Vector-borne pathogens, such as Malaria, Dengue, West Nile and Zika virus, infect hundreds of millions of people each year and lead to widespread human morbidity and mortality, with enormous spatial and temporal variation in disease risk. The recent emergence of West Nile virus (WNV) into the developed world offers a unique opportunity to better understand ecological drivers that contribute to variation in disease risk, as a step toward more effective disease management through targeted interventions. In Chapter 1, we examined correlations between rice cultivation and WNV human disease incidence in rice-growing regions within the United States (US). We found WNV human disease incidence increased with the fraction of each county under rice cultivation in California, but not in the southern US. We show that this is likely due to regional differences in the mosquitoes transmitting WNV. These results illustrate how cultivation of particularly water-demanding agricultural crops can increase mosquito-borne disease risk and how spatial variation in vector ecology can alter the relationship between land cover and disease. In Chapter 2, we examined the effect of irrigation, climate and land cover on mosquito abundance and WNV human disease cases across California. Irrigation made up nearly a third of total water inputs to the region, with irrigation exceeding precipitation in some dry regions. Irrigation reduced seasonal variability in mosquito abundance by more than 40%, and increased abundance by more than an order of magnitude. In addition, irrigation increased human WNV cases and explained 33% of variation in WNV cases among California counties. These results suggest that irrigation can increase and decouple mosquito populations from natural precipitation variability, resulting in sustained and increased disease risk. In Chapter 3, we quantified the risk of WNV transmission to humans from 6 Culex mosquito species by integrating mosquito abundance, infection prevalence, vector competence, and blood feeding patterns, and examined correlations between risk indices and human disease cases. Human WNV cases were strongly correlated with the density of infectious vectors feeding on humans. However, different mosquito vector species contributed to transmission in different land use types and within seasons and across years. Culex tarsalis was more abundant in agricultural areas, whereas Culex pipiens and Culex quinquefasciatus were abundant in developed and agricultural areas, and Culex erythrothorax was abundant in wetland areas. As a result, WNV risk did not change substantially along either agricultural or urbanization land use gradients because the diversity of vectors maintained high disease risk across a range of habitats. These results show how a diversity of vectors can maintain an ecosystem disservice - vector borne disease – by their differential response to environmental disturbance.

Native biodiversity loss and the introduction of exotic species have caused substantial changes in community composition of local communities, with unknown effects on pathogen transmission. Avian malaria (Plasmodium relictum) has driven population declines in native Hawaiian birds, but the role of native and introduced bird species in transmission is poorly understood. Transmission may differ in communities composed primarily of introduced birds compared to communities with natives because natives mount high parasitemia and may have longer-lived infections relative to introduced birds. My dissertation applies fieldwork and molecular tools to investigate the effect of host community composition and land use on malaria transmission in lowland forests on Hawaii Island. In my first chapter, I explore the influence of host community composition on infection prevalence in Culex quinquefasciatus, the primary vector of avian malaria in Hawaii, and examine the reciprocal effect of transmission on the Hawaii amakihi, Chlorodrepanis virens. I found that prevalence in mosquitoes increased with native bird density. Transmission intensity depressed population growth rates of amakihi, but were projected to be above 1 even if incidence was 100%. These results suggest that native birds increase disease transmission, likely because of increased host competence in native compared to introduced birds. In my second chapter, I investigated feeding patterns of Cx. quinquefasciatus and avian malaria infection patterns. I found that Cx. quinquefasciatus fed almost exclusively on birds, with most blood meals coming from Japanese white-eye, Zosterops japonicus, suggesting that ornithophilic feeding by Cx. quinquefasciatus facilitates avian malaria transmission. In my third chapter, I examined land use, larval habitat, and climate drivers of Cx. quinquefasciatus, and another vector species, Aedes albopictus. I found that both species were positively correlated with the proportion of surrounding developed land and the availability of larval habitat, which were themselves positively correlated. These results suggest that conversion of natural habitats to residential and agricultural land may increase larval habitats, with implications for avian malaria transmission in developed areas. This work provides insight into native bird recovery in Hawaii, and underscores the importance of host community composition and land use on the transmission of multi-host vector-borne pathogens.

Transmission of vector-borne disease is driven by contact rates between vectors and hosts. However, little is known about what drives fine-scale variation in mosquito host seeking behavior and the resulting consequences for contact patterns between mosquitoes and their hosts. We examined the roosting behavior of seven avian hosts of West Nile virus (WNV) and patterns of mosquito abundance among communal roost and non-communal roost sites and at different heights where birds roosted. We found some variation in roosting height among avian species coupled with increases in host-seeking mosquito densities higher in the canopy suggesting avian species experience differing vector contact rates influenced by their preferred roosting height. Prior research suggests host-seeking mosquito abundance increase with host group size, however in contrast to a priori predictions, we found significantly fewer host-seeking Culex mosquitoes at American robin communal roosts than non-communal roost sites, and far lower per capita biting mosquitoes and vector-host ratios at roost sites. Focusing specifically on American robins, the preferred host of Culex mosquitoes, our results suggest communal roosting behavior may reduce mosquito-biting rates on roosting individuals. Changes in American robin roosting behavior may partly explain previously observed seasonal changes in feeding patterns of Culex mosquitoes, which has direct implications for the transmission of WNV among birds and humans.

Emerging infectious diseases present a major threat to wildlife populations and have the ability to drive once common species towards extinction. Increasing globalization has resulted in accelerated change in climate, increased anthropogenic movement, and land-use alterations leading to the emergence of infectious diseases in both humans, agriculture and wildlife. Studying disease dynamics at different contexts and scales can provide insight into alternative levers of conservation action. White-nose syndrome, a disease of hibernating bats, was first detected in single tourist cave in northern New York. Pseudogymnoascus destructans the fungal pathogen responsible for WNS has since spread across much of eastern North America causing the collapse of hibernating bat populations. P. destructans was likely introduced to North America from Eurasia, where it is widely distributed, and has likely been present for thousands of years. The data in this dissertation provide insight into the factors determining temporal variation in mortality from WNS. In addition, we will also provide insight into the mechanisms that contribute to species differences in pathogen transmission. More broadly this research provides a synthesis of data across multiple WNS disease contexts, and highlight the substantial conservation insight that can be gained through this approach.

Emerging infectious diseases can place severe pressures on wildlife populations, leading to major population declines, local extirpation, and species extinctions. However, variability in disease impacts, existing among species and across a spatial and temporal scale, can help us identify species or populations persisting with disease either via resistance, tolerance, pathogen evasion, or by existing within environmental refugia. Understanding mechanisms leading to host persistence can inform conservation management priorities and strategies. White-nose Syndrome (WNS) is a recently emerged disease caused by the fungal pathogen, Pseudogymnoascus destructans (Pd), that has led to severe declines in hibernating bat populations in North America. This work examines patterns and mechanisms associated with variability in WNS impacts with implications for the conservation of affected species. My first chapter investigates spatial heterogeneity in initial impacts of Pd spread across half of continental North America. We found that WNS-related impacts were lessened in the southwestern regions of North America, suggesting potential spatial refugia from WNS-related impacts but only for Perimyotis subflavus. We found that annual air surface temperatures driving Pd growth explained, in part, this spatial variation in WNS-related impacts. Despite evidence for lessened WNS-related declines in the southwest, impacts to bat populations are severe throughout North America for most bat species. My second chapter examines colonies of M. lucifugus that have experienced variability in declines over time, persisting potentially due to host-specific responses. Specifically, I investigate if differences in early winter fat reserves could explain survivorship and persistence of M. lucifugus colonies with WNS. We found that bats persisting with WNS in 2016 were significantly fatter than bats colonies sampled during WNS arrival in 2008 and 2009 at four out of our six sampled sites. At another two sites, we found that bats were either fatter in 2008 and 2009 compared to 2016. We used hibernation energetic models to estimate the amount of fat afforded to survival and found that increased fat reserves from bats measured in 2016 could reduce mortality by 65%. These data suggest that increased fat reserves can explain, in part, the persistence of M. lucifugus colonies with WNS. Lastly, my third chapter experimentally investigates one possible cause of variability in WNS impacts, variation host susceptibility via protective bacteria in the skin microbiome. In this chapter, I explore the efficacy of using a probiotic bacterium, harvested from the skin of a species experiencing lessened WNS impacts, Eptesicus fuscus, as a conservation tool applied to a more highly affected bat species, M. lucifugus. We found relative increases in survival for probiotic-treated groups compared to our sham control group. We also found evidence for decreased fungal infection and severity in probiotic-treated groups. Our results suggest that probiotic treatment can reduce incidence of White-nose Syndrome in M. lucifugus although timing of treatment is an important factor. Together, this work finds that variability in spatial, species-specific, and temporal impacts from WNS can inform conservation efforts. Namely, this work suggests that bat conservation should involve a multi-pronged approach that protects colonies where bats are persisting with WNS via habitat restoration, and potentially treating bats for threatened populations not persisting with WNS. Given the continued threat of WNS to bats as it spreads throughout North America, using a variety of tools to combat this disease may be critical to prevent disease-induced extinction and the local extirpation of affected bat species.

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