Opposing Patterns of Spatial Synchrony in Lyme Disease Incidence.

Incidence of Lyme disease, a tick-borne illness prevalent in the US, is increasing in endemic regions and regions with no previous history of the disease, significantly impacting public health. We examined space-time patterns of Lyme disease incidence and the influence of ecological and social factors on spatial synchrony, i.e., correlated incidence fluctuations across US counties. Specifically, we addressed these questions: Does Lyme disease incidence exhibit spatial synchrony? If so, what geographic patterns does Lyme disease synchrony exhibit? Are geographic patterns of disease synchrony related to weather, land cover, access to health care, or tick-borne disease awareness? How do effects of these variables on Lyme disease synchrony differ geographically? We used network analysis and matrix regression to examine geographical patterns of Lyme disease synchrony and their potential mechanisms in 399 counties in the eastern and Midwestern US. We found two distinct regions of synchrony in Northeast and upper Midwest regions exhibiting opposing temporal fluctuations in incidence. Spatial patterns of Lyme disease synchrony were partly explained by land cover, weather, poverty, and awareness of tick-borne illness, with significant predictive variables changing regionally. However, the two regions may have become more synchronous over time, potentially leading to higher-amplitude nation-wide fluctuations in disease incidence.

Cascading impacts of overstory structure in managed forests on understory structure, microclimate conditions, and Ixodes scapularis (Acari: Ixodidae) densities.

Forest management practices designed to meet varied landowner objectives affect wildlife habitat and may interrupt the life-cycle stages of disease vectors, including the black-legged tick, Ixodes scapularis Say (Acari: Ixodidae). Ixodes scapularis transmits multiple pathogens including Borrelia burgdorferi, the causative agent of Lyme disease, which is the most common tick-borne disease in the United States. There is evidence that a range of active forest management practices (e.g., invasive plant removal, prescribed burning) can alter tick densities and pathogen transmission. However, few studies have investigated relationships between forest stand structural variables commonly manipulated by timber harvesting and tick ecology. Foresters may harvest timber to create certain forest structural conditions like the mean number of trees, or basal area, per hectare. This study used a spatially replicated experiment in a blocked design to compare forest stands with a range of overstory structures and document variations in the midstory, understory, and forest floor, as well as microclimate conditions within tick off-host habitat. Greater numbers of trees or basal area per hectare correlated with greater canopy closure but less understory cover, stabilized microclimate temperature, higher microclimate humidity, and greater I. scapularis nymph densities. A random forest model identified understory forest structure as the strongest predictor of nymph densities. There was no relationship between the number of trees or basal area per hectare and daily deer (Odocoileus virginianus Zimmermann) activity or nymphal infection prevalence. These findings provide a deeper understanding of tick-habitat associations within a forest stand and have the potential to inform forest management decisions.

Ticks' attraction to electrically charged hosts.

Ticks are blood-feeding parasites with limited locomotion, known for transmitting multiple pathogens to vertebrates. England et al. suggest that ticks can be easily pulled, via electrostatic induction, toward charged hosts with fluffy coats that are prone to accumulate higher electrostatic potentials. Thus, static electricity may influence ticks' ecology and management.

Epidemic spread on patch networks with community structure.

Predicting and preparing for the trajectory of disease epidemics relies on a knowledge of environmental and socioeconomic factors that affect transmission rates on local and global spatial scales. This article discusses the simulation of epidemic outbreaks on human metapopulation networks with community structure, such as cities within national boundaries, for which infection rates vary both within and between communities. We demonstrate mathematically, through next-generation matrices, that the structures of these communities, setting aside all other considerations such as disease virulence and human decision-making, have a profound effect on the reproduction rate of the disease throughout the network. In high modularity networks, with high levels of separation between neighboring communities, disease epidemics tend to spread rapidly in high-risk communities and very slowly in others, whereas in low modularity networks, the epidemic spreads throughout the entire network as a steady pace, with little regard for variations in infection rate. The correlation between network modularity and effective reproduction number is stronger in population with high rates of human movement. This implies that the community structure, human diffusion rate, and disease reproduction number are all intertwined, and the relationships between them can be affected by mitigation strategies such as restricting movement between and within high-risk communities. We then test through numerical simulation the effectiveness of movement restriction and vaccination strategies in reducing the peak prevalence and spread area of outbreaks. Our results show that the effectiveness of these strategies depends on the structure of the network and the properties of the disease. For example, vaccination strategies are most effective in networks with high rates of diffusion, whereas movement restriction strategies are most effective in networks with high modularity and high infection rates. Finally, we offer guidance to epidemic modelers as to the ideal spatial resolution to balance accuracy and data collection costs.

A citizen science approach to investigate the distribution, abundance, and pathogen infection of vector ticks through active surveillance.

Tick-borne disease poses a growing public health burden in the United States and understanding the patterns of presence and density of infected vector ticks is key to developing and implementing effective public health management strategies. Citizen science has emerged as a highly effective means to generate data sets on the geographical distribution of tick species. But to date, nearly all citizen science studies of ticks are 'passive surveillance' programs in which researchers accept reports of ticks, together with either physical specimens or digital images, found opportunistically on people, pets, and livestock from community members for species identification and in some cases also tick-borne pathogen detection. These studies are limited because data are not collected systematically, making comparisons among locations and over time challenging, and introducing considerable reporting bias. In this study, we engaged citizen scientists in 'active surveillance' of host-seeking ticks, training volunteers to actively collect ticks on their woodland properties in an emergent region of tick-borne disease in the state of Maine, USA. We developed volunteer recruitment strategies, materials to train volunteers in data collection methods, field data collection protocols based on techniques used by professional scientists, and a variety of incentives to promote volunteer retention and satisfaction with their experiences, and we communicated research findings to participants. A total of 125 volunteers in 2020 and 181 volunteers in 2021 collected 7,246 ticks in southern and coastal Maine, including the American dog tick (Dermacentor variabilis, 4,023 specimens), the blacklegged tick (Ixodes scapularis, 3,092 specimens), and the rabbit tick (Haemaphysalis leporispalustris, 102 specimens). We demonstrated the feasibility of citizen scientists collecting ticks using active surveillance methods and found that volunteers were motivated to participate largely by their interest in the scientific problem and a desire to learn about ticks on their properties.

Patterns and Ecological Mechanisms of Tick-Borne Disease Exposure Risk in Acadia National Park, Mount Desert Island, Maine, United States.

National parks are unique and significant vector-borne pathogen transmission settings, engaging over 300 million people in outdoor recreation per year. In this study, we integrated vector surveys and ecological habitat feature data in spatial models to characterize tick-borne disease exposure risk in Acadia National Park (ANP), Maine. To determine the broad-scale patterns of blacklegged tick Ixodes scapularis Say (Acari: Ixodidae) densities in ANP, we conducted host-seeking tick collections at 114 sites across the park over two years. Using these tick survey data and geospatial landscape feature data (i.e., land cover, elevation, forest patch size, and aspect) we developed a random forest model of nymphal tick density. We found that host-seeking tick density varies significantly across the park and is particularly high in areas characterized by deciduous forest cover and relatively low elevation. To explore potential fine-scale ecological drivers of tick density spatial patterns, we quantified microclimate conditions, host activity, and vegetation characteristics at a subset of 19 sites. We identified significant differences in microclimate conditions but not host activity or vegetation metrics across broad-scale landscape feature classes. Mean temperature and mean humidity were correlated to nymphal densities and therefore may provide a mechanistic link between landscape features and blacklegged tick densities. Finally, we detected multiple tick-borne pathogens in both ticks and small mammals sampled in ANP, including Borrelia burgdorferi, Babesia microti, and Anaplasma phagocytophilum. Our findings demonstrate the value of using ecological metrics to estimate vector-borne disease exposure risk and provide insight into habitat characteristics that may drive tick-borne disease exposure risk.

Collaborative Modeling of the Tick-Borne Disease Social-Ecological System: A Conceptual Framework.

Hard-bodied ticks have become a major concern in temperate regions because they transmit a variety of pathogens of medical significance. Ticks and pathogens interact with hosts in a complex social-ecological system (SES) that influences human exposure to tick-borne diseases (TBD). We argue that addressing the urgent public health threat posed by TBD requires an understanding of the integrated processes in the forest ecosystem that influence tick density and infection prevalence, transmission among ticks, animal hosts, and ultimately disease prevalence in humans. We argue that collaborative modeling of the human-tick SES is required to understand the system dynamics as well as move science toward policy action. Recent studies in human health have shown the importance of stakeholder participation in understanding the factors that contribute to human exposure to zoonotic diseases. We discuss how collaborative modeling can be applied to understand the impacts of forest management practices on ticks and TBD. We discuss the potential of collaborative modeling for encouraging participation of diverse stakeholders in discussing the implications of managing forest ticks in the absence of large-scale control policy.

Microclimate conditions alter Ixodes scapularis (Acari: Ixodidae) overwinter survival across climate gradients in Maine, United States.

The incidence and geographic range of vector-borne diseases have been expanding in recent decades, attributed in part to global climate change. Blacklegged ticks (Ixodes scapularis), the primary vector for multiple tick-borne pathogens in North America, are spreading rapidly beyond their historic post-colonial range and are thought to be constrained mainly by winter temperature at northern latitudes. Our research explored whether winter climate currently limits the distribution of blacklegged ticks and the pathogens they transmit in Maine, U.S.A., by contributing to overwinter mortality of nymphs. We experimentally tested tick overwinter survival across large-scale temperature and snowfall gradients and assessed factors contributing to winter mortality in locations where blacklegged tick populations are currently established and locations where the blacklegged tick has not yet been detected. We also tested the hypothesis that insulation in the tick microhabitat (i.e., by leaf litter and snowpack) can facilitate winter survival of blacklegged tick nymphs despite inhospitable ambient conditions. Overwinter survival was not significantly different in coastal southern compared to coastal and inland northern Maine, most likely due to sufficient snowpack that protected against low ambient temperatures at high latitudes. Snow cover and leaf litter contributed significantly to overwinter survival at sites in both southern and northern Maine. To further assess whether the current distribution of blacklegged ticks in Maine aligns with patterns of overwinter survival, we systematically searched for and collected ticks at seven sites along latitudinal and coastal-inland climate gradients across the state. We found higher densities of blacklegged ticks in coastal southern Maine (90.2 ticks/1000 m2) than inland central Maine (17.8 ticks/1000 m2) and no blacklegged ticks in inland northern Maine. Our results suggest that overwinter survival is not the sole constraint on the blacklegged tick distribution even under extremely cold ambient conditions and additional mechanisms may limit the continued northward expansion of ticks.

Active Forest Management Reduces Blacklegged Tick and Tick-Borne Pathogen Exposure Risk.

In the northeastern USA, active forest management can include timber harvests designed to meet silvicultural objectives (i.e., harvesting trees that meet certain maturity, height, age, or quality criteria). Timber harvesting is an important tool in enhancing regeneration and maintaining forest health. It also has considerable potential to influence transmission dynamics of tick-borne pathogens, which are deeply embedded in the forest ecosystem. We conducted a 2-year study to test the hypotheses that recent timber harvesting impacts blacklegged tick density and infection prevalence in managed nonindustrial forests. We found that (1) recent harvesting reduces the presence of nymphal and density of adult blacklegged ticks, (2) recently harvested stands are characterized by understory microclimate conditions that may inhibit tick survival and host-seeking behavior, (3) capture rates of small mammal species frequently parasitized by immature ticks are lower in recently harvested stands compared to control stands with no recent harvest history. In addition, a 1-year pilot study suggests that harvesting does not affect nymphal infection prevalence. Collectively, our results demonstrate that forest structure and understory conditions may impact ticks and the pathogens they transmit via a range of mechanistic pathways, and moreover, active forest management may offer sustainable tools to inhibit entomological risk of exposure to tick-borne pathogens in the landscape.

Interactions between sympatric invasive European fire ants (Myrmica rubra) and blacklegged ticks (Ixodes scapularis).

The blacklegged tick (Ixodes scapularis) and the invasive European fire ant (Myrmica rubra) are both expanding throughout their sympatric range in coastal New England. Ixodes scapularis is the primary vector of the bacterium Borrelia burgdorferi, which is the causative agent of Lyme disease, and Mount Desert Island, Maine, home to Acadia National Park, currently is affected by a high Lyme disease burden. Ticks have many natural predators, including ants, although no previous studies have investigated interactions between these two species. To test the hypothesis that the presence of M. rubra alters I. scapularis abundance, we collected ticks by drag-sampling at eight ant-infested sites and eight uninfested control sites in Acadia National Park. We found that nymph density was significantly higher at ant-infested sites, while larval density was significantly higher at control sites. In addition, we conducted a laboratory bioassay to measure M. rubra aggression against I. scapularis larvae, nymphs, and adults and Dermacentor variabilis adults, and found that ant aggression was significantly higher against D. variabilis adults than I. scapularis adults. Our findings support the hypothesis that M. rubra has divergent effects across I. scapularis life stages, and we discuss possible ecological mechanisms, including optimal microclimate and predation, that could promote density of nymphs while inhibiting density of larvae.

Connectivity, reproduction number, and mobility interact to determine communities' epidemiological superspreader potential in a metapopulation network.

Disease epidemic outbreaks on human metapopulation networks are often driven by a small number of superspreader nodes, which are primarily responsible for spreading the disease throughout the network. Superspreader nodes typically are characterized either by their locations within the network, by their degree of connectivity and centrality, or by their habitat suitability for the disease, described by their reproduction number (R). Here we introduce a model that considers simultaneously the effects of network properties and R on superspreaders, as opposed to previous research which considered each factor separately. This type of model is applicable to diseases for which habitat suitability varies by climate or land cover, and for direct transmitted diseases for which population density and mitigation practices influences R. We present analytical models that quantify the superspreader capacity of a population node by two measures: probability-dependent superspreader capacity, the expected number of neighboring nodes to which the node in consideration will randomly spread the disease per epidemic generation, and time-dependent superspreader capacity, the rate at which the node spreads the disease to each of its neighbors. We validate our analytical models with a Monte Carlo analysis of repeated stochastic Susceptible-Infected-Recovered (SIR) simulations on randomly generated human population networks, and we use a random forest statistical model to relate superspreader risk to connectivity, R, centrality, clustering, and diffusion. We demonstrate that either degree of connectivity or R above a certain threshold are sufficient conditions for a node to have a moderate superspreader risk factor, but both are necessary for a node to have a high-risk factor. The statistical model presented in this article can be used to predict the location of superspreader events in future epidemics, and to predict the effectiveness of mitigation strategies that seek to reduce the value of R, alter host movements, or both.

A Generalized Additive Model Correlating Blacklegged Ticks With White-Tailed Deer Density, Temperature, and Humidity in Maine, USA, 1990-2013.

Geographical range expansions of blacklegged tick [Ixodes scapularis Say (Acari: Ixodidae)] populations over time in the United States have been attributed to a mosaic of factors including 20th century reforestation followed by suburbanization, burgeoning populations of the white-tailed deer [Odocoileus virginianus Zimmerman (Artiodactyla: Cervidae)], and, at the northern edge of I. scapularis' range, climate change. Maine, a high Lyme disease incidence state, has been experiencing warmer and shorter winter seasons, and relatively more so in its northern tier. Maine served as a case study to investigate the interacting impacts of deer and seasonal climatology on the spatial and temporal distribution of I. scapularis. A passive tick surveillance dataset indexed abundance of I. scapularis nymphs for the state, 1990-2013. With Maine's wildlife management districts as the spatial unit, we used a generalized additive model to assess linear and nonlinear relationships between I. scapularis nymph abundance and predictors. Nymph submission rate increased with increasing deer densities up to ~5 deer/km2 (13 deer/mi2), but beyond this threshold did not vary with deer density. This corroborated the idea of a saturating relationship between I. scapularis and deer density. Nymphs also were associated with warmer minimum winter temperatures, earlier degree-day accumulation, and higher relative humidity. However, nymph abundance only increased with warmer winters and degree-day accumulation where deer density exceeded ~2 deer/km2 (~6/mi2). Anticipated increases in I. scapularis in the northern tier could be partially mitigated through deer herd management.

Landscape features predict the current and forecast the future geographic spread of Lyme disease.

Lyme disease, the most prevalent vector-borne disease in North America, is increasing in incidence and geographic distribution as the tick vector, Ixodes scapularis, spreads to new regions. We re-construct the spatial-temporal invasion of the tick and human disease in the Midwestern US, a major focus of Lyme disease transmission, from 1967 to 2018, to analyse the influence of spatial factors on the geographic spread. A regression model indicates that three spatial factors-proximity to a previously invaded county, forest cover and adjacency to a river-collectively predict tick occurrence. Validation of the predictive capability of this model correctly predicts counties invaded or uninvaded with 90.6% and 98.5% accuracy, respectively. Reported incidence increases in counties after the first report of the tick; based on this modelled relationship, we identify 31 counties where we suspect I. scapularis already occurs yet remains undetected. Finally, we apply the model to forecast tick establishment by 2021 and predict 42 additional counties where I. scapularis will probably be detected based upon historical drivers of geographic spread. Our findings leverage resources dedicated to tick and human disease reporting and provide the opportunity to take proactive steps (e.g. educational efforts) to prevent and limit transmission in areas of future geographic spread.

Production of Culex pipiens in Stormwater and Combined Sewer Catch Basins.

Man-made stormwater and sewage infrastructure, particularly roadside catch basins, provides widespread habitats for immature mosquitoes in urban and suburban environments. Historically, throughout much of the USA, stormwater, sewage, and industrial wastewater were conducted together through "combined" sewer systems, discharging a combination of stormwater and wastewater into streams. Within recent decades, many cities have replaced these combined sewers with "stormwater only" systems that separate stormwater from wastewater. The objective of this research was to evaluate the implications of this infrastructure conversion for production of Culex pipiens, a primary vector for West Nile virus. On a weekly basis over 14 wk, 20 catch basins (10 combined sewer and 10 stormwater only) were sampled for mosquito larvae and emerging adults using the dipping collection method and floating emergence traps. Abundance of larval Cx. pipiens was higher in combined sewer compared with stormwater-only catch basins, while to the contrary, abundance of adult Cx. pipiens was lower in combined sewer compared with stormwater-only catch basins. This study is the first to reveal that habitat attractiveness and quality for Cx. pipiens may vary between combined sewer and stormwater-only catch basins, and our results contribute to a growing body of research to inform vector management and urban planning efforts as municipalities consider the environmental and public health implications of conversion from combined sewage management to separation of stormwater and wastewater.

Fatal attraction: lone star ticks (Amblyomma americanum) exhibit preference for human female breath over male breath.

Ticks use a variety of chemical cues to locate hosts, the main cue being carbon dioxide, which is exhaled by hosts. This study sought to experimentally determine whether ticks exhibit preference among human hosts based on host sex, as the chemical components of human male and female breath have been shown to differ. We focused on the lone star tick, Amblyomma americanum, due to its importance as a disease vector in the United States and its active host-seeking behavior. To test the hypothesis that ticks exhibit preference based upon host sex, we conducted a binary choice behavioral bioassay. Male and female human volunteers (n = 20 pairs) breathed into opposite sides of a secured polycarbonate tube containing 10 adult A. americanum and the proportion of ticks that exhibited a host preference was recorded. We found that under controlled conditions, human females attract a significantly larger proportion of ticks than males. Possible mechanisms to explain these results include that (1) female breath contains components that ticks find attractive, and/or (2) male breath contains a repellent chemical component.

Container Size Alters the Outcome of Interspecific Competition Between Aedes aegypti (Diptera: Culicidae) and Aedes albopictus.

Aedes aegypti L. and Aedes albopictus Skuse co-occur in a variety of water-filled containers where they compete for resources. Larvae of Ae. albopictus Skuse often outcompete those of Ae. aegypti L., but variation in biotic and abiotic parameters can modify the outcome of this interspecific competition. We tested whether container size can alter the magnitude and direction of intra- and interspecific competition by rearing three Ae. aegypti and Ae. albopictus larval combinations (100:0, 50:50 and 0:100) in three container sizes (small, medium, and large). For both mosquito species, individuals raised in small- and medium-sized containers had shorter development time to adulthood, higher survival to adulthood, and larger adult body size compared to individuals from large containers. For Ae. aegypti but not Ae. albopictus, survival to adulthood was significantly influenced by a two-way interaction between container size and larval competition. The negative effect of interspecific competition was stronger in the small and medium containers and the negative effect of intraspecific competition was stronger in large containers. Our results show that container size can affect the outcome of intra- and interspecific competition between Ae. aegypti and Ae. albopictus and may help account for the observed patterns of both competitive exclusion and coexistence documented in the field for these two medically important mosquito species.

Discovery and exploitation of a natural ecological trap for a mosquito disease vector.

Ecological traps occur due to a mismatch between a habitat's attractiveness and quality, wherein organisms show preference for low-quality habitats over other available high-quality habitats. Our previous research identified leaf litter from common blackberry (Rubus allegheniensis) as a natural ecological trap for an important vector for West Nile virus (Culex pipiens), attracting mosquitoes to oviposit in habitats deleterious to the survival of their larvae. Here we demonstrate that manipulation of leaf litter in stormwater catch basins, an important source of disease vector mosquitoes in urban environments, can increase Cx. pipiens oviposition but reduce survival. In a series of experiments designed to elucidate the mechanisms that explain the attractive and lethal properties of this native plant, behavioural bioassays suggest that oviposition site selection by Cx. pipiens is mediated primarily by chemical cues as leaves decompose. However, we also show that juvenile mosquito survival is mainly related to the suitability of the bacterial community in the aquatic habitat for mosquito nutritional needs, which does not appear to create a cue that influences oviposition choice. This mismatch between oviposition cues and drivers of larval habitat quality may account for the ecological trap phenomenon detected in this study. Our findings provide new insights into potential mechanistic pathways by which ecological traps may occur in nature and proof-of-concept for a new 'attract-and-kill' tool for mosquito control.

Large-Scale Removal of Invasive Honeysuckle Decreases Mosquito and Avian Host Abundance.

Invasive species rank second only to habitat destruction as a threat to native biodiversity. One consequence of biological invasions is altered risk of exposure to infectious diseases in human and animal populations. The distribution and prevalence of mosquito-borne diseases depend on the complex interactions between the vector, the pathogen, and the human or wildlife reservoir host. These interactions are highly susceptible to disturbance by invasive species, including terrestrial plants. We conducted a 2-year field experiment using a Before-After/Control-Impact design to examine how removal of invasive Amur honeysuckle (Lonicera maackii) in a forest fragment embedded within a residential neighborhood affects the abundance of mosquitoes, including two of the most important vectors of West Nile virus, Culex pipiens and Cx. restuans. We also assessed any potential changes in avian communities and local microclimate associated with Amur honeysuckle removal. We found that (1) removal of Amur honeysuckle reduces the abundance of both vector and non-vector mosquito species that commonly feed on human hosts, (2) the abundance and composition of avian hosts is altered by honeysuckle removal, and (3) areas invaded with honeysuckle support local microclimates that are favorable to mosquito survival. Collectively, our investigations demonstrate the role of a highly invasive understory shrub in determining the abundance and distribution of mosquitoes and suggest potential mechanisms underlying this pattern. Our results also give rise to additional questions regarding the general impact of invasive plants on vector-borne diseases and the spatial scale at which removal of invasive plants may be utilized to effect disease control.

Impact of an Alien Invasive Shrub on Ecology of Native and Alien Invasive Mosquito Species (Diptera: Culicidae).

We examined how leaf litter of alien invasive honeysuckle (Lonicera maackii Rupr.) either alone or in combination with leaf litter of one of two native tree species, sugar maple (Acer saccharum Marshall) and northern red oak (Quercus rubra L.), affects the ecology of Culex restuans Theobald, Ochlerotatus triseriatus Say, and Ochlerotatus japonicus Theobald. Experimental mesocosms containing single species litter or a mixture of honeysuckle and one of two native tree species litter were established at South Farms and Trelease Woods study sites in Urbana, IL, and examined for their effect on 1) oviposition site selection by the three mosquito species, and 2) adult production and body size of Oc. triseriatus and Oc. japonicus. There were no significant effects of study site and leaf treatment on Oc. japonicus and Oc. triseriatus oviposition preference and adult production. In contrast, significantly more Cx. restuans eggs rafts were collected at South Farms relative to Trelease Woods and in honeysuckle litter relative to native tree species litter. Significantly larger adult females of Oc. japonicus and Oc. triseriatus were collected at South Farms relative to Trelease Woods and in honeysuckle litter relative to native tree species litter. Combining honeysuckle litter with native tree species litter had additive effects on Cx. restuans oviposition preference and Oc. japonicus and Oc. triseriatus body size, with the exception of honeysuckle and northern red oak litter combination, which had antagonistic effects on Oc. triseriatus body size. We conclude that input of honeysuckle litter into container aquatic habitats may alter the life history traits of vector mosquito species.

Asymmetric effects of native and exotic invasive shrubs on ecology of the West Nile virus vector Culex pipiens (Diptera: Culicidae).

BACKGROUND: Exotic invasive plants alter the structure and function of native ecosystems and may influence the distribution and abundance of arthropod disease vectors by modifying habitat quality. This study investigated how invasive plants alter the ecology of Culex pipiens, an important vector of West Nile virus (WNV) in northeastern and midwestern regions of the United States. METHODS: Field and laboratory experiments were conducted to test the hypothesis that three native leaf species (Rubus allegheniensis, blackberry; Sambucus canadensis, elderberry; and Amelanchier laevis, serviceberry), and three exotic invasive leaf species (Lonicera maackii, Amur honeysuckle; Elaeagnus umbellata, autumn olive; and Rosa multiflora, multiflora rose) alter Cx. pipiens oviposition site selection, emergence rates, development time, and adult body size. The relative abundance of seven bacterial phyla in infusions of the six leaf species also was determined using quantitative real-time polymerase chain reaction to test the hypothesis that variation in emergence, development, and oviposition site selection is correlated to differences in the diversity and abundance of bacteria associated with different leaf species, important determinants of nutrient quality and availability for mosquito larvae. RESULTS: Leaf detritus from invasive honeysuckle and autumn olive yielded significantly higher adult emergence rates compared to detritus from the remaining leaf species and honeysuckle alleviated the negative effects of intraspecific competition on adult emergence. Conversely, leaves of native blackberry acted as an ecological trap, generating high oviposition but low emergence rates. Variation in bacterial flora associated with different leaf species may explain this asymmetrical production of mosquitoes: emergence rates and oviposition rates were positively correlated to bacterial abundance and diversity, respectively. CONCLUSIONS: We conclude that the displacement of native understory plant species by certain invasive shrubs may increase production of Cx. pipiens with potential negative repercussions for human and wildlife health. These findings may be relevant to mosquito control and invasive plant management practices in the geographic range of Cx. pipiens. Further, our discovery of a previously unknown ecological trap for an important vector of WNV has the potential to lead to novel alternatives to conventional insecticides in mosquito control by exploiting the apparent "attract-kill" properties of this native plant species.