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      Fine-scale variation in microclimate across an urban landscape shapes variation in mosquito population dynamics and the potential of Aedes albopictus to transmit arboviral disease

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          Abstract

          Most statistical and mechanistic models used to predict mosquito-borne disease transmission incorporate climate drivers of disease transmission by utilizing environmental data collected at geographic scales that are potentially coarser than what mosquito populations may actually experience. Temperature and relative humidity can vary greatly between indoor and outdoor environments, and can be influenced strongly by variation in landscape features. In the Aedes albopictus system, we conducted a proof-of-concept study in the vicinity of the University of Georgia to explore the effects of fine-scale microclimate variation on mosquito life history and vectorial capacity (VC). We placed Ae. albopictus larvae in artificial pots distributed across three replicate sites within three different land uses–urban, suburban, and rural, which were characterized by high, intermediate, and low proportions of impervious surfaces. Data loggers were placed into each larval environment and in nearby vegetation to record daily variation in water and ambient temperature and relative humidity. The number of adults emerging from each pot and their body size and sex were recorded daily. We found mosquito microclimate to significantly vary across the season as well as with land use. Urban sites were in general warmer and less humid than suburban and rural sites, translating into decreased larval survival, smaller body sizes, and lower per capita growth rates of mosquitoes on urban sites. Dengue transmission potential was predicted to be higher in the summer than the fall. Additionally, the effects of land use on dengue transmission potential varied by season. Warm summers resulted in a higher predicted VC on the cooler, rural sites, while warmer, urban sites had a higher predicted VC during the cooler fall season.

          Author summary

          Environmental factors influence the dynamics of mosquito-borne disease transmission. Most models used to predict mosquito-borne disease transmission incorporate climate data collected at coarser scales than mosquitoes typically experience. Climate conditions can vary greatly between indoor and outdoor environments, and are influenced by landscape features. We conducted a field experiment with the Asian tiger mosquito to explore how microclimate variation across an urban landscape affects mosquito life history and potential to transmit arboviruses, like dengue. We demonstrate that climate conditions captured by weather stations do not reflect relevant mosquito microclimate, and that subtle variation in mean and diurnal ranges of temperature and relative humidity can lead to appreciable variation in key mosquito / pathogen traits that are important for transmission. Our results have implications for statistical and mechanistic models used to predict variation in transmission across seasons, regions, and land uses, but also for building in realistic environmental variation in laboratory work on mosquito-pathogen interactions. Finally, the variation in microclimate we observed across land use was subtle; likely because our study site is a relatively small city. Nevertheless, these translated into considerable differences in mosquito traits and dengue transmission potential, suggesting these effects could be much larger in more expansive cities.

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          Most cited references115

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          The energetic basis of the urban heat island

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            Two decades of urban climate research: a review of turbulence, exchanges of energy and water, and the urban heat island

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              Potential effect of population and climate changes on global distribution of dengue fever: an empirical model.

              Existing theoretical models of the potential effects of climate change on vector-borne diseases do not account for social factors such as population increase, or interactions between climate variables. Our aim was to investigate the potential effects of global climate change on human health, and in particular, on the transmission of vector-borne diseases. We modelled the reported global distribution of dengue fever on the basis of vapour pressure, which is a measure of humidity. We assessed changes in the geographical limits of dengue fever transmission, and in the number of people at risk of dengue by incorporating future climate change and human population projections into our model. We showed that the current geographical limits of dengue fever transmission can be modelled with 89% accuracy on the basis of long-term average vapour pressure. In 1990, almost 30% of the world population, 1.5 billion people, lived in regions where the estimated risk of dengue transmission was greater than 50%. With population and climate change projections for 2085, we estimate that about 5-6 billion people (50-60% of the projected global population) would be at risk of dengue transmission, compared with 3.5 billion people, or 35% of the population, if climate change did not happen. We conclude that climate change is likely to increase the area of land with a climate suitable for dengue fever transmission, and that if no other contributing factors were to change, a large proportion of the human population would then be put at risk.
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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, CA USA )
                1935-2727
                1935-2735
                30 May 2017
                May 2017
                : 11
                : 5
                : e0005640
                Affiliations
                [1 ]Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia, United States of America
                [2 ]Odum School of Ecology, University of Georgia, Athens, Georgia, United States of America
                [3 ]Center for Tropical and Emerging Global Diseases, University of Georgia, Athens, Georgia, United States of America
                [4 ]Center for the Ecology of Infectious Diseases, Odum School of Ecology, University of Georgia, Athens, Georgia, United States of America
                [5 ]Center for Vaccines and Immunology, College of Veterinary Medicine, University of Georgia, Athens, Georgia, United States of America
                [6 ]University of Georgia Riverbasin Center, University of Georgia, Athens, Georgia, United States of America
                [7 ]Mathematics, University of Arkansas Little Rock, Little Rock, Arkansas, United States of America
                Santa Fe Institute, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                • Conceptualization: CCM TDM.

                • Data curation: CCM MVE.

                • Formal analysis: CCM MVE.

                • Funding acquisition: CCM TDM.

                • Investigation: CCM MVE TDM KLM BT.

                • Methodology: CCM.

                • Project administration: CCM.

                • Resources: CCM.

                • Software: CCM MVE.

                • Supervision: CCM.

                • Validation: CCM MVE.

                • Visualization: CCM MVE.

                • Writing – original draft: CCM MVE.

                • Writing – review & editing: CCM MVE TDM KLM BT.

                Author information
                http://orcid.org/0000-0001-5966-1514
                Article
                PNTD-D-16-02183
                10.1371/journal.pntd.0005640
                5466343
                28558030
                dd3f511c-cb0d-4181-92cd-b59835adffce
                © 2017 Murdock et al

                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
                : 6 December 2016
                : 12 May 2017
                Page count
                Figures: 5, Tables: 3, Pages: 23
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DBI-1156707
                Funded by: Department of Infectious Diseases
                Award ID: Start-up
                Award Recipient : C. C. Murdock
                Funded by: Odum School of Ecology
                Award ID: Start-up
                Award Recipient : C. C. Murdock
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: EF-1442417
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: U54GM111274
                The Population Biology of Infectious Diseases REU program (PI: John Drake) in the Odum School of Ecology, University of Georgia is funded by: National Science Foundation (DBI-1156707, EF-1442417), https://www.nsf.gov/, and National Institutes of Health (U54GM111274), https://www.nih.gov/. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Earth Sciences
                Geography
                Human Geography
                Land Use
                Social Sciences
                Human Geography
                Land Use
                Earth Sciences
                Atmospheric Science
                Meteorology
                Humidity
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Earth Sciences
                Seasons
                Summer
                Earth Sciences
                Seasons
                Autumn
                Earth Sciences
                Seasons
                Research and Analysis Methods
                Research Facilities
                Weather Stations
                Biology and Life Sciences
                Physiology
                Physiological Parameters
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-06-09
                All data files are available from the Dryad database ( http://datadryad.org/review?doi=doi:10.5061/dryad.s3953).

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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