population, 13,500 (95% CI, 12,458-14328) were affected. Vector control strategies are needed to control the spread of this mosquito-borne infection.
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              The Effect of Temperature on Anopheles Mosquito Population Dynamics and the Potential for Malaria Transmission

              The parasites that cause malaria depend on Anopheles mosquitoes for transmission; because of this, mosquito population dynamics are a key determinant of malaria risk. Development and survival rates of both the Anopheles mosquitoes and the Plasmodium parasites that cause malaria depend on temperature, making this a potential driver of mosquito population dynamics and malaria transmission. We developed a temperature-dependent, stage-structured delayed differential equation model to better understand how climate determines risk. Including the full mosquito life cycle in the model reveals that the mosquito population abundance is more sensitive to temperature than previously thought because it is strongly influenced by the dynamics of the juvenile mosquito stages whose vital rates are also temperature-dependent. Additionally, the model predicts a peak in abundance of mosquitoes old enough to vector malaria at more accurate temperatures than previous models. Our results point to the importance of incorporating detailed vector biology into models for predicting the risk for vector borne diseases.
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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
                November 2014
                13 November 2014
                : 8
                : 11
                : e3301
                Affiliations
                [1 ]Key Laboratory of Prevention and Control for Emerging Infectious Diseases of Guangdong Higher Institutes, Department of Pathogen Biology, School of Public Health and Tropical Medicine, Southern Medical University, Guangzhou, China
                [2 ]Program in Public Health, University of California Irvine, Irvine, California, United States of America
                Mahidol University, Thailand
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: XGC GY. Performed the experiments: YJL FK SP CL YXL YZ LY. Analyzed the data: GZ YJL SP. Contributed reagents/materials/analysis tools: YJL FK GZ XGC. Wrote the paper: YJL FK SP GZ GY XGC.

                Article
                PNTD-D-14-00698
                10.1371/journal.pntd.0003301
                4230920
                25393814
                1886bb4e-b326-41c0-8138-7f9384c7451d
                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
                : 25 April 2014
                : 29 September 2014
                Page count
                Pages: 12
                Funding
                This work was supported by grants from the National Institutes of Health, USA (R01 AI083202 and D43 TW009527). 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
                Parasitology
                Medicine and Health Sciences
                Epidemiology
                Disease Vectors
                Vector Biology
                Infectious Diseases
                Viral Diseases
                Dengue Fever
                Vector-Borne Diseases
                Parasitic Diseases
                Tropical Diseases
                Neglected Tropical Diseases
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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