Intraspecific drivers of variation in bat responses to white-nose syndrome and implications for population persistence and management

Abstract

Emerging infectious diseases of wildlife are among the greatest threats to biodiversity. Indeed, when pathogens are introduced into naïve host populations, they can impose novel selective pressures that may cause severe host declines or even extinction. However, disease impacts may vary both within and among host species. Thus, one of the key goals for management is to identify factors that drive variation in host susceptibility to infection, as they may improve our understanding of hosts' potential to develop disease resistance and/or tolerance and inform conservation strategies aimed at facilitating host persistence. For instance, Pseudogymnoascus destructans (Pd) - an invasive pathogenic fungus that causes white-nose syndrome (WNS) in hibernating bats - is highly virulent, has killed millions of bats in North America, and continues to spread at an alarming rate. Yet, the continued persistence of bat colonies in contaminated areas despite initial mass mortality events suggests variation in survival among infected individuals. I thus aimed to better understand intraspecific drivers of variation in bat susceptibility to WNS and their implications for population persistence and management in affected areas. Specifically, my objectives were to: 1) evaluate the extent to which variation in hibernaculum microclimate temperature and humidity affects Pd infection severity and disease progression in affected bats during hibernation, 2) compare how bats from colonies that vary in duration of exposure to Pd and from different age classes behaviorally respond to the infection, and examine how these behavioral changes affect host fitness and 3) model the population dynamics of remnant bat populations to assess the likeliness of persistence and the potential effectiveness of management interventions in affected colonies. I addressed these objectives through field research, experimental infection studies, and demographic modeling of the little brown myotis (Myotis lucifugus). In my dissertation, I first provide causal evidence of environmentally-driven variation in pathogen growth and infection severity on bats in the field. Both warmer and more humid microclimates contribute to the severity of the infection by promoting the production of conidia, the erosion of wing tissues, and, therefore, the transmission potential and virulence of Pd. I then document potential mechanistic links between Pd-induced behavioral change and host fitness. Higher infection levels, independent of bats' past exposure to Pd or age class, may cause individuals to groom longer, prolong euthermic arousals, accelerate the depletion of fat reserves, and ultimately increase mortality risk. Finally, I predict that populations will face a high risk of extirpation in the next decade or two if no management action is taken, but that interventions such as environmental control of Pd and hibernaculum microclimate manipulation can prevent short-term population collapse in remnant bat populations. Together, these studies provide key, mechanistic insight into the pathology of WNS and the probability of persistence of affected bat colonies, while highlighting the importance of prioritizing winter habitat preservation and enhancement for the conservation of hibernating bats.