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Multiple mortality events in bats: A global review

February 2016
Mammal Review 46(3):n/a-n/a

DOI:10.1111/mam.12064

Authors:

Thomas J. O’Shea

United States Geological Survey

Paul Cryan

United States Geological Survey

David T S Hayman

Massey University

Raina K Plowright

Cornell University

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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.

Causes of multiple mortality events in bats, expressed as percentages of all events (n), for each geographic region.

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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 Appendix S1; photograph by Pilot Dovih). (b) Pteropus species for sale at a market in Manado, Northern Sulawesi, Indonesia (photograph by D.T.S. Hayman).

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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

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.

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

100

150

200

250

300

stnevE ytilatroM fo rebm

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.

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.

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,

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

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.

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

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.

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

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.

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

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.

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.

Supplemental Data for Multiple Mortality Events in Bats

Data

November 2017

Thomas J. O’Shea

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AppendixS7

Data

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Thomas J. O’Shea · Paul Cryan · David T S Hayman · Raina K Plowright · Daniel Streicker

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AppendixS10

Data

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Thomas J. O’Shea · Paul Cryan · David T S Hayman · Raina K Plowright · Daniel Streicker

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AppendixS9

Data

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Thomas J. O’Shea · Paul Cryan · David T S Hayman · Raina K Plowright · Daniel Streicker

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AppendixS8

Data

January 2016

Thomas J. O’Shea · Paul Cryan · David T S Hayman · Raina K Plowright · Daniel Streicker

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AppendixS6

Data

January 2016

Thomas J. O’Shea · Paul Cryan · David T S Hayman · Raina K Plowright · Daniel Streicker

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AppendixS4

Data

January 2016

Thomas J. O’Shea · Paul Cryan · David T S Hayman · Raina K Plowright · Daniel Streicker

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AppendixS2

Data

January 2016

Thomas J. O’Shea · Paul Cryan · David T S Hayman · Raina K Plowright · Daniel Streicker

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AppendixS3

Data

January 2016

Thomas J. O’Shea · Paul Cryan · David T S Hayman · Raina K Plowright · Daniel Streicker

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AppendixS5

Data

January 2016

Thomas J. O’Shea · Paul Cryan · David T S Hayman · Raina K Plowright · Daniel Streicker

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AppendixS1

Data

January 2016

Thomas J. O’Shea · Paul Cryan · David T S Hayman · Raina K Plowright · Daniel Streicker

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Aug 2023

Co-infection is an underappreciated phenomenon in contemporary disease ecology despite its ubiquity and importance in nature. Viruses, and other co-infecting agents, can interact in ways that shape host and agent communities, influence infection dynamics, and drive evolutionary selective pressures. Bats are host to many viruses of zoonotic potential and have drawn increasing attention in their role as wildlife reservoirs for human spillover. However, the role of co-infection in driving viral transmission dynamics within bats is unknown. Here, we systematically review peer-reviewed literature reporting viral co-infections in bats. We show that viral co-infection is common in bats but is often only reported as an incidental finding. Biases identified in our study database related to virus and host species were pre-existing in virus studies of bats generally. Studies largely speculated on the role co-infection plays in viral recombination and few investigated potential drivers or impacts of co-infection. Our results demonstrate that current knowledge of co-infection in bats is an ad hoc by-product of viral discovery efforts, and that future targeted co-infection studies will improve our understanding of the role it plays. Adding to the broader context of co-infection studies in other wildlife species, we anticipate our review will inform future co-infection study design and reporting in bats. Consideration of detection strategy, including potential viral targets, and appropriate analysis methodology will provide more robust results and facilitate further investigation of the role of viral co-infection in bat reservoirs.

Common Noctule Nyctalus noctula (Schreber, 1774)

Chapter

Dec 2023

Supplemental Data for Multiple Mortality Events in Bats

Data

Full-text available

Nov 2017

Thomas J. O’Shea

We provide summaries of pertinent details regarding multiple mortality events of bats in a series of nine appendices. Appendix S10 lists all references cited in Appendices S1-S9. Events are given by region alphabetically, then chronologically within regions. The number of events entered into tallies are given in parentheses under the "Description" column. We attempted to be conservative in designating numbers of events. Unfortunately not all sources provide enough information to allow accurate judgments in each case. Generally we considered events extending over multiple years as one event per year, and events observed at more than one dispersed location as separate events. We considered events impacting more than one species of bat as separate events for each species, unless there was insufficient information on numbers per species. Events with insufficient information for each species were treated as single events. Scientific names follow Simmons (2005) in Wilson and Reeder's (2005) Mammal Species of the World, 3 rd edition

Bats as prey of diurnal birds: a global perspective

Cover Page

Full-text available

Jan 2016
MAMMAL REV

article publié en ligne janvier 2016

Declines and trade in fruit bats on Saipan, Tinian, Aguijan, and Rota

Article

Full-text available

Jan 1992

Old World Fruit Bats An Action Plan for their Conservation

Book

Jan 1992

Bats, emerging virus infections and the rabies paradigm

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Jan 2003

Activity patterns of the Mexican free-tailed bat

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Jan 1967

D.G. Constantine

Explaining extreme events of 2014 from a climate perspective

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Jan 2015
B AM METEOROL SOC

Notes on the distribution and ecology of Central African Chiroptera; and field notes

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Status of the Marianas fruit bat (Pteropus mariannus) in the northern Mariana Islands north of Saipan

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Jan 1992

T.O. Lemke

A minimum total population estimate of 7450 fruit bats is derived. Bat populations appeared at much higher densities on lightly hunted islands. Fruit bat populations for heavily and lightly hunted islands increased in similar proportions with increasing island size. In addition to illegal hunting, other threats to bat populations include volcanic activity, typhoons, military training, human development, introduced predators, and feral herbivores. Illegal hunting remains the greatest threat to fruit bats and possibly one of the few factors that can be controlled by human intervention. -from Author

Chiropteran mortality

Article