Landscape structure and ecology influence the spread of a bat fungal disease

Abstract

Abstract1. White-nose syndrome (WNS), affecting multiple North American bat species during the hibernation period, is a highly pathogenic disease caused by the psychrophilic fungus Pseudogymnoascus destructans (Pd). Because the fungal pathogen persists in the hibernation site environment independently of the hosts, previous theory on spatial disease dynamics cannot predict WNS epidemics. However, the ability to understand factors contributing to the spread of white-nose syndrome (WNS) in North America is crucial to the management of infected and susceptible bat populations as well as the conservation of threatened and endangered bat species.2. Utilizing recent theory on environmental opportunistic pathogens, we modelled the effect of (a) landscape clustering, (b) environmental conditions in hibernacula and (c) microbial competition on the spread of WNS. We used available, already published data to construct and parameterize our model, which takes into account the spatial distribution of hibernation sites, temperature conditions in both the outside ambient and hibernation site environment, bat population dynamics, dispersal and infection by the pathogen, which also has its host-independent dynamics with the environment. We also consider the effect of outside-host competition between the pathogen and other micro-organisms on spatial disease dynamics. 3. Our model suggests that pathogen loads accumulate in poorly connected hibernacula at short host dispersal, which can help found the epidemic. In contrast, invasion of the landscape is most successful at long host dispersal distances, with homogenous hibernation site distribution and heterogeneous between-hibernation site temperatures. Also, increasing the mean temperature across hibernacula increases fungal growth rate, leading to higher disease prevalence and faster invasion rate. Increasing spatial heterogeneity in hibernaculum temperatures results in the formation of disease hotspots in warmer hibernacula, facilitating more effective spread of the disease in the landscape. Cold-adapted competing microbes can prevent invasion, and therefore, overwintering in cold hibernacula increases probability of host survival.4. Sites that were suboptimal for overwintering prior to WNS may have importance in preventing local extirpations. Although the model is tailored for WNS, due to

Population connectivity predicts vulnerability to white-nose syndrome in the Chilean myotis (Myotis chiloensis) - a genomics approach

“…The results highlight the importance to assess the population structure which may limit the spread of white-nose syndrome disease. Whether P. destructans or another epizootic in the future could spread depends largely on the population structure and connectedness of hosts (Lilley et al . 2018).…”

Genome-Wide Changes in Genetic Diversity in a Population of Myotis lucifugus Affected by White-Nose Syndrome

“…For instance, during the hibernation period, when the bat hosts are most vulnerable to the pathogen, roost microclimate variables, including humidity and temperature, affect the growth of the fungal pathogen and the survival of the host (Verant et al 2012;Johnson et al 2014;Grieneisen et al 2015;Marroquin et al 2017), and behavioral shifts in roost site selection by bat hosts since the onset of WNS (Johnson et al 2016) could favor energy conservation while reducing fungal growth and infection. Modelling also suggests that environmental factors, including the cave microbiome, have an impact on the proliferation and infectivity of P. destructans (Hayman, Pulliam, Marshall, Cryan, & Webb, 2016;Lilley et al, 2018). This is supported by the discovery of microbes in hibernacula environments and on bats that are able to retard the growth of the fungus (Zhang et al 2014(Zhang et al , 2015Micalizzi et al 2017).…”

“…In light of our results and considering bat life history as a whole, adaptation and evolutionary rescue may not be a fast track for recovery of bat populations affected by WNS (Maslo and Fefferman 2015), although ultimately these will contribute to long term survival of populations (Lilley et al 2019). At the present, therefore, it is more likely that behavioral shifts in selection of hibernation sites that vary in environmental conditions and strong selection for microbial taxa that inhibit P. destructans could explain why some colonies have persisted or may have even begun to recover from the zoonosis (Cheng et al 2016;Johnson et al 2016;Lemieux-Labonté et al 2017;Lilley et al 2018).…”

Population Connectivity Predicts Vulnerability to White-Nose Syndrome in the Chilean Myotis (Myotis chiloensis) - A Genomics Approach

“…The results highlight the importance to assess the population structure which may limit the spread of white-nose syndrome disease. Whether P. destructans or another epizootic in the future could spread depends largely on the population structure and connectedness of hosts (Lilley et al 2018). the work.…”