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  1. Abstract Background

    Effectively controlling heartworm disease—a major parasitic disease threatening animal health in the US and globally—requires understanding the local ecology of mosquito vectors involved in transmission. However, the key vector species in a given region are often unknown and challenging to identify. Here we investigate (i) the key vector species associated with transmission of the parasite,Dirofilaria immitis, in California and (ii) the climate and land cover drivers of vector presence.

    Methods

    To identify key mosquito vectors involved in transmission, we incorporated long-term, finely resolved mosquito surveillance data and dog heartworm case data in a statistical modeling approach (fixed-effects regression) that rigorously controls for other unobserved drivers of heartworm cases. We then used a flexible machine learning approach (gradient boosted machines) to identify the climate and land cover variables associated with the presence of each species.

    Results

    We found significant, regionally specific, positive associations between dog heartworm cases and the abundance of four vector species:Aedes aegypti(Central California),Ae. albopictus(Southern California),Ae. sierrensis(Central California), andCuliseta incidens(Northern and Central California). The proportion of developed land cover was one of the most important ecological variables predicting the presence or absence of the putative vector species.

    Conclusion

    Our results implicate three previously under-recognized vectors of dog heartworm transmission in California and indicate the land cover types in which each putative vector species is commonly found. Efforts to target these species could prioritize surveillance in these land cover types (e.g. near human dwellings in less urbanized settings forAe. albopictusandCs. incidens) but further investigation on the natural infection prevalence and host-biting rates of these species, as well as the other local vectors, is needed.

    Graphical Abstract 
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  2. Abstract

    Mosquito-borne diseases (MBD) threaten over 80% of the world’s population, and are increasing in intensity and shifting in geographical range with land use and climate change. Mitigation hinges on understanding disease-specific risk profiles, but current risk maps are severely limited in spatial resolution. One important determinant of MBD risk is temperature, and though the relationships between temperature and risk have been extensively studied, maps are often created using sparse data that fail to capture microclimatic conditions. Here, we leverage high resolution land surface temperature (LST) measurements, in conjunction with established relationships between air temperature and MBD risk factors like mosquito biting rate and transmission probability, to produce fine resolution (70 m) maps of MBD risk components. We focus our case study on West Nile virus (WNV) in the San Joaquin Valley of California, where temperatures vary widely across the day and the diverse agricultural/urban landscape. We first use field measurements to establish a relationship between LST and air temperature, and apply it to Ecosystem Spaceborne Thermal Radiometer Experiment data (2018–2020) in peak WNV transmission months (June–September). We then use the previously derived equations to estimate spatially explicit mosquito biting and WNV transmission rates. We use these maps to uncover significant differences in risk across land cover types, and identify the times of day which contribute to high risk for different land covers. Additionally, we evaluate the value of high resolution spatial and temporal data in avoiding biased risk estimates due to Jensen’s inequality, and find that using aggregate data leads to significant biases of up to 40.5% in the possible range of risk values. Through this analysis, we show that the synergy between novel remote sensing technology and fundamental principles of disease ecology can unlock new insights into the spatio-temporal dynamics of MBDs.

     
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  3. Abstract

    Experiments and models suggest that climate affects mosquito‐borne disease transmission. However, disease transmission involves complex nonlinear interactions between climate and population dynamics, which makes detecting climate drivers at the population level challenging. By analysing incidence data, estimated susceptible population size, and climate data with methods based on nonlinear time series analysis (collectively referred to as empirical dynamic modelling), we identified drivers and their interactive effects on dengue dynamics in San Juan, Puerto Rico. Climatic forcing arose only when susceptible availability was high: temperature and rainfall had net positive and negative effects respectively. By capturing mechanistic, nonlinear and context‐dependent effects of population susceptibility, temperature and rainfall on dengue transmission empirically, our model improves forecast skill over recent, state‐of‐the‐art models for dengue incidence. Together, these results provide empirical evidence that the interdependence of host population susceptibility and climate drives dengue dynamics in a nonlinear and complex, yet predictable way.

     
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  4. Abstract

    Lyme disease is the most common vector‐borne disease in temperate zones and a growing public health threat in the United States (US). The life cycles of the tick vectors and spirochete pathogen are highly sensitive to climate, but determining the impact of climate change on Lyme disease burden has been challenging due to the complex ecology of the disease and the presence of multiple, interacting drivers of transmission. Here we incorporated 18 years of annual, county‐level Lyme disease case data in a panel data statistical model to investigate prior effects of climate variation on disease incidence while controlling for other putative drivers. We then used these climate–disease relationships to project Lyme disease cases using CMIP5 global climate models and two potential climate scenarios (RCP4.5 and RCP8.5). We find that interannual variation in Lyme disease incidence is associated with climate variation in all US regions encompassing the range of the primary vector species. In all regions, the climate predictors explained less of the variation in Lyme disease incidence than unobserved county‐level heterogeneity, but the strongest climate–disease association detected was between warming annual temperatures and increasing incidence in the Northeast. Lyme disease projections indicate that cases in the Northeast will increase significantly by 2050 (23,619 ± 21,607 additional cases), but only under RCP8.5, and with large uncertainty around this projected increase. Significant case changes are not projected for any other region under either climate scenario. The results demonstrate a regionally variable and nuanced relationship between climate change and Lyme disease, indicating possible nonlinear responses of vector ticks and transmission dynamics to projected climate change. Moreover, our results highlight the need for improved preparedness and public health interventions in endemic regions to minimize the impact of further climate change‐induced increases in Lyme disease burden.

     
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  5. Abstract

    In the aftermath of the 2015 pandemic of Zika virus (ZIKV), concerns over links between climate change and emerging arboviruses have become more pressing. Given the potential that much of the world might remain at risk from the virus, we used a previously established temperature‐dependent transmission model for ZIKV to project climate change impacts on transmission suitability risk by mid‐century (a generation into the future). Based on these model predictions, in the worst‐case scenario, over 1.3 billion new people could face suitable transmission temperatures for ZIKV by 2050. The next generation will face substantially increased ZIKV transmission temperature suitability in North America and Europe, where naïve populations might be particularly vulnerable. Mitigating climate change even to moderate emissions scenarios could significantly reduce global expansion of climates suitable for ZIKV transmission, potentially protecting around 200 million people. Given these suitability risk projections, we suggest an increased priority on research establishing the immune history of vulnerable populations, modeling when and where the next ZIKV outbreak might occur, evaluating the efficacy of conventional and novel intervention measures, and increasing surveillance efforts to prevent further expansion of ZIKV.

     
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  6. Abstract

    The densities of highly competent plant hosts (i.e. those that are susceptible to and successfully transmit a pathogen) may shape pathogen community composition and disease severity, altering disease risk and impacts. Life history and evolutionary history can influence host competence; longer lived species tend to be better defended than shorter lived species and pathogens adapt to infect species with which they have longer evolutionary histories. It is unclear, however, how the densities of species that differ in competence due to life and evolutionary histories affect plant pathogen community composition and disease severity.

    We examined foliar fungal pathogens of two host groups in a California grassland: native perennial and non‐native annual grasses. We first characterized pathogen community composition and disease severity of the two host groups to approximate differences in competence. We then used observational and manipulated gradients of native perennial and non‐native annual grass densities to assess the effects of each host group on pathogen community composition and disease severity in 1‐m2plots.

    Native perennial and non‐native annual grasses hosted distinct pathogen communities but shared generalist pathogens. Native perennial grasses experienced 26% higher disease severity than non‐native annuals. Only the observational gradient of native perennial grass density affected disease severity; there were no other significant relationships between host group density and either disease severity or pathogen community composition.

    Synthesis. The life and evolutionary histories of grasses likely influence their competence for different pathogen species, exemplified by distinct pathogen communities and differences in disease severity. However, there was limited evidence that the density of either host group affected pathogen community composition or disease severity. Therefore, competence for different pathogens likely shapes pathogen community composition and disease severity but may not interact with host density to alter disease risk and impacts at small scales.

     
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  7. Abstract

    Vector‐borne diseases (VBDs) are embedded within complex socio‐ecological systems. While research has traditionally focused on the direct effects of VBDs on human morbidity and mortality, it is increasingly clear that their impacts are much more pervasive. VBDs are dynamically linked to feedbacks between environmental conditions, vector ecology, disease burden, and societal responses that drive transmission. As a result, VBDs have had profound influence on human history. Mechanisms include: (1) killing or debilitating large numbers of people, with demographic and population‐level impacts; (2) differentially affecting populations based on prior history of disease exposure, immunity, and resistance; (3) being weaponised to promote or justify hierarchies of power, colonialism, racism, classism and sexism; (4) catalysing changes in ideas, institutions, infrastructure, technologies and social practices in efforts to control disease outbreaks; and (5) changing human relationships with the land and environment. We use historical and archaeological evidence interpreted through an ecological lens to illustrate how VBDs have shaped society and culture, focusing on case studies from four pertinent VBDs: plague, malaria, yellow fever and trypanosomiasis. By comparing across diseases, time periods and geographies, we highlight the enormous scope and variety of mechanisms by which VBDs have influenced human history.

     
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  8. Abstract Background West Nile virus (WNV) is the leading cause of mosquito-borne illness in the continental USA. WNV occurrence has high spatiotemporal variation, and current approaches to targeted control of the virus are limited, making forecasting a public health priority. However, little research has been done to compare strengths and weaknesses of WNV disease forecasting approaches on the national scale. We used forecasts submitted to the 2020 WNV Forecasting Challenge, an open challenge organized by the Centers for Disease Control and Prevention, to assess the status of WNV neuroinvasive disease (WNND) prediction and identify avenues for improvement. Methods We performed a multi-model comparative assessment of probabilistic forecasts submitted by 15 teams for annual WNND cases in US counties for 2020 and assessed forecast accuracy, calibration, and discriminatory power. In the evaluation, we included forecasts produced by comparison models of varying complexity as benchmarks of forecast performance. We also used regression analysis to identify modeling approaches and contextual factors that were associated with forecast skill. Results Simple models based on historical WNND cases generally scored better than more complex models and combined higher discriminatory power with better calibration of uncertainty. Forecast skill improved across updated forecast submissions submitted during the 2020 season. Among models using additional data, inclusion of climate or human demographic data was associated with higher skill, while inclusion of mosquito or land use data was associated with lower skill. We also identified population size, extreme minimum winter temperature, and interannual variation in WNND cases as county-level characteristics associated with variation in forecast skill. Conclusions Historical WNND cases were strong predictors of future cases with minimal increase in skill achieved by models that included other factors. Although opportunities might exist to specifically improve predictions for areas with large populations and low or high winter temperatures, areas with high case-count variability are intrinsically more difficult to predict. Also, the prediction of outbreaks, which are outliers relative to typical case numbers, remains difficult. Further improvements to prediction could be obtained with improved calibration of forecast uncertainty and access to real-time data streams (e.g. current weather and preliminary human cases). Graphical Abstract 
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    Free, publicly-accessible full text available December 1, 2024
  9. Abstract Individual animals in natural populations tend to host diverse parasite species concurrently over their lifetimes. In free‐living ecological communities, organismal life histories shape interactions with their environment, which ultimately forms the basis of ecological succession. However, the structure and dynamics of mammalian parasite communities have not been contextualized in terms of primary ecological succession, in part because few datasets track occupancy and abundance of multiple parasites in wild hosts starting at birth. Here, we studied community dynamics of 12 subtypes of protozoan microparasites ( Theileria spp.) in a herd of African buffalo. We show that Theileria communities followed predictable patterns of succession underpinned by four different parasite life history strategies. However, in contrast to many free‐living communities, network complexity decreased with host age. Examining parasite communities through the lens of succession may better inform the effect of complex within host eco‐evolutionary dynamics on infection outcomes, including parasite co‐existence through the lifetime of the host. 
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    Free, publicly-accessible full text available July 1, 2024
  10. Most vector control activities in urban areas are focused on household environments; however, information relating to infection risks in spaces other than households is poor, and the relative risk that these spaces represent has not yet been fully understood. We used data-driven simulations to investigate the importance of household and non-household environments for dengue entomological risk in two Kenyan cities where dengue circulation has been reported. Fieldwork was performed using four strategies that targeted different stages of mosquitoes: ovitraps, larval collections, Prokopack aspiration, and BG-sentinel traps. Data were analyzed separately between household and non-household environments to assess mosquito presence, the number of vectors collected, and the risk factors for vector presence. With these data, we simulated vector and human populations to estimate the parameter m and mosquito-to-human density in both household and non-household environments. Among the analyzed variables, the main difference was found in mosquito abundance, which was consistently higher in non-household environments in Kisumu but was similar in Ukunda. Risk factor analysis suggests that small, clean water-related containers serve as mosquito breeding places in households as opposed to the trash- and rainfall-related containers found in non-household structures. We found that the density of vectors (m) was higher in non-household than household environments in Kisumu and was also similar or slightly lower between both environments in Ukunda. These results suggest that because vectors are abundant, there is a potential risk of transmission in non-household environments; hence, vector control activities should take these spaces into account. 
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    Free, publicly-accessible full text available July 1, 2024