Abstract

BackgroundUrbanization is occurring rapidly on a global scale and is altering mosquito communities, creating assemblages that are characteristically less diverse. Despite high rates of urbanization and ample examples of vector-borne diseases transmitted by multiple species, the effects of urbanization-driven mosquito diversity losses on disease transmission has not been well explored. We investigated this question using the dog heartworm, a filarial parasite vectored by numerous mosquito species.MethodsWe trapped host-seeking mosquitoes in undeveloped areas and neighborhoods of different ages in Wake County, North Carolina, USA, analyzing captured mosquitoes for heartworm DNA. We compared within-mosquito heartworm infection across land-use types by Kruskal–Wallis and likelihood ratio tests. Using zip code level data acquired from dogs in a local shelter, we performed linear regressions of within-host heartworm prevalence by within-mosquito heartworm prevalence as well as by three mosquito diversity measures. We also determined the best predictor of host-level prevalence among models including within-mosquito infection, mosquito diversity and abundance, and socioeconomic status as variables.ResultsSuburban areas had lower within-mosquito heartworm prevalence and lower likelihood of heartworm-positive mosquitoes than did undeveloped field sites, although no differences were seen between suburban and undeveloped wooded sites. No relationships were noted between within-mosquito and within-host heartworm prevalence. However, mosquito diversity metrics were positively correlated with host heartworm prevalence. Model selection revealed within-host prevalence was best predicted by a positive relationship with mosquito Shannon–Wiener diversity and a negative relationship with household income.ConclusionsOur results demonstrate that decreases in mosquito diversity due to urbanization alter vector-borne disease risk. With regard to dog heartworm disease, this loss of mosquito diversity is associated with decreased heartworm prevalence within both the vector and the host. Although the response is likely different for diseases transmitted by one or few species, mosquito diversity losses leading to decreased transmission could be generalizable to other pathogens with multiple vectors. This study contributes to better understanding of the effects of urbanization and the role of vector diversity in multi-vectored pathosystems.

Highlights

  • Urbanization is occurring rapidly on a global scale and is altering mosquito communities, creating assemblages that are characteristically less diverse

  • The earliest D. immitis-positive pool of mosquitoes was collected during the first week of June, which coincided with the beginning of our trapping season, and the latest D. immitis-positive pool of mosquitoes was collected during the third week of October

  • We found that suburban areas generally had the lowest within-mosquito heartworm prevalence, and that mosquito diversity was positively correlated with heartworm prevalence within the canine host

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Summary

Introduction

Urbanization is occurring rapidly on a global scale and is altering mosquito communities, creating assemblages that are characteristically less diverse. Despite high rates of urbanization and ample examples of vector-borne diseases transmitted by multiple species, the effects of urbanization-driven mosquito diversity losses on disease transmission has not been well explored We investigated this question using the dog heartworm, a filarial parasite vectored by numerous mosquito species. At least in the context of suburban areas, mosquito communities do not recover from these diversity losses after the initial landuse change; diversity decreases as neighborhoods age, resulting in the lowest diversity mosquito assemblages in the most established suburban areas [10] For both suburban and urban areas generally, anthropogenic disturbance is associated with increased abundance of vectors of human disease, including container-breeding Aedes that transmit dengue, Zika, or chikungunya viruses, and Culex mosquitoes, which transmit West Nile virus and human filarial pathogens [10, 11, 13, 14]. An ideal system for further examining the effects of mosquito diversity on vector-borne disease transmission is that of the dog heartworm, Dirofilaria immitis

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