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.

Full text

Received: 9 October 2023 Revised: 2 April 2024 Accepted: 15 July 2024
DOI: 10.1111/cobi.14390
CONTRIBUTED PAPER
Vulnerability of Southern Hemisphere bats to white-nose
syndrome based on global analysis of fungal host specificity and
cave temperatures
Nicholas C. Wu1Justin A. Welbergen1Tomás Villada-Cadavid1
Lindy F. Lumsden2Christopher Turbill1,3
1Hawkesbury Institute for the Environment,
Western Sydney University, Richmond, New South
Wales, Australia
2Department of Energy, Environment and Climate
Action, Arthur Rylah Institute for Environmental
Research, Heidelberg, Victoria, Australia
3School of Science, Western Sydney University,
Richmond, New South Wales, Australia
Correspondence
Nicholas C. Wu, Hawkesbury Institute for the
Environment, Western Sydney University, Science
Rd, Richmond NSW 2753, Australia. Email:
nicholas.wu.nz@gmail.com
Article impact statement: White-nose syndrome, a
global threat to bats, has the potential to spread to
the Southern Hemisphere, requiring urgent
biosecurity action.
Funding information
Australian Research Council, Grant/Award
Number: LP200100331
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 temper-
ate 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 South-
ern 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 suit-
able 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 pos-
sible regardless of relatedness to infected species in the Northern Hemisphere. Predicting
the consequences of infection remains difficult due to lack of species-specific informa-
tion 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, disease, hibernation, Pseudogymnoascus destructans, vulnerability ecological naivety
INTRODUCTION
Emerging infectious diseases are a growing threat for biodiver-
sity worldwide (Daszak et al., 2000; Jones et al., 2008; Tompkins
et al., 2015), primarily due to climate change and an increase
in global transportation and human movement (Altizer et al.,
2013; Banks et al., 2015; Cavicchioli et al., 2019; Lafferty, 2009).
Given the negative ecological and socioeconomic repercussions
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is
properly cited.
© 2024 The Author(s). Conservation Biology published by Wiley Periodicals LLC on behalf of Society for Conservation Biology.
of emerging infectious diseases (Lafferty et al., 2015; Scheele
et al., 2019), it is crucial to predict the likely exposure and
sensitivity of populations to the global spread of pathogens
(Daszak et al., 2000; Lips et al., 2006), particularly because novel
pathogens can have severe impacts on evolutionarily naive hosts
(Frick et al., 2010; Hulcr & Dunn, 2011). Attempts to make such
predictions are important for identifying and prioritizing biose-
curity, research, and management efforts to mitigate the risk of
Conservation Biology. 2025;39:e14390. wileyonlinelibrary.com/journal/cobi 1of11
https://doi.org/10.1111/cobi.14390

CONSERVATION BIOLOGY 2of11
emerging infectious diseases before arrival, when they are most
effective (Langwig et al., 2015).
White-nose syndrome (WNS) is a disease of hibernating bats
caused by the fungal pathogen Pseudogymnoascus destructans (Pd)
and is of particular interest due to its recent invasion from Eura-
sia and rapid spread across North America (Frick et al., 2010;
Warnecke et al., 2012). It is responsible for the death of mil-
lions of cave-roosting insectivorous bats since its introduction
in 2006 to North America; some populations have declined
by >90% (Cheng et al., 2021; Frick et al., 2017). To date, Pd
has not been detected in the countries sampled in the South-
ern Hemisphere (i.e., Australia and Chile) (Holz et al., 2018;
Lilley et al., 2020), likely indicating Pd has yet to cross the equa-
tor. The accidental introduction of Pd to bat communities in
the Southern Hemisphere that are naive to this pathogen could
have serious ecological, evolutionary, and economic implica-
tions (Faulkner et al., 2020; Pyšek et al., 2020). This is because
the Southern Hemisphere hosts a diverse range of bat species,
endemism of cave-roosting bats in the Austral-Oceania region is
high (Tanalgo et al., 2022), and some species act as agricultural
pest controls (Bouarakia et al., 2023). An expert risk assess-
ment undertaken in Australia in late 2016 concluded that it was
likely that Pd would be accidently introduced into an Australian
cave within the next 10 years (Holz et al., 2019), and accidental
introduction is similarly likely or more likely in South America
and Africa given their proximity to Pd spread by humans and
migrating bats from North America and Eurasia, respectively.
Therefore, determining where Pd is likely to spread and how it
may affect local bat species in the Southern Hemisphere is of
global conversation priority.
Predicting the vulnerability of naive bat populations to Pd
infection is challenging because information on the key fac-
tors that influence their sensitivity to the pathogen is lacking.
These factors include overwintering behavior and hibernation
patterns, metabolic physiology, immune function, diversity of
cutaneous microbiomes and their response to Pd infection, as
well as knowledge about spatial distribution of cave habitats
and other factors that determine exposure to Pd (Fritze et al.,
2021; Jackson et al., 2022a; Moore et al., 2018; Vanderwolf
et al., 2021). However, one can make some predictions of risk
of exposure to Pd and possible sensitivity to developing WNS
and hence work toward estimating vulnerability (Williams et al.,
2008) by focusing on some more general risk factors identified
by research efforts in North America and Europe. At a broad
level, the risk of exposure to WNS can be predicted by whether
a species roosts in caves during winter (roost preference) and
whether cave temperatures and humidity would allow for Pd
growth (suitability) (Marroquin et al., 2017; Verant et al., 2012).
If a bat population is exposed to Pd, its sensitivity to WNS can
be predicted by inference about the likelihood of infection for
a given species, its response to infection (i.e., Pd load) (Lang-
wig et al., 2016; Zukal et al., 2016), and the severity of winter
and length of hibernation (hibernation biology) (Reeder et al.,
2012; Verant et al., 2014). However, winter length is not always a
predictor of WNS-associated declines for some species, such as
the tricolored bats (Perimyotis subflavus) and northern long-eared
bats (Myotis septentrionalis) (Gabriel et al., 2022; Loeb & Winters,
2022; Perea et al., 2024). Although not perfect, such an analy-
sis would still be valuable given the possibility of severe effects
from WNS on bat populations and the value of identifying
geographic regions and populations most at risk of developing
WNS before its arrival (Langwig et al., 2015).
One way to infer sensitivity to Pd infection for a species
that has not yet been exposed to Pd is to examine the known
responses of related species because related species are likely
to share disease-relevant traits, as observed in other taxonomic
groups (Hoverman et al., 2011). Zukal et al. (2014) found that
Pd infection is phylogenetically independent across 48 species
of bats examined in North America and Eurasia. However, since
this study, 17 additional species have been sampled for Pd, pro-
viding scope for an updated assessment on the phylogenetic
vulnerability to Pd infection. Information on the likelihood of
infection among bat species with varying degrees of evolution-
ary relatedness (i.e., host specificity) can provide the starting
point for prioritizing research efforts on species sensitivity to
WNS. If Pd shows low host specificity, as indicated by Zukal
et al. (2014), vulnerability to WNS is determined more by other
factors that influence sensitivity, such as the hibernation biology,
combined with factors that affect exposure, such as roosting
preference and roost environmental suitability for Pd growth.
For example, the temperature-dependent growth of Pd is used
to determine the optimal growth and growth limits of this fun-
gal pathogen where hibernating bats can be exposed (Escobar
et al., 2014; Frick et al., 2022; Haase et al., 2021; Turbill &
Welbergen, 2020; Verant et al., 2012). Therefore, understanding
phylogeny and climate-dependent exposure risk is a necessary
component for determining vulnerability to infectious diseases
in the absence of direct experimental exposure of Pd to naive
bat species.
We used data from the literature to investigate the threat of
WNS to naive Southern Hemisphere bats via a global assess-
ment of cave thermal conditions and fungal host specificity.
We first examined whether Pd infection is phylogenetically con-
served in bats using host-specificity models of bats tested for
Pd. We then examined whether there are regions in the South-
ern Hemisphere with caves that would provide suitable thermal
conditions for Pd if the fungus were introduced there. Finally,
we used species-specific roosting preferences and hibernation
data (derived from a literature search) to estimate the potential
exposure risk to WNS. We based our predictions of exposure
risk to WNS on cave temperature and roost preference, and
predictions of broad-scale sensitivity to developing WNS on
the number of frost days as a proxy for hibernation duration.
We considered the potential risk of Pd exposure for cave-
roosting bats in the Southern Hemisphere and the implications
for conservation management.
METHODS
IUCN and roost preference search
We extracted species-level biological classification (family,
genus, species), geographic distribution, and conservation sta-

3of11 WU ET AL.
tus (least concern, near threatened, vulnerable, endangered,
critically endangered, data deficient) for 1332 species from
the order Chiroptera from the International Union for Con-
servation of Nature (IUCN) Red List of Threatened Species
database (IUCN, 2022) (downloaded 16 May 2022). Because
WNS develops only during winter hibernation and mostly
affects cave-roosting species, we also collected information on
hibernation biology and use of cave roosts for these bat species.
For cave roost, we identified species that at least sometimes
roost in caves based on Tanalgo et al. (2022), who defined cave-
roosting species as those that “occur, use, roost, or hibernate in
caves and subterranean habitats for any part of their life histo-
ries.” The Tanalgo et al. (2022) database, which categorizes 679
species as cave-roosting bats, provides the most conservative
estimate because it includes species that even only occasion-
ally roost in caves. We included additional species that fit the
definition of cave-roosting used by Tanalgo et al. (2022)but
were not present in their database and made further changes
to their database based on the literature search described below
(detailed in Appendix S1). This revised database included 713
species with records of cave-roosting behavior. The definition
of cave-roosting that we followed from Tanalgo et al. (2022)
includes species that are primarily tree-roosting but have been
observed at least once in a cave or roost in caves only in small
parts of their range. For example, populations of the Australian
chocolate wattled bat (Chalinolobus morio) can roost either in
trees or in caves in parts of their range (e.g., no cave-roosting
populations in Tasmania, but roost exclusively in caves in the
Nullarbor Plain). Because we were interested in bat species that
primarily roost in caves during winter, we revised this list by
excluding species that rarely been recorded in caves to derive
a list of primarily cave-roosting species. This resulted in a list
of 441 primarily cave-roosting species. The roost preference for
many species has not been adequately surveyed and can vary by
season. Therefore, the number of species at risk of exposure
presented would exclude many data-deficient species. Pd can
survive in caves and mine-type habitats even with the absence
of bats. This means that even bats that rarely enter caves or only
use them in certain seasons could still be exposed to and spread
Pd.
Roost preference was obtained from Churchill (2008), Har-
vey et al. (2011), Monadjem et al. (2020), Moyers Arévalo et al.
(2020), Nowack et al. (2020), and a primary literature search on
Google Scholar for the terms “species name” and either “roost
preference”or“cave.” We included species if their geographical
distribution was publicly available from the IUCN. We also cat-
egorized the geographical hemisphere of occurrence for each
species based on whether a species’ geographic range is either
in the northern or the Southern Hemisphere or in both hemi-
spheres. Data curation was formatted following Schwanz et al.
(2022).
Frost days
The severity of WNS also depends on the duration of hiber-
nation by cave-roosting bats, which in turn is influenced by
the winter length (Hranac et al., 2021). To predict winter
length, we used the average number of frost days per year
because this variable more accurately predicts hibernation dura-
tion than other environmental factors (Hranac et al., 2021).
We estimated the average number of frost days at the ground-
surface level based on an air temperature threshold of 2◦C,
which indicates that the temperature at the ground-surface
level is approaching 0◦C (Campbell & Norman, 2000). We
extracted the mean daily minimum air temperature (at 0.5′
resolution) from 1991 to 2020 from the CPC Global Uni-
fied Temperature database provided by the National Oceanic
and Atmospheric Administration Physical Sciences Labora-
tory, Boulder, Colorado (United States) (https://psl.noaa.gov/
data/gridded/data.cpc.globaltemp.html). Bats do not necessar-
ily hibernate during frost days; however, this provides a broad
indication of potential hibernation duration available.
Hibernation studies
There have been relatively few studies of the thermal biology
of bats during winter, and available data on torpor use were
often difficult to interpret in terms of confirming if the species
uses prolonged torpor during a season of hibernation. Conse-
quently, we could not confidently assign the trait of hibernation.
Given the importance of hibernation to understanding sensitiv-
ity to WNS, we examined research effort on winter hibernation
in free-ranging bats in the Northern and Southern Hemisphere
and used these data to identify gaps in knowledge for species
predicted to be exposed to Pd. To do this, a Boolean search
of titles, abstracts, and keywords with the string (bat$) AND
(hibernation or torpor) AND (winter)NOT(mouse OR mice OR rat$
OR rodent OR squirrel OR vole$ORlemming$) NOT (bird$) was
performed on Web of Science on 15 December 2022, resulting
in 195 records. This broad search allowed us to capture differ-
ent methods used to quantify hibernation in free-ranging bats.
We then performed a full-text search of these 195 records on
whether hibernation was recorded in a bat species during win-
ter in the field and what species were recorded. An additional
search on Google Scholar for the term “bat winter hibernation”
was also performed.
Studies on laboratory-induced torpor were excluded because
of the artificial conditions in which torpor was exhibited and
because laboratory studies do not provide information about
the winter behavior of wild bats. From both Web of Science and
Google Scholar, a total of 193 peer-reviewed articles in English
were retained. Articles were categorized by survey methods used
to quantify winter hibernation, either by measuring skin tem-
perature of free-ranging bats or through other methods that
provide information on hibernation behavior of bats in the wild
(acoustic monitoring, cave survey, banding, camera trap, collec-
tion, PIT tagging). We measured skin temperature in the field
because it provided information on hibernation length, torpor
bout duration, number of arousal periods, and the thermoreg-
ulatory scope (difference between euthermic body temperature
and torpor body temperature) under natural conditions (Geiser,
2021)—all important components of sensitivity to WNS (Jack-

CONSERVATION BIOLOGY 4of11
son et al., 2022a, 2022b; Reeder et al., 2012). Articles were also
classified as Northern Hemisphere or Southern Hemisphere
based on the country where the study was conducted.
Pd infection search
To test the host specificity of bats to Pd infection, a Boolean
search using the string [(bat*ORmicrobat*ORChiroptera) AND
(white-nose syndrome OR Pseudogymnoascus destructans OR Geomyces
destructans)] was performed on Web of Science (from 1 Jan-
uary 2007 to 15 March 2022), resulting in 661 records. Title
and abstract screening of the comprehensive search was con-
ducted in Rayyan (Ouzzani et al., 2016). Additional species were
searched for on the WNS website (https://whitenosesyndrome.
org/static-page/bats-affected-by-wns). We collected informa-
tion on whether bats were tested for Pd and whether mean Pd
load (per unit of area) was determined via polymerase chain
reaction.
Data analyses
We created 2 subsets from the full dataset (combined IUCN,
hibernation, and Pd dataset): species examined for Pd (n=65)
and whether they developed WNS (n=53). Next, we computed
the pairwise distance (matrix D) between pairs of tips from
the bat phylogeny based on its branch length with the cophe-
netic.phylo function from the ape package (Paradis & Schliep,
2018). We then transformed the matrix to log base 10 follow-
ing Gilbert et al. (2012). We used a time-calibrated, species-level
phylogeny from Shi and Rabosky (2015) that consisted of 812
extant species of bats (62.5% of current bat diversity estimates
based on the IUCN Red List of Threatened Species database)
that we organized according to species-specific data on hemi-
sphere region, roost preference, whether they had been studied
for winter hibernation, and whether they were tested for Pd
(Figure 1). Only 783 species used by Shi and Rabosky (2015)
matched the bat species listed on the IUCN Red List of Threat-
ened Species database. We then generated an incidence matrix
(matrix I) coding a species that had tested positive or negative
for Pd with the get incidence matrix function from the geotax
Rpackage(https://github.com/alrobles/geotax).
To estimate the probability that a species would be detected
with Pd and the probability of a species to develop WNS, we
calculated the logistic regression relating the bat Pd or bat WNS
indices, respectively, in the matrix Ito the host phylogenetic
distance in matrix Dwith phylogenetic distance as the indepen-
dent variable via the log reg boostrap function from geotax. A
matrix of probabilities, P, was then generated by applying the
regression coefficients to the logistic transformation of matrix
I. The mean intercept and slope coefficient of the regression
were obtained by repeating the previous procedure 1000 times.
Phylogenetic signal as Pagels lambda (λ) was also quantified for
mean Pd load on each bat species using the phylosig function
from the phytools Rpackage, with 1000 simulation replicates
(Revell, 2012). We also conducted a host specificity analysis on
probability of a species to develop WNS and the estimated phy-
logenetic signal of mean Pd load for Eurasian bats only because
the outcomes could be influenced by geographical bias (North
America vs. Eurasia).
We obtained spatial data of geographic distribution for
439 cave-roosting bat species from the IUCN Red List of
Threatened Species database (at 0.25′resolution grid cell) and
calculated the sum of cave-roosting bat species in each grid
cell using the calcSR function from the rasterSp R package
(https://github.com/RS-eco/rasterSp). We added 2 additional
species (Rhinolophus robertsi,Miniopterus orianae) from Australia
not available on the IUCN Red List using distribution ranges
provided by local experts in the BatMap dataset (https://www.
ausbats.org.au/batmap.html).
To estimate the maximum possible spatial extent of exposure
to Pd, we mapped the geographic distribution of thermal con-
ditions between 0 and 19.8◦C allowing growth of Pd (Verant
et al., 2012). We used extrapolated spatial data on mean annual
surface temperature (MAST) from WorldClim 2.0 (Fick & Hij-
mans, 2017) as a proxy for cave temperature at a given location
(Blejwas et al., 2021; Lecoq et al., 2017; Leivers et al., 2019;
Perry, 2013; Vanderwolf & McAlpine, 2021). We also generated
the temperature-dependent risk map that included a formula
for adjusting cave temperature based on MAST according to
distance from the cave entrance because during winter cave tem-
perature can be cooler than MAST closer to the cave entrance.
A regression model was used based on McClure et al. (2020)
and included an interaction between the effects of MAST and
distance to the cave entrance, and predictions were validated
against the observed winter cave temperatures from the liter-
ature and McClure et al. (2020) (Appendix S2). We modeled
cave distances between 50 and 100 m from the entrance because
50 m is considered the start of the dark zone where bats might
prefer to roost in winter (Vanderwolf & McAlpine, 2021), but
even colder cave temperatures could be available if bats roost
closer to the cave entrance (which potentially would result in an
even larger area of suitability for Pd growth).
We then intersected the global spatial layer for richness of
cave-roosting species against areas of the MAST and cave
depth-adjusted MAST layers that predicted winter cave temper-
atures from 0 to 19.8◦C to visualize regions of high numbers
of cave-roosting bat species in areas with the potential for Pd
growth. The upper thermal limit for Pd growth is estimated
as 19.0–19.8◦C across all strains tested (Verant et al., 2012); we
used 19.8◦C as a conservative upper limit for Pd growth. Finally,
we calculated the percentage of species-level range overlap with
Pd growth for cave-roosting species in the Southern Hemi-
sphere to predict which species are at risk of Pd exposure. We
excluded Pteropodidae and Mormoopidae families because they
are not known to hibernate under laboratory or wild settings
(Stawski et al., 2014). Data and Rcodes are publicly available in
the GitHub repository: www.github.com/nicholaswunz/WNS-
global

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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/).
RESULTS
Diversity of cave-roosting bats
Of the 441 species that primarily roost in caves, 247 occur in the
Northern Hemisphere, 127 in the Southern Hemisphere, and 67
in both hemispheres.
Host specificity and pathogen load
Of the 65 species tested for Pd, the likelihood of detec-
tion of Pd across the bat phylogeny (intercept =15.37,
slope =−6.83, p=0.56) (Figure 2a) and the likelihood of
developing WNS (intercept =2, slope =−1.1, p=0.54)
(Figure 2b) showed low host specificity. However, Myotis species
were more likely to show WNS-associated declines (Figure 2c).
This is reflected in the phylogenetic relatedness (Pagels λ=0.90,
p=0.0003), where the mean Pd load was higher for Myotis
than for species sampled from Miniopterus,Rhinolophus,Hypsugo,
Corynorhinus,Murina,Eptesicus,andPlecotus (Figure 2d). These
results should be treated with caution because sampling efforts
were biased toward the Myotis genus (48.4% of species sampled
for Pd) and the correlation between phylogeny and geography
(North America vs. Eurasia) may confound the results given
that closely related species are typically found on the same

CONSERVATION BIOLOGY 6of11
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)asa
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).
continent. However, a sensitivity analysis conducted on bats
from just Eurasia showed low host specificity for developing
WNS (intercept =2.7, slope =−1.24, p=0.53) (Appendix S3)
and a moderate phylogenetic signal for mean Pd load (Pagels
λ=0.58, p=0.016).
Pd exposure
Based on MAST and cave depth-adjusted MAST from 50 to
100 m as a proxy for winter cave temperatures, there were
caves suitable for Pd growth in the ranges of cave-roosting bat
species that occur in southern regions of South America, Africa,
and Australia (Figure 3a,b). These regions thermally suitable for
Pd growth in the Southern Hemisphere also contained numer-
ous karst regions likely to provide deep caves (Appendix S4),
but cave-roosting bats also roosted in disused mines and cul-
verts, which extend the thermally suitable regions of hibernacula
beyond karst regions alone. Some regions in the Southern
Hemisphere had >100 frost days per year, particularly in south-
ern South America (Appendix S5). As an index of the duration
of winter and the period when hibernation is required, this indi-
cated that some bat species in regions of predicted Pd exposure
could exhibit a substantial period of winter hibernation.

7of11 WU ET AL.
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).
Of the Southern Hemisphere bats that roost in caves, there
were 89 species with >5% overlap in their geographic distribu-
tion with regions thermally suitable for Pd growth (both MAST
and cave depth-adjusted MAST [list in Appendix S6]). There
were 46 species predicted to have some parts of their range at
risk of Pd exposure in Africa, 28 species in South America, and
15 species in the Oceania region. Most of these species with
some overlap with Pd exposure risk had little-to-no information
on their hibernation patterns (Appendix S6). Published stud-
ies on hibernation by free-ranging bats increased by 80% since
2000 (Appendix S7), but studies in the Southern Hemisphere
comprised only 10.4% of this research relative to the Northern
Hemisphere.
DISCUSSION
Novel pathogens can have catastrophic impacts on wildlife, as
shown by the devastating effect of Pd on naive bat populations
in North America (Cheng et al., 2021; Hoyt et al., 2021). Despite
the risk that Pd could spread into Southern Hemisphere regions,
there is little awareness of the likelihood of Pd infection and
the potential severity of a WNS outbreak in these regions. We
found that cave-roosting bats in the Southern Hemisphere are
likely to be at risk of Pd exposure due to low host specificity
of developing WNS and the widespread suitable environmental
temperatures in caves for Pd growth. Our study also highlighted
how little is known about the winter biology of bats in Southern
Hemisphere regions, which hinders more accurate predictions
of their sensitivity to WNS if exposed to Pd. The range of
Pd exposure in North America has, until recently, been limited
to temperate regions; consequently, there are few examples to
inform predictions of the impacts of WNS among naive bat
species in similar climates in the Southern Hemisphere. Hence,
the global significance of assessing the potential spread and
impact of Pd on bat species in the Southern Hemisphere makes
it a matter of considerable concern.
Previous studies have attempted to quantify exposure risk
in the Southern Hemisphere at the continental scale (Esco-
bar et al., 2014; Turbill & Welbergen, 2020), but ours is the
first assessment of exposure risk with some attempt to also
predict sensitivity (e.g., roosting preference, phylogeny) for
cave-roosting bats in the entire Southern Hemisphere. We iden-
tified considerable areas of exposure for cave-roosting bats
across southern parts of South America, Africa, and Australia.
Our spatial analysis showed that the low-latitude region acted

CONSERVATION BIOLOGY 8of11
as a thermal barrier to Pd crossing naturally into the Southern
Hemisphere. However, with the growing unintended trans-
portation of pathogens globally (Tatem et al., 2006)andthe
resilience of fungal spores carried by fomites, Pd could read-
ily cross the equator and so represents an important emerging
threat to bat fauna worldwide. Spatial information on the risk
of exposure for bats is a first step to understanding their vulner-
ability to WNS and can help establish targeted research efforts
and mitigation planning before Pd might arrive in the Southern
Hemisphere.
Most cave-roosting bat species in the Southern Hemisphere
with distributions overlapping with the temperature-dependent
growth of Pd did not have information on their hiberna-
tion biology or winter energetics. This is important because
of the low host specificity of developing WNS, meaning any
species can potentially develop WNS. The correlation of Pd load
between related species may suggest similar ecology in related
species that influences WNS susceptibility, such as wintering
energetics. Research from North America indicates a number of
biological factors such as hibernation behavior and overwinter
energetics are key predictors of species sensitivity to developing
WNS (Cheng et al., 2019; Hayman et al., 2016; Jackson et al.,
2022a; Moore et al., 2018). Many cave-roosting bats use torpor
to conserve energy during winter when food resources are low
(Ruf & Geiser, 2015). The amount of fat stored prior to win-
ter is closely linked to torpor and arousal patterns (Humphries
et al., 2002; Kunz et al., 1998), and Pd is known to increase
winter energy expenditure through increased torpor metabolic
rate and an increase in the frequency and duration of interbout
arousal periods (Lilley et al., 2017; Mayberry et al., 2018;Ver-
ant et al., 2014). Therefore, predicting sensitivity to Pd during
hibernation for naive species requires information on 3 key fac-
tors: the amount of fat stored before winter, torpor and arousal
patterns that determine energy expenditure during winter, and
duration of hibernation (Hranac et al., 2021; Jackson et al.,
2022b). Due to the paucity of studies describing hibernation for
Southern Hemisphere bats, understanding of their sensitivity to
Pd infection would benefit from research focused on the winter
biology of species shown here to be most at risk of pathogen
exposure.
We highlight that although the winter lengths for countries
in the Southern Hemisphere are generally shorter than coun-
tries in the Northern Hemisphere (Appendix S5), suggesting
that Southern Hemisphere bats are at lower risk of Pd exposure,
there are uncertainties in host–pathogen dynamics that drive Pd
sensitivity beyond winter length alone. Evidence of Pd exposure
for cave-roosting bats in subtropical regions of North America
(https://whitenosesyndrome.org/where-is-wns) suggests that
bats in mild climates (e.g., parts of Southern Hemisphere) might
be more at risk than previously anticipated. To our knowledge,
only 2 countries in the Southern Hemisphere, Australia and
Chile, have tested for Pd (Holz et al., 2018; Lilley et al., 2020).
Further surveillance efforts are required to detect the possi-
ble invasion of Pd in the Southern Hemisphere. Preemptive
biosecurity measures should also be considered for Southern
Hemisphere caves, and data could be collected to better under-
stand the probability of entry of cave fungal spores into caves
via different mechanisms (e.g., human visitation, abundance and
diversity of bats in the cave, and the connectivity of cave sys-
tems) for better targeting of biosecurity measures and increased
confidence in models of risk. There are notable regions with
high species richness in the Southern Hemisphere where tar-
geted research efforts are recommended. This includes most
of the Andean Mountain Range, southeastern Brazil, southern
South Africa, the mountainous regions of eastern Africa, Mada-
gascar, southeastern Australia, and the mountainous regions of
Papua New Guinea.
Furthermore, there is a need to establish baseline population
monitoring of bats in Southern Hemisphere regions, particu-
larly for cave-roosting species identified as most likely to be at
risk of developing WNS to determine how population numbers
change if Pd is introduced. Species in the families Miniopteri-
dae, Rhinolophidae, and Vespertilionidae are known to develop
WNS in the Northern Hemisphere, and 12 species in the fam-
ily Miniopteridae, 18 species in the family Rhinolophidae, and
9 species in the family Vespertilionidae found in the South-
ern Hemisphere may be at risk of developing WNS if exposed.
There are also 2 families, Cistugidae (2 species) and Furipteri-
dae (1 species), that are only found in the Southern Hemisphere.
There is little knowledge on the wintering biology of species in
these families, and their risk of developing WNS is uncertain
and requires further research. Finally, several threatened species
(based on the IUCN Red List) should be of high research
priority because when bats are affected by other threats in
addition to WNS, further declines may result. These species
include Rhinolophus cohenae (vulnerable), Rhinolophus smithersi (near
threatened), and Rhinolophus ruwenzorii (endangered) from the
African continent and Mormopterus phrudus (vulnerable), Platalina
genovensium (near threatened), Tomopeas ravus (endangered), and
Amorphochilus schnablii (Vulnerable) in South America. How-
ever, many species listed as least concern and data deficient
(Appendix S6) should also be of research interest in the context
of WNS risk.
Given the increased risk of emerging pathogens globally
(Jones et al., 2008; Scheele et al., 2019) and their impact on
wildlife (Hoyt et al., 2021;Wu,2023), predicting where and how
they will affect naive ecosystems is an important One Health
objective (Cunningham et al., 2017; Daszak et al., 2000), even
if based on limited information. For example, Pd-infected bats
have increased viral load of coronaviruses (Davy et al., 2018). A
Pd invasion of the Southern Hemisphere may also have poten-
tial risks for human public health given the concerns of rising
zoonotic diseases (Ruiz-Aravena et al., 2022). Such work can
direct research and management efforts, which can be most
effective in reducing negative outcomes from emerging wildlife
diseases when initiated as early as possible (Skerratt et al., 2016;
Smith et al., 2009). There is clearly a potential for spread of Pd to
regions in the Southern Hemisphere, where thermal conditions
are suitable for Pd growth. Even if Southern Hemisphere bat
species are phylogenetically distant from Northern Hemisphere
species, they are likely to be sensitive to infection, although lim-
ited information about bat winter biology hampers predictions
of sensitivity to the WNS disease. Nevertheless, we advocate for
a proactive response to increase targeted research efforts and

9of11 WU ET AL.
instigate biosecurity and management actions that reduce the
risk of entry of Pd and potentially help limit potential impacts
of WNS on bats in the Southern Hemisphere.
AUTHOR CONTRIBUTIONS
Nicholas C. Wu collected and analyzed the data, produced the
figures, and wrote the initial draft. All authors contributed to
conceiving the study and to the revisions.
ACKNOWLEDGMENTS
We thank C. G. Haase (Austin Peay State University) for pro-
viding advice on the cave depth-adjusted MAST calculations.
This research was funded by the Australian Research Council
Linkage Grant (LP200100331).
ORCID
Nicholas C. Wu https://orcid.org/0000-0002-7130-1279
Justin A. Welbergen https://orcid.org/0000-0002-8085-5759
Tomás Villada-Cadavid https://orcid.org/0000-0002-1743-
0694
Lindy F. Lumsden https://orcid.org/0000-0002-4967-4626
Christopher Turbill https://orcid.org/0000-0001-9810-7102
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SUPPORTING INFORMATION
Additional supporting information can be found online in the
Supporting Information section at the end of this article.
How to cite this article: Wu, N. C., Welbergen, J. A.,
Villada-Cadavid, T., Lumsden, L. F., & Turbill, C. (2025).
Vulnerability of Southern Hemisphere bats to
white-nose syndrome based on global analysis of fungal
host specificity and cave temperatures. Conservation
Biology,39, e14390. https://doi.org/10.1111/cobi.14390