Vulnerability of Southern Hemisphere bats to white-nose syndrome based on global analysis of fungal host specificity and cave temperatures

Abstract

White-nose syndrome (WNS), a disease affecting hibernating bats, is caused by the fungal pathogen Pseudogymnoascus destructans (Pd). Since the initial introduction of Pd from Eurasia to the United States in 2006, WNS has killed millions of bats throughout the temperate parts of North America. There is concern that if Pd is accidentally introduced to the Southern Hemisphere, WNS could pose similar threats to the bat fauna of the Southern Hemisphere's more temperate regions. Efforts are required to better understand the vulnerability of bats globally to WNS. We examined phylogenetic distances among cave roosting bat species globally to estimate the probability of infection by Pd. We predicted cave thermal suitability for Pd for 441 cave-roosting bat species across the globe via spatial analysis. We used host specificity models based on 65 species tested for Pd to determine phylogenetic specificity of Pd. Phylogenetic distance was not an important predictor of Pd infection, confirming that Pd has low host specificity. We found extensive areas (i.e., South America, Africa, and Australia) in the Southern Hemisphere with caves that were suitable for cave-roosting bat species and for Pd growth. Hence, if Pd spreads to the Southern Hemisphere, the risk of exposure is widespread for cave-roosting bats, and infection is possible regardless of relatedness to infected species in the Northern Hemisphere. Predicting the consequences of infection remains difficult due to lack of species-specific information about bat winter biology. Nevertheless, WNS is an important threat to naive Southern Hemisphere bat populations. Hence, biosecurity measures and planning of management responses that can help prevent or minimize a potential WNS outbreak in the Southern Hemisphere are urgently needed.

Keywords: Chiroptera; Pseudogymnoascus destructans; disease; enfermedad; hibernación; hibernation; ingenuidad ecológica; vulnerabilidad; vulnerability ecological naivety.

FIGURE 1

Phylogenetic reconstruction of 782 bat species from Shi and Rabosky (2015) (branches, color grouped by family; solid branches, suborder Yangochiroptera; dashed branches, suborder Yinpterochiroptera; inner first ring, hemisphere in which bats occur; second ring, whether species roosts primarily in caves; third ring, whether winter hibernation has been studied for this species in the wild; outer forth ring, whether the species has been tested and recorded as positive for Pd [red] or as negative for Pd [gray]; outer lines circling tree, 6 most diverse bat families). Bat silhouettes for families obtained from PhyloPic 2.0 (https://www.phylopic.org/).

FIGURE 2

(a) Probability of host bat species being detected with Pseudogymnoascus destructans (Pd) based on current sampling effort in North America and Eurasia, where Pd occurs, as a function of phylogenetic distance between species, based on the 65 species that have been tested to date (curved line, main effect predicted from logistic regressions with coefficients in millions of years [my]); (b) probability of host bat species developing white‐nose syndrome (WNS) as a function of phylogenetic distance between species; (c) phylogenetic relationship of species tested for Pd in Eurasia and North America (yellow, species from North America; purple, species from Eurasia; pink, species detected with Pd; gray, species negative for Pd; dark pink, species known to develop WNS; red, species with known populations declining from WNS); and (d) base 10 logarithm of mean Pd load (ng/mm) sampled from bat species (color gradient represents Pd load intensity).

FIGURE 3

Spatial distribution of cave‐roosting bat species richness in areas with thermal conditions suitable for growth of the fungal pathogen Pseudogymnoascus destructans (Pd), which causes white‐nose syndrome, based on mean annual (a) surface temperature or (b) surface temperature adjusted for effect of distance to the cave entrance (50–100 m) (horizontal dashed line, equator).