The Asian tiger mosquito, Aedes albopictus, transmits several arboviruses of public health importance, including chikungunya and dengue. Since its introduction to the United States in 1985, the species has invaded more than 40 states, including temperate areas not previously at risk of Aedes-transmitted arboviruses. Mathematical models incorporate climatic variables in predictions of site-specific Ae. albopictus abundances to identify human populations at risk of disease. However, these models rely on coarse resolutions of environmental data that may not accurately represent the climatic profile experienced by mosquitoes in the field, particularly in climatically heterogeneous urban areas. In this study, we pair field surveys of larval and adult Ae. albopictus mosquitoes with site-specific microclimate data across a range of land use types to investigate the relationships between microclimate, density of larval habitat, and adult mosquito abundance and determine whether these relationships change across an urban gradient. We find no evidence for a difference in larval habitat density or adult abundance between rural, suburban, and urban land classes. Adult abundance increases with increasing larval habitat density, which itself is dependent on microclimate. Adult abundance is strongly explained by microclimate variables, demonstrating that theoretically derived, laboratory-parameterized relationships in ectotherm physiology apply to the field. Our results support the continued use of temperature-dependent models to predict Ae. albopictus abundance in urban areas.
BackgroundMosquitoes are strongly influenced by environmental temperatures, both directly and indirectly via carry-over effects, a phenomenon by which adult phenotypes are shaped indirectly by the environmental conditions experienced in previous life stages. In landscapes with spatially varying microclimates, such as a city, the effects of environmental temperature can therefore lead to spatial patterns in disease dynamics. To explore the contribution of carry-over effects on the transmission of dengue-2 virus (DENV-2), we conducted a semi-field experiment comparing the demographic and transmission rates of Aedes albopictus reared on different urban land classes in the summer and autumn season. We parameterized a model of vectorial capacity using field- and literature-derived measurements to estimate the bias introduced into predictions of vectorial capacity not accounting for carry-over effects.ResultsThe larval environment of different land classes and seasons significantly impacted mosquito life history traits. Larval development and survival rates were higher in the summer than the autumn, with no difference across land class. The effect of land class on adult body size differed across season, with suburban mosquitoes having the smallest wing length in the summer and the largest wing length in the autumn, when compared to other land classes. Infection and dissemination rates were higher in the autumn and on suburban and rural land classes compared to urban. Infectiousness did not differ across land class or season. We estimate that not accounting for carry-over effects can underestimate disease transmission potential in suburban and urban sites in the summer by up to 25%.ConclusionsOur findings demonstrate the potential of the larval environment to differentially impact stages of DENV-2 infection in Ae. albopictus mosquitoes via carry-over effects. Failure to account for carry-over effects of the larval environment in mechanistic models can lead to biased estimates of disease transmission potential at fine-scales in urban environments.Electronic supplementary materialThe online version of this article (10.1186/s13071-018-3013-3) contains supplementary material, which is available to authorized users.
word count (max 250): 216 17 Text word count: 3753 18 ABSTRACT 30The Asian tiger mosquito, Aedes albopictus, transmits several arboviruses of public 31 health importance, including chikungunya and Zika. Since its introduction to the United States in 32 1985, the species has invaded over forty states, including temperate areas not previously at risk 33 of Aedes-transmitted arboviruses. Mathematical models incorporate climatic variables in 34 predictions of site-specific Ae. albopictus abundances to identify human populations at risk of 35 disease. However, these models rely on coarse resolutions of environmental data that may not 36 accurately represent the climatic profile experienced by mosquitoes in the field, particularly in 37 climatically-heterogeneous urban areas. In this study, we pair field surveys of larval and adult 38Ae. albopictus mosquitoes with site-specific microclimate data across a range of land use types 39 to investigate the relationships between microclimate, density of larval habitat, and adult 40 mosquito abundance and determine whether these relationships change across an urban 41 gradient. We find no evidence for a difference in larval habitat density or adult abundance 42 between rural, suburban, and urban land classes. Adult abundance increases with increasing 43 larval habitat density, which itself is dependent on microclimate. Adult abundance is strongly 44 explained by microclimate variables, demonstrating that theoretically derived, lab-parameterized 45 relationships in ectotherm physiology apply to the field. Our results provide support for the 46 continued use of temperature-dependent models to predict Ae. albopictus abundance in urban 47 areas. 48 49 cooler climates than Ae. aegypti. Following initial establishment in Texas, Ae. albopictus has 56 invaded over 40 states, 7 and models predict its range will expand as the climate warms. 8,9 At 57 present, established populations of Ae. albopictus are found in the United States as far north as 58Connecticut and New York, 10,11 well outside the present range of Ae. aegypti. Ae. albopictus is 59 implicated in transmission cycles of dengue and chikungunya in the Mediterranean region of 60 Europe, 12,13 which suggests that temperate regions of the US may be similarly vulnerable. 61Given the potential role of Ae. albopictus in disease transmission, it is important to 62 understand what factors influence its abundance. Ae. albopictus is sensitive to variation in 63 temperature due to temperature-dependent life history traits such as development rates, 64 fecundity, and survival. [14][15][16] Climate or meteorological predictors are widely used in mechanistic 65 models and statistical models. [17][18][19][20][21][22] Models leverage these relationships to predict mosquito 66 presence, population growth rates, and abundances based on temperature metrics derived from 67 weather stations or remotely-sensed datasets. However, urban landscapes are composed of a 68 variety of land classes (e.g. residential, developed, vegetated), which vary in th...
Vector-borne viruses (arboviruses) are emerging threats to both human and animal health. The global expansion of dengue virus, West Nile virus, chikungunya, and most recently Zika virus are prominent examples of how quickly mosquito-transmitted viruses can emerge and spread. We currently lack high quality data from a diversity of mosquito-arbovirus systems on the specific mosquito and viral traits that drive disease transmission. Further, the factors that contribute to variation in these traits and disease transmission remain largely unidentified. In this chapter, we outline and explore the following: 1. the specific mechanisms governing the outcome of vector-virus interactions 2. how genetic variation across mosquito populations and viral strains, as well as environmental variation in abiotic and biotic factors shape the mosquito-virus interaction and 3. the implications of these interactions for understanding and predicting arbovirus transmission, as well as for control of mosquito species that transmit human pathogens.
Climate shapes the transmission of mosquito-borne pathogens through impacts on both the vector and the pathogen. In addition to direct effects of the environment, carry-over effects from previous life history stages can influence mosquito traits relevant to disease transmission.While this has been explored in a laboratory setting, the net effect of temperature-mediated carryover effects due to relevant environmental variation in the larval stage is ambiguous. Here, we use data collected from a semi-field experiment investigating dengue dynamics in Aedes albopictus across a natural environmental gradient to parameterize a dengue transmission model. We reared Ae. albopictus across three different land classes characterized by their proportion of impervious surface. Emerged females were offered a dengue infectious bloodmeal, kept at a constant 27°C, and assayed for infection, dissemination, and infectiousness 21 days post infection. Incorporating carryover effects of larval environment on measures of vector competence resulted in lower predicted dengue transmission potential across land class and season, however a strong positive relationship with larval environmental temperature remained. Given the significant impact of carry-over effects, future mechanistic models of disease transmission should include both direct and carry-over effects of environmental temperature.
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