Autochthonous Chikungunya Transmission and Extreme Climate Events in Southern France

BackgroundExtreme precipitation events are increasing as a result of ongoing global warming, but controversy surrounds the relationship between flooding and mosquito-borne diseases. A common view among the scientific community and public health officers is that heavy rainfalls have a flushing effect on breeding sites, which negatively affects vector populations, thereby diminishing disease transmission. During 2014 in Montpellier, France, there were at least 11 autochthonous cases of chikungunya caused by the invasive tiger mosquito Aedes albopictus in the vicinity of an imported case. We show that an extreme rainfall event increased and extended the abundance of the disease vector Ae. albopictus, hence the period of autochthonous transmission of chikungunya.Conclusions/SignificanceOur empirical data suggests that heavy rainfall events did increase the risk of arbovirus transmission in Southern France in 2014 by favouring a rapid rise in abundance of vector mosquitoes. Further studies should now confirm these results in different ecological contexts, so that the impact of global change and extreme climatic events on mosquito population dynamics and the risk of disease transmission can be adequately understood.     

Strategies for introducing Wolbachia to reduce transmission of mosquito-borne diseases

Certain strains of the endosymbiont Wolbachia have the potential to lower the vectorial capacity of mosquito populations and assist in controlling a number of mosquito-borne diseases. An important consideration when introducing Wolbachia-carrying mosquitoes into natural populations is the minimisation of any transient increase in disease risk or biting nuisance. This may be achieved by predominantly releasing male mosquitoes. To explore this, we use a sex-structured model of Wolbachia-mosquito interactions. We first show that Wolbachia spread can be initiated with very few infected females provided the infection frequency in males exceeds a threshold. We then consider realistic introduction scenarios involving the release of batches of infected mosquitoes, incorporating seasonal fluctuations in population size. For a range of assumptions about mosquito population dynamics we find that male-biased releases allow the infection to spread after the introduction of low numbers of females, many fewer than with equal sex-ratio releases. We extend the model to estimate the transmission rate of a mosquito-borne pathogen over the course of Wolbachia establishment. For a range of release strategies we demonstrate that male-biased release of Wolbachia-infected mosquitoes can cause substantial transmission reductions without transiently increasing disease risk. The results show the importance of including mosquito population dynamics in studying Wolbachia spread and that male-biased releases can be an effective and safe way of rapidly establishing the symbiont in mosquito populations.     

Assessment of the Impact of Climate Shifts on Malaria Transmission in the Sahel

Climate affects malaria transmission through a complex network of causative pathways. We seek to evaluate the impact of hypothetical climate change scenarios on malaria transmission in the Sahel by using a novel mechanistic, high spatial- and temporal-resolution coupled hydrology and agent-based entomology model. The hydrology model component resolves individual precipitation events and individual breeding pools. The impact of future potential climate shifts on the representative Sahel village of Banizoumbou, Niger, is estimated by forcing the model of Banizoumbou environment with meteorological data from two locations along the north–south climatological gradient observed in the Sahel—both for warmer, drier scenarios from the north and cooler, wetter scenarios from the south. These shifts in climate represent hypothetical but historically realistic climate change scenarios. For Banizoumbou climatic conditions (latitude 13.54 N), a shift toward cooler, wetter conditions may dramatically increase mosquito abundance; however, our modeling results indicate that the increased malaria transmissibility is not simply proportional to the precipitation increase. The cooler, wetter conditions increase the length of the sporogonic cycle, dampening a large vectorial capacity increase otherwise brought about by increased mosquito survival and greater overall abundance. Furthermore, simulations varying rainfall event frequency demonstrate the importance of precipitation patterns, rather than simply average or time-integrated precipitation, as a controlling factor of these dynamics. Modeling results suggest that in addition to changes in temperature and total precipitation, changes in rainfall patterns are very important to predict changes in disease susceptibility resulting from climate shifts. The combined effect of these climate-shift–induced perturbations can be represented with the aid of a detailed mechanistic model.     

Mathematical modelling of mosquito dispersal in a heterogeneous environment

Mosquito dispersal is a key behavioural factor that affects the persistence and resurgence of several vector-borne diseases. Spatial heterogeneity of mosquito resources, such as hosts and breeding sites, affects mosquito dispersal behaviour and consequently affects mosquito population structures, human exposure to vectors, and the ability to control disease transmission. In this paper, we develop and simulate a discrete-space continuous-time mathematical model to investigate the impact of dispersal and heterogeneous distribution of resources on the distribution and dynamics of mosquito populations. We build an ordinary differential equation model of the mosquito life cycle and replicate it across a hexagonal grid (multi-patch system) that represents two-dimensional space. We use the model to estimate mosquito dispersal distances and to evaluate the effect of spatial repellents as a vector control strategy. We find evidence of association between heterogeneity, dispersal, spatial distribution of resources, and mosquito population dynamics. Random distribution of repellents reduces the distance moved by mosquitoes, offering a promising strategy for disease control.     

Combining hydrology and mosquito population models to identify the drivers of rift valley Fever emergence in semi-arid regions of west Africa

Background

Rift Valley fever (RVF) is a vector-borne viral zoonosis of increasing global importance. RVF virus (RVFV) is transmitted either through exposure to infected animals or through bites from different species of infected mosquitoes, mainly of Aedes and Culex genera. These mosquitoes are very sensitive to environmental conditions, which may determine their presence, biology, and abundance. In East Africa, RVF outbreaks are known to be closely associated with heavy rainfall events, unlike in the semi-arid regions of West Africa where the drivers of RVF emergence remain poorly understood. The assumed importance of temporary ponds and rainfall temporal distribution therefore needs to be investigated.

Methodology/Principal Findings

A hydrological model is combined with a mosquito population model to predict the abundance of the two main mosquito species (Aedes vexans and Culex poicilipes) involved in RVFV transmission in Senegal. The study area is an agropastoral zone located in the Ferlo Valley, characterized by a dense network of temporary water ponds which constitute mosquito breeding sites.The hydrological model uses daily rainfall as input to simulate variations of pond surface areas. The mosquito population model is mechanistic, considers both aquatic and adult stages and is driven by pond dynamics. Once validated using hydrological and entomological field data, the model was used to simulate the abundance dynamics of the two mosquito species over a 43-year period (1961–2003). We analysed the predicted dynamics of mosquito populations with regards to the years of main outbreaks. The results showed that the main RVF outbreaks occurred during years with simultaneous high abundances of both species.

Conclusion/Significance

Our study provides for the first time a mechanistic insight on RVFV transmission in West Africa. It highlights the complementary roles of Aedes vexans and Culex poicilipes mosquitoes in virus transmission, and recommends the identification of rainfall patterns favourable for RVFV amplification.     

Mosquito-bite infection of humanized mice with chikungunya virus produces systemic disease with long-term effects

Chikungunya virus (CHIKV) is an emerging, mosquito-borne alphavirus responsible for acute to chronic arthralgias and neuropathies. Although it originated in central Africa, recent reports of disease have come from many parts of the world, including the Americas. While limiting human CHIKV cases through mosquito control has been used, it has not been entirely successful. There are currently no licensed vaccines or treatments specific for CHIKV disease, thus more work is needed to develop effective countermeasures. Current animal research on CHIKV is often not representative of human disease. Most models use CHIKV needle inoculation via unnatural routes to create immediate viremia and localized clinical signs; these methods neglect the natural route of transmission (the mosquito vector bite) and the associated human immune response. Since mosquito saliva has been shown to have a profound effect on viral pathogenesis, we evaluated a novel model of infection that included the natural vector, Aedes species mosquitoes, transmitting CHIKV to mice containing components of the human immune system. Humanized mice infected by 3–6 mosquito bites showed signs of systemic infection, with demonstrable viremia (by qRT-PCR and immunofluorescent antibody assay), mild to moderate clinical signs (by observation, histology, and immunohistochemistry), and immune responses consistent with human infection (by flow cytometry and IgM ELISA). This model should give a better understanding of human CHIKV disease and allow for more realistic evaluations of mechanisms of pathogenesis, prophylaxis, and treatments.     

Mosquito Population Regulation and Larval Source Management in Heterogeneous Environments

An important question for mosquito population dynamics, mosquito-borne pathogen transmission and vector control is how mosquito populations are regulated. Here we develop simple models with heterogeneity in egg laying patterns and in the responses of larval populations to crowding in aquatic habitats. We use the models to evaluate how such heterogeneity affects mosquito population regulation and the effects of larval source management (LSM). We revisit the notion of a carrying capacity and show how heterogeneity changes our understanding of density dependence and the outcome of LSM. Crowding in and productivity of aquatic habitats is highly uneven unless egg-laying distributions are fine-tuned to match the distribution of habitats’ carrying capacities. LSM reduces mosquito population density linearly with coverage if adult mosquitoes avoid laying eggs in treated habitats, but quadratically if eggs are laid in treated habitats and the effort is therefore wasted (i.e., treating 50% of habitat reduces mosquito density by approximately 75%). Unsurprisingly, targeting (i.e. treating a subset of the most productive pools) gives much larger reductions for similar coverage, but with poor targeting, increasing coverage could increase adult mosquito population densities if eggs are laid in higher capacity habitats. Our analysis suggests that, in some contexts, LSM models that accounts for heterogeneity in production of adult mosquitoes provide theoretical support for pursuing mosquito-borne disease prevention through strategic and repeated application of modern larvicides.     

Heavy rainfall increases nestling mortality of an arctic top predator: experimental evidence and long-term trend in peregrine falcons

Although animal population dynamics have often been correlated with fluctuations in precipitation, causal relationships have rarely been demonstrated in wild birds. We combined nest observations with a field experiment to investigate the direct effect of rainfall on survival of peregrine falcon (Falco peregrinus) nestlings in the Canadian Arctic. We then used historical data to evaluate if recent changes in the precipitation regime could explain the long-term decline of falcon annual productivity. Rainfall directly caused more than one-third of the recorded nestling mortalities. Juveniles were especially affected by heavy rainstorms (≥8 mm/day). Nestlings sheltered from rainfall by a nest box had significantly higher survival rates. We found that the increase in the frequency of heavy rain over the last three decades is likely an important factor explaining the recent decline in falcon nestling survival rates, and hence the decrease in annual breeding productivity of the population. Our study is among the first experimental demonstrations of the direct link between rainfall and survival in wild birds, and clearly indicates that top arctic predators can be significantly impacted by changes in precipitation regime.     

Soil water balance and ecosystem response to climate change

Some essential features of the terrestrial hydrologic cycle and ecosystem response are singled out by confronting empirical observations of the soil water balance of different ecosystems with the results of a stochastic model of soil moisture dynamics. The simplified framework analytically describes how hydroclimatic variability (especially the frequency and amount of rainfall events) concurs with soil and plant characteristics in producing the soil moisture dynamics that in turn impact vegetation conditions. The results of the model extend and help interpret the classical curve of Budyko, which relates evapotranspiration losses to a dryness index, describing the partitioning of precipitation into evapotranspiration, runoff, and deep infiltration. They also provide a general classification of soil water balance of the world ecosystems based on two governing dimensionless groups summarizing the climate, soil, and vegetation conditions. The subsequent analysis of the links among soil moisture dynamics, plant water stress, and carbon assimilation offers an interpretation of recent manipulative field experiments on ecosystem response to shifts in the rainfall regime, showing that plant carbon assimilation crucially depends not only on the total rainfall during the growing season but also on the intermittency and magnitude of the rainfall events.     

Follow up estimation of Aedes aegypti entomological parameters and mathematical modellings

The dengue virus is a vector-borne disease transmitted by mosquito Aedes aegypti and the incidence is strongly influenced by temperature and humidity which vary seasonally. To assess the effects of temperature on dengue transmission, mathematical models are developed based on the population dynamics theory. However, depending on the hypotheses of the modelling, different outcomes regarding to the risk of epidemics are obtained. We address this question comparing two simple models supplied with model's parameters estimated from temperature-controlled experiments, especially the entomological parameters regarded to the mosquito's life cycle in different temperatures. Once obtained the mortality and transition rates of different stages comprising the life cycle of mosquito and the oviposition rate, we compare the capacity of vector reproduction (the basic offspring number) and the risk of infection (basic reproduction number) provided by two models. The extended model, which is more realistic, showed that both mosquito population and dengue risk are situated at higher values than the simplified model, even that the basic offspring number is lower.     

Backward Bifurcation and Optimal Control in Transmission Dynamics of West Nile Virus

The paper considers a deterministic model for the transmission dynamics of West Nile virus (WNV) in the mosquito-bird-human zoonotic cycle. The model, which incorporates density-dependent contact rates between the mosquito population and the hosts (birds and humans), is rigorously analyzed using dynamical systems techniques and theories. These analyses reveal the existence of the phenomenon of backward bifurcation (where the stable disease-free equilibrium of the model co-exists with a stable endemic equilibrium when the reproduction number of the disease is less than unity) in WNV transmission dynamics. The epidemiological consequence of backward bifurcation is that the classical requirement of having the reproduction number less than unity, while necessary, is no longer sufficient for WNV elimination from the population. It is further shown that the model with constant contact rates can also exhibit this phenomenon if the WNV-induced mortality in the avian population is high enough. The model is extended to assess the impact of some anti-WNV control measures, by re-formulating the model as an optimal control problem with density-dependent demographic parameters. This entails the use of two control functions, one for mosquito-reduction strategies and the other for personal (human) protection, and redefining the demographic parameters as density-dependent rates. Appropriate optimal control methods are used to characterize the optimal levels of the two controls. Numerical simulations of the optimal control problem, using a set of reasonable parameter values, suggest that mosquito reduction controls should be emphasized ahead of personal protection measures.     

Modeled response of the West Nile virus vector Culex quinquefasciatus to changing climate using the dynamic mosquito simulation model

Climate can strongly influence the population dynamics of disease vectors and is consequently a key component of disease ecology. Future climate change and variability may alter the location and seasonality of many disease vectors, possibly increasing the risk of disease transmission to humans. The mosquito species Culex quinquefasciatus is a concern across the southern United States because of its role as a West Nile virus vector and its affinity for urban environments. Using established relationships between atmospheric variables (temperature and precipitation) and mosquito development, we have created the Dynamic Mosquito Simulation Model (DyMSiM) to simulate Cx. quinquefasciatus population dynamics. The model is driven with climate data and validated against mosquito count data from Pasco County, Florida and Coachella Valley, California. Using 1-week and 2-week filters, mosquito trap data are reproduced well by the model (P < 0.0001). Dry environments in southern California produce different mosquito population trends than moist locations in Florida. Florida and California mosquito populations are generally temperature-limited in winter. In California, locations are water-limited through much of the year. Using future climate projection data generated by the National Center for Atmospheric Research CCSM3 general circulation model, we applied temperature and precipitation offsets to the climate data at each location to evaluate mosquito population sensitivity to possible future climate conditions. We found that temperature and precipitation shifts act interdependently to cause remarkable changes in modeled mosquito population dynamics. Impacts include a summer population decline from drying in California due to loss of immature mosquito habitats, and in Florida a decrease in late-season mosquito populations due to drier late summer conditions.     

Heterogeneity,Mixing, and the Spatial Scales of Mosquito-Borne Pathogen Transmission

The Ross-Macdonald model has dominated theory for mosquito-borne pathogen transmission dynamics and control for over a century. The model, like many other basic population models, makes the mathematically convenient assumption that populations are well mixed; i.e., that each mosquito is equally likely to bite any vertebrate host. This assumption raises questions about the validity and utility of current theory because it is in conflict with preponderant empirical evidence that transmission is heterogeneous. Here, we propose a new dynamic framework that is realistic enough to describe biological causes of heterogeneous transmission of mosquito-borne pathogens of humans, yet tractable enough to provide a basis for developing and improving general theory. The framework is based on the ecological context of mosquito blood meals and the fine-scale movements of individual mosquitoes and human hosts that give rise to heterogeneous transmission. Using this framework, we describe pathogen dispersion in terms of individual-level analogues of two classical quantities: vectorial capacity and the basic reproductive number, . Importantly, this framework explicitly accounts for three key components of overall heterogeneity in transmission: heterogeneous exposure, poor mixing, and finite host numbers. Using these tools, we propose two ways of characterizing the spatial scales of transmission—pathogen dispersion kernels and the evenness of mixing across scales of aggregation—and demonstrate the consequences of a model''s choice of spatial scale for epidemic dynamics and for estimation of , both by a priori model formulas and by inference of the force of infection from time-series data.     

Response of a Mediterranean semiarid community to changing patterns of water supply

Climate change may cause profound effects on terrestrial ecosystems. Changes in rainfall patterns may have large effects on a wide range of biological processes such as seed germination, seedling establishment, plant growth, community composition, and population and community dynamics. Climate change models for the Mediterranean region forecast reduced annual precipitation and more extreme rain events (i.e., fewer rainy days and longer drought periods between rainfall events), along with seasonal changes. We experimentally addressed the response of a semiarid Mediterranean community to higher aridity and changes in seasonal rainfall patterns in two glasshouse experiments in which we manipulated water supply. We simulated a delay in the onset of autumn rainfalls (i.e., a longer summer drought period), decreased watering amount and frequency as predicted by climate models, and manipulated the seasonality of water supply. We found that delayed watering led to decreases in plant community productivity and to delays in flowering time, in terms of both date and number of days of water supply. Decreased watering amount and frequency, and accentuated seasonality, also diminished biomass and individuals recruited, but did not change flower phenology. Species diversity was not affected by watering delays; however, it was reduced by changes in frequency, amount and seasonality. Overall, these data underline the need to consider rainfall patterns as an important element that might alter community dynamics and ecosystem structure and functioning. Therefore, the analysis of climate change consequences must not depend on climatic means-based scenarios but must take into account expected seasonal changes in rainfall quantity and frequency.     

Assessing the suitability for Aedes albopictus and dengue transmission risk in China with a delay differential equation model

Dengue is considered non-endemic to mainland China. However, travellers frequently import the virus from overseas and local mosquito species can then spread the disease in the population. As a consequence, mainland China still experiences large dengue outbreaks. Temperature plays a key role in these outbreaks: it affects the development and survival of the vector and the replication rate of the virus. To better understand its implication in the transmission risk of dengue, we developed a delay differential equation model that explicitly simulates temperature-dependent development periods and tested it with collected field data for the Asian tiger mosquito, Aedes albopictus. The model predicts mosquito occurrence locations with a high accuracy (Cohen’s κ of 0.78) and realistically replicates mosquito population dynamics. Analysing the infection dynamics during the 2014 dengue outbreak that occurred in Guangzhou showed that the outbreak could have lasted for another four weeks if mosquito control interventions had not been undertaken. Finally, we analyse the dengue transmission risk in mainland China. We find that southern China, including Guangzhou, can have more than seven months of dengue transmission per year while even Beijing, in the temperate north, can have dengue transmission during hot summer months. The results demonstrate the importance of using detailed vector and infection ecology, especially when vector-borne disease transmission risk is modelled over a broad range of climatic zones.     

Impact of Land-use Change on Dengue and Malaria in Northern Thailand

Land-use change, a major constituent of global environmental change, potentially has significant consequences for human health in relation to mosquito-borne diseases. Land-use change can influence mosquito habitat, and therefore the distribution and abundance of vectors, and land use mediates human–mosquito interactions, including biting rate. Based on a conceptual model linking the landscape, people, and mosquitoes, this interdisciplinary study focused on the impacts of changes in land use on dengue and malaria vectors and dengue transmission in northern Thailand. Extensive data on mosquito presence and abundance, land-use change, and infection risk determinants were collected over 3 years. The results of the different components of the study were then integrated through a set of equations linking land use to disease via mosquito abundance. The impacts of a number of plausible scenarios for future land-use changes in the region, and of concomitant behavioral change were assessed. Results indicated that land-use changes have a detectable impact on mosquito populations and on infection. This impact varies according to the local environment but can be counteracted by adoption of preventive measures.     

Predicting the Timing and Magnitude of Tropical Mosquito Population Peaks for Maximizing Control Efficiency

The transmission of mosquito-borne diseases is strongly linked to the abundance of the host vector. Identifying the environmental and biological precursors which herald the onset of peaks in mosquito abundance would give health and land-use managers the capacity to predict the timing and distribution of the most efficient and cost-effective mosquito control. We analysed a 15-year time series of monthly abundance of Aedes vigilax, a tropical mosquito species from northern Australia, to determine periodicity and drivers of population peaks (high-density outbreaks). Two sets of density-dependent models were used to examine the correlation between mosquito abundance peaks and the environmental drivers of peaks or troughs (low-density periods). The seasonal peaks of reproduction (r) and abundance () occur at the beginning of September and early November, respectively. The combination of low mosquito abundance and a low frequency of a high tide exceeding 7 m in the previous low-abundance (trough) period were the most parsimonious predictors of a peak''s magnitude, with this model explaining over 50% of the deviance in . Model weights, estimated using AIC_c, were also relatively high for those including monthly maximum tide height, monthly accumulated tide height or total rainfall per month in the trough, with high values in the trough correlating negatively with the onset of a high-abundance peak. These findings illustrate that basic environmental monitoring data can be coupled with relatively simple density feedback models to predict the timing and magnitude of mosquito abundance peaks. Decision-makers can use these methods to determine optimal levels of control (i.e., least-cost measures yielding the largest decline in mosquito abundance) and so reduce the risk of disease outbreaks in human populations.     

A statistical model of Rift Valley fever activity in Egypt

Rift Valley fever (RVF) is a viral disease of animals and humans and a global public health concern due to its ecological plasticity, adaptivity, and potential for spread to countries with a temperate climate. In many places, outbreaks are episodic and linked to climatic, hydrologic, and socioeconomic factors. Although outbreaks of RVF have occurred in Egypt since 1977, attempts to identify risk factors have been limited. Using a statistical learning approach (lasso‐regularized generalized linear model), we tested the hypotheses that outbreaks in Egypt are linked to (1) River Nile conditions that create a mosquito vector habitat, (2) entomologic conditions favorable to transmission, (3) socio‐economic factors (Islamic festival of Greater Bairam), and (4) recent history of transmission activity. Evidence was found for effects of rainfall and river discharge and recent history of transmission activity. There was no evidence for an effect of Greater Bairam. The model predicted RVF activity correctly in 351 of 358 months (98.0%). This is the first study to statistically identify risk factors for RVF outbreaks in a region of unstable transmission.     

Weather variability impacts on oviposition dynamics of the southern house mosquito at intermediate time scales

Oviposition is a major event in the life history of mosquitoes, shaping both individual fitness and vectorial capacity. Several exogenous factors have been shown as important for the dynamic forcing of oviposition at finely (hourly) and coarsely (monthly or season to season) grained temporal scales. However, field studies addressing the interplay of weather factors on oviposition dynamics at the intermediate (days to weeks) time scale are missing. Here, we present the results from a field study that showed the oviposition dynamics of the southern house mosquito, Culex quinquefasciatus Say (Diptera: Culicidae), to be: (i) primarily dictated by relative humidity; and (ii) disrupted by rainfall events that resulted in a modified sensitivity to relative humidity. Rainfall changed the concentration of ammonia, a major limiting resource of microbes used as food by mosquito larvae. Following major rainfall events, the importance of relative humidity in forcing the oviposition dynamics also changed. Finally, our results indicate that qualitative changes in oviposition habitats modify the importance of weather variables as predictors of mosquito oviposition dynamics.     

Rainfall triggered dynamics of Aedes mosquito aggressiveness

Inspired by Davidson method of estimating daily survivals of a structureless population of mosquitoes, we present a model which describes the behavior of floodwater mosquitoes in terms of emergence functions following a rainfall event, blood feeding frequency and parous stages, and survival at various stages. As a generalization of the Davidson formula, we have developed an approach for dealing with the dynamics of structured population of mosquitoes, and derived various formulas allowing assessment of demographic parameters like durations of gonotrophic cycles and (apparent) daily survivals. The method was subsequently applied to field data of floodwater mosquitoes Aedes vexans arabiensis, potential vectors of Rift Valley fever in West Africa, collected during the 2003 rainy season in Barkedji, Senegal. We found that mosquitoes emerged about 3 to 4 days following an efficient rainfall, and mosquito emergences, described by a bell shaped function, lasted for about 2 days. The mean duration of the gonotrophic cycle was 3 days and the apparent daily survival about 0.87.