Environmental and geographical factors influence the occurrence and abundance of the southern house mosquito, Culex quinquefasciatus, in Hawai'i.

Hawaiian honeycreepers, a group of endemic Hawaiian forest birds, are being threatened by avian malaria, a non-native disease that is driving honeycreepers populations to extinction. Avian malaria is caused by the parasite Plasmodium relictum, which is transmitted by the invasive mosquito Culex quinquefasciatus. Environmental and geographical factors play an important role in shaping mosquito-borne disease transmission dynamics through their influence on the distribution and abundance of mosquitoes. We assessed the effects of environmental (temperature, precipitation), geographic (site, elevation, distance to anthropogenic features), and trap type (CDC light trap, CDC gravid trap) factors on mosquito occurrence and abundance. Occurrence was analyzed using classification and regression tree models (CART) and generalized linear models (GLM); abundance (count data) was analyzed using generalized linear mixed models (GLMMs). Models predicted highest mosquito occurrence at mid-elevation sites and between July and November. Occurrence increased with temperature and precipitation up to 580 mm. For abundance, the best model was a zero-inflated negative-binomial model that indicated higher abundance of mosquitoes at mid-elevation sites and peak abundance between August and October. Estimation of occurrence and abundance as well as understanding the factors that influence them are key for mosquito control, which may reduce the risk of forest bird extinction.

Assessing the Efficiency of Local Rabies Vaccination Strategies for Raccoons (Procyon lotor) in an Urban Setting.

Raccoon rabies virus (RRV) has been managed using multiple vaccination strategies, including oral rabies vaccination and trap-vaccinate-release (TVR). Identifying a rabies vaccination strategy for an area is a nontrivial task. Vaccination strategies differ in the amount of effort and monetary costs required to achieve a particular level of vaccine seroprevalence (efficiency). Simulating host movement relative to different vaccination strategies in silico can provide a useful tool for exploring the efficiency of different vaccination strategies. We refined a previously developed individual-based model of raccoon movement to evaluate vaccination strategies for urban Hamilton, Ontario, Canada. We combined different oral rabies vaccination baiting (hand baiting, helicopter, and bait stations) with TVR strategies and used GPS data to parameterize and simulate raccoon movement in Hamilton. We developed a total of 560 vaccination strategies, in consultation with the Ontario Ministry of Natural Resources and Forestry, for RRV control in Hamilton. We documented the monetary costs of each vaccination strategy and estimated the population seroprevalence. Intervention costs and seroprevalence estimates were used to calculate the efficiency of each strategy to meet targets set for the purpose of RRV control. Estimated seroprevalence across different strategies varied widely, ranging from less than 5% to more than 70%. Increasing bait densities (distributed using by hand or helicopter) led to negligible increase in seroprevalence. Helicopter baiting was the most efficient and TVR was the least efficient, but helicopter-based strategies led to lower levels of seroprevalence (6-12%) than did TVR-based strategies (17-70%). Our simulations indicated that a mixed strategy including at least some TVR may be the most efficient strategy for a local urban RRV control program when seroprevalence levels >30% may be required. Our simulations provide information regarding the efficiency of different vaccination strategies for raccoon populations, to guide local RRV control in urban settings.

Accounting for animal movement improves vaccination strategies against wildlife disease in heterogeneous landscapes.

Oral baiting is used to deliver vaccines to wildlife to prevent, control, and eliminate infectious diseases. A central challenge is how to spatially distribute baits to maximize encounters by target animal populations, particularly in urban and suburban areas where wildlife such as raccoons (Procyon lotor) are abundant and baits are delivered along roads. Methods from movement ecology that quantify movement and habitat selection could help to optimize baiting strategies by more effectively targeting wildlife populations across space. We developed a spatially explicit, individual-based model of raccoon movement and oral rabies vaccine seroconversion to examine whether and when baiting strategies that match raccoon movement patterns perform better than currently used baiting strategies in an oral rabies vaccination zone in greater Burlington, Vermont, USA. Habitat selection patterns estimated from locally radio-collared raccoons were used to parameterize movement simulations. We then used our simulations to estimate raccoon population rabies seroprevalence under currently used baiting strategies (actual baiting) relative to habitat selection-based baiting strategies (habitat baiting). We conducted simulations on the Burlington landscape and artificial landscapes that varied in heterogeneity relative to Burlington in the proportion and patch size of preferred habitats. We found that the benefits of habitat baiting strongly depended on the magnitude and variability of raccoon habitat selection and the degree of landscape heterogeneity within the baiting area. Habitat baiting improved seroprevalence over actual baiting for raccoons characterized as habitat specialists but not for raccoons that displayed weak habitat selection similar to radiocollared individuals, except when baits were delivered off roads where preferred habitat coverage and complexity was more pronounced. In contrast, in artificial landscapes with either more strongly juxtaposed favored habitats and/or higher proportions of favored habitats, habitat baiting performed better than actual baiting, even when raccoons displayed weak habitat preferences and where baiting was constrained to roads. Our results suggest that habitat selection-based baiting could increase raccoon population seroprevalence in urban-suburban areas, where practical, given the heterogeneity and availability of preferred habitat types in those areas. Our novel simulation approach provides a flexible framework to test alternative baiting strategies in multiclass landscapes to optimize bait-distribution strategies.

The role of native and introduced birds in transmission of avian malaria in Hawaii.

The introduction of nonnative species and reductions in native biodiversity have resulted in substantial changes in vector and host communities globally, but the consequences for pathogen transmission are poorly understood. In lowland Hawaii, bird communities are composed of primarily introduced species, with scattered populations of abundant native species. We examined the influence of avian host community composition, specifically the role of native and introduced species, as well as host diversity, on the prevalence of avian malaria (Plasmodium relictum) in the southern house mosquito (Culex quinquefasciatus). We also explored the reciprocal effect of malaria transmission on native host populations and demography. Avian malaria infection prevalence in mosquitoes increased with the density and relative abundance of native birds, as well as host community competence, but was uncorrelated with host diversity. Avian malaria transmission was estimated to reduce population growth rates of Hawai'i 'amakihi (Chlorodrepanis virens) by 7-14%, but mortality from malaria could not explain gaps in this species' distribution at our sites. Our results suggest that, in Hawaii, native host species increase pathogen transmission to mosquitoes, but introduced species can also support malaria transmission alone. The increase in pathogen transmission with native bird abundance leads to additional disease mortality in native birds, further increasing disease impacts in an ecological feedback cycle. In addition, vector abundance was higher at sites without native birds and this overwhelmed the effects of host community composition on transmission such that infected mosquito abundance was highest at sites without native birds. Higher disease risk at these sites due to higher vector abundance could inhibit recolonization and recovery of native species to these areas. More broadly, this work shows how differences in host competence for a pathogen among native and introduced taxa can influence transmission and highlights the need to examine this question in other systems to determine the generality of this result.

Variation in host home range size decreases rabies vaccination effectiveness by increasing the spatial spread of rabies virus.

Animal movement influences the spatial spread of directly transmitted wildlife disease through host-host contact structure. Wildlife disease hosts vary in home range-associated foraging and social behaviours, which may increase the spread and intensity of disease outbreaks. The consequences of variation in host home range movement and space use on wildlife disease dynamics are poorly understood, but could help to predict disease spread and determine more effective disease management strategies. We developed a spatially explicit individual-based model to examine the effect of spatiotemporal variation in host home range size on the spatial spread rate, persistence and incidence of rabies virus (RABV) in raccoons (Procyon lotor). We tested the hypothesis that variation in home range size increases RABV spread and decreases vaccination effectiveness in host populations following pathogen invasion into a vaccination zone. We simulated raccoon demography and RABV dynamics across a range of magnitudes and variances in weekly home range size for raccoons. We examined how variable home range size influenced the relative effectiveness of three components of oral rabies vaccination (ORV) programmes targeting raccoons-timing and frequency of bait delivery, width of the ORV zone and proportion of hosts immunized. Variability in weekly home range size increased RABV spread rates by 1.2-fold to 5.2-fold compared to simulations that assumed a fixed home range size. More variable host home range sizes decreased relative vaccination effectiveness by 71% compared to less variable host home range sizes under conventional vaccination conditions. We found that vaccination timing was more influential for vaccination effectiveness than vaccination frequency or vaccination zone width. Our results suggest that variation in wildlife home range movement behaviour increases the spatial spread and incidence of RABV. Our vaccination results underscore the importance of prioritizing individual-level space use and movement data collection to understand wildlife disease dynamics and plan their effective control and elimination.

Per- and polyfluoroalkyl substances in two different populations of northern cardinals.

The northern cardinal (Cardinalis cardinalis) is a good indicator species for environmental contaminants because it does not migrate and its range covers a diversity of habitats, including metropolitan Atlanta, GA and the geographically isolated Hawaiian Islands. In addition, the cardinal is often found near people's homes, making it likely to be exposed to the same outdoor elements, including soil, groundwater, and air, that surrounding humans experience. In this study, blood serum concentrations of 12 per- and polyfluoroalkyl substances (PFASs) were measured in 40 cardinals from Atlanta and 17 cardinals from the Big Island (Hawaii), HI. We observed significantly higher median concentrations of four PFASs and significantly higher detection frequencies of seven PFASs in the cardinals from Atlanta, relative to the PFAS median concentrations and detection frequencies observed in the cardinals from Hawaii (α = 0.05). Among the PFASs measured, perfluorooctane sulfonate (PFOS) was observed in the highest concentrations. A linear regression model controlling for sex, age, and airport distance did not explain PFOS variation within the Atlanta samples, but a similar model explained 90% of PFOS variation within the Hawaii samples. To our knowledge, these are the first measurements of PFASs in northern cardinals.

Land Use and Larval Habitat Increase Aedes albopictus (Diptera: Culicidae) and Culex quinquefasciatus (Diptera: Culicidae) Abundance in Lowland Hawaii.

Vector abundance plays a key role in transmission of mosquito-borne disease. In Hawaii, Aedes albopictus (Skuse) (Diptera: Culicidae), the Asian tiger mosquito, has been implicated in locally-transmitted dengue outbreaks, while Culex quinquefasciatus Say (Diptera: Culicidae), the southern house mosquito, is the primary vector of avian malaria, a wildlife disease that has contributed to declines and extinctions of native Hawaiian birds. Despite the importance of these introduced species to human and wildlife health, little is known about the local-scale drivers that shape mosquito abundance across lowland Hawaii, where forest, agricultural, and residential land uses are prevalent. We examined landscape, larval habitat, and climate drivers of Ae. albopictus and Cx. quinquefasciatus abundance in eight lowland wet forest fragments on the Big Island of Hawaii. We found that the abundance of both species increased with the proportion of surrounding developed land and the availability of larval habitat, which were themselves correlated. Our findings suggest that conversion of natural habitats to residential and agricultural land increases mosquito larval habitats, increasing the abundance of Ae. albopictus and Cx. quinquefasciatus and increasing disease risk to humans and wildlife in Hawaii. Our results further indicate that while source reduction of artificial larval habitats-particularly moderately-sized human-made habitats including abandoned cars and tires-could reduce mosquito abundance, eliminating larval habitat will be challenging because both species utilize both natural and human-made larval habitats in lowland Hawaii.

From superspreaders to disease hotspots: linking transmission across hosts and space.

Since the identification and imprisonment of "Typhoid Mary," a woman who infected at least 47 people with typhoid in the early 1900s, epidemiologists have recognized that 'superspreading' hosts play a key role in disease epidemics. Such variability in transmission also exists among species within a community (amplification hosts) and among habitat patches across a landscape (disease 'hotspots'), underscoring the need for an integrative framework for studying transmission heterogeneity. Here, we synthesize literature on human, plant, and animal diseases to evaluate the relative contributions of host, pathogen, and environmental factors in driving transmission heterogeneity across hosts and space. We show that host and spatial heterogeneity are closely linked and that quantitatively assessing the contribution of infectious individuals, species, or environmental patches to overall transmission can aid management strategies. We conclude by posing hypotheses regarding how pathogen natural history influences transmission heterogeneity and highlight emerging frontiers in the study of transmission heterogeneity.