Multiple mortality events in bats: A global review

Abstract

Despite conservation concerns for many species of bats, factors causing mortality in bats have not been reviewed since 1970. Here, we review and qualitatively describe trends in the occurrence and apparent causes of multiple mortality events ( MMEs ) in bats around the world.
We compiled a database of MMEs , defined as cases in which ≥ 10 dead bats were counted or estimated at a specific location within a maximum timescale of a year, and more typically within a few days or a season. We tabulated 1180 MMEs within nine categories.
Prior to 2000, intentional killing by humans caused the greatest proportion of MMEs in bats. In N orth A merica and E urope, people typically killed bats because they were perceived as nuisances. Intentional killing occurred in S outh A merica for vampire bat control, in A sia and A ustralia for fruit depredation control, and in A frica and A sia for human food. Biotic factors, accidents, and natural abiotic factors were also important historically. Chemical contaminants were confirmed causes of MMEs in N orth A merica, E urope, and in islands. Viral and bacterial diseases ranked low as causes of MMEs in bats.
Two factors led to a major shift in causes of MMEs in bats at around 2000: the global increase of industrial wind‐power facilities and the outbreak of white‐nose syndrome in N orth A merica. Collisions with wind turbines and white‐nose syndrome are now the leading causes of reported MMEs in bats.
Collectively, over half of all reported MMEs were of anthropogenic origin. The documented occurrence of MMEs in bats due to abiotic factors such as intense storms, flooding, heat waves, and drought is likely to increase in the future with climate change. Coupled with the chronic threats of roosting and foraging habitat loss, increasing mortality through MMEs is unlikely to be compensated for, given the need for high survival in the dynamics of bat populations.

Full text

REVIEW
Multiple mortality events in bats: a global review
Thomas J. O’SHEA* Fort Collins Science Center, United States Geological Survey (USGS), Fort Collins,
CO 80526, USA. E-mail: osheat@usgs.gov
Paul M. CRYAN Fort Collins Science Center, United States Geological Survey (USGS), Fort Collins, CO
80526, USA. E-mail: cryanp@usgs.gov
David T.S. HAYMAN Molecular Epidemiology and Public Health Laboratory, Hopkirk Research
Institute, Massey University, Private Bag 11222, Palmerston North 4442, New Zealand. E-mail:
d.t.s.hayman@massey.ac.nz
Raina K. PLOWRIGHT Department of Microbiology and Immunology, Montana State University,
Bozeman, MT 59717, USA. E-mail: raina.plowright@montana.edu
Daniel G. STREICKER Institute of Biodiversity, Animal Health and Comparative Medicine,
MRC-University of Glasgow Centre for Virus Research, University of Glasgow, G12 8QQ Scotland, UK.
E-mail: daniel.streicker@glasgow.ac.uk
Keywords
bats, conservation, disease, mortality, wind
turbines
*Correspondence author.
Submitted: 23 July 2015
Returned for revision: 3 September 2015
Revision accepted:11 November 2015
Editor: KH
doi:10.1111/mam.12064
ABSTRACT
1. Despite conservation concerns for many species of bats, factors causing mortal-
ity in bats have not been reviewed since 1970. Here, we review and qualitatively
describe trends in the occurrence and apparent causes of multiple mortality events
(MMEs) in bats around the world.
2. We compiled a database of MMEs, defined as cases in which ≥10 dead bats
were counted or estimated at a specific location within a maximum timescale of a
year, and more typically within a few days or a season. We tabulated 1180 MMEs
within nine categories.
3. Prior to 2000, intentional killing by humans caused the greatest proportion of
MMEs in bats. In North America and Europe, people typically killed bats because
they were perceived as nuisances. Intentional killing occurred in South America
for vampire bat control, in Asia and Australia for fruit depredation control, and in
Africa and Asia for human food. Biotic factors, accidents, and natural abiotic
factors were also important historically. Chemical contaminants were confirmed
causes of MMEs in North America, Europe, and in islands. Viral and bacterial dis-
eases ranked low as causes of MMEs in bats.
4. Two factors led to a major shift in causes of MMEs in bats at around 2000: the
global increase of industrial wind-power facilities and the outbreak of white-nose
syndrome in North America. Collisions with wind turbines and white-nose syn-
drome are now the leading causes of reported MMEs in bats.
5. Collectively, over half of all reported MMEs were of anthropogenic origin. The
documented occurrence of MMEs in bats due to abiotic factors such as intense
storms, flooding, heat waves, and drought is likely to increase in the future with
climate change. Coupled with the chronic threats of roosting and foraging habitat
loss, increasing mortality through MMEs is unlikely to be compensated for, given
the need for high survival in the dynamics of bat populations.
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Mammal Review ISSN 0305-1838
1Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd

INTRODUCTION
Bats number over 1300 species and occur in all continents
except Antarctica (Fenton & Simmons 2014). Losses of
roosting and foraging habitat and other stressors have led to
widespread declines of bat populations (e.g. Mickleburgh
et al. 1992, Hutson et al. 2001). Nevertheless, mortality in
bats has not been reviewed since the work of Gillette and
Kimbrough (1970). Many species of bats are highly gregari-
ous and thus potentially vulnerable to ‘die-offs’, also refer-
enced as multiple mortality events (MMEs). Additionally,
bats are sources of zoonotic viral diseases (e.g. Calisher et al.
2006, Luis et al. 2013). Few viral disease-induced MMEs
seem to have been documented in bats (e.g. Messenger
et al. 2003, O’Shea et al. 2014), suggesting that many
microparasites of bats are low in virulence or do not cause
MMEs. However, documentation of die-offs due to any
cause may be rare simply because bats are secretive, and
thus MMEs due to disease may not be disproportionately
uncommon. Here, we review and qualitatively describe
trends in the occurrence of MMEs, including those caused
by disease, in bats around the world.
METHODS AND SCOPE
We defined an MME as a case in which ≥10 dead bats were
counted or estimated in a given locality within a maximum
timespan of 1 year, and more typically within a few days or
a season. We included accounts in which the authors quali-
tatively estimated the number of deaths (as many, dozens,
hundreds, etc.). With few exceptions, we did not include a
report unless it involved observations of carcasses. Because
Mickleburgh et al. (2009) reviewed the consumption of bats
for human food, we did not include observations of bats at
marketplaces or as imports, unless the report indicated the
number of bats killed over a given period of time at a spe-
cific location. We did not include records of bats killed by
researchers. We compiled published literature and Internet-
accessible reports that included observations of carcasses.
We did not solicit unpublished material or personal com-
munications. We searched Web of Science, Internet search
engines (e.g. Google), regional mammal summaries, special-
ised outlets and newsletters (e.g. ‘Bats’ magazine), and other
resources. Our search terms included the union of the terms
‘bats’ or ‘Chiroptera’ with mortality, die-offs, disease, epizo-
otics, killing, mass mortality, multiple mortality, and so
forth.
We identified nine categories of MMEs, according to the
cause of death: 1) intentional killing by humans; 2) biotic
factors other than disease (e.g. predation, biotoxins); 3)
natural abiotic factors (e.g. weather, floods, fire, volcanism);
4) exposure to environmental contaminants, including pes-
ticides; 5) accidents (e.g. entrapment, impalement, colli-
sions with objects other than wind turbines); 6) collisions
with wind turbines; 7) infectious viral and bacterial dis-
eases; 8) the fungal disease white-nose syndrome (WNS);
and 9) unexplained causes of death. We also classified
MMEs geographically, as occurring in: Africa, Asia, Austra-
lia, Europe (including the British Isles, Cyprus, Malta),
North America, South America (including Trinidad,
Curacao), or in islands (>100 km from continental main-
land). Primary sources and detailed information about
these MMEs are tabulated as online supporting information
(Appendices S1–S9, with supporting literature cited listed
separately as Appendix S10). We limit our analyses to
descriptive summaries because the literature we compiled
has many biases.
RESULTS AND DISCUSSION
We compiled 1180 accounts of MMEs in 152 species of bats
in all regions, beginning in 1790 (Table 1 and Fig. 1).
Cumulatively, collisions with wind turbines caused the
highest number of MMEs (a number biased by regulatory
reporting requirements in North America and Europe), fol-
lowed by MMEs due to WNS (Table 1 and Fig. 2). MMEs
attributed to infectious viral and bacterial diseases ranked
lowest (Table 1 and Fig. 2).
A notable temporal shift in causes of MMEs in bats took
place around 2000 (Fig. 3). From 1790 to 1999, 58% of
reported MMEs globally were due to intentional killing by
humans (39%) or biotic causes (19%; Fig. 3). From 2000
onwards, 70% of all MMEs were due to collisions with wind
turbines (35%) and WNS (35%; Fig. 3). These two latter
categories represent new and alarming challenges to bat
populations.
Anthropogenic sources (human-caused categories and
human-caused MMEs within other categories, e.g. acci-
dents, contaminants) account for 54% of MMEs in all years
(593 anthropogenic vs. 514 natural, unexplained cases
excluded). WNS in North America was not considered
anthropogenic. Comparisons with other mammals suggest
that the high proportion of anthropogenic MMEs in bats is
a cause for concern. In one analysis, from 1940–2012
‘human perturbations’ were listed as a cause for 20–25% of
die-offs of all animal groups combined, but only 0–25%
each decade for mammals with no increase in magnitude
through time (Fey et al. 2015, bats not included). In another
study, anthropogenic causes accounted for 52% of 2209
MMEs involving 10 or more deaths in 27 species of large-
and medium-sized (>1 kg) mammals of North America, but
more than half of that fraction was due to managed legal
harvests (Collins & Kays 2011).
We present an overview of findings within the major cat-
egories of MMEs, highlighting regional differences where
pertinent. Reports of MMEs in bats are biased regionally
Multiple mortality events in bats T. J. O‘Shea et al.
2Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd

Table 1. Summary of numbers of mass mortality events (MMEs) reported in bats, by category and region (see Appendices S1–S10 for details and
references). The order of magnitude for maximum unadjusted numbers of carcasses documented for the largest MME within each category is
given in parentheses, following the number of reports for each region and category
Category Africa Asia Australia Europe Islands
North
America
South
America Events (n)
Species
(n)
Intentional killing
(Appendix S1)
11 (104) 20 (104) 13 (104) 21 (104) 50 (103) 58 (104) 32 (105) 205 (105)69
Biotic (Appendix S2) 5 (101) 1 (101) 19 (103) 16 (102) 16 (102) 40 (103) 10 (101) 107 (103)75
Abiotic (Appendix S3) 0 6 (103) 71 (103) 0 13 (103) 24 (105) 0 114 (105)23
Contaminants (Appendix S4) 0 0 1 (101) 27 (104) 1 (102) 14 (103) 0 43 (104)16
Accidental (Appendix S5) 1 (101) 0 8 (101) 34 (102) 1 (101) 22 (104) 0 66 (104)37
Wind turbines (Appendix S6) 1 (102) 0 2 (101) 59 (102) 2 (101) 213 (102) 4 (101) 281 (102)41
Viral or bacterial disease
(Appendix S7)
1 (102) 1 (101) 2 (103) 2 (103) 6 (103) 13 (103) 0 25 (103)14
White-nose syndrome
(Appendix S8)
0 0 0 0 0 266 (104) 0 266 (104)6
Unexplained (Appendix S9) 0 0 3 (102) 30 (103) 2 (103) 38 (105) 0 73 (105)20
Totals 19 (104) 28 (104) 119 (104) 189 (104) 91 (103) 688 (104) 46 (105) 1180 152
Fig. 1. Numbers and proportions of reported multiple mortality events in bats over time (1790–2015). All 1180 events included in this review are
shown.
T. J. O‘Shea et al. Multiple mortality events in bats
3Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd

0
50
100
150
200
250
300
stnevE ytilatroM fo rebm
uN
Causes of Mortality Events
Wind Turbines
White-Nose Syndrome
Intenonal Kills
Natural Abioc
Bioc
Unexplained
Accidents
Contaminants
Viral/Bacterial Disease
Fig. 2. Cumulative (1790–2015) frequencies of 1180 reported multiple mortality events in bats, by causal category.
0
5
10
15
20
25
30
35
40
45
Causes of Mortality
Before 2000 Since 2000
Percentage of Reported Mortality Events (%)
Fig. 3. Percentages of reported multiple mortality events in bats by causal category, before 2000 (n=409 events) and from 2000 and thereafter
(n=771 events).
Multiple mortality events in bats T. J. O‘Shea et al.
4Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd

towards North America, Europe, Australia, and islands;
comparatively few events are recorded for Africa, Asia, and
South America (Table 1 and Fig. 4). Similar biases are
apparent in the reporting of mass mortality for all animals
(Fey et al. 2015). We encourage greater reporting and docu-
mentation of MMEs in bats globally, perhaps in conjunc-
tion with other ongoing bat-monitoring programmes.
MMEs due to intentional killing
Prior to 2000, humans intentionally killing bats caused the
greatest number of reported MMEs. These events occurred
worldwide and are recorded as early as the 1800s; in total,
we documented 205 cases involving millions of individuals
of at least 69 species (Table 1 and Appendix S1). Intentional
killing was widespread, and continues today, but education
and protective legislation have undoubtedly helped reduce
its occurrence. Reports of people killing bats for food are
common in Asia, Africa, and in islands, but extremely rare
in South America, and absent elsewhere (Appendix S1).
Reports of people legally and illegally killing fruit bats
(ostensibly for crop protection) are common in Australia,
and to a lesser extent elsewhere (primarily in the
Paleotropics). Killing of bats for crop protection is likely to
be under-reported (e.g. Vincenot et al. 2015). In parts of the
Americas within the range of common vampire bats
Desmodus rotundus, state-sanctioned poisoning of bats and
uncontrolled destruction of roosts aimed at reducing
common vampire bat bites on livestock has affected thou-
sands of caves and is likely to have killed millions of bats
including many non-target species [see later and Appen-
dix S1; dozens of other species share roosts with common
vampire bats (Greenhall et al. 1983)]. In addition to the
intentional killing of bats for food, crop protection, and
common vampire bat control, people have attempted to
exterminate colonies by acts of vandalism, including
burning, shooting, bludgeoning, and fumigation with
poisons (Appendix S1). We provide further summaries of
MMEs in this category by region.
AFRICA
We found reports of people intentionally killing bats in
Africa dated a century ago (Appendix S1). Lang and Chapin
(1917a) noted “Night after night they [caverniculous insec-
tivorous bats in central Africa] return to their accustomed
roosts, which they do not abandon even when frequent
raids made upon them by the natives have thinned out their
numbers. Large, juicy lumps of fat, deposited in and about
their abdominal cavity, stimulate the natives to kill all they
can.” Lang and Chapin (1917b) provide other accounts of
people killing apparently large numbers of insectivorous
bats from other types of roosts. Deaths of multiple
pteropodids (family Pteropodidae) taken for food at specific
locations are reported primarily for straw-coloured fruit
bats Eidolon helvum (Appendix S1), but other species have
been reported at markets (Mickleburgh et al. 2009).
AUSTRALIA
Starting in the 1800s, people decimated roosting camps and
killed pteropodids for fruit crop protection (Appendix S1;
Hall & Richards 2000). A limited number of these MMEs
meet our documentation criteria (Appendix S1), however
evidence suggests that millions of pteropodids were inten-
tionally killed. Early methods included shooting, netting,
trapping, explosives, fire and smoke; recent methods include
electrified grids (Martin 2011). This culling was widespread
and common, predicated on beliefs that local aggregations
of bats consumed commercial fruit and could be controlled,
0
10
20
30
40
50
60
70
80
90
North America
(n = 688)
South America
(n = 46)
Europe
(n = 189)
Africa
(n = 19)
Asia
(n = 28)
Australia
(n = 119)
Islands
(n = 91)
World Region
Intenonal Kills
Bioc
Natural Abioc
Contaminants
Unexplained
Accidents
Wind Turbines
V/B Disease
White-Nose Syndrome
Percentage of Reported Events (%)
Fig. 4. Causes of multiple mortality events in bats, expressed as percentages of all events (n), for each geographic region.
T. J. O‘Shea et al. Multiple mortality events in bats
5Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd

and that the bats sent ‘scouts’ to search for ripening crops.
Research suggests that such beliefs are largely erroneous.
Grey-headed flying foxes Pteropus poliocephalus, for
example, exist in large open populations in which major
eruptive movements follow the availability of native food
(mostly nectar and pollen from eucalypts; see reports in Eby
& Lunney 2002). Exclusion nets protect fruit crops but are
too expensive for some growers. From 2000, legal protec-
tions designated for some species led to heated conflicts
over pteropodid conservation and crop protection (Eby &
Lunney 2002). Some states are phasing out legal killing, or
regulating take by issuing permits. For example, the govern-
ment of Queensland issued permits to kill 10580 bats of
four species in 2013–2014 (Anonymous 2014a). Despite
protections, illegal killing continues. We found little infor-
mation about intentional killing of microchiropteran bats
in Australia. In 1965, about 200 long-fingered bats
(Miniopterus sp.) were found dead on the floor of a cave
with traumatic injuries caused by vandals (Appendix S1).
ASIA
Commercial fruit growers entangled and killed over 1000
pteropodids (of more than one species) in Thailand
(Appendix S1). Egyptian fruit bats Rousettus aegyptiacus in
Israel were fumigated with ethylene dibromide and lindane,
leading to mass mortality and declines in several non-target
species of cave-dwelling insectivorous bats. Mortality
through fumigation was reported from 1958 to 1985
(Appendix S1) and led to the ‘complete extermination’ of
Geoffroy’s myotis Myotis emarginatus and greater horseshoe
bats Rhinolophus ferrumequinum at an Israeli nature reserve
(Makin & Mendelssohn 1987). Market-hunters killed 10000
frugivorous, nectarivorous, and insectivorous bats every
month in one cave in Thailand during the early 1980s. Large
numbers of insectivorous as well as pteropodid bats were,
and still are, killed for food markets in Laos, peninsular
Malaysia, and Nagaland (India; Fig. 5; Appendix S1).
EUROPE
Stebbings (1988) summarised multiple instances of people
intentionally killing bats at roosts in Europe from the 1920s
through the 1980s. Many thousands of bats were killed by
fires, shooting, bludgeoning, gassing, explosives, and direct
application of insecticides as poisons. Nine species in three
families were subject to this intentional killing in England,
Scotland, Norway, Gibraltar, Malta, France, Germany,
Cyprus, and the former Yugoslavia (Appendix S1; Stebbings
1988). People directly fumigated roosts with insecticides in
Europe, causing MMEs such as the loss of 2000 individuals
of Pipistrellus sp. at a building in Scotland during 1971
(Stebbings 1988).
ISLANDS
In Borneo, hundreds of individuals of the nearly extinct
Bulmer’s fruit bat Aproteles bulmerae were shot in their cave
roost for food on a single day, and about 4500 large flying
foxes Pteropus vampyrus natunae were killed by hunters at a
forest patch in 2003 (Appendix S1). Goodman (2006)
reported recent food hunts for three species of insectivorous
bats at caves in Madagascar, including about 2700
Commerson’s leaf-nosed bats Hipposideros commersoni
killed in a 3-month season (Appendix S1). Currently, a cull
targeting tens of thousands of greater Mascarene flying
foxes Pteropus niger is underway in Mauritius in the belief
that the bats depredate fruit crops (Aldred 2015).
NORTH AMERICA
People intentionally killed at least 11 species of North
American bats by burning, shooting, bludgeoning, poison-
(a)
(b)
(a)
(b)
Fig. 5. Intentional killing of bats for food. (a) Dead bats on the ground
outside a cave in Nagaland, India, where villagers kill several thousand
bats as an annual event extending back perhaps 150 years (see Appen-
dix S1; photograph by Pilot Dovih). (b) Pteropus species for sale at a
market in Manado, Northern Sulawesi, Indonesia (photograph by
D.T.S. Hayman).
Multiple mortality events in bats T. J. O‘Shea et al.
6Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd

ing, and other activities (Appendix S1). Reports of eradica-
tion extend over 100 years into the past. For example, “over
two washtubfulls of the pesky critters” (presumed Brazilian
free-tailed bats Tadarida brasiliensis)weredestroyedata
Texas building in 1908 (Appendix S1).
Discovery of rabies in North American bats in the 1950s
increased public fear of health risks, leading to attempted
eradication of entire bat colonies, especially in buildings.
Killing was widespread and became commercialised within
the pest control industry. Additionally, fear or misunder-
standing of bats also motivated killing at colonies, often
referred to as ‘vandalism’. Some MMEs from deliberate
eradication are documented in the literature (Appendix S1).
People used chemical control methods (primarily fumiga-
tion with dichlorodiphenyltrichloroethane – DDT) to
poison colonies of multiple species at buildings in the USA,
Canada, and Mexico (Appendix S1). Considering the large
number of pest control companies operating in North
America, the true number of MMEs from chemical eradica-
tion until the 1980s is probably orders of magnitude larger
than reported in the literature. Killing bats with chemicals
may continue in some parts of North America, but is more
restricted and is considered less effective than physical
exclusion.
SOUTH AMERICA
In the late 1950s, people used organochlorine pesticides to
kill insectivorous bats considered nuisances in houses in
Trinidad: 1592 Pallas’s mastiff bats Molossus molossus and
339 black mastiff bats Molossus rufus were found dead after
up to 15 houses were sprayed (Appendix S1). Killing of bats
for vampire control, however, is the most heavily reported
cause of MMEs in South America. Common vampire bats
have been recognised as an economic and health problem in
Latin America for at least a century. These bats consume
blood from livestock, reducing animal health and produc-
tivity; more significantly, common vampire bats transmit
rabies to cattle, which has been estimated to cause tens to
hundreds of thousands of livestock deaths annually (Baer
1991). Recently, vampire-bat transmission of rabies to
humans has also become recognised as a serious health
problem in rural areas (e.g. Streicker et al. 2012). People use
various methods to control common vampire bats in
response to livestock and human health problems, including
lighting or covering corrals, hanging spiny branches around
cattle, capturing vampires in livestock corrals or roosts with
nets and bat traps, clubbing and shooting bats at roosts, poi-
soning, setting fires in roosts, and offering bounties for
vampire bat carcasses (Constantine 1970, Flores-Crespo &
Arellano-Sota 1991). Some control methods at roosts have
been indiscriminate, killing many bats of other species,
whereas other methods specifically target common vampire
bats. More targeted state-sanctioned killing of common
vampire bats now makes use of gels with oral anticoagulants
applied to the bodies of common vampire bats captured at
ranches; the bats return to roosts, spread the substance
within the colony, and ingest the toxic compounds during
grooming (including allogrooming; Arellano-Sota 1988,
Flores-Crespo & Arellano-Sota 1991, Johnson et al. 2014).
Bite wounds on cattle are also treated with anticoagulants
that are then ingested by common vampire bats during
feeding (Flores-Crespo & Arellano-Sota 1991).
People caused MMEs at common vampire bat roosts
using methods such as flamethrowers, dynamite, fumigation
with gases and poisons, electrocution, introduction of
disease agents, shooting, netting, trapping, and application
of anticoagulants (Greenhall & Schmidt 1988, Brown 1994;
Appendix S1). Concerned biologists and conservationists
have issued resolutions against destroying multi-species
roosts for common vampire bat control (Anonymous 1968,
1998) and some governments have banned the destruction
of bat roosts on state-owned reserves (e.g. Kikuti et al.
2011). Nonetheless, agencies and private individuals con-
tinue to destroy multi-species roosts and misapply antico-
agulants to non-target species (e.g. Mayen 2003, Aguiar
et al. 2010, Streicker et al. 2012, D. Streicker, personal obser-
vation). Recent quantitative analyses suggest that culling
vampire bats may be ineffective for controlling bovine
rabies (e.g. Streicker et al. 2012, Blackwood et al. 2013,
Johnson et al. 2014).
Governments still try to control common vampire bats as
part of national rabies control plans (D. Streicker, personal
observation) and improving methods of control is an area
of active research (Corrêa-Scheffer et al. 2014), but reports
chronicling the current extent and effects of these practices
on non-target species are limited. Earlier literature suggests
a severe impact that may be ongoing. In Venezuela, people
indiscriminately dynamited and discharged poisonous
organophosphate gas into caves, killing an estimated 900000
bats of multiple species each year from 1964 to 1967 (see
Constantine 1970 for references). In 1963–1968, authorities
in the state of Rio Grande do Sul, Brazil, indiscriminately
killed bats in 8240 caves (Constantine 1970). In an unusual
approach in Colombia, a cave was fumigated with atomised
Newcastle’s disease virus (a Paramyxovirus of poultry),
and an estimated 5000 common vampire bats were later
found sick or dead, apparently from the virus (Constantine
1970).
MMEs due to biotic factors other
than disease
MMEs caused by biotic factors other than disease princi-
pally involve predation; however, impalement on burrs of
T. J. O‘Shea et al. Multiple mortality events in bats
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plants, paralysis from tick neurotoxins, and poisoning by a
toxic algal bloom were also reported (Appendix S2). We
tabulated 107 MMEs beginning in the 1890s, involving over
75 species of bats globally (Table 1 and Appendix S2). Bats
have numerous predators, nearly all opportunistic, and the
literature includes many anecdotal accounts of individual
cases (Gillette & Kimbrough 1970). However, MMEs involv-
ing 10 or more bats taken as prey at specific locations have
been reported for well over a century and have occurred
globally. The predators known to cause MMEs in bats
include invertebrates, snakes, birds, and mammalian
mesocarnivores (Appendix S2). Birds are most widely cited
as predators of bats globally, and may be a selective force for
nocturnality (Mikula et al. in press). Two species of raptor
specialise on bats, one in the Paleotropics (Macheiramphus
alcinus) and one in the Neotropics (Falco rufigularis). These
specialists hunt at dusk, particularly during emergence of
bats, but rely on other prey as well. Predation by birds can
be substantial globally, but estimates are unavailable. The
author of the most extensive regional study estimated that
avian predation in the British Isles accounted for over
200000 bat deaths per year (Speakman 1991). In some areas,
predation by house cats also can be extensive: in one study it
was estimated that cats kill 170000 bats annually in Britain
(Appendix S2).
MMEs due to natural abiotic factors
Unseasonably cold weather, snow storms, flooding of roosts
during heavy rainfall, overheating during unusual hot spells,
burning or suffocation during landscape-level fires, and vol-
canic eruptions all cause MMEs in bats (Appendix S3).
MMEs due to such abiotic factors have been known since
the 1790s. Reports are unevenly spread globally: most obser-
vations are made in Australia, North America, and in
islands. We documented 114 MMEs due to natural abiotic
factors involving 23 species (Table 1), but found no pub-
lished reports of such events in Africa, Europe, or South
America.
ASIA
MMEs in pteropodid bats were reported at several locations
in India as a result of unusually hot periods during 2010
and 2015 (Appendix S3).
AUSTRALIA
Deaths of many thousands of pteropodid bats due to
extremely hot spells were reported in eastern Australia as
recently as 2014 (Appendix S3). Ambient temperatures
exceeded 48 °C at numerous locations during the 2014
event (Anonymous 2014b). Large numbers of flying foxes
died during presumably lesser heat spells in 1790 and
during the early 1900s (Appendix S3), and many thousands
of grey-headed and black flying foxes Pteropus alecto died
during 2000–2007, presumably from excessive heat (Appen-
dix S3; Welbergen et al. 2008). The main cause of these
MMEs is hyperthermia. Welbergen et al. (2008) found that
ambient temperatures of ≥42 °C were associated with lethal
hyperthermia; up to 13% of the black flying foxes in one
large, well-studied colony died from hyperthermia, the
majority being dependent young. These MMEs took place
during the summer when bats are in optimal body condi-
tion. MMEs from hyperthermia are expected to increase in
number and severity with climate change (Welbergen et al.
2008). Droughts and resulting bush fires often accompany
extreme heat, and have also killed ‘many’ flying foxes
through smoke inhalation, heat exposure, or immolation
(Hall & Richards 2000). Droughts also reduce food supplies
and cause MMEs in grey-headed flying foxes through star-
vation (Appendix S3). At the other abiotic extreme, over
1000 flying foxes (species unspecified) died in northeastern
New South Wales and southeastern Queensland in 1990 and
1991 during wet, windy, cold winter weather when food
supplies were low (Hall & Richards 2000).
ISLANDS
Major storms (hurricanes, typhoons, cyclones; Appen-
dix S3) have caused MMEs in bats in islands. These MMEs
primarily involved pteropodid bats, including Pacific flying
foxes Pteropus tonganus in the Vava’u islands of Tonga in
2001, Pacific flying foxes and and Solomons flying foxes
Pteropus rayneri in the Solomon Islands in 1986, Pacific
flying foxes and Samoan flying foxes Pteropus samoensis in
Tutuila, American Samoa in 1990 and 1991, Rodrigues
flying foxes Pteropus rodricensis in Rodrigues, Mauritius in
1979, and greater Mascarene flying foxes in Réunion during
1960 and 1979 (Appendix S3). In many of these cases, some
of the mortality following severe storms was delayed and
attributable to lack of food caused by winds stripping veg-
etation, and to opportunistic hunting by people (e.g. Cheke
& Dahl 1981, Appendix S3). Such MMEs are exacerbated by
increased vulnerability to hunting due to lack of concealing
vegetation, and by bats being forced to forage in daylight on
the ground where they also are vulnerable to predation by
dogs, cats, and pigs (Pierson & Rainey 1992, Stinson et al.
1992).
One report confirmed storms causing an MME of insec-
tivorous bats in islands: flooding from Cyclone Hyacinthe in
1980 drowned over 3000 Mauritian little mastiff bats
Mormopterus acetabulosus in a cave in Réunion (Cheke &
Dahl 1981). Hurricanes in Puerto Rico in 1989 and 1994
preceded dramatic declines in populations of the red fig-
eating bat Stenoderma rufum, but no carcasses were
reported (Gannon & Willig 1994). Similarly, marked
Multiple mortality events in bats T. J. O‘Shea et al.
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decreases and changes in relative abundance among fru-
givorous species of bats followed the 1989 hurricane in
Montserrat in the Caribbean (Pedersen et al. 2009).
Eruptions have caused MMEs in bats in volcanic islands.
Direct mortality of multiple individuals of Seychelles flying
foxes Pteropus seychellensis was observed in Grande Comore
in the Comoros Islands in the Indian Ocean (Appendix S3).
Volcanic activity may also have caused MMEs in pteropodid
bats in some Pacific islands (Lemke 1992). Beginning in
1995, volcanic activity in Monserrat in the Caribbean
“reduced the eastern and western flanks of the volcano to an
ecological wasteland and have buried much of the southern
half of the island under varying amounts of volcanic ash”
(Pedersen et al. 2009). Volcanic action destroyed roosts in
Monserrat, and frugivorous bat abundance decreased;
although no mortality was directly observed and no species
were lost, survivors showed signs of sublethal pathologies
(Pedersen et al. 2009, 2012).
NORTH AMERICA
Flooding of caves during unusually rainy weather or spring
runoff has caused MMEs in bats in North America. Floods
in the Ohio River valley, USA, in 1964 led to declines in four
species of bats at one hibernaculum in Kentucky, which
dropped from about 6000 bats in February to about 500 in
March after the flood; numerous carcasses were found
trapped among flood debris and mud after the waters
receded (Appendix S3). Similarly, about 6500 dead south-
eastern myotis Myotis austroriparius were observed awash in
one Florida cave in 1989 following a summer downpour, an
estimated 57000 individual southeastern myotis died in a
second cave during record high water in 1990, and flooding
in 1994 killed 85000 individual southeastern myotis in
Snead’s Cave, Florida (Appendix S3). An estimated 10000
grey bats Myotis grisescens were found dead after flooding in
a Tennessee cave in 1970 (Appendix S3). Based on skeletal
deposits, an estimated 300000 Indiana bats Myotis sodalis
died from past flooding at Bat Cave, Kentucky, thought by
some to be a major flood in 1937 (Appendix S3). MMEs in
Indiana bats caused by flooding at other caves involved 3000
individuals in 1997, and hundreds at two caves in 1996
(Appendix S3).
Despite the thermal stability of caves and mines used by
bats for hibernation, extremely cold weather has caused
MMEs at hibernacula in North America. Subfreezing tem-
peratures killed 200 individual Indiana bats at a hibernacu-
lum in Indiana in 1977, and “large numbers” at a
hibernaculum in Missouri (Appendix S3). Over 100 big
brown bats Eptesicus fuscus were found dead in snow drifts
formed by an early winter storm that blocked access to
hibernacula in Minnesota in 1940 (Appendix S3). Hundreds
of little brown bats Myotis lucifugus were found dead or
dying in the streets of a Wisconsin town in autumn 1936,
and were thought to have become exhausted while migrat-
ing in association with a cold front (Appendix S3). In the
Mojave Desert of California, over 40 Brazilian free-tailed
bats attempting to drink in a normally ice-free pond were
entrapped and frozen at the surface during an unusual cold
snap in 1930 (Appendix S3).
MMEs due to exposure to environmental
contaminants
Chemical contaminants caused MMEs in bats in Australia,
Europe, New Zealand and North America, and at a global
scale are suspected of causing far more mortality than has
been clearly documented. We compiled 43 accounts of
MMEs caused by chemical contaminants in 16 species of
bats since 1952; organochlorine pesticides such as DDT
were the most prevalent agents (Appendix S4). Worldwide
use of many organochlorines markedly declined in recent
decades due to legislative action and international treaties.
Impacts of substitute chemicals on bats have not been
adequately investigated (e.g. O’Shea & Johnston 2009).
Organochlorine insecticides and their metabolites can
persist in the environment and may become concentrated in
fatty tissues of insects and the bats that eat them. Organo-
chlorines may reside in the bodies of bats with no overt
effects until stored fats are metabolised, whereupon the
chemicals increase in brains until they reach lethal, neuro-
toxic concentrations. Research has established threshold
concentrations in bat brains that are diagnostic of lethality,
and correlated concentrations measured in carcasses or
guano also indicate lethal exposure (Clark & Shore 2001,
O’Shea & Johnston 2009). Although circumstantial evidence
and simple presence of chemical residues in carcasses are
not truly diagnostic of this cause of death, some die-offs
due to unexplained causes (Appendix S9) were very likely to
have been caused by chemical contaminants. MMEs
described below and in Appendix S4 pertain to poisoning
through the food-web or other environmental exposures,
and to unintended consequences of pesticide treatments of
timber at roosts in buildings. Cases where chemicals were
applied directly to bats or their roosts for ‘pest control’ are
summarised under intentional killing (Appendix S1). We
found no conclusive evidence that chemical contaminants
directly caused MMEs through food-chain exposures in
Africa, Asia, or South America, although organochlorines
were applied much more recently in these regions.
AUSTRALIA
About 30% of the flying foxes (three species, Appendix S4)
found dead in urban areas of Brisbane during the 1980s had
histopathological lesions and concentrations in tissues indi-
T. J. O‘Shea et al. Multiple mortality events in bats
9Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd

cating exposure to lethal amounts of lead, likely as an atmo-
spheric pollutant. Investigators hypothesised that insecticide
exposure caused die-offs of long-fingered bats in the 1960s,
but reported no corroborating diagnostic evidence (Appen-
dix S4).
EUROPE
Treating of timbers in buildings with organochlorine com-
pounds (DDT, dieldrin, lindane, pentachlorophenol) as
protection against wood-boring insects, which took place
from about 1950 to the 1980s, is thought to have been “the
most important factor in killing bats and reducing breeding
success” in Europe (Stebbings & Griffith 1986). First docu-
mented in the literature during the early 1970s (Appen-
dix S4), timber treatment occurred on a massive scale; over
1500 private companies were directly involved in Britain
alone during the 1980s (Mitchell-Jones et al. 1989). Many
species of bats in Europe are highly dependent on wooden-
frame buildings for roosts. Organochlorine compounds
were used in hundreds of thousands of such buildings, and
remained available for uptake by roosting bats through
contact, ingestion while grooming, and inhalation of
vapours for years after application (e.g. Shore et al. 1990).
Captive bats experimentally exposed to treated timbers died
(reviewed in Clark & Shore 2001), and such uptake has been
implicated in killing nine species of bats in the wild
(Appendix S4). We are unaware of reports of food-web
exposure to environmental contaminants causing MMEs in
Europe. Researchers detected potentially toxic concentra-
tions of lead in pipistrelles Pipistrellus sp. in England, but
not definitively in association with MMEs (Appendix S4).
ISLANDS
The anti-coagulant rodenticide diphacinone caused the
death of at least 115 New Zealand lesser short-tailed bats
Mystacina tuberculata in North Island, New Zealand; pre-
sumably it was ingested from prey or while ground-foraging
(Appendix S4).
NORTH AMERICA
Dieldrin (or the parent compound aldrin) clearly caused
MMEs through food-web exposure (including juveniles
nursing contaminated milk) in grey bats in the USA during
the 1970s (Appendix S4). Grey bats roost in caves where
carcasses can be easily found. Although the full extent of
organochlorine-caused die-offs is unknown, lethal concen-
trations of dieldrin, DDT, endrin, heptachlor, and their
metabolites have also been found in Indiana bats (Appen-
dix S4) and possibly Brazilian free-tailed bats (Reidinger
1976). Similarly, exposure to DDT and its metabolites have
been linked to major declines in populations of Brazilian
free-tailed bats in the southwestern USA (Geluso et al. 1976,
Clark 2001), but these data were not obtained from car-
casses found during MMEs. The role of other classes of
insecticides in causing MMEs is more difficult to determine,
but has been long suspected. For example, Brazilian free-
tailed bats were found dead in Arizona agricultural fields
where organophosphate insecticides were applied near a
large colony that suffered a major contemporaneous decline
(Clark & Shore 2001; Appendix S9). Carbamate poisoning
was recently reported in bats in Idaho (Appendix S4).
Mining operations that utilise cyanide for gold extraction
and then store contaminated waters in ponds on site attract
bats to drink. MMEs in bats at these ponds due to cyanide
poisoning have been recorded in South Carolina, Arizona,
and Nevada (Appendix S4), and are likely to be more preva-
lent globally than documented in the literature.
MMEs due to accidents
Since at least 1906, accidental deaths of multiple bats have
been reported from Africa, Australia, Europe, the Sey-
chelles Islands, and North America (Appendix S5), and
stem from both natural and anthropogenic sources. We
tabulated 66 MMEs involving 37 species of bats. ‘Natural’
accidental mortality includes entrapment of bats in build-
ings (e.g. Dietz et al. 2009), entrapment of lasiurine bats
(Genus Lasiurus; not normally cavernicolous) that cannot
find their way out of large caves in North America, first
noted in 1907 (Appendix S5), and odd accidents such as
being crushed by falling trees (Appendix S5). Accidental
falls from roost ceilings probably caused mortality of juve-
nile bats of several species in North America (Appen-
dix S5). Such MMEs involved about 13000 young in one
season in dense populations of Brazilian free-tailed bats in
Texas caves, and as few as 36 per season for grey bats in
Kentucky (Appendix S5). This mortality is strongest in the
first days of life (Foster et al. 1978, Hermanson & Wilkins
1986), and fallen young are sometimes eaten by scavengers.
Some young bats may fall from weakness due to disease,
malnutrition, or pesticide poisoning, but ultimate causes
are generally unknown.
Human-caused MMEs from accidents (Appendix S5)
include electrocution of flying foxes on utility wires in Aus-
tralia and in islands, incidental demolition of buildings with
roosts (Europe), collisions with aircraft (Australia), and col-
lisions with motor vehicles on roadways (Europe, North
America). Collisions with motor vehicles may be a large, but
widely unrecognised mortality factor for bats. Globally
there are over 35 million km of roadways (Anonymous
2015); most reported MMEs on roads have been from
studies in Europe that covered only about 150 km of
roadway in total, yet revealed deaths in 26 species of bats
(Appendix S5).
Multiple mortality events in bats T. J. O‘Shea et al.
10 Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd

MMEs due to collisions with wind turbines
A recent and unexpected form of MMEs in bats is associ-
ated with the global expansion of industrial wind energy
production. Multiple fatalities have been reported from
wind turbines in North America, Europe, South America,
Africa, and Australia, most during the past decade (Appen-
dix S6). Wind turbines are increasing globally and MMEs in
bats are likely to occur at most facilities, but the majority of
available reports are limited to Europe and North America.
We tabulated 281 MMEs involving 41 species; some carcass
counts numbered in the hundreds (Table 1 and Appen-
dix S6). This cause of MMEs is very recent (Figs 1 and 3),
widespread, and growing rapidly. Numbers of deaths vary
among sites for unknown reasons (Arnett et al. 2008).
However, estimates that include bias corrections (see
Appendix S6) range to thousands of bat deaths annually at
some facilities (Appendix S6). Cumulative deaths of bats at
turbines tabulated for Europe for the period 2003–2013
involved 5626 bats of 27 species in 18 countries (Rodrigues
et al. 2014), only a fraction of the likely mortality. Most
deaths of bats at wind turbines in temperate latitudes occur
during late summer and autumn, and disproportionately
affect migratory species that roost in trees (Cryan & Barclay
2009, Arnett & Baerwald 2013). In some regions, deaths of
some species at wind turbines far exceed other known
sources of mortality (Cryan 2011). Causes of susceptibility
to wind turbines are not fully understood, but some bats
seem attracted to them (Cryan et al. 2014).
MMEs attributable to or suggestive of viral
or bacterial diseases
Despite the high number of viruses known to infect bats
(e.g. Calisher et al. 2006, Luis et al. 2013), MMEs attribut-
able to infectious viral or bacterial diseases are rarely
reported. The absence of epizootics in bats has been noted
as remarkable by field researchers over many years. In his
review of Australian pteropodid ecology, Ratcliffe (1932)
stated: “No reliable evidence of the occurrence of epidemics
among the fruit-bat population was discovered.” In studies
of the southeastern myotis Myotis austroriparius, Rice
(1957) remarked “Disease is apparently unimport-
ant...During the course of this study, which involved
observations on over a million bats in every known cave
colony in Florida, I have never found a dead bat, and have
seen only one which appeared diseased.” In extensive
research on cavernicolous bats in North America, Twente
(1955) concluded “it would not seem probable that disease
is an important limiting factor.” Similarly, in ecological
studies of Brazilian free-tailed bats in Texas, which form the
largest aggregations of mammals on Earth, Davis et al.
(1962) observed that “Better conditions for epizootic spread
of disease can hardly be imagined, yet we did not observe
anything that looked like epizootic disease”.
We found 25 MMEs in 14 species of bats (Table 1) attrib-
utable to or suggestive of disease other than WNS, many
without confirmatory evidence of a specific agent or with
unexplained components (Appendix S7). MMEs in this cat-
egory involved maximum numbers in the thousands,
included some of the earliest (1839) reported die-offs of bats,
and occurred in Africa, Asia, Australia, Europe, North
America, and in islands (Appendix S7). Nine MMEs involved
pteropodid bats (six in islands). Brazilian free-tailed bats
accounted for seven of the 13 cases in North America (Appen-
dix S7). One event in North America provided supporting
evidence (bacterial isolation and pathology) for a bacterial
agent (Pasteurella multocida) killing about 100 individual big
brown bats during a 4-week period at a roost in Wisconsin,
USA (Blehert et al. 2014). With the exception of rabies, few of
the other MMEs had strong confirmatory evidence of a causal
organism; only three non-rabies reports suggested a specific
agent. A Bunyavirus was implicated in deaths of wrinkle-
lipped free-tailed bats Chaerephon plicatus in Cambodia,
Lagos bat virus (a rabies-like lyssavirus) was found in about
10–15% of several hundred dead Wahlberg’s epauletted fruit
bats Epomophorus wahlbergi examined in South Africa
(Appendix S7), and the recently identified Lloviu filovirus
was found in carcasses of Schreiber’s long-fingered bat
Miniopterus schreibersii that were sampled during MMEs
involving tens to hundreds of bats at two locations in Spain
(Appendix S7). In this latter case, the finding of the filovirus is
possibly incidental and the responsible cause remains uncon-
firmed (Olival & Hayman 2014). Multiple roosts in Spain,
France, and Portugal were also subject to MMEs contempo-
raneously, but these populations were not extensively
sampled diagnostically, and pathological and virological
results were inconclusive (Appendix S9).
Rabies is enzootic in populations of Brazilian free-tailed
bats, and given the huge size of some of these colonies, it is
not unexpected that deaths of 10 or more bats from rabies
have been reported within a season at roosts (Appendix S7).
These deaths from rabies, however, are not of epizootic pro-
portions (e.g. Davis et al. 2012 in Appendix S7). MMEs in
Brazilian free-tailed bats during the 1950s at Carlsbad
Caverns were equivocal: although >10 individuals had died
of rabies each year, others may have died of pesticide poi-
soning (Clark 2001), whereas inclement weather and abnor-
mally cool conditions may have been associated with many
of the deaths in 1955 and 1956, but not in 1957 (Appen-
dix S7 and references therein). Constantine (1967) postu-
lated that inclement, cool weather during periods of
migratory stress contributed to or perhaps caused the
MMEs at Carlsbad Caverns, as well as some unexplained
MMEs in this highly migratory species elsewhere (Appen-
dix S9). The Old World Schreiber’s long-fingered bat is also
T. J. O‘Shea et al. Multiple mortality events in bats
11Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd

a migrant that gathers in large colonies, and similarly has
been reported to suffer mortality that is unexplained or sus-
pected to be due to pesticides, migratory stress, or inclem-
ent weather (Appendices S3 and S9).
MMEs suggested to be due to disease affected large
numbers of pteropodid bats in islands (Appendix S7).
Perhaps disease is more likely to kill pteropodids in immu-
nologically naïve populations in islands, but corroborating
evidence for any infectious agents remains slim. In two
MMEs, disease was suspected because the die-off was con-
temporaneous with epidemics in humans (measles and dys-
entery). In a third case, subsequent authors suggested
alternatively that invasive ants may have been a causal factor
(Appendices S2 and S7). Two events involving mass abor-
tions of pteropids in Australia (Appendix S7) may have
been due to disease, but there was no confirmatory evi-
dence, and other possible causes (malnutrition, weather,
non-infectious agents) were not ruled out. However, as in
other cases, availability and application of diagnostic tools
for diseases of bats has been limited.
MMEs attributable to WNS
WNS is a fungal disease recognised in bats within the past
decade in North America. WNS is the only epizootic disease
known to cause widespread and high mortality in multiple
species of bats over multiple years. First documented at a
cave in New York, USA, during 2006, WNS has spread in
subsequent winters to affect most species of hibernating
bats in eastern North America (Turner et al. 2011). This
ongoing epizootic has killed millions of bats and is affecting
six or more species (Turner et al. 2011; Appendix S8);
important populations are in serious decline due to WNS
(Frick et al. 2010a, Thogmartin et al. 2013).
WNS is caused by the cold-growing fungus Pseudo-
gymnoascus destructans, which severely infects the skin
tissues of hibernating bats and catastrophically disrupts
hibernation and physiology during winter (e.g. Lorch et al.
2011, Warnecke et al. 2012). The fungus also infects bats in
Europe, where it is not known to cause MMEs (Puechmaille
et al. 2011). Macroecological analysis supports a hypothesis
that more severe WNS mortality in Europe may have
occurred much earlier than in North America (Frick et al.
2015). WNS continues to spread across North America, and
will probably continue to cause MMEs in additional species
and regions.
Unexplained MMEs
Seventy-three MMEs in 20 species of bats in Australia,
Europe, North America, and in islands lacked causal evi-
dence (Table 1 and Appendix S9). Nearly all of these MMEs
involved species that depend strongly on caves as roosts.
Two MMEs in Peter’s ghost-faced bat Mormoops
megalophylla during the 1950s in Mexico and cave myotis
Myotis velifer in the USA were mysterious; thousands of
mummified remains covered the walls and floors of caves
(Appendix S9). Other cases occurred in the 1960s during
peak usage and impacts of organochlorine insecticides; pes-
ticide poisoning may have caused some of these MMEs, as
previous authors speculated (Appendix S9). Forty-one
unexplained MMEs involved migratory species (Brazilian
free-tailed bats, Schreiber’s long-fingered bat, mouse-eared
myotis Myotis myotis); some researchers suggest migratory
stress as a possible cause (Appendix S9).
Bat population dynamics, MMEs, and
implications for the future
Recent studies indicate that population dynamics of bats
may be particularly sensitive to mortality. These studies pri-
marily involved temperate-zone species, but similar dynam-
ics are seen in large tropical pteropodids (Hayman et al.
2012). A recent brief review noted the similarity in the rela-
tive importance of life history traits of bats to those of many
large mammals: for the size of a bat population to remain
stable or to increase, annual survival of adults must be rela-
tively high: >75–80% (O’Shea et al. 2011a). Population
growth rates of bats show greater sensitivity and elasticity to
adult survival than to reproduction or juvenile survival.
This suggests that, compared with that of other small
mammals, the demography of bats is adapted to a narrow
range of mortality drivers, such as the natural biotic and
abiotic factors, disease, and natural accidents documented
in this review. These natural factors (with the recent excep-
tion of WNS) may operate more diffusely than some
anthropogenic factors. The magnitude of mortality due to
past intentional killing, recent incidence of WNS, and
increases in levels of accidental mortality from collisions
with wind turbines are likely to be additive; we doubt that
bat populations can sustain such additive mortality for
long. Furthermore, future climate change may increase the
frequency of MMEs through severe weather events, such as
extreme droughts, more frequent storms, and flooding
(examples in Appendix S3). Recent researchers (see Herring
et al. 2014) have concluded that climate change drove the
high temperatures in Australia in 2013 and 2014 that killed
hundreds of thousands of flying foxes (Appendix S3). Popu-
lation growth can also be negatively impacted through the
suppressed reproduction and reduced juvenile survival of
bats seen during periods of drought (Adams 2010, Frick
et al. 2010b, O’Shea et al. 2010, 2011b).
CONCLUSIONS
Many MMEs in bats have been reported over the years. Of
the nine potential causes that we differentiated, intentional
Multiple mortality events in bats T. J. O‘Shea et al.
12 Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd

killing by people caused the greatest proportion of MMEs
prior to 2000. People killed bats because they were consid-
ered sources of zoonotic disease, nuisances (e.g. bats that
roosted in buildings), or, in Australia and Asia, competitors
for fruit crops. People still kill and eat both insectivorous
and pteropodid bats in Asia, Africa, and in some islands.
Efforts to control bovine rabies transmitted by common
vampire bats in South America and southern North
America led to indiscriminate killing of non-target caverni-
colous bat species that continues to the present. Prior to
2000, about 11% of the reported MMEs were attributed to
natural abiotic factors. Projected extreme weather due to
continuing climate change (e.g. severe storms, flooding, and
drought) may increase the number of abiotic MMEs in the
future.
Two new causes of MMEs have taken precedence since
around 2000: death due to collisions with wind turbines
globally, and the fungal disease causing WNS in eastern
North America. Reports of MMEs due to these two causes
will probably soon outnumber all prior reports from all cat-
egories combined. Among all categories, MMEs due to viral
or bacterial diseases were most rarely reported. Unexplained
MMEs were not very common. This supports the hypoth-
esis that many microparasitic infections of bats do not
result in MMEs.
We believe that the life history attributes of bats histori-
cally allowed populations to compensate more easily for
natural causes of mortality. Intentional killing by humans
and very recent increases in mortality from other anthropo-
genic sources has put markedly greater pressures on many
populations of bats. Bats globally could benefit from policy,
education, and conservation actions targeting human-
caused mortality. Such actions are particularly important in
the face of the new and increasing threats of the 21st
century.
ACKNOWLEDGEMENTS
We thank Peggy Eby, Alan Hicks, Lee McMichael, Danilo
Russo, and anonymous reviewers for comments. This work
is a product of the Small Mammals Working Group of the
Research and Policy for Infectious Disease Dynamics
(RAPIDD) programme of the Science and Technology
Directorate (US Department of Homeland Security) and
the Fogarty International Center (National Institutes of
Health, NIH). RKP was supported by NIH IDeA Pro-
gramme grants P20GM103474 and P30GM110732, P. Thye
and the Commonwealth of Australia, the State of New
South Wales, and the State of Queensland under the
National Hendra Virus Research Program. Any use of
trade, product or firm names is for descriptive purposes
only and does not imply endorsement by the US
government.
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SUPPORTING INFORMATION
Additional supporting information may be found in the
online version of this article at the publisher’s web-site:
Appendix S1. Reports of multiple bat deaths due to inten-
tional killing by humans, including counts of dead bats
taken for use as food.
Appendix S2. Reports of multiple bat deaths due to biotic
factors other than infectious disease.
Appendix S3. Reports of multiple bat deaths due to natural
abiotic factors.
Appendix S4. Reports of multiple bat deaths due to envi-
ronmental contaminants, including pesticides.
Appendix S5. Reports of multiple bat deaths due to acci-
dents other than collisions with wind turbines.
Appendix S6. Reports of multiple deaths due to fatal inter-
actions with the blades of industrial wind turbines.
Appendix S7. Reports of multiple bat deaths due to or sug-
gestive of infectious viral or bacterial disease.
Appendix S8. Reports of multiple bat deaths due to the
fungal agent of white-nose syndrome, Pseudogymnoascus
destructans.
Appendix S9. Reports of multiple bat deaths due to unex-
plained causes.
Appendix S10. Literature cited for Appendices S1–S9.
Multiple mortality events in bats T. J. O‘Shea et al.
16 Mammal Review (2016) © 2016 The Mammal Society and John Wiley & Sons Ltd