Fascinating Life Sciences

Lauren Moretto · Joanna L. Coleman

Christina M. Davy · M. Brock Fenton
Carmi Korine · Krista J. Patriquin Editors

Urban
Bats
Biology, Ecology,
and Human Dimensions
Fascinating Life Sciences
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Lauren Moretto  •  Joanna L. Coleman
Christina M. Davy  •  M. Brock Fenton
Carmi Korine  •  Krista J. Patriquin
Editors

Urban Bats
Biology, Ecology, and Human Dimensions
Editors
Lauren Moretto Joanna L. Coleman
Vaughan, ON, Canada Department of Biology
Queens College at the City University of
Christina M. Davy New York
Department of Biology Flushing, NY, USA
Carleton University
Ottawa, ON, Canada M. Brock Fenton
Department of Biology
Carmi Korine University of Western Ontario
Mitrani Department of Desert Ecology London, ON, Canada
Ben-Gurion University of the Negev
Midreshet Ben- Gurion, Israel Krista J. Patriquin
Department of Biology
Saint Mary’s University
Halifax, NS, Canada

ISSN 2509-6745     ISSN 2509-6753 (electronic)

Fascinating Life Sciences
ISBN 978-3-031-13172-1    ISBN 978-3-031-13173-8 (eBook)
https://doi.org/10.1007/978-3-031-13173-8

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Preface

The current geological epoch, the Anthropocene, is characterised by human activi-

ties that are so extensive and intense that they are leaving durable signals in strati-
graphic material. At the same time, wildlife must now contend with new challenges
in the Anthropocene, and previous work has shown that bats are no exception (e.g.,
Voigt & Kingston’s 2016 Bats in the Anthropocene). Nowhere is this truer than in
cities, which are the focus of Urban Bats: Biology, Ecology, and Human
Dimensions. Bats in urban areas experience the pressures of profound and ongoing
land cover change and other diverse challenges. Research on urban bats in recent
decades indicates that most bat species are negatively impacted by urbanisation. Yet
some species of bats succeed and even thrive in cities and towns. These observations
have inspired questions about bats in relation to urbanisation. Which traits and
behaviours equip bats for urban success? What features of urban areas increase the
likelihood that bats will successfully persist there or even colonise new areas? And
how does the success of urban bats affect human urbanites? To address these ques-
tions, Urban Bats: Biology, Ecology, and Human Dimensions builds on the foun-
dation of knowledge of bats in cities and adjacent areas, and aims to inspire future
research and promote the conservation of urban bats.
Intended primarily for environmental managers and an academic audience, this
book brings together authors and researchers from around the world to explore the
interactions between bats and urban environments. Thirteen chapters, organised into
three parts, explore these interactions through case studies or a summary of the
existing literature.
Part I, What is an Urban Bat? Morphological, Physiological, Behavioural,
and Genetic Adaptations, reviews the biology of urban bats. Chapter 1 addresses
traits related to stress and thermal physiology that might confer an advantage to bats
using urban areas. Chapter 2 explores the genetic impacts of urbanisation on the
family Pteropodidae, and Chap. 3 follows with a look at possible pre-adaptations of
molossid bats to life in cities. Phenotypic changes in urban bats are also explored
through their interactions with their ecto- and endoparasites (Chap. 4). Finally,
Chap. 5 examines the reproductive success and social structure of urban, frugivo-
rous bats.

v
vi Preface

Part II, How do Bats Inhabit Urban Environments? Uses of Artificial Roosts,
Aerial Habitats, and Green Spaces, examines the interactions between urban bats
and their environments. Chapters 6 and 7 explore bats’ use of natural and artificial
habitats in cities, with foci on bat box structures, urban green spaces, and water bod-
ies (blue spaces). Chapter 8 discusses some of the particular challenges that bats
face in navigating urban, aerial habitats. Chapter 9 investigates how insectivorous
bats in the Brazilian Atlantic Forest area are responding to recent and rapid growth
of nearby cities.
Part III, How do Bats and Humans Interact in Urban Environments?
Human Perceptions, Public Health, and Ecosystem Services of Bats, offers
insight into relationships between urban-dwelling bats and humans, including
human knowledge and attitudes (Chap. 10), public health considerations (Chap.
11), and bat-mediated ecosystem services (Chap. 12).
Finally, Chap. 13 offers a “big picture” perspective on urban bats, reflecting on
the information presented in previous chapters. In this chapter, we conclude the
book by considering how urban bats’ responses to urbanisation compare to those of
other, urban-dwelling mammals. Finally, we identify key knowledge gaps that can
be prioritised for future research and conservation efforts.

Vaughan, ON, Canada  Lauren Moretto

Flushing, NY, USA  Joanna L. Coleman
Ottawa, ON, Canada  Christina M. Davy
London, ON, Canada  M. Brock Fenton
Midreshet Ben- Gurion, Israel  Carmi Korine
Halifax, NS, Canada  Krista J. Patriquin
Acknowledgements

We are grateful to Burton K. Lim for guidance in the early stages of this project, and
to all who provided support during the writing and editing process.

vii
Contents

Part I What is an Urban Bat? Morphological, Physiological,

Behavioural, and Genetic Adaptations
1 
Stress Physiology, Foraging, and Ecophysiology of Bats in Urban
Environments��������������������������������������������������������������������������������������������    3
Carmi Korine, Phillip J. Oelbaum, and Agustí Muñoz-Garcia
2 
Genetic Impoverishment in the Anthropocene: A Tale from Bats������   19
Balaji Chattopadhyay, Kritika M. Garg, Rajasri Ray,
Ian H. Mendenhall, and Frank E. Rheindt
3 
Are Molossid Bats Behaviourally Preadapted to Urban
Environments? Insights from Foraging, Echolocation,
Social, and Roosting Behaviour��������������������������������������������������������������   33
Rafael Avila-Flores, Rafael León-Madrazo, Lucio Perez-Perez,
Aberlay Aguilar-Rodríguez, Yaksi Yameli Campuzano-Romero,
and Alba Zulema Rodas-Martínez
4 
Urban Bats and their Parasites��������������������������������������������������������������   43
Elizabeth M. Warburton, Erin Swerdfeger, and Joanna L. Coleman
5 
Bat Societies across Habitat Types: Insights from a Commonly
Occurring Fruit Bat Cynopterus sphinx������������������������������������������������   61
Kritika M. Garg, Balaji Chattopadhyay, D. Paramanatha Swami Doss,
A. K. Vinoth Kumar, and Sripathi Kandula

Part II How do Bats Inhabit Urban Environments? Uses of Artificial

Roosts, Aerial Habitats, and Green Spaces
6 
Bat Boxes as Roosting Habitat in Urban Centres: ‘Thinking
Outside the Box’��������������������������������������������������������������������������������������   75
Cori L. Lausen, Pia Lentini, Susan Dulc, Leah Rensel,
Caragh G. Threlfall, Emily de Freitas, and Mandy Kellner

ix
x Contents

7 
Aerial Habitats for Urban Bats��������������������������������������������������������������   95
Lauren A. Hooton, Lauren Moretto, and Christina M. Davy
8 
City Trees, Parks, and Ponds: Green and Blue Spaces as Life
Supports to Urban Bats ��������������������������������������������������������������������������  107
Lauren Moretto, Leonardo Ancillotto, Han Li, Caragh G. Threlfall,
Kirsten Jung, and Rafael Avila-Flores
9 
Assessing the Effects of Urbanisation on Bats in Recife Area,
Atlantic Forest of Brazil��������������������������������������������������������������������������  123
Enrico Bernard, Laura Thomázia de Lucena Damasceno,
Alini Vasconcelos Cavalcanti de Frias, and Frederico Hintze

Part III How do Bats and Humans Interact in Urban Environments?

Human Perceptions, Public Health, and Ecosystem Services
of Bats
10 Human
 Dimensions of Bats in the City��������������������������������������������������  139
Leonardo Ancillotto, Joanna L. Coleman, Anna Maria Gibellini,
and Danilo Russo
11 Urban
 Bats, Public Health, and Human-­Wildlife Conflict������������������  153
Christina M. Davy, Arinjay Banerjee, Carmi Korine, Cylita Guy,
and Samira Mubareka
12 Ecosystem
 Services by Bats in Urban Areas������������������������������������������  167
Danilo Russo, Joanna L. Coleman, Leonardo Ancillotto,
and Carmi Korine
13 The
 Big Picture and Future Directions for Urban Bat
Conservation and Research��������������������������������������������������������������������  181
Krista J. Patriquin, Lauren Moretto, and M. Brock Fenton

Index������������������������������������������������������������������������������������������������������������������  189
 Part I
What is an Urban Bat? Morphological,
Physiological, Behavioural, and Genetic
Adaptations
Chapter 1
Stress Physiology, Foraging,
and Ecophysiology of Bats in Urban
Environments

Carmi Korine, Phillip J. Oelbaum, and Agustí Muñoz-Garcia

Abstract  Urban environments alter various physiological responses of sympatric

animals. In this chapter, we provide an overview of stress physiology and the
responses of bats to different urban stressors, such as light and noise pollution. We
suggest future directions of research connecting urbanisation and stress responses
of bats, whose life history traits determine an idiosyncratic response to urbanisation.
We review how foraging behaviour and the physiological ecology of bats vary with
the urban environment and present data on the effect of roost microclimate on
metabolism and water balance of bats. We discuss these findings under an evolu-
tionary lens and conclude that synanthropic species of bats possess preadaptations.
These adaptations include resilience to urban stressors, fast flight, use of sheltered
roosts, and relatively low metabolic rates to survive and thrive in urban habitats.

Keywords  Stress physiology · Noise and light pollution · Roost energetics ·

Water balance

Supplementary Information The online version contains supplementary material available at

[https://doi.org/10.1007/978-­3-­031-­13173-­8_1].

C. Korine (*)
Mitrani Department of Desert Ecology, Ben-Gurion University of the Negev,
Midreshet Ben- Gurion, Israel
e-mail: [email protected]
P. J. Oelbaum
Department of Cell and Systems Biology, University of Toronto, Toronto, ON, Canada
A. Muñoz-Garcia
Department of Evolution, Ecology and Organismal Biology, Ohio State University at
Mansfield, Mansfield, OH, USA

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 3

L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_1
4 C. Korine et al.

1 Introduction

In the last two centuries, the human population has increased exponentially, with a
massive migration of people from rural to urban centres. Currently, 25% of the
world’s population lives in cities with over one million inhabitants.1 Modern cities
are a relatively new environment for animals, and many species have found oppor-
tunities to exploit new niches or have traits that make them well suited to coexist
with humans. These species can be described as synanthropic. Among 1450 known
species of bats, few can be considered synanthropic, and most bat species are nega-
tively affected by urbanisation [1, 2]. Environmental conditions in urban habitats,
such as light and noise pollution, possibly air and water pollution, and low diversity
of suitable roosts, may be detrimental to bats. Other factors, including increased
ambient temperature (Ta), high availability of food through the introduction of orna-
mental and invasive species of plants and animals, high density of food patches,
abundance of drinking water sources, and high availability of certain roost types,
may favour the presence of bats in urban environments [3].
In this chapter, we present studies that test the stress responses of birds and mam-
mals to urban disturbances and review how alteration of environmental variables in
urban environments may affect the stress response, foraging behaviour, and physi-
ological ecology of urban bats. Further, we present data on the effect of roost micro-
climate on metabolism and water balance of bats and synthesise these physiological
and dietary responses. We discuss how the physiology of bats might be affected by
the urban conditions and conclude that synanthropic species of bats may possess
preadaptations to survive and thrive in urban habitats.

2 Stress Physiology

The stress response has been defined as an organism’s behavioural or physiological

reactions to a variety of external stressors (e.g. pesticide levels, handling, captivity,
predation, heat load) and internal factors such as parasite load or starvation [4, 5].
Stressors may have short- or long-term effects, and animals may experience both
types of effects during their lifetime. Responses to stressors are regulated by the
hypothalamic-pituitary-adrenal (HPA) axis, through the elevation of glucocorticoid
(GC) hormone levels. Other neuroendocrine systems, such as the secretion of mela-
tonin by the pineal gland, also interact with the HPA axis.  These hormones are
responsible for maintaining the energetic balance needed to cope with stressors, and
under normal conditions, they regulate growth, circadian activity, reproduction, and
immune function in animals [6]. However, high levels of stress hormones are known
to inhibit the reproductive system and depress immune responses [6].

 https://ourworldindata.org/urbanization,
1
https://data.worldbank.org/indicator/EN.URB.
MCTY.TL.ZS)
1  Stress Physiology, Foraging, and Ecophysiology of Bats in Urban Environments 5

In bats, studies have shown that cortisol is the primary GC occurring in plasma.
However, available data are scarce because only 15 species have been studied (Table
S1.1). Other physiological responses may be associated, either directly or indirectly,
with stress hormones, including changes in haematological variables, depression of
immune function, increases in oxidative stress, and decreases in body condition [6].
Stress responses are commonly estimated by measuring the concentrations of
baseline plasma GC; however, this method is invasive, not suitable for use in small
animals, and only reflects variation in GC concentrations over the preceding hour.
For that reason, those who research wildlife stress physiology often use measure-
ments of faecal glucocorticoid metabolites (FGM) and cortisol levels in urine or
hair [Table S1.1 for studies on bats; 6–10]. Faecal or urine concentrations of cortisol
reflect average daily levels of the hormones, whereas cortisol concentrations in hair
reflect circulating levels over periods of several weeks or months [5]. The FGM
method is recommended when studying insectivorous bats because they are small
and sensitive to handling. However, the FGM method has certain limitations, such
as the inability to assign collected samples from daily roosts to specific individuals
or sexes. When studying fruit bats, plasma GC levels may also be obtained (Table
S1.1), as long as the whole blood sampling procedure takes less than 3 min of han-
dling [11]. Furthermore, because GC concentrations follow daily rhythms [11], it is
essential to measure baseline concentrations of the hormone before inferring the
effects of stressors.
Stress responses of animals are related to many external factors, such as season-
ality, city size, and experimental set-up [6]. These factors reflect the stressor type
and magnitude, and the duration of exposure to the stressor. In addition, stress
responses are modulated by intrinsic factors, such as sex, age, reproductive status,
food availability and quality, degree of plasticity to the response, and genetic back-
ground [12, 13]. The complex relationships between stress hormones and extrinsic
and intrinsic factors may explain the contradictory physiological responses of wild-
life to urbanisation. Indeed, reviews on birds [13] and several other vertebrate taxa
[6] have found that baseline or stress-induced plasma GC levels show no consistent
pattern in the short-term responses to chronic stress. However, these studies also
reported that, across all vertebrate taxa analysed, anthropogenic disturbances are
significantly associated with increased FGM concentrations. In a recent meta-­
analysis across a range of vertebrate taxa, Iglesias-Carrasco et  al. [14] found no
significant effect of urbanisation on corticosterone or cortisol concentrations in
plasma, faeces, hair, or feathers. The lack of associations between stress hormone
levels and the magnitude of environmental stressors could reflect differences in
assay methodologies [14], specific measures of physiological responses (i.e. GC
levels in hair vs. blood), types of stressors to which the animals were exposed, and
intrinsic factors that affect the response to the stressor (e.g. age, reproductive sta-
tus). These contradicting physiological responses should therefore be considered
when evaluating the stress responses of bats to urbanisation.
Studies of animals in natural habitats are mainly limited to short-term stress
responses, while life in urban environments also entails exposure to chronic stress-
ors, such as anthropogenic noise, artificial light at night (ALAN), and air and water
6 C. Korine et al.

pollution. Stressors imposed on wildlife in urban habitats force animals to modify

their behavioural and physiological responses in a way that either avoids or allevi-
ates the stress [15, 16]. In the next section, we summarise known physiological
stress responses to specific urban stressors that may affect bats.

3 Extrinsic Factors that Affect the Stress Response in Bats

Bats are highly mobile, mostly social, small, and sensitive to handling. As such,
their physiological responses to stress may be particularly complicated to study –
perhaps this explains why only a few stress physiology studies have focused on bats
(Table S1.1). Most such studies have aimed either to evaluate basic concentrations
of stress hormones in blood or faecal samples or to test how intrinsic factors, such
as sex, restraint, seasonality, and reproductive status, may affect the stress responses
(Table S1.1). Only two studies have addressed the stress response of bats in direct
relation to urbanisation [15, 17], while a third examined the effect of contaminated
water [18], and a fourth considered the effect of wind turbines [19].

3.1 Stress and Light Pollution

Artificial light at night (ALAN) is among the most striking environmental changes
associated with the expansion of urbanisation [20]. Artificial light at night disrupts
the natural spatial and temporal patterns that regulate light-dependent biological
processes in many organisms, including bats. In most bat species, ALAN elicits
avoidance behaviour [21–23] except for a few opportunistic species that forage on
insects or fruits [21]. Exposure to ALAN can eliminate the natural circadian rhythm
of GC release and increase GC concentrations in captive [24] and free-living ani-
mals [25] across different taxa, but studies on urban bats are yet to be performed.
Nevertheless, Injaian et al. [26] did not find a general relationship between ALAN
and baseline stress-induced corticosterone in birds and reptiles in their review. In
mammals, ALAN decreased GC concentrations, immune function, and body mass
[26–27]. However, these studies were mainly done under laboratory conditions and
high light intensities.  No evidence of a decrease in FGM levels, body mass, nor
survival probability were found when conducted with free-living bank voles
(Myodes glareolus) [28].

3.2 Stress and Noise Pollution

There is overwhelming evidence that anthropogenic noise constitutes an ecological

pollutant, with many deleterious effects on wildlife [29], although known physiolog-
ical responses of wildlife are variable. Noise from motorways seems to increase
1  Stress Physiology, Foraging, and Ecophysiology of Bats in Urban Environments 7

FCM concentrations of free-living wood mice [Apodemus sylvaticus; 30]. Brearley

et al. [31] reported that cortisol concentrations in the hair of squirrel gliders (Petaurus
norfolcensis) were elevated in animals that lived in edge habitats along major roads
that were noisy and with limited availability of hollow nests. In contrast, Łopucki
et al. [32] reported that corticosterone concentrations in faecal samples from a rural
population of striped field mice (Apodemus agrarius) were not different from those
of an urban population exposed to various anthropogenic stressors, including noise;
their findings might reflect a habituation response to urban noise.
For most bat species, echolocation is a crucial activity for navigating and detect-
ing resources, such as water and food. Thus, noise pollution may alter echo reception
and processing in bats, impairing the basic functioning of their echolocation abilities,
and may interfere with drinking behaviour [33] and passive detection of prey-­
generated acoustic cues [34–35]. Allen et al. [15] found that nonreproductive or lac-
tating female Mexican free-tailed bats (Tadarida brasiliensis) roosting under bridges
in Texas, United States, had lower baseline plasma GC concentrations than females
roosting in caves, suggesting that bats may not be affected by noise and light distur-
bances. However, during pregnancy, the highest baseline GC concentrations were
found in bats roosting under a bridge in a suburban area. Parry-Jones et al. [17] found
that urban grey-headed flying foxes (Pteropus poliocephalus) in Sydney, Australia,
had higher FGM concentrations than rural bats, but linked their findings to food
shortages that the bats experienced during the study, not to the chronic stress of
urbanisation. Wada et al. [18] and Medina-Cruz et al. [19] found no significant dif-
ferences in GC concentrations between bats captured in control and disturbed sites in
South River, Virginia, United States, and Oaxaca, Mexico, respectively.

4 Intrinsic Factors That Affect the Stress Response in Bats

In addition to the urban disturbances mentioned above, specific traits of bats should
be considered when studying their physiological response to stress in urban envi-
ronments. Most bat species are sensitive to anthropogenic disturbances [1]; how-
ever, stress responses of populations of conspecifics might vary with the degree of
urbanisation. It is reasonable to predict that, within a species, stress responses will
be stronger in populations that avoid urban habitats than in populations that occupy
them. Additionally, a city’s size, age, and composition (e.g. presence of large parks,
high-rise buildings, human population density) may play a role in how bats respond
to and adapt to urban stressors. To understand the magnitude of the stress responses
to urbanisation, we suggest studying the stress physiology of several colonies of a
sympatric species that vary in their association with urban environments or the size
of cities they inhabit, considering their colony size and degree of mobility, as well
as other intrinsic factors, such as diet and trophic guild (see below). In addition,
incorporating the genomic variation associated with responses to increased urban-
isation will facilitate testing whether stress responses result from phenotypic plas-
ticity or represent adaptive responses to urbanisation [12].
8 C. Korine et al.

4.1 Mobility

Bats can compensate for the short-term effects of stressors through flight. Generally,
bats may be divided into fast flyers with low manoeuvrability and slow flyers with
high manoeuvrability. In temperate areas, the most common urban-dwelling bats are
insectivores with high-aspect ratio wings and high wing loading, which allow them
to forage in open spaces, fly fast, and cover long distances [36]. These characteristics
allow bats to move at high speeds with relatively low-energy expenditure, but only at
the expense of reducing manoeuvrability in enclosed spaces, such as dense forests
[37, 38]. These traits are positively associated with body size, which allows urban
bats to feed on large prey (e.g. moths), with high-energy returns that diminish forag-
ing time [39]. It would be interesting to test whether sympatric and more mobile bat
species are less affected than sedentary bat species by short-term urban stressors and
whether mobility is a (pre)adaptive trait that allows them to cope with these stressors.

4.2 Sociality

Most species of bats live in groups and are philopatric. As a result, size, composition,
structure, and formation of groups may affect behavioural and physiological responses
and reproductive success. Urban bats are more likely to live in larger groups compared
to non-urban conspecifics because cities offer high availability of potential roosts and
food sources. As such, they may experience higher levels of chronic stressors.
Interestingly, Allen et al. [15] found that even though numbers of T. brasiliensis varied
from several thousand roosting under a bridge in a suburban residential area to more
than one million in one cave, the plasma GC concentrations of bats did not differ
between roost sites. In the meridional serotine (Eptesicus isabellinus), FCM concen-
trations did not vary among colonies of different sizes [40]. Reeder et al. [41] suggest
that being in a breeding group is chronically stressful for male pteropodids. Indeed,
male large (Pteropus vampyrus) and little golden-­mantled flying foxes (Pteropus
pumilus) living in secondary forests in Malaysia exhibit increases in total GC concen-
trations during the breeding season [41]. Furthermore, GC concentrations were higher
in captive males that were in the process of group formation than in males that were
already in stable groups [41]. Thus, the effects of colony size on stress responses, in
rural and particularly urban habitats, might be confounded with the impacts of roost
quality, social challenges, and breeding. More studies that control for at least one of
those factors are required to better understand these relationships.

4.3 Diet and Foraging Behaviour

Diet and foraging behaviour of urban bat populations may differ significantly
from populations in their natural habitats. Changes in foraging behaviour can
negatively impact bats through nutrient stress and tissue impairment and
1  Stress Physiology, Foraging, and Ecophysiology of Bats in Urban Environments 9

contribute to higher levels of GC plasma concentrations, causing long-term del-

eterious health effects [42]. Geggie and Fenton [43] found that big brown bats
(Eptesicus fuscus) spent more time foraging in urban areas than in rural areas of
Canada’s National Capital Region, suggesting lower prey density in cities. In
contrast, several other studies have noted decreased foraging periods in urban
environments leading to the hypothesis that this may be the result of greater prey
availability in cities [2]. These findings may be attributed to differences in patch-
iness of resources and resource accessibility [2, 36, 44]. In Mexico City, Mexico,
for example, large, vegetated areas are important foraging sites for bats, espe-
cially insectivores that are drawn in by swarms of insects around streetlights
[44]. Additionally, elsewhere in the Neotropics, frugivores and nectarivores
exploit ornamental plants in parks and green spaces as important dietary resources
[45]. We therefore suggest evaluating whether feeding in dense food patches may
buffer bats against energetic stress, enabling them to cope with consistent high
exposure to anthropogenic stressors. We suggest that this could be done by com-
paring the FGM concentrations and movements of bats between food-rich and
nearby food-poor patches.
Some frugivorous and insectivorous bat species seem to preferentially seek out,
or at least tolerate, urban areas. Aerial insectivores in general, and especially mem-
bers of the family Molossidae, are well adapted to open spaces and more abundant
in many temperate and Neotropical cities than members of other trophic guilds [44].
Urban populations of the greater noctule bat (Nyctalus lasiopterus) in Seville,
Spain, avoided wooded areas and had smaller, but more variable, home ranges com-
pared to populations found in a forest preserve – this shift between foraging strate-
gies in forests and cities could affect and help to modulate stress responses in urban
bats [46]. This means that if bats spend more time searching for food in forests than
in cities where patches of resources are more predictable and concentrated [46],
then this reduced hunting effort may modulate the impacts of other negative anthro-
pogenic stressors.
Bats with generalist diets and wide trophic niche breadth may also be better
adapted to urban life, because they can take advantage of novel resources [2].
Frugivorous bats in both the Neotropics and Paleotropics are well adapted to
feed from abundant fruit sources which are popular ornamental or agricultural
plants in urban areas [4, 44]. Studies that link dietary preference, diet quality,
and foraging time with stress hormone levels have shown that diet quality and
choice are associated with body condition and elevated stress responses in mam-
mals [47] and birds [48]. Experiments on frugivorous bats may determine how
fruit quality and dietary diversity affect FGM, considering other extrinsic and
intrinsic factors. For example, the neutrophil to lymphocyte ratio, a putative
stress indicator, in Neotropical frugivores increased under conditions of forest
loss  – a finding indicative of chronic stress [49]. These types of experiments
may also show whether urban bats with generalist diets have moderated stress
responses, which could indicate their degree of plasticity or preadaptation to
urban habitats.
10 C. Korine et al.

5 Ecophysiology of Bats in Urban Environments

The remarkable taxonomical and ecological diversity of bats may relate to their
ability to fly. Powered flight is associated with the presence of large, vascularised
wing membranes that increase the surface area-to-volume ratio, which, in turn, is
associated with high rates of metabolism and evaporative water loss. Therefore, bats
face potential challenges when it comes to maintaining their energy and water bal-
ances and demonstrate physiological and behavioural strategies to cope with these
challenges. For example, many bats can enter daily torpor, which significantly
decreases daily energy expenditure and water loss [50]. Additionally, many species
of bats use roosts whose microclimates help individuals maintain energy and water
balance [51]. Bats in urban habitats may therefore benefit from warmer microcli-
mates (see below) in daily or temporary roosts and artificial water sources.

5.1 Roosts and Energetics

Bats spend most of their lives in day roosts [51]. The appropriate roost microenvi-
ronment for temperature and humidity can reduce the thermoregulatory costs of
individuals and prevent frequent energetically costly arousals. Thus, the selection of
suitable roosts can have a tremendous impact on energy and water balance of indi-
vidual bats.
Urban environments provide a large availability of potential roosts but a low
diversity of roost types [1]. In cities, many bat species roost in buildings, under
bridges, and in other artificial structures. These roosts are usually occupied by indi-
viduals for long periods of time, a feature that might represent an advantage for
taxa, such as bats, that are at the slow end of the life history continuum [i.e. long-­
lived, with low reproductive outputs; 3]. Buildings can also serve as roosts for bats
that forage in adjacent areas where roosts are scarce [38]. Housing density was one
of the main determinants of bat species richness in Sydney, Australia, perhaps due
to high roost availability [36]. The benefits of roosting at urban settlements might
differ among different groups of bats. For example, in their natural habitats, molos-
sids tend to roost in crevices, which are not very abundant; in principle, the transi-
tion from roosting in crevices to roosting in buildings seems very plausible, and
these bats will find many potential roost sites in urban habitats [37, 44].
Because artificial roosts in urban environments are usually more sheltered than
natural roosts, they may provide higher thermal stability for bats, buffering against
external environmental conditions. Indeed, roost type can significantly influence
energy expenditure in bats. Czenze et al. [52] found that bats in buffered roosts have
a lower heat tolerance compared to those living in roosts that are more exposed,
with larger fluctuations in temperature. Marroquin and Muñoz-Garcia (pers. comm.)
tested the effect of roost type on mass-specific metabolic rate (msMR, calculated as
MR/body mass) of bats while controlling for phylogeny. They gathered data from
1  Stress Physiology, Foraging, and Ecophysiology of Bats in Urban Environments 11

the literature on msMR of euthermic individuals at ambient temperatures (Ta) rang-

ing from 0 °C to >40 °C (the range of natural roost temperatures) for 46 bat species.
They classified roosts into seven categories: (1) “no roost”, for exposed surfaces; (2)
“tree foliage and bark”, which included plant tents, tree bark and foliage, and leaf
litter; (3) “rock crevices”; (4) “tree cavities and hollow trees”; (5) “anthropogenic
tunnels and mines”; (6) “caves”; and (7) “buildings”. To account for the influence of
diet on metabolic rates, they assigned bats to one of the five dietary categories: car-
nivory, frugivory (includes nectarivory), insectivory (mainly consuming arthro-
pods), sanguinivory, and omnivory (consuming plants and animals). For each bat
species, they analysed the relationship between msMR and Ta in three temperature
regions: (1) below the lower critical temperature, where they estimated conductance
(the slope of the relationship between msMR and Ta) for each species; (2) the ther-
moneutral zone, using the lowest msMR value for each bat species at Ta ≥ 25 °C
(msMRmin) as a proxy for basal metabolic rate; and (3) above the upper critical
temperature, considering values of msMR for 15 species at Ta = 40 °C (msMRHT).
In their analyses of msMR, Marroquin and Muñoz-Garcia (pers. comm.) found
that below the lower critical temperature, conductance was higher for species in
more sheltered roosts (buildings and caves) than it was for bats in more exposed
roosts (no roost, tree foliage and bark). Also, species in sheltered roosts had a lower
msMRmin but higher msMRHT than species in exposed roosts. Finally, bats that use
more buffered roosts have a higher msMRHT than bats in exposed roosts (Table 1.1,
Fig. 1.1). Conductance was higher for insectivores and omnivores than for carnivo-
rous, frugivorous, and sanguivores. Frugivores had the highest msMRmin, whereas
insectivores had the lowest msMRmin (Fig. 1.1).
Overall, these results suggest that there is an association between energy expen-
diture and roost selection in bats. It seems that species that show low conductance
at ambient temperatures below the lower critical temperature use more exposed
roosts, whereas species with high conductance use sheltered roosts. We suggest that

Table 1.1  Relationship between msMR and Ta below the lower critical temperature in species of
bats in different dietary categories and different kinds of roost types
Slope of msMR Intercept of msMR Minimum MR msMR at
Roost type against Ta (mW/g °C) against Ta (mW/g) (mW/g) 40 °C (mW/g)
Buildings −1.0362 43.66 7.98 11.97 (n = 3)
Caves −1.1478 47.79 9.98 19.26 (n = 3)
Man-made – – 8.14 (n = 2) 16.05 (n = 2)
tunnels and
mines
Rock crevices −0.419 19.98 4.58 (n = 1) 7.21 (n = 2)
Tree cavities and −1.0772 37.69 7.41 8.74 (n = 1)
hollow trees
Tree foliage and −0.9093 37.92 9.60 9.90 (n = 3)
bark
No roost −0.7174 29.56 6.5 (n = 1) 10.51 (n = 1)
Data from Marroquin and Muñoz-Garcia (Submitted)
12 C. Korine et al.

Fig. 1.1  Minimum mass-specific metabolic rate (msMRmin) of euthermic animals for each roost
type. (Data from Marroquin and Muñoz-Garcia, submitted)

bats that live in more exposed roosts may have evolved physiological responses to
exposure to low temperatures. For example, decreasing conductance would result in
lower msMR at low ambient temperatures. Compared to bats with low conductance,
bats that exhibit higher conductance would be forced to use more energy at low
temperatures if they roost in exposed locations. We propose that these species
evolved behavioural responses; instead of adjusting their metabolic machinery to
face low temperatures, they select appropriate roost microclimates in sheltered
roosts, such as buildings, to save energy.
In natural habitats, roosts most likely represent valuable and scarce resources for
bats, whereas urban environments offer a greater availability of more sheltered
roosts, and species that use them likely do not face intense competition for those
kinds of roosts [1]. Cities also offer relatively exposed roosts, such as tree cavities,
trees, foliage, and others. Bats can also occupy these roosts, although there is evi-
dence that they may often be outcompeted by birds and insects [53]. Therefore, we
suggest that most bat species in urban habitats would use sheltered roosts in their
natural habitats, which would facilitate the transition to human-made structures.
The urban heat island effect, defined as the phenomenon whereby cities are
warmer than outlying areas [54], might also impact energy expenditure in roosts.
The higher conductance and the lower msMRmin found in building-roosting bats
indicate that these bats use less energy at moderate Tas compared to bats in more
1  Stress Physiology, Foraging, and Ecophysiology of Bats in Urban Environments 13

exposed sites (Marroquin and Muñoz-Garcia, pers. comm.). Thus, we suggest that
bats whose natural roosts are more sheltered might be preadapted to roosting in
buildings or other anthropogenic structures, which are abundant and readily avail-
able in urban environments. The finding that insectivory was the dietary category
associated with the highest conductance and the lowest msMRmin is consistent with
the idea that insectivory is another preadaptation to urban environments [2, 50].

5.2 Water Balance

Bats gain water by drinking and from their food (preformed water). Nonreproductive
bats lose water in faeces and urine, but up to 80–85% of water loss is total evapora-
tive water loss [TEWL; 50]. We collected data on TEWL across a wide range of Ta
from 22 species of bats and assigned bats to the same, seven abovementioned roost
categories (see Roosts and Energetics). Preliminary analysis showed that bats that
used exposed roosts had a lower mass-specific TEWL compared to bats that used
sheltered roosts, at Ta, ranging from 0 to 45 °C (P < 0.04; Fig. 1.2). These results
support the hypothesis that bats in exposed roosts mainly rely on physiological
adaptations to maintain their water and energy balance. They have low msMR

Fig. 1.2  Relationship between mass-specific total evaporative water loss (msTEWL) and ambient
temperature in euthermic bats that use exposed roosts (no roost, tree bark and foliage, and rock
crevices, dashed line) or sheltered roosts (buildings, caves, man-made tunnels, and tree cavities
and hollow trees, solid line). TEWL increases slowly at low and moderate ambient temperatures.
Beyond a breakpoint temperature, TEWL increases exponentially. The breakpoint temperature was
31.4 °C for bats in exposed roosts and 28.8 °C for bats in sheltered roosts; this difference was not
significant (P = 0.14). However, msTEWL was significantly lower at all temperatures in bats that
used exposed roosts compared with those bats that used sheltered roosts (P < 0.04)
14 C. Korine et al.

(Table 1.1) and seem to more efficiently use water at high temperatures. In contrast,
bats with higher msMR and TEWL rates at high temperatures may mostly depend
on behavioural selection of cooler roost microclimates found in buffered roosts,
such as buildings.
Urban environments usually have abundant permanent water, which not only
provides necessary drinking water for bats with high mass-specific TEWL rates but
also increases food availability compared with non-urban areas. For example,
Myotis spp. exhibit high activity close to water sources in urban environments,
where they can also find the water-emergent insects on which they feed [55]. Access
to drinking water is often the main limiting resource that determines distribution of
bats in their natural habitats [56, 57]. However, water balance of urban bats will
likely be less affected than in natural habitats, due to the high availability of drink-
ing water in urban environments.
As in all mammals, food and water requirements of female insectivorous bats
increase substantially during pregnancy and even more so during nursing. Milk pro-
duction by lactating females represents another significant avenue of water loss
[58]. Pregnant and lactating females must use warmer roosts to prevent entering
torpor, which prolongs gestation and decreases milk production [59]. Warm roosts
are relatively abundant in urban environments. However, exposure to higher tem-
peratures also leads to increased evaporative water loss; this fact, combined with the
increased water demands of milk production, implies that reproductive females
need to drink more often and maternity roosts should be close to water bodies
[56, 58].

6 Conclusions

Urban environments pose various insurmountable challenges for many species of

bats, which results in their absence from these ecosystems. It is difficult to predict
which species will succeed in cities. Urban species have unique strategies to cope
with pollution, anthropogenic noise and light, and other environmental factors that
are absent (or, at least, less prevalent) in their natural habitats [51]. The findings on
birds and mammals and preliminary studies on bats that we present in this chapter
highlight how physiological stress responses to anthropogenic disturbances can be
modulated by numerous extrinsic and intrinsic factors, which may mask general
patterns and should be considered when studying stress physiology. Specific factors
that should be considered for bats include their ability to fly, high degree of social-
ity, trophic niche, and use of diverse roost types. Furthermore, anthropogenic distur-
bances may have short- or long-term influences on wildlife, and we predict that
urban bats show a high degree of phenotypic plasticity in their physiological
responses to stress.
Urban bat species seem to share some key traits that make them preadapted to
succeed in cities. Species that flourish in urban environments have morphologies
that help them fly fast and commute over long distances at a relatively low energetic
1  Stress Physiology, Foraging, and Ecophysiology of Bats in Urban Environments 15

cost and locate and exploit patchily distributed resources. The abundance of food
patches in cities might significantly decrease foraging time and cost and widen tro-
phic niche breadths for bats.
Bats that use sheltered roosts seem to have lower metabolic rates at moderate Ta;
because cities are heat islands and are more thermally stable compared to adjacent,
non-urban areas, these species of bats might have lower-energy expenditures than
their counterparts that use more exposed roosts. Bats that use sheltered roosts seem
to have higher mass-specific TEWL rates than those using more exposed roosts, but
that will presumably not affect water balance of urban bats due to the high avail-
ability of drinking water in these environments.
Overall, there seem to be species of Chiropterans that show an “urban physiolog-
ical syndrome” that allows them to successfully colonise cities. Urban bats typi-
cally  are physiologically and behaviourally resistant to urban stressors; are
insectivorous or frugivorous; are fast, efficient flyers; use sheltered roosts; and have
relatively low metabolic rates compared with other bat species. This syndrome may
represent a preadaptation that results in high foraging efficiencies and low energetic
costs in urban environments.

Acknowledgements  This is publication 1114 of the Mitrani Department of Desert Ecology.

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Chapter 2
Genetic Impoverishment
in the Anthropocene: A Tale from Bats

Balaji Chattopadhyay, Kritika M. Garg, Rajasri Ray, Ian H. Mendenhall,

and Frank E. Rheindt

Abstract  Habitat loss, fragmentation, and anthropogenic climate change are major
drivers of biodiversity declines during the ongoing Anthropocene epoch.
Understanding the evolutionary trajectories of organisms with diverse life histories
in response to these threats can enable us to predict the fate of the extant biota facing
accelerated habitat loss and climate change. Genetic data contain vital clues about
species diversity and have been widely used to assess the impacts of non-­
anthropogenic climate change (since the Last Glacial Maximum and during the
Holocene) on a range of species. Recent advances in sequencing technologies and
analytical approaches have broadened the scope of genetic investigations. They
have allowed us to directly test for recent population bottlenecks linked to rapid,
anthropogenic environmental change. In this chapter, we discuss the utility of
genomic data in identifying evolutionary trajectories of bats in response to climate
change and habitat modification. We show that these nocturnal mammals are par-
ticularly sensitive to environmental and habitat fluctuations. We also summarise and
discuss our recent investigations of an urban population of the lesser short-nosed
fruit bat (Cynopterus brachyotis) from the island nation of Singapore and assess the

B. Chattopadhyay (*)
Trivedi School of Biosciences, Ashoka University, Sonipat, Haryana, India
Department of Biology, Ashoka University, Sonipat, Haryana, India
e-mail: [email protected]
K. M. Garg
Department of Biology, Ashoka University, Sonipat, Haryana, India
Centre for Interdisciplinary Archaeological Research, Ashoka University, Sonipat, India
R. Ray
Centre for Studies in Ethnobiology, Biodiversity and Sustainability (CEiBa),
West Bengal, India
I. H. Mendenhall
Duke-NUS Medical School, Singapore, Singapore
F. E. Rheindt
Department of Biological Sciences, National University of Singapore, Singapore, Singapore

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 19

L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_2
20 B. Chattopadhyay et al.

response of this population to rapid urbanisation during the Anthropocene.

Comparisons of genetic diversity estimates and evolutionary models through coales-
cent simulations revealed that this local population had been on a slow decline for
centuries but faced a more drastic bottleneck a few decades ago. We also observed
an astonishing level of decline in indicators of genetic diversity in the local popula-
tion over the past century, coinciding with the rapid urbanisation of Singapore. Our
observations show that even commonly occurring, synanthropic species of bat (i.e.
lives within and appears to benefit from urban environments) have been negatively
impacted by rapid urbanisation. Our results also highlight the necessity of assessing
the impact of urban green spaces on the evolution and survival of organisms like
bats, which often rely on these remnant habitats.

Keywords  Cynopterus brachyotis · Bottleneck · Genomic diversity · Lesser

short-nosed fruit bat · Urbanisation

1 Introduction

The Anthropocene is the age of human dominance and urbanisation [1–4], charac-
terised by rapid loss of natural habitats, climate change, and an ongoing biotic
extinction crisis of unprecedented proportions [1, 2, 4, 5]. Recent human activities
associated with global industrialisation have radically altered ecosystems, with
effects approaching the magnitude of natural events such as tectonic movements,
glacial cycles, volcanic eruptions, and other major disruptions [4]. The precise start
date of the Anthropocene epoch is still debated, but for the purposes of this chapter,
we set it at 1945, after which humanity has undergone a period of ‘great accelera-
tion’ during which human activities increased on an exponential scale [1]. These
activities drove an almost unparalleled episode of destruction of natural habitats,
sudden rise in global temperature, alteration of the prevalent climate, and the sixth
mass extinction in the history of life [2]. The Earth is being stripped of its biodiver-
sity as species are lost at a rate that is magnitudes higher than that of previous mass
extinctions, in which comparable losses occurred across tens of millions of years [2,
6]. We are losing species that have not even been discovered or described [7],
prompting scientists and governments to prioritise efforts to understand and miti-
gate damages to wildlife.
One of the key goals of contemporary biological sciences is to understand the
vulnerability of species or biotic communities to habitat modification and climate
change, not only to conserve and manage biodiversity but also to understand the
impact of biodiversity loss on human survival and well-being. Species’ vulnerabil-
ity to future climate change can sometimes be predicted based on their responses to
historic climatic alterations and concomitant habitat fluctuations [8, 9]. Quaternary
climatic fluctuations caused multiple periods of glacial maxima over the past two
2  Genetic Impoverishment in the Anthropocene: A Tale from Bats 21

million years that resulted in repeated range shifts for many species globally [8–11].
Significant reduction in global temperatures led to increased glaciation and arid-
ity. This reduced the available habitat for many taxa and forced them into isolated,
local refugia. However, sea levels also fell during these periods, connecting previ-
ously isolated landmasses (through land bridges) and expanding available habitat
for many other taxa [10–12]. These alternating periods of high isolation and high
connectivity drove fluctuations in population size and genetic diversity and in some
cases increased rates of speciation [8–11, 13, 14]. For example, increasing subdivi-
sion and speciation caused by Pleistocene glacial cycles are documented in many
bird species that inhabit islands and prefer forested habitats (specialists), while bird
species that use a much wider range of habitats (habitat generalists) exhibit lower
rates of speciation [13].
Bats are an interesting group with which to study the effects of climate change on
population size and genetic diversity. The order Chiroptera is the second largest
mammalian order, comprising more than 1400 known species of bat and harbouring
an enormous range of cryptic diversity [15–19]. Bats are also keystone species to
many ecosystems and serve as excellent bioindicators [20–22]. They are very sensi-
tive to abrupt climatic fluctuations, and heat stress during heatwaves has been linked
to mass mortalities in several regions [23–25]. Large, frugivorous species are suscep-
tible to heatwaves, as shown by mass mortalities of fruit bats recorded in Australia
during summer heatwaves [25]. The impact of climate change on bats is not always
negative as it may enable range expansions to cooler regions as observed in Mexican
free-tailed bats (Tadarida brasiliensis) [26]. Bats are ubiquitous and often associated
with human-modified habitat [20–22], but their evolutionary response to climate
change, both historical and current (i.e. human-mediated), is unclear.
To fill this lacuna in the framework of a long-term initiative to understand the
effects of climate change on wildlife, we assessed how bats have responded to
historic climatic fluctuations and further investigated the links between urbanisa-
tion and population endangerment. While studying the long-term effects of Earth’s
historic climate change, we reconstructed species’ evolutionary histories from
single genomes (PSMC analysis: pairwise sequentially Markovian coalescent)
and palaeohabitats of 11 phylogenetically divergent bat species with a wide range
of biological and ecological traits [8]. In that study, we assessed whether changes
in palaeohabitats during periods of climatic fluctuations correlate with changes in
effective population size. We observed a significant correlation between available
palaeohabitat and effective population size during the last glacial period.
Frugivores were particularly susceptible to global warming, with their population
size dramatically decreasing after the Last Glacial Maximum. Our comparative
genomic analysis also indicated that large insectivores generally have a low effec-
tive population size and that bat species generally entered the Holocene with low
effective population sizes [8]. These observations indicate overall vulnerability of
bats to climate change and concomitant habitat fluctuations. They also suggest
that a species’ biology and ecology play an important role in determining its resil-
ience during future climate change and habitat modifications [8]. Comparative
PSMC analyses across vertebrates remain rare in the scientific literature. However,
the available studies (e.g. 6 felids and 38 species of birds) reveal similar patterns
22 B. Chattopadhyay et al.

of declines in effective population size during the last glacial period for most taxa
and especially those that are currently endangered [9, 27].
Studying species’ responses to historic climatic fluctuations has highlighted that
knowledge of the past can shed light on the effects of more recent climate change.
This includes the changes during the past few centuries marked by the industrial
revolution in general and specifically during the last few decades that were charac-
terised by ultra-rapid urbanisation, mechanisation, and habitat loss [28]. In many
cases, however, the available methods of demographic reconstruction cannot suffi-
ciently capture the signals of these recent effects [28–30]. Rather, a comparison of
pre- and post-decline populations can alleviate this limitation and provide resolu-
tion of demographic histories during the Anthropocene [28, 30]. In this context,
biological collections are a treasure trove. Specimens collected over the last few
centuries and preserved in natural history museums worldwide can provide us with
genetic samples that reflect a population’s status prior to intense urbanisa-
tion. This enables a direct comparison with the contemporary (post-urbanisation)
population and generates a much deeper resolution into the nature of demographic
fluctuations [30]. Next-generation sequencing and bioinformatic pipelines capable
of analysing large datasets make it possible to generate and analyse genomic data
from degraded museum specimens. This approach has provided insights into his-
torical factors associated with endangerment of natural populations [28, 31, 32].
Armed with these technological advances, scientists hope to leverage species histo-
ries to predict their responses to environmental change and their mid- and long-term
viability [8, 28].
In old museum specimens, DNA is often heavily degraded due to storage time
and chemical damage from historically popular preservatives such as formaldehyde
[33]. This has long limited the utility of this valuable resource for genomic analyses.
Propitiously, it is now possible to generate large-scale DNA sequencing data even
from degraded biological material preserved in museums [33]. For example, a
recent study compared DNA from a woolly mammoth (Mammuthus primigenius)
fossil from about 45,000  years ago, when mammoths were plentiful across the
Holarctic region and the effective population size was around 13,000, with those
retrieved from a sample dating 4300 years ago from Wrangel Island in the Arctic
Ocean, where the population consisted of roughly 300 individuals and represented
one of the species’ last strongholds prior to extinction [34]. The analysis revealed
the accumulation of detrimental mutations in the isolated, island population, consis-
tent with the hypothesis of ‘genomic meltdown’ prior to extinction.

2 Temporal Genomic Data Reveal Drastic Population

Genetic Diversity Decline in a Tropical Fruit Bat

Although bats are one of the most common mammals in anthropogenically altered
habitats, the effects of urbanisation on the genetic diversity of bat populations are
unclear [8, 22, 28]. As part of our research to understand the sensitivity of bats
to Anthropocene habitat alterations, we investigated potential genomic
2  Genetic Impoverishment in the Anthropocene: A Tale from Bats 23

impoverishment in the Sunda lineage of the lesser short-nosed fruit bat (Cynopterus
brachyotis) following urbanisation of the island nation of Singapore. This medium-
sized, generalist fruit bat is widely distributed across Southeast Asia [35, 36]. It is
synanthropic (lives within and appears to benefit from urban environments) and is
often observed in cities, towns, and villages, in close proximity to humans.
Cynopterus brachyotis is broadly sympatric with at least two congeners: the larger
Horsfield’s fruit bat (C. horsfieldii) and a smaller, forest-dwelling species whose
taxonomic affinity remains unresolved [36].
Based on its synanthropic tendencies, we predicted that C. brachyotis would be
resilient to deforestation and would be able to use clusters of urban green space for
foraging. The Singapore Strait has largely isolated the population of C. brachyotis
of Singapore from its nearest neighbours in Peninsular Malaysia since the begin-
ning of the Holocene [37, 38]. Therefore, this study location allowed us to confi-
dently exclude most of the confounding effects of migration and gene flow.
Over the past century, Singapore lost about 95% of its forest cover in parallel
massive urbanisation and industrialisation. This caused a considerable loss in biodi-
versity and an estimated 34–87% loss of species in some taxa experiencing local
extinctions [7, 39]. However, careful planning and management have facilitated tree
canopy cover over 30% of the island’s area, which is high compared with many
other large cities (http://senseable.mit.edu/treepedia/cities/singapore).
To understand the impact of urbanisation on a commonly occurring species, we
compared the genomic diversity in C. brachyotis collected before and after the
intensive urbanisation of Singapore. We sampled bats collected in 1931 (pre-­
industrialisation, pre-urbanisation; n = 21) from the Lee Kong Chian Natural History
Museum (LKCNHM), Singapore [28], and from the contemporary population, sam-
pled in 2011–2012 (n = 20). Genomic diversity of these historic samples was com-
pared to contemporary samples collected in 2011–2012 (n = 20). We isolated DNA
in dedicated ancient DNA facilities designed for work with historic samples. We
targeted ~1.5 Mb of the C. brachyotis genome through sequence capture methods,
which are highly effective in comparing similar regions of the genome among sam-
ples [28, 40]. We designed our own sequence capture panel to target 1184 loci dis-
tributed across the genome (see Fig. 2.1 for target locus design). These loci were

Fig. 2.1  Target locus design used to isolate genome-wide data (see Chattopadhyay et al. [28] for
further details). In brief, we first selected exons from the little brown bat (Myotis lucifugus) genome
that are more than 200 bp long and are conserved across bats. Following this, we identified these
exons in the in-house generated genome of the lesser short-nosed fruit bat (Cynopterus brachyo-
tis). For every such exon in C. brachyotis genome, we also retrieved sequence data 500 bp upstream
and downstream; each of these intron-exon-intron segments was considered one locus for the study
24 B. Chattopadhyay et al.

amplified using sequence capture protocols and sequenced on an Illumina

HiSeq4000 platform (see Chattopadhyay et al. [28] for further details).
We generated over 634 million reads and retained approximately 483 million
reads after clean-up (removal of adapters, low-quality reads, PCR duplicates) [28].
Historic samples carried characteristic signatures of DNA damage: excessive cyto-
sine to thymine substitutions at the 5′ end and guanine to adenine substitutions at the
3′ end. All reads from these historic samples were rescaled and trimmed using map-
Damage 2 [41]. The cleaned reads were processed in two ways: first, by generating
sequence data for all 1184 target loci (using HybPiper pipeline 1.2 [42] and, second,
by aligning these reads directly to the C. brachyotis genome and mining genome-­
wide single-nucleotide polymorphisms (SNPs) (ANGSD [43]). This dual approach
helped us to generate diversity estimates informed by over a million base pairs of
sequence data and thousands of SNP loci. Our analyses required genetic markers
that are unlinked (i.e. have independent evolutionary histories), are selectively neu-
tral (i.e. do not directly affect the fitness of the organism and are therefore not under
selection) and have not undergone recombination. We checked our data for signa-
tures of these evolutionary processes and pruned loci identified in this screening,
retaining 874 loci for sequence-based analysis (990,087 bp) and 24,782 SNPs (see
Chattopadhyay et al. [28] for additional details).

2.1 Decline in Genetic Diversity

We compared genetic diversity and inbreeding coefficients of the historic and con-
temporary populations of C. brachyotis. For the sequence data, we estimated the
number of variable sites, number of parsimony informative sites, proportion of vari-
able sites, and proportion of parsimony informative sites using AMAS [44]. We
observed significant differences in genomic diversity estimated for all four sum-
mary statistics, with higher genomic diversity in historic populations than in con-
temporary ones (Fig 2.2a–d). We used the SNP data to measure internal relatedness,
homozygosity by loci, proportion of heterozygous loci, and standardised heterozy-
gosity relative to mean expected heterozygosity, using the R package GENHET [45,
46], pairwise relatedness using COANCESTRY 1.0.1.7 [47], and inbreeding coef-
ficients with PLINK 1.9 [48]. We also generated estimates of genome-wide proba-
bility of heterozygosity per individual in ANGSD for all individuals. All SNP-based
summary statistics other than homozygosity by loci were significantly different
between historic and contemporary populations (Fig. 2.2e–k). All summary statis-
tics suggested that the contemporary population is genetically impoverished relative
to the historic sample, with higher inbreeding coefficients and higher pairwise relat-
edness between individuals (Fig. 2.2).
2  Genetic Impoverishment in the Anthropocene: A Tale from Bats 25

Fig. 2.2  Comparison of genetic diversity estimates for historic and contemporary samples of the
lesser short-nosed fruit bat (Cynopterus brachyotis) from Singapore based on the sequence dataset
(A–D) and SNP dataset (E–K). * denotes p values less than 0.05, ** denotes p values less than
0.01, and *** denotes p values less than 0.001
26 B. Chattopadhyay et al.

Our observations illustrate an overall reduction in genetic diversity over the past
~90  years within the Singapore population of C. brachyotis (Fig.  2.2). The
Palaeotropical ecosystems of Asia have experienced large-scale destruction of for-
ests and other natural habitats in the past century [7, 39, 49–51]. This region also
harbours major biodiversity hotspots and cryptic diversity, with ongoing and regular
discovery of species new to science [49, 50, 52]. However, the pace and extent of
ongoing habitat destruction and the local effects of global climate change in
Southeast Asia may drive many species to extinction even before they are described
[7, 39, 49–51]. The island nation of Singapore is a microcosm of these challenges,
with rapid urbanisation during the past century in conjunction with drastic defores-
tation driving local extinction of multiple species during the last five decades [7, 39,
53, 54]. Cynopterus brachyotis can be synanthropic but is also a keystone species in
forests acting as both pollinator and seed disperser [55]. Declining genetic diversity
in the Singapore population of C. brachyotis suggests population declines concur-
rent with urbanisation, implying that urbanisation can drive even ubiquitous species
to become rare [28].

2.2 Drastic Population Bottleneck Coinciding

with Urbanisation

The correlation between low genetic diversity and extinction is well established in
the scientific literature; genetic factors partly predict the viability of small popula-
tions [56, 57]. Accumulation of deleterious mutations and overall loss of genetic
diversity in some isolated populations have also been speculatively linked to local
extinctions [31, 34]. Temporal sampling allows the empirical evaluation of genetic
diversity loss over time [28–30, 58], and reduced genetic diversity between historic
and contemporary samples implies fluctuations in population size. Comparisons of
ancient and contemporary diversity have revealed demographic trends over long
periods of time (e.g [58].).  However,  application of temporal sampling to under-
stand the potential effects of the Anthropocene on the genetic diversity of wild pop-
ulations is a relatively new approach [28, 30, 59, 60].
To understand the effects of human-mediated changes on the evolutionary trajec-
tory of the Singapore population of C. brachyotis, we assessed support for compet-
ing models of demographic history. We constructed six different scenarios of
population decline, including gradual decline, population bottlenecks (i.e. rapid,
dramatic decreases in population size), and a combination of both decline and bot-
tlenecks. We also included a model of constant population size and a model for
gradual population expansion. We used the site frequency spectrum (SFS) for
demographic reconstructions in fastsimcoal 2.6.02 [61] to compare these eight
models (see Chattopadhyay et al. [28] for further details). We used a temporal sam-
pling approach for demographic reconstructions as it can robustly identify bottle-
necks under most circumstances compared to only analysing modern samples [29].
2  Genetic Impoverishment in the Anthropocene: A Tale from Bats 27

Fig. 2.3  Visual representation of the best fit model of demographic history of the Singapore popu-
lation of the lesser short-nosed fruit bat (Cynopterus brachyotis)

We observed that the best model was the most complex one (Fig.  2.3), positing
historic gene flow from an ancestral, unsampled population and a continuous decline
that started 195 generations ago (range: 63 to 507 generations ago). Assuming a
generation time of 8 years for C. brachyotis, this suggests that this decline started
approximately 1600 years ago. This model also estimated a very recent bottleneck
at nine generations ago (~1939, but range 2–11 generations ago).

2.3 Common Species Are Not Immune to the Effects

of Fragmentation

Our demographic models provide strong evidence of direct impacts of urbanisation

on natural populations, which may also apply to wildlife in other rapidly changing
landscapes. The estimated timing of the recent bottleneck in the Singapore popula-
tion of C. brachyotis coincides with the advent of the Anthropocene [1], a period of
rapid urbanisation and drastic decline of forest cover in the island nation [7, 39, 54].
Ongoing efforts to promote habitat regeneration in Singapore may support the
recovery of this and other affected populations, and long-term monitoring of these
populations can assess the impact of such efforts.
The severity of the estimated bottleneck is considerable, as the nearly 30-fold
decrease (range: 3–96-fold decline) is likely detrimental to population viability
(Fig.  2.3). Bottlenecks increase a population’s vulnerability to stochastic events
increasing the probability of local extinctions [56, 57, 62]. Loss of genetic diversity
and population bottlenecks due to human interference has been documented in
many endangered vertebrates [5, 31, 56]. Our results build on this literature by dem-
onstrating these effects in a common species in response to urbanisation.
The low genetic diversity and effective population size of C. brachyotis in
Singapore (Fig.  2.3) raise concerns about the long-term viability of this island
28 B. Chattopadhyay et al.

population and provide a sobering example of the effect that urbanisation may have
on wildlife. Human-mediated habitat alterations are not only severely detrimental to
the survival of rare species but also affect common species coexisting closely with
humans [28]. The Anthropocene, the epoch of human dominance, is synonymous
with devastating defaunation due to human activities [1, 2, 4]. A recent study showed
declining population sizes and shrinking ranges in ~9000 vertebrates, including
common species, over the last century [6]. These ongoing declines imply an accel-
erated pace of genetic impoverishment that can interact with small population sizes
to increase extinction risk [6]. Our study illustrates how modern sequencing tech-
nologies and genomic analyses can untangle the patterns and processes driving
diversity loss, elucidating its causes and consequences in the medium and long
term. Our study also illustrates the value of museum collections in enabling tempo-
ral sampling and comparisons of pre- and post-urbanisation populations, to quantify
the true effects of the Anthropocene. We particularly acknowledge the value of
museum collections that have been built by the massive efforts of various collectors
in the past.

3 Conclusion

Taken together, our observations from bats provide insights into the effects of
human-induced climate change and landscape modifications, particularly urbanisa-
tion, on resident wildlife. In a synthesis of multiple studies, we found that bats are
particularly sensitive to climatic fluctuations and habitat loss. Our integrative
research paradigm connecting past climate and habitat alterations with genome-­
scale data allowed us to identify detailed evolutionary patterns of natural popula-
tions from present diversity to historical fluctuations going back millions of years.
Our results add to the growing body of literature showing the threat posed to wild-
life by human encroachment. They also provide direct evidence of genetic impacts
of urban development, indicating that even common, synanthropic species are
threatened by urbanisation and climate change. Fruit bats such as C. brachyotis are
keystone species that play a primary role in pollination, germination, and regenera-
tion of native tree species [55, 63]. As such, the decline of these bats may adversely
affect not only the function of the ecosystems they inhabit but also their long-term
ability to support populations of humans and other wildlife.

4 Acknowledgements

B.C. acknowledges funding from the Trivedi School of Biosciences start-up fund.
IHM acknowledges NUS Global Asia Institute Grant NIHA-2011-1-005 for sam-
pling. KMG acknowledges the support of DBT Ramalingaswami Fellowship (No.
2  Genetic Impoverishment in the Anthropocene: A Tale from Bats 29

BT/HRD/35/02/2006). The authors thank the Lee Kong Chian Natural History
Museum for providing historic samples.

5 Data Availability

The data used for this study are available on Sequence Read Archive (project acces-
sion number is PRJNA666066) and GenBank (genome accession ID:
GCA_009793145.1).

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Chapter 3
Are Molossid Bats Behaviourally
Preadapted to Urban Environments?
Insights from Foraging, Echolocation,
Social, and Roosting Behaviour

Rafael Avila-Flores, Rafael León-Madrazo, Lucio Perez-Perez,

Aberlay Aguilar-Rodríguez, Yaksi Yameli Campuzano-Romero,
and Alba Zulema Rodas-Martínez

Abstract  For most wildlife, cities are fairly hostile and resource-limited environ-
ments. However, some species of bats can persist and even thrive in cities. Species
of Molossidae dominate urban bat assemblages in many tropical and subtropical
cities around the world, but which intrinsic traits explain their ability to persist in
cities? We explore how molossids may be preadapted to cities, with particular atten-
tion to their foraging, echolocation, social, and roosting behaviours. We hypothesise
that behavioural plasticity strongly drives their ability to exploit the urban
environment.

Keywords  Preadaptation · Molossidae · Behavioural plasticity · Urban exploiters

· Fast-flying bats

1 Introduction

Urbanisation is a human-driven process of land cover change that reduces the size
and connectivity of natural and agricultural habitats and that modifies the biophysi-
cal attributes of the remaining, inner fragments. At finer scales, urban spaces repre-
sent novel ecosystems in which abiotic conditions, biotic interactions, and
distribution and abundance of resources are all altered, to varying degrees, relative

R. Avila-Flores (*) · R. León-Madrazo · L. Perez-Perez · A. Aguilar-Rodríguez ·

Y. Y. Campuzano-Romero · A. Z. Rodas-Martínez
División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco,
Villahermosa, Tabasco, Mexico

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 33

L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_3
34 R. Avila-Flores et al.

to the native ecosystem. During the process of urbanisation, living organisms face
novel environmental conditions that may represent a challenge or an opportunity
depending on their specific traits. Within a population, natural selection favours
those individuals whose morphological, physiological, and behavioural traits are
better suited to face the novel, urban conditions. Consequently, evolutionary adapta-
tion may gradually take place after many generations in animal populations living
in cities [1].
Evolutionary adaptation, a process that occurs over many generations, is not the
only mechanism that allows populations to successfully exploit urban environ-
ments. The phenotypes of organisms facing novel urban conditions may help to
predict individual-, population-, and species-specific responses to urbanisation.
Urban adaptedness, or the ability to immediately respond to challenges imposed by
urban environments [1], is largely determined by pre-existing adaptations or pread-
aptations (also known as exaptations) of species. Among bats, insectivorous species
with long, narrow, and pointed wings seem preadapted to successfully exploit urban
areas [2, 3]. To explain this pattern, it has been hypothesised that a fast, economical
flight allows individuals to readily move among patches of food within the city
while also favouring the efficient exploitation of insects that swarm at streetlamps.
In addition, fast-flying bats might avoid many dangers of the urban environment by
flying at high altitudes [4, 5].
The family Molossidae (free-tailed bats), the fourth most diverse among
Chiropteran families with 122 species [6], includes the most prominent examples of
bats having relatively long, narrow, and pointed wings [7]. As expected, molossid
species are among the most successful urban exploiters in the world [3], with rela-
tively abundant urban populations in Africa (e.g. large-eared free-tailed bat,
Otomops martiensseni), Europe (e.g. European free-tailed bat, Tadarida teniotis),
Oceania (e.g. white-striped free-tailed bat, Tadarida australis), and the Americas
(e.g. Mexican free-tailed bat, Tadarida brasiliensis and Molossus spp.). However,
molossids’ responses to urbanisation are species-specific and geographically vari-
able. Not all molossids can be considered urban exploiters, and, indeed, some
appear to be urban avoiders (e.g. hairless bat, Cheiromeles torquatus, and dwarf
dog-faced bat, Molossops temminckii) [2, 8]. This begs the question of whether
molossid bats are really preadapted to urban environments. What factors besides
flight style may help to explain this family’s differential responses to urbanisation?
In this chapter, we explore the potential roles of foraging, echolocation, roosting,
and social behaviours in molossid preadaptation to urbanisation and discuss the
importance of behavioural plasticity to urban tolerance.

2 Foraging Behaviour

More than any other mammalian order, bats have extremely diverse morphofunc-
tional adaptations that allow them to successfully forage in specific environmental
contexts [9]. For example, insectivorous bats that have gracile skulls, thin
3  Are Molossid Bats Behaviourally Preadapted to Urban Environments? Insights… 35

mandibles, and small teeth tend to feed upon soft-bodied insects such as lepidopter-
ans, whereas species that have crested skulls, thick mandibles, and larger teeth usu-
ally hunt hard-shelled insects, such as beetles [10]. Meanwhile, wing morphology
largely determines which microhabitat (e.g. cluttered vs uncluttered, open vs edge)
bats will use to forage [7]. Because the distribution of preferred food resources var-
ies over space and time (even at small spatiotemporal scales), species’ morphologi-
cal traits may relate to other aspects of foraging behaviour, such as flight altitude
[11], maximal distance travelled to forage [7], or temporal patterns of activity
[which might be coupled with temporal availability of food; 12].
Molossids are the most remarkably adapted bats when it comes to hawking on
high-flying insects. They have high aspect ratio (long and narrow) wings with high
wing loading (heavy-bodied bats). This design may not confer the manoeuvrability
needed in cluttered microhabitats, but it does promote fast and economical (low-­
energy expenditure) flight, which is well-suited to hunting in open spaces [7]. This
flight style allows some species to move unusually long distances (≤ 50 km) at high
altitude (> 3000 m) to reach suitable patches of food each night [13]. Molossids also
exhibit high foraging efficiency (high capture success), which may explain why
some species have extremely short periods of activity [14]. Furthermore, the ten-
dency of many species to emerge from their roost around sunset/sunrise [12] sug-
gests that high ambient light does not significantly impede their foraging and
commuting. Support for this hypothesis comes from observations that moonlight
may not affect foraging by some molossids [e.g. velvety free-tailed bats (Molossus
molossus); 15].
Molossid bats could take advantage of some behavioural and morphofunctional
traits to successfully forage in highly urbanised landscapes. For example, flying fast
and economically could help them access distant patches of food across spatially
large cities [4, 5, 16] or in non-urban (e.g. rural, natural) areas outside cities [17].
Furthermore, high-altitude flight might mitigate (or entirely eliminate) many urban
challenges for bats, including human activity, vehicles, and noise. Light tolerance
might partly explain why some molossid species thrive in heavily urbanised envi-
ronments [17]. For example, the bimodal pattern of emergence (sunset/sunrise)
observed in black mastiff bats (Molossus nigricans, previously known as Molossus
rufus [18]) in natural habitats [15] has also been observed in urban settings  – it
likely helps this bat hunt crepuscular urban beetles [14]. Being able to tolerate
bright light must also surely be a prerequisite to exploiting clusters of insects at
streetlamps. Even species that do not emerge from their roosts until well after dark
(e.g. big free-tailed bats, Nyctinomops macrotis) may forage in the open at street-
lights in highly urbanised sites [4].
The above-mentioned traits (wing morphology and light tolerance) typify molos-
sids, and although at first glance this might seem to make all molossid species pre-
adapted to forage in cities, that is not the case. In fact, some species of generally
urban-tolerant genera (Tadarida, Otomops, Eumops, Molossus) are rare in urban
environments. As such, factors besides flight style must explain urban tolerance
among molossid bats. Future research could analyse, for example, whether and how
dietary plasticity helps bats to hunt novel urban insect assemblages, the importance
36 R. Avila-Flores et al.

of vertical and horizontal distribution of potential prey in cities, or the role of learn-
ing in detecting high-quality food patches that are ephemeral and unpredictable
(e.g. insect cluster swarms at stadium lamps). Although these lines of inquiry are
worthwhile, they are challenging to pursue because of how difficult it is to record
bats at high altitudes.

3 Echolocation Behaviour

Echolocation is used by most bats to create a three-dimensional image of the sur-

rounding environment and involves the emission of high-frequency vocalisations
(calls) and the subsequent decoding of the returning echoes [19]. Bats use echoloca-
tion to deal with the challenges of nocturnality and specifically to detect, track, and
capture prey (or forage on other foods), to navigate and avoid obstacles, and to cre-
ate acoustic landmarks. Echolocation, in combination with social calls, can be used
to transfer information (e.g. about sources of food) between group members inside
and outside roosts and plays a role in mother-pup communication and mate selec-
tion [20]. Call design is not a fixed attribute, and it may be adjusted by echolocating
bats depending on the immediate task and spatial context [21].
Molossids (but not Molossops spp.) typically emit long duration, low-frequency
(20–40  kHz), search-phase echolocation calls with narrow bandwidth and long
interpulse intervals – a strategy that lets them detect large insects in the open over
savannas and forest canopies [7, 22], but not discriminate objects against cluttered
backgrounds [23]. However, individual T. brasiliensis have been shown to greatly
modify call design during mass emergence from cave roosts, increasing both the
bandwidth and the frequency to get a more detailed picture of their surroundings
[24]. Other molossids also exhibit a high call plasticity, especially when it comes to
adjusting the shape, frequency, and bandwidth, which might represent an “advanced
evolutionary trait” of these bats, as argued by Jung, Molinari, and Kalko [22].
In combination with wing morphology, echolocation call design is identified as
a key predictor of bats’ urban tolerance. Urban tolerance is correlated with lower
(peak or characteristic) call frequencies among Asian, Australian, and North
American bats and longer call durations among Australian and South American bats
[2]. The ability to detect distant objects, coupled with a fast and economical flight,
allows molossid bats to move and hunt in the open above buildings, noisy areas, and
other urban features. Compared to slow-flying insectivores, molossids might rely
less on acoustic landmarks on the ground to orientate and commute in cities [4].
The fact that not all molossids succeed in cities raises the question of whether
echolocation behaviour differs between urban-tolerant and urban-sensitive species.
Species of Molossops, for example, would not be expected to succeed in highly
urbanised sites because they produce higher-frequency, shorter calls than other
molossids [22]. Following the conclusions of Jung and Threlfall [2], it is likely that
larger molossids that emit lower-frequency calls are better preadapted to forage in
open spaces above urban features than smaller species. However, some ability to
3  Are Molossid Bats Behaviourally Preadapted to Urban Environments? Insights… 37

detect trees, power cables, poles, and even other foraging bats at relatively short
distances would help molossid bats forage in the proximity of streetlights. Such an
ability would also be useful to detect and avoid obstacles when bats emerge from or
return to roosts, especially roosts in low-rise structures. In addition, the capacity to
adjust call frequency would reduce interference from urban noise. Therefore, we
hypothesise that vocal plasticity is an important determinant of a species’ preadap-
tation to urban landscapes. In fact, high variation in the echolocation call structure
of T. brasiliensis (an urban-tolerant bat) has been reported for individuals flying at
different altitudes, from a few to more than 800 m above the ground [25]. Adjustments
in call frequencies have also been reported for individual T. brasiliensis foraging in
the presence of conspecifics at urban streetlights [26]. However, the study of vocal
plasticity in urban bats is a research area that has received little attention.

4 Social Behaviour

Most species of bats spend most of their lives in groups, exhibiting a remarkable
diversity of social organisation systems (including mating, roosting, and foraging
systems). Although most bat groupings gather exclusively inside roosts, they may
also do so outside roosts for reproductive or foraging purposes. Within roosts, bats
exhibit diverse group forms that can be characterised based on their structure, com-
position, and sociality. According to Kerth [27], groupings may involve large num-
bers of individuals that are rarely in physical contact (aggregations), moderate
numbers of individuals that are usually in physical contact (colonies), or smaller
numbers of bats which direct more affiliative or sexual interactions towards their
own group mates than towards members of neighbour groups (social groups). The
benefits of group life for individual bats include thermoregulatory efficiency (and,
hence, energy savings), optimisation of pup growth, information exchange,
enhanced detection of suitable roosts, defence of mating partners, and, in some
cases, enhanced cooperative behaviours such as allogrooming and food
exchange [28].
Molossids exhibit a variety of grouping strategies within day roosts. In natural
environments, group sizes may range from tens [29] to millions [30] of individuals,
depending on roost permanency, roost availability, and the species’ social system.
Within roosts, some molossids, such as Florida bonneted bats (Eumops floridanus),
giant mastiff bat (O. martiensseni), Midas free-tailed bats (Tadarida midas), and
little free-tailed bats (Trichopsis pumila), exhibit polygyny [31, 32], while others,
such as broad-eared bats (Nyctinomops laticaudatus) and T. brasiliensis, are pro-
miscuous [31, 33]. On the other hand, the nature and intensity of molossids’ social
interactions are poorly studied [except for the well-documented mother-pup bond-
ing T. brasiliensis; 34]. In many molossids, chemical signals produced by gular
glands (especially in males) seem to play a prominent role in the selection of sexual
partners and/or the marking of territory during the mating season [35, 36].
Interestingly, studies on E. floridanus and T. brasiliensis suggest that the role of
38 R. Avila-Flores et al.

gular gland secretions of molossids may change depending on the size of the group-
ing to optimise energy expenditure associated with resource defence [32, 37].
Cities potentially offer molossids many available roosts (albeit smaller ones
compared to natural settings), in which it is possible to establish social groups or
colonies of varying sizes [37]. Groups of T. brasiliensis, M. nigricans, Sinaloan
mastiff bats (Molossus sinaloae), and dwarf bonneted bats (Eumops bonariensis)
are relatively common in Neotropical cities [30, 35, 38], where they exhibit colony
or group sizes like those in natural settings (except for T. brasiliensis, whose urban
colonies tend to be much smaller than cave colonies). Scattered information in the
literature suggests that the social structure of urban molossids is relatively flexible,
with either male- or female-biased sex ratios [e.g. Eumops glaucinus, M. nigricans,
E. bonariensis, M. sinaloae, N. laticaudatus, T. teniotis, and T. brasiliensis and big
crested mastiff bat, Promops centralis; 35, 38]. In T. brasiliensis, social flexibility
might extend to the mating system, as small groups kept in captivity may exhibit
polygyny with territorial defence [39] – an observation which suggests that some
urban molossids might adjust their social structure to group size (which is in turn
limited by roost dimensions). Furthermore, the fact that many molossids have gular
glands speaks to the potential for males to defend territories in small roosts like
those commonly encountered in cities. We suggest that molossids’ flexible social
organisation (as a function of group size) could be an additional factor that favours
some species in urban environments. However, the limited information on the social
system of most molossid species [31] makes this hypothesis difficult to test.

5 Roosting Behaviour

Because bats spend most of their lives roosting, the selective pressures of the roost
environment are of paramount importance. A suitable roost offers protection against
predators and the elements, favours social interactions, facilitates the care and
growth of pups, and reduces the energetic costs of thermoregulation [40]. It has
been suggested that microclimate (temperature, humidity, and wind speed) is the
most important determinant of roost selection in bats [41], and for many species,
roost permanency affects roost fidelity [42]. Therefore, it is not surprising that caves
(permanent structures with stable microclimates) are a common type of roost for
most bats, although many species commonly use permanent anthropogenic struc-
tures, such as mines, buildings, roofs, culverts, and bridges.
Except for some species (e.g. T. brasiliensis), the natural roosting behaviour of
most molossids is poorly known. There is scattered evidence that molossids in natu-
ral environments use diverse roosts, including caves [43], tree cavities [44], crevices
in rocky cliffs [45], or even holes in archaeological ruins [33]. Most molossids do
not regularly roost in caves, but when they do, they can form huge aggregations (e.g.
T. brasiliensis and N. laticaudatus). Depending on the season, T. brasiliensis may
use caves as mating roosts, maternity roosts, or unisexual non-reproductive roosts
[46]. In this review, we did not find any studies of roost selection (contrasting used
3  Are Molossid Bats Behaviourally Preadapted to Urban Environments? Insights… 39

with unused/available roosts) by molossids in natural areas, which likely reflects the
natural scarcity of suitable roosts for these bats. It is also likely that most molossid
roosts are in high, open areas (e.g. crevices in cliffs or holes in tall trees) that are
hard for researchers to find and access. High entrances with open surroundings
could be an obvious requirement for fast-flying bats that must drop down into flight
from the roost entrance [14]. Therefore, it is not surprising that anthropogenic struc-
tures near natural areas are heavily used by molossid bats even when some natural
roosts may be available [47].
Some morphological traits may preadapt molossids to exploit anthropogenic
roosts in urban and non-urban environments. Some species are dorsoventrally flat-
tened, which facilitates occupancy of narrow crevices, including inbuilt structures
[48, 49]. The posterior flexion of the first phalanxes of wing digits three and four, in
combination with robust and muscular forelimbs, helps them crawl rapidly on the
ground, on walls, and inside narrow spaces. In addition, the thick patagium could
make molossid wings more resistant to constant friction with coarse or rocky sur-
faces in narrow spaces [50].
The commonality of the above-mentioned morphological traits among all molos-
sids might seem to suggest that they are all preadapted to occupy narrow crevices
with high entrances in urban buildings. However, the ability to occupy urban roosts
seems to vary among species. T. brasiliensis, probably the most abundant urban bat
in the New World, prefers abandoned buildings that have large and high roost
entrances and are surrounded by scarce vegetation [37]. In contrast, western mastiff
bats (Eumops perotis), the largest molossids, usually occupy attics and may take off
from exceptionally low heights (≥ 2 m). Therefore, the height of the roost entrance
may not be as limiting for molossids as previously thought. Plasticity, when it comes
to roost microclimate requirements, may offer another clue to the urban success of
some species. For example, Angolan free-tailed bats (Mops condylurus) roost in
narrow spaces under metal sheet roofs in small houses (spaces that often exceed
40 °C) and yet can enter torpor when ambient temperature falls to 15 °C; this unique
plasticity makes M. condylurus well suited to occupy a variety of man-made roosts
[51]. A similar tolerance of warm roosts has been reported for T. brasiliensis [51].
Another important preadaptation that maximises the roosting plasticity of some
molossids (e.g. M. molossus, M. nigricans, T. teniotis, and little northern free-tailed
bats, Mormopterus loriae) is the ability to enter torpor-like physiological states at
moderate and relatively high ambient temperatures [51, 52]. No doubt, detailed
studies of roost selection in natural and urban contexts will elucidate which factors
promote the urban success of some molossid bats.

6 Conclusions

Global meta-analyses using ecological, behavioural, and life history traits have
identified increased mobility as the most important factor explaining the success of
molossid bats in urban landscapes. Here, we suggest that some foraging,
40 R. Avila-Flores et al.

echolocation, social, and roosting behavioural traits contribute to preadapt many

molossid species to persist in highly urbanised environments. These traits include
(1) high-altitude flight, (2) light tolerance, (3) lack of reliance on acoustic land-
marks for orientation, (4) vocal plasticity (to detect near and distant objects), (5) the
ability to adjust social systems to group size, (6) the ability to occupy narrow spaces
in diverse built elements, and (7) physiological tolerance to a wide range of roost
temperatures. Combined, these traits may make some species preadapted to urban-
isation. Because so much information on the behavioural ecology of molossid bats
is anecdotical and still scarce, our conclusions should be interpreted as hypotheses
that need to be tested.

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Chapter 4
Urban Bats and their Parasites

Elizabeth M. Warburton, Erin Swerdfeger, and Joanna L. Coleman

Abstract  Understanding host-parasite relationships in urban environments pro-

vides information critical for understanding bat ecology in anthropogenically
altered landscapes. Although most current evidence comes from bat-virus systems,
links between bats and their ectoparasites and endoparasites can provide key exam-
ples of how anthropogenic change affects bat health, roosting and foraging ecol-
ogy, and, ultimately, bat conservation. This chapter examines the current state of
knowledge and identifies potentially understudied aspects of urban bats and their
parasites. Urbanisation can potentially modulate bat-parasite associations by
affecting resource availability, ecophysiology, behaviour, and life history of bats.
Urbanisation may also influence how these effects vary among parasites, bat spe-
cies, and bat age classes. We distinguish between the effects of urbanisation in
relation to ectoparasites and endoparasites, with one illustrative case study of each.
The first case study examines ectoparasites of little brown bats (Myotis lucifugus)
along an urban-rural gradient. It found some indications that M. lucifugus were
more heavily parasitised in the city, likely because this was where the bats were
most abundant and because ectoparasitism often rises along with host population
density. The second case study investigates how anthropogenic habitat disturbance
contributes to shifting helminth communities in big brown bats (Eptesicus fuscus).
Land cover categories with more intense human activities were most likely to have
similar helminth communities, likely because worms that parasitise more ecologi-
cally sensitive, intermediate hosts are more prone to extirpation with increasing
anthropogenic disturbance. Finally, we conclude by suggesting that the tightly
linked nature of the host-parasite relationship provides unique opportunities to

E. M. Warburton (*)
Center for the Ecology of Infectious Diseases, Odum School of Ecology,
University of Georgia, Athens, GA, USA
E. Swerdfeger
Department of Biology, University of Regina, Regina, SK, Canada
J. L. Coleman
Department of Biology, Queens College at the City University of New York,
Queens, NY, USA

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 43

L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_4
44 E. M. Warburton et al.

address key urban ecology questions related to host foraging and roosting in urban
areas, host-vector contact rates in disturbed habitat, and host susceptibility in
response to anthropogenic stressors.

Keywords  Endoparasites · Ectoparasites · Vectors · Chiroptera · Urbanisation

1 Introduction

As cities expand and human populations in urban areas progressively outnumber

those in rural areas, bats, like other wildlife, must increasingly contend with more
frequent and intense human activities in urban areas relative to other land uses.
These activities can drastically alter the amount, configuration, and quality of habi-
tat for bats, especially via replacement of vegetation by built cover. As such, they
can also alter bats’ relationships with their parasites.
While early definitions of parasitism focus on trophic implications (i.e. parasites
‘feed off’ their hosts and often include the concept of harming their hosts [e.g.
Crofton 1971, cited in [1]]), this trophic focus is a narrow view of parasitism.
Indeed, parasites constitute not one but many taxa and must be at least somewhat
adapted to their hosts (i.e. to evade immune responses [1]). Thus, parasitism may be
viewed through the lens of hosts as habitat, with food sources located within the
host habitat [1]. Some of these host-parasite relationships are visually dramatic
when encountered in nature, such as with ectoparasites (Fig. 4.1), whereas endo-
parasites remain hidden inside their bat hosts. This chapter adopts this ecological-
and evolutionary-based definition of parasitism.
Studying bats and their host-parasite relationships in cities can provide critical
ecological information, such as selection of foraging and roosting sites, that directly
impacts bat conservation, as urbanisation is a key extinction threat for bats [2].
Parasitism of wildlife generally is modulated by diverse environmental parameters
and linked to the distribution, population dynamics, and health of hosts [3] – all of
which may vary with urbanisation. For bats, much evidence comes from virus-­
related research. For example, certain flying foxes (Pteropus spp.) exhibit dramatic
behavioural adjustments to recent land use and land cover change in Australia [4, 5].
In their ancestral forest habitat, they migrate over long distances searching for spa-
tially and temporally patchy food resources. However, amid deforestation pushing
them out of forests, they have been drawn into cities, where cultivated (native and
exotic) trees offer fruit and/or nectar year-round. These conditions favour sedentary
behaviour so that there are now permanent, large, aggregations of flying foxes in
many cities, where none existed historically [4]. Additionally, pteropodids are the
natural reservoirs for Hendra virus (HeV), and modelling suggests that these altered
behaviours drive disease dynamics [6]. As bats become more urbanised and seden-
tary, connectivity between local populations and herd immunity across the meta-
population declines. This results in more sporadic but more intense outbreaks in
4  Urban Bats and their Parasites 45

Fig. 4.1  This wingless bat fly (Nycteribiidae: Penicillidia sp.) nearly covers the entire face of a
Mozambican long-fingered bat (Miniopterus mossambicus). (Photo credit: Dr. Piotr Naskrecki,
Minden Pictures)

urban populations  – a phenomenon with significant medical and veterinary

implications.
Though the above example focuses on a virus, it illustrates the generalised,
expected effect of higher host densities increasing host-parasite contact rates [7 and
others therein], including parasites that present zoonotic disease risks. Pteropodids
are not the only bats whose distributions and population dynamics may vary with
urbanisation, which may ultimately influence bat-parasite dynamics. Other species
may be more abundant in cities, especially synanthropes that readily exploit subsi-
dised food resources or anthropogenic roosts [see also 8]. Moreover, species such as
Kuhl’s pipistrelle [Pipistrellus kuhlii; 9] and little brown bats [Myotis lucifugus; 10]
46 E. M. Warburton et al.

may exhibit altered fecundity in relation to urbanisation – a phenomenon that could

modulate bat-parasite dynamics by altering the relative availability of pups and
juveniles. The naïve immune systems of young bats and their reduced ability to self-­
groom may make them more susceptible to parasitism. Alternatively, parasites may
prefer adult hosts, given their higher overwintering survival [11 and others therein].
Thus, altered host age structure could affect parasite populations.
Urban-associated pollutants and other stressors in cities may compromise
immune function or other aspects of host health with possible parasitological con-
sequences. For example, adult female and juvenile Pipistrellus kuhlii foraging over
a more polluted reservoir in the Negev Desert harboured more ectoparasites com-
pared to individuals foraging over cleaner ponds [12]. However, the focus of this
study was not urban pollutants, and a lack of site replication makes it difficult to
conclusively attribute differential parasitism to water quality. Other taxa offer addi-
tional evidence of these phenomena. Serieys et al. [13] investigated the causes of a
deadly outbreak of Notoedric mange, a parasitic skin disease that decimated an
urban population of bobcats (Felis rufus) in California, United States of America
(USA). Comparison of blood samples from F. rufus along an urbanisation gradient
showed that exposure to rodenticides and urban land use was linked to reduced
immune function and skin health and higher susceptibility to mange.
Although understanding bat-parasite relationships is relevant to bat biology and
ecology, only 21% of 570 publications on bat parasites identified in our literature
search were in the topic areas (defined by Web of Science) of ecology and conserva-
tion (Fig. 4.2). Other dominant research foci and/or motivations were biodiversity
discovery and phylogeny (39%) and zoonoses (19%). Studies of these associations
in urban areas are rare, i.e. a total of 29 potentially relevant papers – all but 4 pub-
lished since 2015 and strongly biased towards the Neotropics (18 studies) and zoo-
notic questions (16 studies). The nearly universal approach has been to document
parasites of bats in urban areas and sometimes compare findings with published
data from non-urban areas, as opposed to conducting  simultaneous comparisons
(e.g. along urban gradients), which could help elucidate the urban ecology of bats
and their parasites. As such, this chapter examines the current state of knowledge
and identifies potentially understudied aspects of urban bats and their parasites. The
central theme is urbanisation modulating the dynamics of bat-parasite associations
via its effects on resource availability, ecophysiology, behaviour, and life history of
bats. These impacts can vary among parasites, bat species, and bat cohorts; conse-
quently, bat ectoparasites and endoparasites are discussed in detail with one illustra-
tive case study each.

2 Ectoparasites

Bats host a huge diversity of ectoparasitic arthropods that spend their whole lives on
the outside of bats’ bodies and/or in their roosts and often have high host specificity
[14]. Thus, their diversity and abundance are inexorably linked to aspects of bat
4  Urban Bats and their Parasites 47

Fig. 4.2  Results of a literature search on 27 April 2021. (a) In step 1, we searched Web of Science
(WoS) with the search terms ‘bats’ and ‘parasite’ in the topics. Scanning all titles and abstracts
allowed us to exclude 176 records. We then read the 560 accessible abstracts of the resulting
unique, relevant records and examined their distribution among WoS categories (in WoS analytics)
and 2 research foci: (1) biodiversity discovery and phylogeny/systematics (i.e. species checklists,
taxonomic revisions, evolution) and (2) zoonoses of human and veterinary importance, i.e.
abstracts prominently mention diseases of humans, pets, or livestock). (b) In step 2, we performed
a new WoS search with the search terms ‘urban’, ‘bat’, and ‘parasite’ in the topics and supple-
mented this with a Google Scholar search to identify other unique records (not indexed in WoS) in
the first ten pages of results. We retained studies that reported original fieldwork (as opposed to
meta-analyses) and classified these by location to explore geographic clustering of studies.
(Histogram, country ISO codes on y-axis)

health, ecology, and behaviour that should be responsive to urbanisation.

Additionally, various urban-related environmental changes (e.g. climate, pollution)
may affect these ectoparasites independently of their hosts. Finally, these parasites
may be disease vectors. Therefore, studying ectoparasitism in relation to urbanisa-
tion could help answer timely questions in urban ecology and bat roost selection,
two key components of bat conservation.
48 E. M. Warburton et al.

2.1 What Are the Parasitological Consequences of Altered

Roosting Behaviours By Urban Bats?

In most biomes, urban development reduces the availability of natural roosts while
increasing that of anthropogenic structures. Therefore, any bat species’ urban adapt-
edness is at least somewhat predicted by flexible roosting habits. Indeed, divergent
behaviours between urban and non-urban bat populations are well-documented.
These include shifts to commensal roosting, as in Brazil, where 84 species that
inhabit cities mainly use built elements, especially buildings [15]. Other shifts
include increased roost fidelity, as in the case of Indiana bats (Myotis sodalis),
which switch less often at the edge of a developing urban area than in contiguous
forest [16].
Both shifts have parasitological implications. First, not only does frequent roost
switching correlate with reduced ectoparasitism, which may have evolved as an
anti-parasitic strategy, but also this roost-switching declines in commensal roosts [7
and others therein]. Next, commensal roosts, being generally larger and more per-
manent than natural ones, favour larger colonies and tighter social networks among
bats, and thus parasite transfers between individuals [7]. They also promote repro-
duction of insects (e.g. bat flies: Diptera, Streblidae, Nycteribiidae) that complete
part of their life cycles in roosts [17]. Finally, ectoparasites may exhibit greater host
specificity in commensal roosts occupied by a single bat species. For instance, four
bat fly species parasitise a single species in Singapore, where their bat hosts use
commensal roosts, but use multiple hosts elsewhere in Southeast Asia, where they
roost with other bat species in caves [17].

2.2 Does Urbanisation Have Linked Fitness

and Parasitological Implications for Bats?

Urbanisation could modulate either the prevalence or the intensity of ectoparasitism

by impacting various indicators of bat fitness or affect bat fitness by modulating
ectoparasitism factors. One indicator of this modulation is bat body condition,
which may vary with urbanisation [3, 10] and often correlates with ectoparasitism –
sometimes positively [e.g. various parasites on M. lucifugus; 18], sometimes nega-
tively [e.g. bat flies on fruit bats; 17]. Yet, while the ectoparasites clearly gain
resources, for example, by consuming the blood or lymph of their hosts, whether
they directly and substantially reduce body condition is debatable [14] because
establishing cause and effect is difficult. For example, finding that bats in better
body condition harbour fewer parasites could indicate either that fitter individuals
are better able to cope with parasites (e.g. have more energy to groom) or that they
are not preferred hosts.
4  Urban Bats and their Parasites 49

Another indicator of fitness that could vary with urbanisation is reproductive

output. Evidence remains scant, but in Italy, as urban land cover around building
maternity roosts of Pipistrellus kuhlii increases, so do numbers of pups per female
[9]. Higher urban proportions of immature bats could, as mentioned, have either
positive or negative effects on ectoparasitism levels, depending on their host age-­
class preferences. Additionally, these P. kuhlii give birth earlier in more urbanised
roosts [9]. For temperate zone bats, earlier parturition is a fitness gain – it leaves
more time for mothers and juveniles to accumulate fat reserves needed to overwin-
ter. Earlier parturition could also be detrimental to various ectoparasites by reducing
their optimal reproduction window. For example, two nycteribiid flies, one wing
mite (Spinturnix psi) and one hard tick (Ixodes simplex simplex), on Schreiber’s bat
(Miniopterus schreibersii) in Portugal mainly reproduce on adult females and volant
pups and mostly during pregnancy and lactation [19]. This is likely because preg-
nant females and pups have reduced behavioural and immune defences, and lacta-
tion enhances opportunities for vertical transmission while reducing the mother’s
available energy to groom [19].

2.3 Do Urban Abiotic Changes Modulate

Bat-Ectoparasite Relationships?

Compared to surrounding areas, most cities are warmer and less humid, with altered
precipitation and dampened seasonality – this is the urban heat island (UHI). For
ectoparasites of bats, especially ones that live part of their lives off their hosts, such
shifts could alter survival, reproduction, and/or host-seeking behaviour. Though this
possibility has not been tested specifically in relation to the UHI, temperature and
precipitation do affect bat flies parasitising bats in Venezuela, albeit differentially
depending on the bat species [20]. Additionally, the UHI in Poland seemed linked to
reduced abundance of Ixodes ricinus [21], which rarely parasitise bats but are in the
same genus as other hard ticks that do.
Cities also tend to have high levels of various forms of pollution. One is heavy
metal contamination, and evidence from a small sample of Daubenton’s bats (Myotis
daubentonii) in Finland [22] suggests that it might disrupt bat-ectoparasite associa-
tions. The likelihood that an individual harboured wing mites rose with its cadmium
and copper exposures but declined with lead exposure, while arsenic and cobalt
levels were negatively correlated with the presence of bat flies. Another urban issue
is the presence of light and noise pollution. The implications for bats and their ecto-
parasites are unknown but may be worth studying given strong evidence that both
stressors disrupt associations between túngara frogs (Engystomops pustulosus) and
the Corethrella midges that bite them, namely, by reducing midge abundance [23].
50 E. M. Warburton et al.

2.4 Could Urban Changes in Ectoparasite Loads Alter the Risk

of Disease?

Bats are a species-rich order [24] and, as such, host a wide diversity of micropara-
sites and macroparasites, increasing the likelihood of parasite co-occurrence within
the same host. This intra-host parasite diversity creates opportunities for one para-
site to be a vector for another. Indeed, several ectoparasites transmit pathogens
between bats, and bat species that host more ectoparasite species also host greater
viral richness [25]. Consequently, if urbanisation alters bat-ectoparasite associa-
tions, it could also alter dynamics of pathogen transmission.
One such pathogen of concern is the fungus Pseudogymnoascus destructans.
This fungus causes white nose syndrome, a disease that mainly kills bats during
hibernation and has pushed some North American species to the brink of extinction
[26]. Recently, it was detected on spinturnicid mites collected from bats in Kentucky,
USA, raising the possibility that ectoparasites are involved in spreading the disease
[27]. The fact that these bats were sampled in late summer further suggests that bats
might transport the fungus from summer habitats, which may be urban, to their
hibernacula, where mating occurs, during which time ectoparasites may move
between hosts. Thus, the urban ecology of bat-ectoparasite associations may have
conservation implications.

Box 4.1 Ectoparasites of Bats in Relation to Urbanisation

The following case study is extracted from unpublished data from Coleman JL,
Swerdfeger E and RMR Barclay.
Problem
Only 29 of the 570 relevant studies identified (Fig. 4.2) assessed bat-­parasite
relationships along urbanisation gradients, and none did so for colonial insec-
tivorous bats in temperate zone cities. As outlined above, examination of bat
ectoparasites in urban environments could be key to understanding host roost-
ing behaviour and fitness.
Methodology
Ectoparasites on M. lucifugus were documented in relation to urbanisation in
Calgary, Alberta, Canada. The urban gradient consisted of three zones: urban
(within city limits and surrounded by development), rural (≥ 40 km from city
limits), and transition (from city limits out to 40 km, 11 sites). Each zone had at
least nine replicate sites (11 urban, 11 transition, 9 rural), all located in treed,
riparian areas to minimise confounding effects of habitat. From May to mid-
September in 2007 and 2008, the authors captured 884 bats by mist-netting and
recorded their body condition, demographics, and ectoparasites. The authors
considered three cohorts (adult females, adult males, and juveniles) and calcu-
lated total ectoparasite prevalence (percentage of bats infested), total

(continued)
4  Urban Bats and their Parasites 51

Box 4.1  (continued)

ectoparasite intensity (ectoparasites per infested bat), and intensity and preva-
lence per parasite taxon. Associations between zone and infestation (total ecto-
parasite prevalence and per parasite taxon) were assessed using two-way
contingency tables. The influence of urbanisation on intensity (total ectoparasite
intensity and per taxon) was compared for each bat cohort using negative bino-
mial generalised linear mixed models. Finally, non-­parametric measures of asso-
ciations between individual parasite load and body condition were determined.
Findings
The relationship between urbanisation and ectoparasites of M. lucifugus
reveals a complex response that varies among parasite taxa, over time, and
with demographics and body condition. Most bats (60%) harboured at least
one ectoparasite (Fig. 4.3), including various mites (Acarina: Macronyssidae,
Spinturnicidae), bat fleas (Myodopsilla spp., G.  Chilton, pers. comm.), bed

Fig. 4.3  Variation in ectoparasitism on three cohorts of little brown bats, Myotis lucifugus,
with urbanisation in Calgary, Alberta, Canada. Upper charts for adult females, middle charts
for adult males, lower charts for juveniles, different colours for different zones. (a)
Differences in ectoparasite prevalence (total ectoparasite prevalence = TEP). Different letters
above columns indicate significantly different values – columns with no letters are not differ-
ent. (b) Variation in intensity of parasites. Symbols represent total ectoparasites (squares),
triangles (mites), and circles (fleas). On the chart for juveniles, closed symbols are 2007
values and open symbols are 2008 values. For adult females and juveniles, values are means
over both years. All values are least-squared means with back-transformed standard errors

(continued)
52 E. M. Warburton et al.

Box 4.1  (continued)

bugs (Cimex spp.), chiggers (Trombiculidae, H.  Proctor, pers. comm.), and
soft ticks (Argasidae). Intensities and yearly variation were generally low,
especially in the urban population (Fig.  4.3b). Links between urbanisation
and ectoparasitism were obvious in adult female bats. Maximal prevalence
(except for fleas in 2007; Fig. 4.3a) and total ectoparasite intensity (Fig. 4.3b)
occurred in the transition zone. Total ectoparasite intensity also peaked on
lactating females and in 2008. For fleas, intensity differed between years (but
not during pregnancy) and with reproductive status in 2008, but not with
urbanisation (Fig. 4.3b). Body condition was positively correlated with ecto-
parasitism (total ectoparasite intensity and intensities of mites and bed bugs)
but only on adult females. For adult male bats, the only link between urban-
isation and ectoparasitism was that urban males were the only ones with fleas
in 2008 (Fig. 4.3a).
Juvenile bats’ ectoparasite associations mirrored those of adult females in
some respects. For example, they had higher total ectoparasite and mite inten-
sities in 2007, and rural juveniles were less likely to harbour mites in 2008
(Fig. 4.3). Prevalence and intensity measures for other juvenile bat-ectopara-
site associations either did not vary with urbanisation or varied inconsistently
between years (i.e. significant year-zone interactions).
Synthesis
By some measures, M. lucifugus were more parasitised in the city. This is
likely because bats were most abundant there [10] and ectoparasitism often
rises along with host population density [28]. However, for adult females,
parasitism increased in the transition zone. This could reflect divergent roost-
ing ecology along the urban-rural gradient. Urban and rural bats mainly
roosted in large, enclosed, built structures, while those in the transition zone
roosted in tree cavities or under shingles. Though switching among tree roosts
can reduce infestations [29], it could also facilitate some dispersal of tempo-
rary parasites through passive transport between roosts [30]. Additionally,
urbanisation could affect body condition, which was best in the transition
zone, and increased parasitism with better body condition is predicted by the
hypothesis that parasites prefer healthier hosts [31]. The near lack of variation
in ectoparasite associations of adult males along the gradient may simply
reflect the fact that they are widely dispersed in summer and harbour few
parasites.
For juveniles, low variation in intensities may reflect age-biased parasit-
ism. On one hand, the transition zone, where reproductive output peaks [10],
presumably offers ectoparasites the greatest availability of young, vulnerable
hosts [28]. On the other, because juveniles experience the highest overwinter
mortality, permanent parasites should avoid independent young prior to win-
ter [11] regardless of urbanisation.
4  Urban Bats and their Parasites 53

Box 4.1  (continued)

Overall, this case demonstrates that ectoparasitic associations and their
links to urbanisation can vary widely among conspecific cohorts. This high-
lights how the ecology of colonial bats can differ within as well as among
species. It also illustrates that short-term studies might not reveal the full pic-
ture of urbanisation-mediated ectoparasitism. In some ways, parasitism did
differ between years but it was most consistent in the city. This could reflect
the potential for reduced urban seasonality (i.e. UHI) affecting parasites
directly, by influencing their survival or, indirectly, by influencing host popu-
lation dynamics and movements [28]. Ultimately, this case underscores the
importance of multi-year investigations of multiple infestation metrics and
parasitic taxa along urbanisation gradients to elucidate the role of urbanisa-
tion in mediating bat-ectoparasite relationships.

3 Endoparasites

As human encroachment on bat habitat grows, so do worries about bats acting as

reservoirs for parasites, including some of public health concern. However, bat par-
asites that do not infect humans or domestic animals can provide key clues to eco-
logical differences between urban and non-urban bats, such as feeding and roosting
preferences. Additionally, comparing parasite diversity between urban and non-­
urban bats can help elucidate whether key phenomena, such as biological homogeni-
sation, occur at multiple scales within anthropogenically disturbed habitat.
Eukaryotic bat endoparasites, typically single-celled protozoans and worm-like hel-
minths, represent both tropically transmitted and vector-borne groups. Thus, these
parasites can reveal the influence of land use and land cover change on host suscep-
tibility, parasite contact rates, and transmission pathways and the potential conse-
quences of land use and land cover change on biodiversity at the scales of the host
and parasite.

3.1 Protozoan Parasites and Host-Vector Contact Rates

Blood-borne parasites in the genera Trypanosoma and Leishmania (phylum

Euglenozoa) are transmitted by hematophagous insects. Although both New and
Old World Leishmania spp. have been documented infecting bats [e.g. 32 and others
therein], only New World Trypanosoma spp. have been found in bats [33, 34]. One
such species, T. cruzi, which causes Chagas disease in humans, infects various
mammals, and there are concerns that bats could act as reservoirs of this parasite.
Indeed, the prevalence of Trypanosoma spp. infecting Jamaican fruit-eating bats
(Artibeus jamaicensis) is higher in forest fragments in a residential and agricultural
54 E. M. Warburton et al.

matrix than in continuous tropical forest in Panama [34]. Likewise, trypanosomes

were isolated from five bat species within rainforest fragments and surrounding
farms in Espirito Santo, Brazil, but not from 20 other species of wild mammals [33].
The prevalence of Leishmania spp. within urban and peri-urban bats may be rela-
tively high. For example, over 59% of common pipistrelle (Pipistrellus pipistrellus)
sampled in and around Madrid harboured L. infantum [32], whereas Miniopterus
schreibersii in Spanish wildlands demonstrated no evidence of Leishmania infec-
tion [35]. Although the dichotomous findings of these studies could reflect differ-
ences in tissues examined (i.e. the spleen [32] versus peripheral blood [35]),
human-modified landscapes provide phlebotomine sandflies, the vectors of
Leishmania spp., with hospitable habitat [36], and these flies can feed successfully
on multiple species of bats [37]. Thus, an increase in phlebotomine sandflies in
urban areas could be responsible for higher urban infection rates. Given that both
parasite genera (Leishmania and Trypanosoma) have generalist species and general-
ist arthropod vectors, urbanisation could increase parasite contact rates for
urban bats.
Members of the phylum Apicomplexa parasitise a wide variety of birds and
mammals, including bats, and some are of zoonotic concern [38]. Apicomplexans
can enter hosts via a hematophagous arthropod vector (e.g. Plasmodium) or through
faecal-oral transmission (e.g. Eimeria). Therefore, effects of urbanisation in this
phylum could vary with the life cycle and vector. For instance, Indian flying foxes
(Pteropus medius) were slightly more likely to host Hepatocystis sp., vectored by
mosquitos, and Babesia sp., vectored by ticks, in peri-urban than in rural areas of
Bangladesh [39]. Meanwhile, the prevalence of Polychromophilus sp., vectored by
bat flies, in Australian bent-wing bats (Miniopterus orianae) was up to 1.9 times
higher at sites that retained ≤18% of their original habitat than at sites with ≥45%
[40]. Thus, land use changes may promote apicomplexan infections, perhaps by
increasing vector-host contact rates and/or susceptibility of hosts.

3.2 Helminths Provide Insights into Host Foraging

Although roundworms (Nematoda) and spiny-headed worms (Acanthocephala)

infect bats, flukes (Trematoda) and tapeworms (Cestoda) often dominate bat hel-
minth communities [41]. Many of these parasites have complex life cycles involv-
ing one or more invertebrate intermediate hosts. Whereas bat trematodes require
two aquatic intermediate hosts (freshwater snails and larval insects; Fig. 4.4), ces-
todes have fully terrestrial life cycles, with arthropods, e.g. beetles, acting as single
intermediate hosts [42]. Thus, habitat diversity of bat helminth life cycles varies,
and anthropogenic disruption of any of these habitats may shift helminth communi-
ties. Urbanisation can affect both parasite community diversity and host traits, e.g.
body condition and immune function. It could also cause ecologically sensitive
intermediate hosts to decline, while more resilient taxa could become dominant
[43]. Similarly, certain urban stressors could increase host susceptibility via
4  Urban Bats and their Parasites 55

Fig. 4.4  Representative life cycle diagram of a trematode belonging to Lecithodendriidae, a fam-
ily that almost exclusively parasitises bats. Trematode eggs are passed with faeces as a bat flies
over a body of freshwater, such as when drinking (a). They then infect a snail where larvae meta-
morphose, grow, and exit their host as another free-swimming larval stage (b). These larvae swim
until they contact a larval insect (e.g. a dragonfly nymph) and encyst within it (c). When the drag-
onfly metamorphoses into an adult, it carries the encysted trematode larvae (d). When a bat ingests
the adult dragonfly, the encysted larvae break free and grow into adult worms in the bat’s intestine,
where they begin shedding eggs with the bat’s faeces (e)

physiological processes [44]. Ultimately, understanding urban-related shifts in hel-

minth communities may reveal the responses of bat hosts to extreme habitat
disturbance.

Box 4.2 The Link Between Bat Helminth Communities and

Anthropogenic Land Use
This information is extracted from Warburton et al. (2016) [41].
Problem
The ecology of endoparasite communities that inhabit bats is understudied not
only in relatively undisturbed settings but also in relation to urbanisation.
These helminth communities exist across a variety of environmental condi-
tions, including not only ‘natural’ but also highly altered land covers, such as
urbanised ones. Biological communities are typically thought to exhibit a
distance-decay relationship where their species compositions become increas-
ingly dissimilar with increasing physical distance. However, environments

(continued)
56 E. M. Warburton et al.

Box 4.2 (continued)
themselves, especially anthropogenically altered ones, can also shift the spe-
cies composition of biological communities. Further, understanding how
parasite communities change with urbanisation may elucidate how bat hosts
function in cities by revealing key aspects of bat foraging ecology in urban
environments.
Methodology
To understand how anthropogenic habitat disturbance contributes to shifting
parasite communities, Eptesicus fuscus from a three-state region (Michigan,
Indiana, and Kentucky) in the Midwestern USA were captured, and their hel-
minth communities were assessed. Two hundred sixty bats consisting of adult
and juvenile members of both sexes were captured from 13 maternity colonies
with a mean inter-roost distance of 315.7 km (range = 6.9–660.7 km). The
authors used GIS layers from the US National Land Cover Database and
National Wetlands Inventory to quantify the area covered by 16 land cover
categories, including designations such as barren land, croplands, forests,
wetlands, and city centres, within 12-km radii of each colony (i.e. the maxi-
mum recorded foraging distance for E. fuscus). Using redundancy analysis,
an extension of multiple linear regression that accounts for multiple response
and explanatory variables, the effects of physical distances between roosts
and land cover on helminth communities were assessed.
Findings
Helminth community composition was largely predicted by land cover around
roosts. Indeed, land cover categories with more intense human activities had
similar helminth communities. The effect was most significant (p < 0.004) in
developed open spaces (e.g. parks, golf courses) and high-­impervious cover
sites (e.g. central business districts) and approached significance (p = 0.0504)
in cultivated land covers (e.g. croplands, orchards). However, more urbanised
sites did not have less species rich or less diverse helminth communities;
instead, their species composition changed. Certain helminths, e.g. the ces-
tode Hymenolepis roudabushi and the trematode Paralecithodendrium swan-
soni, were more closely associated with more developed land cover, while
others, e.g. the nematodes Rictularia lucifugus and Litomosoides guitaresi,
were more closely associated with cropland. Still other species, e.g. the trem-
atode Acanthatrium eptesici, were associated with relatively undisturbed
habitats such as woody wetlands.
Synthesis
These shifts in the helminth communities of bats in different land covers
likely reflect shifts in intermediate host community composition and struc-
ture. Parasites with ecologically sensitive intermediate hosts, such as may-
flies, might be more prone to extirpation with increasing anthropogenic

(continued)
4  Urban Bats and their Parasites 57

Box 4.2 (continued)
disturbance. However, instead of producing a net loss in parasite species rich-
ness, the ecological niches left vacant by such extirpations could be filled by
other helminths whose intermediate hosts are more resilient, such as chryso-
melid beetles. Thus, understanding how helminth communities change in
urban areas can reveal bats use resources in anthropogenically altered
landscapes.

4 Concluding Perspectives

After surveying the literature, there is clearly still much to learn about bat-parasite
relationships in the context of urbanisation. This knowledge gap is unfortunate,
although perhaps not surprising given that bats and parasites are high-diversity
groups, and they occur in many cities around the world. Further, the tightly linked
nature of the host-parasite relationship provides excellent opportunities to address
key urban ecology questions.
Questions about host foraging and roosting habits in urban areas, host-vector
contact rates in disturbed habitat, and host susceptibility in response to anthropo-
genic stressors can be readily addressed within urban bat-parasite systems. For
example, many ectoparasites contact bat hosts in roosts, whereas many helminths of
bats are tropically transmitted. As such, comparing the diversity of ectoparasite and
endoparasite communities between urban and non-urban bats can provide insight
into how urban bats use resources in response to anthropogenic disturbance.
Additionally, certain human activities could increase transmission pathways, but
this phenomenon is largely unexamined for most parasitic taxa. In one well-known
example [5], urban planting of ornamental trees increased aggregations of flying
foxes and consequently led to increased HeV transmission. Given that HeV relies
on faecal-oral transmission, parasites with faecal-oral transmission (e.g. coccidia)
could increase in these cities as well. Other human activities, such as draining wet-
lands for residential or agricultural use, should eliminate transmission pathways for
trematodes that use aquatic intermediate hosts. However, anthropogenic effects on
transmission pathways are poorly studied for most parasitic taxa, including those
parasitising bats, and represent key knowledge gaps that require further
investigation.
Urban bat-parasite systems could also be useful for examining broader ecologi-
cal hypotheses. One is the diversity dilution hypothesis, which predicts increasing
parasitism with declining diversity of hosts. Although evidence is equivocal [45],
some findings in anthropogenically disturbed habitats [46–48] support key aspects
of the hypothesis, namely, that preserving biodiversity in urban areas can reduce
disease incidence.
Because parasitic associations are strong selective forces on both partners [14],
urbanisation could have evolutionary implications for hosts and parasites. For
58 E. M. Warburton et al.

example, pigeons (Columbia livia) exhibit hereditary variation in colouration along

the urban gradient in Paris, France  – variation that apparently reflects divergent
strategies to cope with urban-related changes in blood-parasite pressure [49].
Although urban evolutionary ecology studies have not yet focused on bats and their
parasites, doing so could elucidate the role of cities as drivers of evolution.
Research on urban bats and their parasites could also have important ecotoxico-
logical applications as diverse parasites are increasingly perceived as useful bioin-
dicators of habitat quality [50]. Finally, the potential effects of anthropogenic
stressors, such as light pollution and roost disturbance, on the immune system of
urban bats are not well known. These stressors could have a negative impact on
disease susceptibility in urban bats, thereby increasing parasite prevalence or abun-
dance. Thus, future work linking environmental health, anthropogenic activities,
and host susceptibility could shed more light on our understanding of urban bat-­
parasite systems.

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ronmental parasitology’. Parasit Vectors 10(1):65
Chapter 5
Bat Societies across Habitat Types:
Insights from a Commonly Occurring
Fruit Bat Cynopterus sphinx

Kritika M. Garg, Balaji Chattopadhyay, D. Paramanatha Swami Doss,

A. K. Vinoth Kumar, and Sripathi Kandula

Abstract  Bats constitute the second most speciose order of mammals and are
known for their gregarious and flexible social structure. Urbanisation can lead to
changes in the availability of, or access to, resources, such as roosting sites, food,
and mates, and thus can potentially affect the social and mating systems. In this
chapter, we summarise knowledge of the effects of urbanisation on the social struc-
ture of bats and highlight gaps in the literature. Further, we discuss the social struc-
ture and reproductive output of Cynopterus sphinx, a fruit bat ubiquitous across
human-dominated habitats in South and Southeast Asia. We followed two C. sphinx
colonies over multiple seasons to understand how urbanisation impacts the social
systems of these colonies. We used direct observational and genetic data to compare
the colony size, social subunit size, relatedness, and reproductive output of both
colonies. On average, the rural colony was larger than the urban colony. The two

K. M. Garg (*)
Department of Biology, Ashoka University, Sonipat, India
Centre for Interdisciplinary Archaeological Research, Ashoka University, Sonipat, India
e-mail: [email protected]
B. Chattopadhyay
Trivedi School of Biosciences, Ashoka University, Sonipat, India
School of Biological Sciences, Madurai Kamaraj University, Madurai, India
D. Paramanatha Swami Doss
School of Biological Sciences, Madurai Kamaraj University, Madurai, India
St. John’s College, Palayamkottai, India
A. K. Vinoth Kumar
School of Biological Sciences, Madurai Kamaraj University, Madurai, India
S. Kandula
School of Biological Sciences, Madurai Kamaraj University, Madurai, India
Faculty of Allied Health Sciences, Chettinad Academy of Research and Education,
Chettinad Health City, India

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 61

L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_5
62 K. M. Garg et al.

colonies did not differ significantly with respect to social subunit size and related-
ness, suggesting minimal impact of urbanisation on social structure. However, there
was a significant difference in reproductive output, with the reproductive success of
females from the rural colony being 1.7 times greater than that of the urban colony.
Our results from a single rural and urban colony located nearly 500 km apart sug-
gest that urbanisation may reduce fecundity and urban areas may act as ecological
traps. Future studies with more extensive sampling are needed to identify the main
drivers of female reproductive success and the cause of reduced female fecundity in
urbanised habitats.

Keywords  Urbanisation · Reproductive success · Social system · India

1 Introduction

Humans have had a drastic impact on the natural environment, altering most of the
terrestrial landscape and causing major loss of suitable habitat and biodiversity [1–
4]. While human activities have profoundly affected the planet since the late
Pleistocene [1], conversion of large tracts of forests to agricultural lands in the past
century has caused an unprecedented level of environmental degradation and the
sixth mass extinction [1, 2]. However, it is only now that we are beginning to under-
stand and appreciate the impact of urbanisation on animal societies [3–5].
A social system is the relationship between conspecifics of a group, where indi-
viduals within a group interact more with each other than with conspecifics from
another group [6]. Such interactions are in turn influenced by the individuals’ envi-
ronment [6], including distribution of resources, predation risk, and access to mates
[6–8]. The distribution and abundance of resources in a given area directly affect
how many individuals are supported, group size, dispersal rates, and mating oppor-
tunities, and thus ultimately affect the social system, social structure, and mating
system [5, 7–9]. Urbanisation leads to habitat fragmentation, altered predation pres-
sure, and an imbalance in resource availability, thereby potentially affecting social
and mating systems [1–4, 9]. Throughout this chapter, we follow Kappeler and van
Schaik’s [6] definition of social system and social structure, wherein social system
consists of the social organisation, mating system, and social structure. Social
organisation refers to the group composition (size and sex ratio) of the social group.
Social structure refers to the social interactions and relationships among individu-
als. Mating system encompasses behavioural and genetic components of mat-
ing [6–8].
Interestingly, bats are among the most common mammals inhabiting urbanised
landscapes [4, 10]. They are keystone species in many ecosystems and particularly
sensitive to environmental disturbance, making them good indicators of ecosystem
quality [11]. Most bats are gregarious and exhibit flexible mating and social systems
[10, 12, 13]. However, knowledge of the impact of urbanisation on social systems
of the more than 1400 bat species known to date is limited.
5  Bat Societies across Habitat Types: Insights from a Commonly Occurring Fruit Bat… 63

Roosting sites are key resources for bats and [4, 10, 14] play an important role in
shelter, protection from predators, rearing of offspring, and social interactions [4,
10, 14]. In many species, males defend these roost sites, resulting in uneven access
to females and a polygynous mating system [12, 14]. Urban landscapes may provide
ample roosting sites for bats that are specialised for roosting in cliff crevices [4].
Bats can occupy tunnels, bridges, and crevices in buildings. But not all species can
use these structures, especially cave- and foliage-roosting species, and these species
might be negatively affected by urbanisation if required resources for these spe-
cies are not available in urban areas [4, 10, 14].
Urbanisation can also bring about a change in social organisation [5, 9]. Due to
limited resources, sex-biased difference in exploitation of urban habitats is observed
in many species [4, 5, 9, 10, 15–27]. For example, Linott et al. found that, in soprano
pipistrelles (Pipistrellus pygmaeus), differential habitat use between males and
females has been observed [15]. Females were less likely than males to use poorly
connected woodlands with few mature trees. Further, females were most likely to be
captured in woodlands surrounded by waterways. In contrast, no preferential habitat
use by males was observed [15], and male capture rates did not vary with habitat
quality [15]. However, the impact of poor habitat quality on male reproductive suc-
cess is yet to be ascertained [15]. Similarly, in many insectivorous bats, due to high-­
energy demands, lactating females prefer better quality habitats compared to males,
especially habitats associated with water bodies [15, 17]. Thus, urbanisation can
affect a population’s sex ratio, social organisation, and, ultimately, its social system.
Some bats can effectively occupy urban habitats and are suspected to thrive in
urban environments. However, detailed long-term studies are required to assess if
urban areas provide suitable habitat for multiple bat species. One of the pioneering
studies quantifying the effect of urbanisation on the synanthropic (species which are
common and may benefit from living in urban areas) little brown bat (Myotis lucifu-
gus) observed that bats in the transition habitat between rural and urban areas had
the highest reproductive success and their body condition was better than that of
urban and rural bats [18]. Conversely, higher reproductive output and juvenile fledg-
ing rate were observed in urban than in non-urban populations of Kuhl’s pipistrelle
(P. kuhlii), suggesting the need for detailed studies on the impact of urbanisation in
multiple species [19]. In this chapter, we summarise current knowledge of the
impact of urbanisation on social and mating systems of a commonly occurring fruit
bat and highlight areas of future research.

2 Societies of the Short-Nosed Fruit Bat Cynopterus sphinx

Across Urban and Rural Landscapes

We investigated the impact of urbanisation on the synanthropic fruit bat C. sphinx,

a generalist species found across South and Southeast Asia [20]. Males of this spe-
cies modify foliage to construct their own tents, which they use as roosts [20–22].
64 K. M. Garg et al.

Individuals also use human-made structures as roosts, allowing them to exploit a

variety of habitat types [20, 23]. Given that the species is omnipresent in human-­
occupied landscapes and can use artificial structures for its benefit, this is an ideal
system to understand the impacts of urbanisation.
Typically, once the male constructs a tent, females join the tent and reside with
the male, suggestive of a harem-like social and mating unit [20, 22, 23]. Although
the species has two reproductive periods (February to March and October to
November), harems are observed throughout the year [20]. Long-term behavioural
and genetic studies on this species have demonstrated that despite this species’
harem-like social organisation, its social structure and mating system do not truly
conform to a harem system [22–24]. Rather, group composition changes on a regu-
lar basis; with females moving freely between groups [22–24], the mating system is
promiscuous, and there is no correlation between harem size and male reproductive
success [22]. Males in a colony enjoy greater reproductive success compared to
solitary males [22]. Thus, the term harem is a misnomer in this species, and for the
rest of the chapter, we use the term “social subunit” instead [23, 24]. In this species,
multiple subunits along with solitary males that are clustered in an area are collec-
tively termed as a “colony”, which constitutes the main social and reproductive unit
[20, 22, 23].
In this study, we compared the social organisation of two colonies of C. sphinx,
one each from an urban and rural habitat in India. The urban population was located
in the metropolitan city of Bangalore, at the Indian Institute of Science campus
(12.99° N, 77.59° E). C. sphinx occupied both human-made (window eaves) and
natural roosts (kitul palm, Caryota urens fruiting body, and ornamental palm leaves)
at this site [23]. The rural population was located approximately 500 km away at
Samyathu village (8.638° N, 77.958° E), in the state of Tamil Nadu, and the popula-
tion only roosted in leaves of palmyra palm, Borassus flabellifer [22, 24]. The rural
colony was surrounded by farmland, and banana is regularly cultivated in the region
[22, 24]. We used long-term behavioural observations and genetic data to compare
the social organisation and reproductive output between both colonies. We specifi-
cally asked if there were any differences in colony size, relatedness levels, and
reproductive output. We predicted that the rural colony would be larger than the
urban colony because the rural habitat can support more individuals due to the pres-
ence of higher resources. Further, behavioural observations suggest similar colony
composition of both rural and urban colonies. Therefore, we expected no differ-
ences in social organisation between rural and urban colonies.
The rural population was part of a long-term study that we sampled twice (to
capture both reproductive periods) every year from 2008 to 2012 (N = 10 observa-
tions) [22, 24]. We sampled the urban population for three consecutive reproductive
seasons, from August 2011 to 2013 (N = 3 observations) [23]. Our sampling timing
was such that most of the females had already given birth, but the pups were not yet
weaned [22–24]. This common protocol ensured that we could assign most pups to
their mothers based on their associations and test these associations using genetic
markers. Generally, we sampled both colonies approximately 4 weeks after observ-
ing parturition (through the visual inspection of newborns attached to adult females).
5  Bat Societies across Habitat Types: Insights from a Commonly Occurring Fruit Bat… 65

We carried out a visual census of the entire colony prior to sampling. We used hoop
nets to capture the social subunit and sampled entire colonies, noting any escapees.
We kept bats in cloth bags prior to sampling. For each individual, we measured its
forearm length and body mass and noted its sex, age, and reproductive status [22–
24]. We collected a 6-mm/4-mm sterile biopsy punch from both wings for genetic
analysis. We also tagged all captured individuals using colour-coded bead necklaces.
We captured a total of 396 adults across 10 sampling periods at the rural colony
and 81 adults across 3 sampling periods at the urban colony [22–24]. We extracted
DNA using either modified salt chloroform extraction protocol or Qiagen DNeasy
Blood and Tissue Kit. We genotyped all samples for nine microsatellite loci and
checked all genotypes manually twice to test for consistency. We removed one locus
from all analyses due to the presence of null alleles [22–24]. For further details on
microsatellite typing and subsequent processing of genetic data, see Garg et al. [22].
Our analyses revealed that the rural colony (only considering adults) was slightly
larger (mean  =  40 adults ± 14 SD; N  =  10 observations) than the urban colony
(mean = 32 adults ± 7 SD; N = 3 observations). The rural colony had nearly twice
as many social subunits (11.1 ± 2.6 SD) as the urban colony did (6.3 ± 2.1 SD).
Although the average social subunit size was slightly smaller in the rural colony
(mean = 2.48) than in the urban colony (mean = 3.22), social subunit size did not
differ significantly between the two (117 rural subunits, 18 urban subunits, Wilcoxon
rank sum test W = 925.5, P = 0.39; Fig. 5.1).
We further computed each colony’s reproductive output, which we defined as the
number of offspring captured from a social subunit divided by the number of adult
females captured from that subunit. Our observations revealed a significant differ-
ence in the reproductive output of females, where 78% of adult females from the
rural colony gave birth to at least one offspring compared to 45% of adult females
from the urban colony (number of observations for the rural colony, 117; number of
observations for the urban colony, 18; Wilcoxon rank sum test W = 1491, P = 0.002;
Fig. 5.2). Overall, to test if differential body condition explained the difference in

Fig. 5.1  Violin plot

depicting the variation in
the number of females
associated with a male in a
social subunit across rural
and urban colonies of
Cynopterus sphinx
66 K. M. Garg et al.

Fig. 5.2  Violin plot depicting the significant difference in reproductive output of rural and urban
colonies of Cynopterus sphinx (number of subunits from the rural colony, 114; number of subunits
from the urban colony, 20; Wilcoxon rank sum test p value = 5.503E−05). Reproductive output is
quantified as the ratio of the number of offspring captured from a social subunit to the number of
adult females captured from that social subunit. ** denotes p value <0.01

reproductive output, we further compared forearm length, body mass, and ratio of
body mass to forearm length of females from both colonies. Our data revealed that
females from the rural colony were significantly smaller than females from the
urban colony (N = 283 rural females, 50 urban adult females, Welch two sample
t-test, P = 1E−07; body mass, Wilcoxon rank sum test P = 4.693E−06; ratio of body
mass to forearm length, Wilcoxon rank sum test W = 5064.5, P = 0.0014; Fig. 5.3).
This was unexpected because given the difference in reproductive output, the body
condition of bats should be worse in the urban than in the rural colony. However,
given that clinal variation is observed in Cynopterus sphinx and bats from the south-
ern latitudes are smaller than bats from the northern latitude [26–28], body size/
condition may not be a good predictor of female reproductive fitness in this fruit bat.
Even after controlling for clinal variation by comparing the ratio of body mass to
forearm length, we observed that rural females were smaller than urban females
(Fig. 5.3c). Future studies must control for latitudinal effects to understand the bio-
logical reason for low reproductive output of urban colonies.
Finally, we compared the genetic relatedness between colony members. We esti-
mated pairwise Queller-Goodnight relatedness [29] between adult individuals
within a colony in COANCESTRY v 1.0.1.7 software [30]. Although the social and
mating implications remain unclear, relatedness plays an important role in the for-
mation of C. sphinx social subunits, wherein the male is related to one of the females
in the social subunit irrespective of the time of sampling [31]. Therefore, we also
investigated average relatedness of the social subunit. For all social subunits where
there were no escapees during capture, we calculated pairwise relatedness between
all adults within the social subunit. We tested whether a social subunit’s average
5  Bat Societies across Habitat Types: Insights from a Commonly Occurring Fruit Bat… 67

Fig. 5.3  Violin plot depicting the significant difference in (a) forearm length, (b) body mass, and
(c) ratio of body mass to forearm length of adult females of Cynopterus sphinx across rural and
urban colonies (number of females captured from the rural colony, 283; number of females cap-
tured from the urban colony, 50; forearm length, Welch two sample t-test, p value = 1E−07; body
mass, Wilcoxon rank sum test p value  =  4.693E−06). **denotes p value <0.01, ***denotes p
value <0.001

Fig. 5.4  Violin plot depicting the distribution of (a) pairwise relatedness between adults from
rural and urban colonies, (b) average relatedness of social subunits from rural and urban colonies,
and (c) high relatedness of male-female pairs form each social subunit from urban and rural
colonies

relatedness differs significantly between rural and urban colonies. Further, we

selected the male-female pair within a social subunit that had the highest relatedness
values and tested whether this value differed between both colonies. We discarded
the rare observations (three in the rural colony, one in the urban colony) of two adult
males in the same social subunit from our analysis of social subunit relatedness.
Overall relatedness among the colony members was low, and we did not find any
significant correlation between long-term association among colony members and
genetic relatedness [23, 24]. We also observed no significant difference in pairwise
relatedness between both colonies, suggesting that social organisation of C. sphinx
does not differ drastically (N = 78,934 and 2775 pairwise observations for the rural
and urban colonies, respectively; Wilcoxon rank sum test W  =  110,770,000,
P = 0.27; Fig. 5.4a). There was also no significant difference in social subunit for-
mation in both colonies. The average relatedness of the social subunit in both colo-
nies was similar (N = 78 rural and 15 urban social subunits; Wilcoxon rank sum test
W = 588.5, P = 0.97; Fig. 5.4b). Even the highly related male-female pairs from
each social subunit exhibited similar relatedness values across both urban and rural
colonies (N  =  78 rural and 15 urban social subunits; Wilcoxon rank sum test
W = 585, P = 1; Fig. 5.4c).
68 K. M. Garg et al.

3 Discussion

Urbanisation is a strong selective force that is currently shaping the biodiversity of

our planet [3, 4]. As urban areas continue to expand, many species face rapid decline
and even local extinction. We are now in the Anthropocene epoch, characterised in
part by the sixth mass extinction, so there is a pressing need to prevent further
declines and conserve our current biodiversity [32]. Species biology plays an impor-
tant role in determining the impacts of urbanisation, with many bat species exhibit-
ing negative responses to urbanisation and only a handful of them being  able to
occupy the new “urban niche” that is available to them [4, 9, 10]. Research on the
impacts of individual interactions, behaviour, and mating is still in its infancy, and
these impacts remain more difficult to quantify than species abundance and genetic
connectivity. However, multiple research groups are making strides in this area, and
we are beginning to quantify the life history differences between urban and non-­
urban populations, which are of paramount importance for effective conservation
planning.

3.1 Potential Impact of Urbanisation on Cynopterus sphinx

In the present study, we did not observe any major difference in the social organisa-
tion, social structure, social subunit size, and genetic relatedness of C. sphinx
between the rural and urban colonies (Figs. 5.1 and 5.4). However, the size of social
subunits in the urban colony was nearly half that of the rural colony, and there was
a dramatic decline in the reproductive output of the females in the urban colony
(Fig. 5.2). Body condition did not appear to influence female fecundity within our
urban C. sphinx colony, and future studies will hopefully shed more light on why
reproductive output was lower. It should be noted that the current study is based on
data collected from two colonies separated by hundreds of kilometres. The lack of
replication and possible latitudinal effects (e.g. temperature, precipitation, prey
availability) may explain differences in reproductive success independent of urban-
isation. Differences in access to mates may be involved as well. Thus, to clearly
determine if in fact urbanisation is influencing populations of C. sphinx, future stud-
ies must also incorporate data from multiple colonies across a habitat gradient and
control for latitudinal variation.
Future studies must also consider species-specific and sex-specific differences in
resource requirements while studying the impact of urbanisation. Resource distribu-
tion and availability have a strong impact on the distribution of individuals, social
organisation, mating system, and ultimately social system [7]. Most bats are gre-
garious in nature, and flight allows them to traverse greater distances than other
terrestrial species of similar body size [12–14]. However, this does not make them
immune to the effects of urbanisation. The impact of urbanisation on bats is
5  Bat Societies across Habitat Types: Insights from a Commonly Occurring Fruit Bat… 69

species-­specific because bats have different roosting requirements and diets.

Therefore, it is necessary to identify trends across multiple species. Further, urban-
isation can differentially affect males and females of the same species [9, 15–17].
Females have a higher reproductive cost than males as they nurse and carry develop-
ing offspring until weaning. Thus, there is a sex-based difference in resource
requirements, and females tend to prefer areas with better foraging habitat, roosting
sites, and water [4, 15–17]. Females need water for successful reproduction and
lactation, and many maternity colonies are located near water bodies [4, 10, 15–17].
Subtle differences between males and females in terms of preference for foraging
and roosting habitats are now being observed in multiple insectivorous bats, with
females in urban landscapes preferring better quality habitat and roosting sites com-
pared to males [4, 10, 15–17].

3.2 Urban Areas as Ecological Traps

Urban habitats may act as ecological traps for synanthropic species and may be
detrimental to species in the long run [4]. Reduction in reproductive output in urban
spaces can eventually be detrimental to species persistence, and strong conservation
actions are needed to prevent further biodiversity loss. Many species may appear to
be thriving in urban habitats, but this may not be the case. With the handful of stud-
ies comparing the reproductive output of synanthropic bats, varied effects of urban-
isation are being observed. In contrast to our C. sphinx preliminary data, M. lucifugus
reproductive success (measured as number of juveniles relative to number of adult
females) did not differ between urban and rural areas in Alberta, Canada.
Reproductive success was, however, higher in transition zones between urban and
rural areas [18]. By contrast, earlier parturition and higher fecundity were observed
in P. kuhlii populations from urban areas. Urban habitat provided P. kuhlii with
ample insects to increase reproductive output [19]. More studies are required to
quantify the impact of urbanisation on the social and mating systems of bats, includ-
ing reproductive success, because these can ultimately affect the genetic diversity
and persistence of urban populations.

Acknowledgements  This study was based on the data collected during the PhD duration of
KMG. The authors thank Prof. Uma Ramakrishnan for her support to carry out this research. The
study was supported by NCBS-TIFR and DST (SR/S0/AS-65/2021). KMG acknowledges the sup-
port of DBT-Ramalingaswami Fellowship (No. BT/HRD/35/02/2006). BC acknowledges the sup-
port of Trivedi School of Biosciences, Ashoka University.
We are grateful to the Registrar of IISc for allowing us to work on the bat colony present on the
campus. We also thank Dhanabalan, Sivarajan, Pilot Dohvi, Avik Ray, Rajasri Ray, Subhajit Saha,
Sandeep Kumar Rana, and M.Sc. Genomics students for their support in the fieldwork.
70 K. M. Garg et al.

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32. Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJ, Collen B (2014) Defaunation in the
Anthropocene. Science 345(6195):401–406
 Part II
How do Bats Inhabit Urban
Environments? Uses of Artificial Roosts,
Aerial Habitats, and Green Spaces
Chapter 6
Bat Boxes as Roosting Habitat in Urban
Centres: ‘Thinking Outside the Box’

Cori L. Lausen, Pia Lentini, Susan Dulc, Leah Rensel, Caragh G. Threlfall,

Emily de Freitas, and Mandy Kellner

Abstract  Bats in urban environments depend on human-made structures or rem-

nant natural habitats for roosting. Bat boxes are commonly used artificial structures
that aim to replace lost tree or building roosts, but they are not a universal solution,
or panacea, as few species use them, and other options exist that more closely mimic
natural tree cavities. As long-lived mammals, bats may be lured into human-built
structures with unstable conditions. These structures could act as ‘ecological traps’
if they suddenly become inaccessible with few other roost options available.
Problems arising from the use of bat boxes, such as mortality events resulting from
overheating, may reflect limited roost availability rather than inherent flaws in bat
box designs. Mimicking a natural roosting area requires accommodating requisite
roost switching. This can be accomplished in urban centres by manipulating exist-
ing trees or erecting multiple, varied bat boxes in close proximity, which could
require purposeful urban planning. Engaging the public in community-driven bat
conservation initiatives may hold the key to ensuring bats thrive in human-­dominated

C. L. Lausen (*)
Wildlife Conservation Society Canada, Kaslo, BC, Canada
e-mail: [email protected]
P. Lentini
School of Global, Urban, and Social Studies, RMIT University, Melbourne, VIC, Australia
S. Dulc
Thompson Rivers University, Kamloops, BC, Canada
L. Rensel
University of British Columbia Okanagan, Kelowna, BC, Canada
C. G. Threlfall
School of Life and Environmental Science, The University of Sydney,
Sydney, NSW, Australia
E. de Freitas
University of Northern British Columbia, Prince George, BC, Canada
M. Kellner
British Columbia Community Bat Program, Revelstoke, BC, Canada

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 75

L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_6
76 C. L. Lausen et al.

landscapes. Here, we discuss problems associated with bat boxes and propose solu-
tions, using case studies from Canada and Australia.

Keywords  Bat box · Bat house · Artificial roosts · Overheating · Community-­

driven conservation

1 Introduction

Habitats for urban hollow- or crevice-roosting bats are in limited supply in cities
and towns, where natural features have been replaced by artificial structures such as
buildings, bridges, and culverts. Some bats have been able to compensate for this by
taking advantage of roosting opportunities in older buildings, and some species are
able to exploit the myriad of microclimates that these artificial roosts offer. These
building-roosting bats may benefit from lower predation risk and ideal microcli-
mates [1], but the occupancy of building roosts is not without risk. These roosting
spaces may be lost to building demolition or renovations, particularly since modern
building designs often eliminate entrances to cavities (e.g. Energy Star for homes
[2]), and potential alternative roosts may not be available nearby. Bat boxes, some-
times also referred to as bat houses, are an increasingly popular measure used to
replace roosting habitat for bats that are evicted from buildings [3] or to compensate
for a paucity of natural features. Bat boxes are also used for habitat enhancement,
particularly in areas where few tree hollows exist [4].
Bat boxes  – rectangular, often wooden containers in which bats can roost
(Figs. 6.1 and 6.2) [4, 5] – are designed to provide roosting spaces for bats akin to
a hollow or crevice in a large diameter tree, but how effective are they as replace-
ment roosts? Despite recommendations for their installation, few studies have
examined how well bats fare in these structures against a range of fitness measures
(such as reproductive success), and guidance for their use has often focused on
capacity or how many individuals they can accommodate [6]. There may be risks
associated with large groups of bats occupying a bat box; for example, overcrowd-
ing can reduce the ability of the colony to dissipate heat, and mass mortality from
overheating has been observed in various areas of the world (e.g. Spain [7],
Australia [8]). Here, we explore the use of bat boxes as replacement roosts. Through
case studies from Australia and Canada, two countries where bat box use has raised
concerns in relation to a warming climate [8, 9], we demonstrate problems and
opportunities that arise when urban bat boxes are used and suggest some potential
future directions.
6  Bat Boxes as Roosting Habitat in Urban Centres: ‘Thinking Outside the Box’ 77

Fig. 6.1  Common North

American bat box style –
Bat Conservation
International’s four-
chamber maternity box.
Two boxes are mounted
back to back, with an
enclosed space between, to
increase microclimate
options. (Photo by Jared
Hobbs)

2 Bat Roosting Behaviours in Light of Roost Availability

Bat roosting behaviours reflect the type of roosts available [10]. Bats typically
express a high degree of site fidelity [11] and natal philopatry [12], returning to the
same set of roosts in a home range as long as they remain available and suitable (but
see [13]). Reproductive females seek appropriately warm microclimates to expedite
gestation and support lactation and growth of pups [14]. To achieve the most suit-
able microclimates and to reduce predation risk and parasite loads, bats typically
switch roosting locations [11, 15]. Roost-switching behaviours often differ between
natural and artificial roosts. While colonies using natural roosts may spread out and
occupy several roosts in a small area (e.g. [16]), bats using human-built structures
will typically use fewer alternate roosts and move less frequently between roosts
[17]. For example, reproductive (maternity) colonies in attics will switch roosting
locations within the same attic space [e.g. 1], and those in bat boxes may switch
roosts every 1–3 days, if such roosts are available, to find optimal microclimates
78 C. L. Lausen et al.

Fig. 6.2 Two-chamber
rocket box. (Photo by
Susan Dulc)

which are critical for reproductive success and development [13, 18]. Bats in natural
roosts typically move among crevice or cavity roosts (e.g. switch trees) every
1–2 days (e.g. [11, 19, 20]).
The tendency of bats that use artificial roosts to use fewer roosts may strengthen
social associations between bats [21], but dependency on few roost locations also
puts the colony’s social structure at risk. For example, Webber et al. [17] compared
social behaviour of big brown bat (Eptesicus fuscus) maternity colonies between
tree and building roosts, and bats in buildings formed denser, more highly con-
nected social networks. Over many generations, colonies of building-roosting bats
can become heavily dependent on these structures, roosting in the same roof or attic
for much of the reproductive season and returning to the same structure across con-
secutive seasons (e.g. [22]). This dependency on a single roosting structure may put
the colony at risk should this structure be lost and alternate roosts be unavailable.
This is in contrast to bats in forests, where the social network of a maternity colony
remains intact until approximately 20% of roosts are removed [23].
Limited availability of artificial roosts may pose additional challenges in light of
seasonally changing roost requirements. The suitability of a roost for a bat will vary
depending on time of year, sex, and reproductive status [24]. Reproductive females
avoid deep or prolonged bouts of torpor because even though it saves energy, torpor
6  Bat Boxes as Roosting Habitat in Urban Centres: ‘Thinking Outside the Box’ 79

delays offspring development and reduces milk production [25]. Instead, reproduc-
tive females typically seek roost microclimates within a particular temperature
range to offset the metabolic demands of gestation, lactation, and juvenile develop-
ment [1, 15, 26, 27]. Within this temperature range, referred to as the thermoneutral
zone, the bat is not expending additional energy to generate or dissipate heat.
Thermoneutral zones can vary among species, with some desert-adapted bats toler-
ating high temperatures [e.g. 45.8 °C for free-tailed bats (Mormopterus sp.) [28]]
that would be lethal to others [e.g. 44.5 °C for little brown myotis (Myotis lucifu-
gus), Yuma myotis (M. yumanensis), and fringed myotis (M. thysanodes) [29]].
Many species employ an additional strategy of cooperatively roosting with conspe-
cifics during the breeding season in maternity colonies to influence microclimates
and reduce heat loss and energy expenditure [30]. Lactating females often prefer
roosting in buildings to bat boxes [18, 31], possibly due to the insulating nature of
building roosts. In comparison, bat boxes more closely track ambient temperatures
[26, 31, 32] and typically provide cooler night-time conditions that are less condu-
cive to growth of pups [15, 25]. In contrast, cooler roosts are needed to facilitate the
use of torpor for energy savings for males, non-reproductive females, and reproduc-
tive females in early pregnancy or post-lactation or in times of food scarcity [25]. If
roosts with specific microclimatic conditions are limited or eliminated, reproductive
success and survival may suffer.

3 Providing a New Space to Roost: Bat Box Design

Bat boxes have a long history of being used to compensate for the loss of natural
roosts or eviction of bats from buildings [32]. Bat boxes are intended to mimic natu-
ral hollow or cavity roosts, have been deployed worldwide [4, 5], and vary in size,
shape, internal volume, number of chambers, colour, and construction materials.
Because of high rates of occupancy when affixed to buildings or poles [5], boxes
can be readily deployed in urban centres where suitable roost trees may not exist.
Because species differ with respect to roosting requirements, environmental condi-
tions (e.g. solar exposure, daily weather), seasonality (e.g. reproductive stage), and
box design (e.g. volume, ventilation, colour, addition of jackets, mounting tech-
niques) all influence the likelihood of occupancy.
The most commonly used boxes have one or more rectangular chambers, often
based on the designs of Stebbings and Walsh [33], or, in North America, the four-­
chamber and vented maternity box design of Bat Conservation International
(Fig. 6.1) [32]. These designs provide an interior with enough space for large mater-
nity colonies [32], while boxes with multiple chambers and vertical orientation pro-
vide a variety of microclimate options [31, 34]. The number of chambers and
internal volume can also be modified to promote certain species assemblages [32].
A second popular option in North America is the rocket box (Fig. 6.2). It features
concentric chambers (typically two), allowing bats to access different temperature
regimes within the structure. Although some studies report bats preferring rocket
80 C. L. Lausen et al.

boxes [34], others document a preference for four-chamber maternity boxes [35],
though more research is needed to identify the attributes that encourage occupancy
of rocket boxes and other large, maternity-style boxes [34]. A recent comparison
[36] of box modifications determined that adding a water jacket around a rocket box
may be beneficial by slightly raising night temperatures, which promotes growth of
pups, while slightly lowering daytime temperatures for adult females.
In recent years, large bat condos and mini condos have also gained popularity in
North America (Fig. 6.3). These structures aim to replicate the conditions found in

Fig. 6.3  A ‘bat condo’, an elevated structure built with many chambers inside to house thousands
of bats. (Photo by Jared Hobbs)
6  Bat Boxes as Roosting Habitat in Urban Centres: ‘Thinking Outside the Box’ 81

buildings by including multiple sets of roosting baffles and, in many cases, interior
flight space, with additional roosting space under the roof and siding. Bat condos
offer a wider variety of microclimates than bat boxes do and can host extremely
large maternity colonies [32]. Several bat condos have been occupied by large colo-
nies (thousands) of bats in North America [37] (S. Dulc, unpublished data).
Regardless of design, early guidance from Bat Conservation International sug-
gested using multiple (three or more) bat boxes to effectively replace a lost building
roost [32], but this guidance has changed. Today, wildlife/bat organisations tend to
recommend installing one multi-chamber box, likely as a ‘quick fix’ that entices
landowners to replace roosts lost through evictions of building-roosting bats. To
simulate the myriad of roosting options in a natural ‘roosting area’ [16] or within an
attic roost [1], it is necessary to promote the use of multiple boxes of varying styles
and solar exposure in close proximity. This ‘Goldilocks’ approach may provide the
roost temperatures that are ‘just right’ and promote successful gestation, lactation,
pup rearing, and preparation for hibernation. In addition, providing multiple bat
boxes could also facilitate beneficial behaviours such as roost switching, which
reduces predation risk and parasite loads.

4 Bat Boxes Are Not a Universal Solution or ‘Panacea’

Here, we describe the two key motivations for the installation of bat boxes in urban
areas: (1) to replace roosting habitat for bats that are evicted from buildings and (2)
to provide supplementary roosts for local bat assemblages in areas where natural
features have been lost or are lacking. We also elaborate on concerns that surround
‘quick fix’ adoption of bat boxes in urbanising landscapes.

4.1 Successfully Replacing an Eliminated Roost Post-eviction

Findings from research on bat boxes as effective replacement roosts are equivocal –
eliminated roosts are unlikely to be adequately replaced by one bat box [38]. If
boxes do not provide the same microclimates used in the building roost from which
bats were evicted, this inadequate roost replacement could be detrimental to bats.
This is especially true where the eliminated roost(s) provided ideal conditions for
maternity colonies and few alternate roosts are available [39]. If replacement boxes
are not high-quality habitat and more suitable alternate roosts are nearby, boxes may
remain unoccupied. Only 1% [40] to 46% [13] of marked, evicted individuals are
recaptured near an erected replacement roost. Although few studies have assessed
the impacts of eviction on reproductive success, evidence suggests that reproductive
rate declines post-eviction when bats are forced to use alternate roosts ([41],
C. Lausen, unpublished data).
82 C. L. Lausen et al.

We further suggest that landowners reconsider the need to exclude bats from
buildings because there may be alternative solutions that would allow bats to remain
safely in existing urban roosts. Indeed, some landowners have lived successfully
with bats in their buildings for years without negative consequence, by employing
relatively simple adaptations, such as ensuring separation of human and bat living
spaces and yearly cleaning of guano after bats have left for the season (BC
Community Bat, M. Kellner, pers. obs.; also [42]). Wherever it is practical, existing
roost sites in the urban landscape should be identified and protected, with bat boxes
as a complementary measure. If exclusion is indeed necessary and bat boxes are
used, then minimising the risk of boxes becoming ecological traps hinges on ensur-
ing an adequate number and diversity of boxes and placements and installing them
at a height inaccessible to ground-based predators (i.e. ideally  ≥5  m from the
ground; predator-guard at base of pole, or away from roof if building-mounted).

4.2 How a Bat Box Might Become an ‘Ecological Trap’

How can we know whether a bat box is an ecological trap? Ecological traps occur
when animals select poor-quality habitat (or other resources) over higher-quality
resources [43]. Occupancy of bat boxes is often naïvely equated with success and
may be incorrectly interpreted as a preference for this roost type. Bats may choose
to roost in a box for reasons other than preference, such as site fidelity after exclu-
sion from an adjacent building, lack of alternate roosts within a preferred foraging
area, or social cohesion. The cues that drive bats to use bat boxes are not well under-
stood and may not accurately reflect the quality of the box as roosting habitat.
Fidelity of bats to a roosting area [11] may lead to maladaptive roost choice when
high-quality roosts are lost [41]. Bats may subsequently experience reduced repro-
ductive fitness or increased mortality risk, perhaps due to poor box placement,
insufficient numbers of boxes, and/or low variation among box microclimates.
Bat boxes may function as ecological traps if they increase predation risk. For
example, bats in boxes may be at increased risk of predation by urban animals, such
as corvids, owls [44], and rodents [45], that are attracted to occupied boxes by scent
or sound, and domestic cats (Felis catus) which can reach particularly high densities
in urban areas [46]. Free-ranging domestic cats are opportunistic, subsidised preda-
tors that can have a significant impact on maternity colonies of bats [47, 48]. In
Sydney, Australia, scent-hunting predators, including possums, rodents, and cor-
vids, were attracted to bat boxes containing guano – interestingly, they were more
likely to investigate boxes with small rather than large accumulations of guano,
suggesting a negative correlation between group size and vulnerability to predation
[45]. Although no studies have explicitly assessed cat predation on bat boxes, a
recent review identified 86 bat species, including 19 (40%) of Australia’s hollow-­
roosting bats [46], that are known to be preyed upon or threatened by cats globally.
The continued use of bat boxes as habitat replacement or enhancement tools with
incomplete knowledge of bat roosting and environmental context may
6  Bat Boxes as Roosting Habitat in Urban Centres: ‘Thinking Outside the Box’ 83

unintentionally facilitate the creation of ecological traps. In other words, it is only

by paying attention to the behaviour and health of a colony of bats in artificial struc-
tures that we can understand where bats truly thrive.

4.3 Supplementing Existing Habitat: Environmental Context,

Bat Assemblages, and Box Design

Environmental context, bat assemblage, and box designs and arrangements are criti-
cal considerations when supplementing existing roosts in an area to promote bat
abundance. Landscape context and box design can lead to the preferential use and
domination of bat boxes by only one or a few species [49]. This has triggered con-
cerns that the installation of boxes may cause an overall shift in community compo-
sition. For example, while some tree crevice-roosting bats in the United States and
Canada have adapted to human-built structures, only 15 of 47 species (32%) have
been documented using bat boxes (M. Kellner, unpublished data; also [32]). This
concern was also raised in the Southern Hemisphere [50, 51]. However, evidence
from Australian studies suggest that this shift may not occur. One 5-year study on
18 sites across Greater Melbourne found no evidence of assemblage shift [52].
Similarly, in a comparison between reserves with and without bat boxes in Sydney,
reserves with boxes exhibited no shift in assemblage composition, but they did have
greater activity of one species, Gould’s wattled bat (Chalinolobus gouldii), that
occupies boxes and less activity of other bats [53]. This suggests that although spe-
cies diversity persists in reserves with bat boxes, box availability may affect relative
abundance.

4.4 How Hot Is Too Hot?

Bat boxes with full solar exposure throughout the day maintain warm temperatures.
These conditions may be advantageous during some parts of the reproductive cycle,
but there is a fine line between an ‘optimally warm microclimate’ and too hot.
Reproductive bats select roosts based on microclimate [15], and even natural roosts
can reach extremely high temperatures, which are likely to be lethal for most spe-
cies (e.g. rock crevice roosts >50 °C [54] but see [28]). Having a selection of avail-
able roosts with varying microclimates typically ensures that bats can switch roosts
to appropriately thermoregulate and avoid overheating. However, global warming
may raise the risk of overheating for bats in boxes [7, 8, 55] (see Box 6.1: Case
Study – Overheating Bat Boxes). If roost choice becomes limited, as is increasingly
true in many cities, maternity colonies may remain in bat boxes that overheat, lead-
ing to heat stress and potential mortality.
84 C. L. Lausen et al.

Box 6.1: Case Study – Overheating Bat Boxes

Overheating of occupied bat boxes seems to be a new phenomenon in south-
ern British Columbia (BC), Canada, with record summer heat in recent years.
In Greater Vancouver, a mixed Myotis lucifugus and M. yumanensis colony
(~600 individuals total, L. Rensel, unpublished data) used a set of three identi-
cal, south-facing, multi-chambered bat boxes that replaced a lost adjacent
building roost in an area of relatively few buildings and trees. Similarly,
S. Dulc (unpublished data), working in Creston, monitored a M. yumanensis
colony (~300 individuals) occupying one multi-chambered bat box erected
near a building from which the bats were evicted. In both cases, the bat colo-
nies occupied boxes continuously, raising young throughout the summer, sug-
gesting that alternate roosts were not available or not being used.
In 2018 and 2019, bat box microclimates were recorded, and overheating
was observed in both Creston and Vancouver maternity colonies. In 2019, in
Creston, pregnant females with wet fur (from urinating on themselves to facil-
itate evaporative cooling (e.g. [54])) were observed crowding at the box
entrance midday, in mid-June (pre-parturition). Several bats then flew to roost
on shaded bark of adjacent trees as the bat box exceeded 40 °C and 100%
humidity (maximum ambient temperature and relative humidity were 31.7 °C
and 75%, respectively). During a 2018 summer heatwave in Greater
Vancouver, adults and juveniles fell out of the three bat boxes, seemingly due
to heat exhaustion (bat box temperature reached 46 °C), and ~75 bats died
(J. Saremba, Burke Mountain Naturalists, pers. comm.). This mass mortality
event suggested that the bat boxes became too hot for bats.
Immediately after the mass mortality in Vancouver, the boxes were painted
a light colour (to reflect light). Although this change successfully reduced box
temperatures in times of extreme heat, it also lowered internal box tempera-
tures in spring and, thus, could prolong gestation. Therefore, alternative cool-
ing measures for boxes were identified; the above-mentioned box colour
decision was reversed, and, instead, an additional bank of north-facing boxes
was built next to the south-facing boxes so that bats can choose from a cooler
set of boxes.
In June 2021, when BC citizens were forewarned of another heatwave,
volunteers mobilised to shade bat boxes with awnings or white sheets. No
mass mortalities of bats were reported during this heatwave. In some cases,
this could be attributed to the precautionary actions. For example, at one site
where microclimate was being recorded, the temperature in the bat box
dropped from 44.1  °C (nearing the lethal 44.5  °C [24]) to 42.6  °C within
30 min of installing a sunshield (S. Dulc, unpublished data), although adults
and young were still observed crowding the box entrance and vent (Fig. 6.4).
In other cases, where alternate roosts presumably existed, the bats simply
abandoned their bat boxes.

(continued)
6  Bat Boxes as Roosting Habitat in Urban Centres: ‘Thinking Outside the Box’ 85

Box 6.1  (continued)

Fig. 6.4 (a) Adult and juvenile bats crowding the opening and vent of an overheating four-­
chamber maternity bat box in Creston, British Columbia. Fur wetted by urine is a cooling
mechanism. (b) A temporary white shade erected on the box during this heatwave pre-
vented lethal microclimates. (Photo by Susan Dulc)

(continued)
86 C. L. Lausen et al.

Box 6.1  (continued)

These Canadian examples of overheating bat boxes and heat stress during
unprecedented heatwaves raise the question of what role context plays in
determining whether a bat box is detrimental to a maternity colony. Perhaps
as there become less roost options available to a colony raising young, the risk
of bats roosting in unsuitable microclimates rises. These risks include cold
temperatures that do not support growth of young, hot temperatures that
exceed thermal tolerances [56], or a lethal combination of temperature and
humidity (i.e. heat stress, temperature-humidity index) in which evaporative
water loss (and consequently heat loss) no longer occur in high humidity.
It is not yet understood why bats would remain in a bat box that overheats.
New local weather patterns and unusual heatwaves that are not anticipated by
bats may be partially to blame [55], but this behaviour may also stem from the
reduced choice of roosting habitat, with options likely to become increasingly
scarce as our landscapes continue to urbanise or be otherwise transformed.

5 Thinking Outside the Box: Recommendations

for the Installation and Use of Bat Boxes and Other
Complementary Roost Structures

Bat boxes may not be a panacea, as described above, but in urbanising landscapes,
they may still play a crucial role in bat conservation. Increasingly, humans control
the availability of habitat for bats, and where bats control arthropod pests [32],
retaining bat populations is desirable and can be promoted (see Box 6.2:  Case
Study – Engaging Citizens). Purposeful planning of roosting habitat for bats is nec-
essary (see Sect. 6 below: Urban Planning for Bats). Problems with bat boxes, par-
ticularly where they act as ecological traps, may result from placement rather than
an inherent design flaw.
The literature presents a variety of reports on the use and success of bat boxes,
including design and placement performance relative to geographic location.
Species-specific requirements, as well as local climate, weather patterns, landforms,
and solar exposure, provide important context for boxes being used by bats. Many
studies report high usage of boxes by common or widespread species, especially
those tolerant of urbanization [47, 57]. The inherent variability of occupied artificial
roosts should not be surprising given that natural roosts and bats are also diverse.
6  Bat Boxes as Roosting Habitat in Urban Centres: ‘Thinking Outside the Box’ 87

Box 6.2: Case Study – Engaging Citizens

Retaining bats and roosting habitat in urban centres can be further supported
through the education and engagement of local citizens. Two successful com-
munity bat programmes in western Canada (albertabats.ca in Alberta; bcbats.
ca in BC) promote the conservation of urban bats and the creation of bat-­
friendly communities by providing guidance and support to landowners who
live with or wish to evict bats without harming them. As a result, interest in
bat conservation and volunteer participation has grown, enabling a broad-­
scale and long-term summer roost monitoring program (e.g. 360 roosts in BC
in 2020). A bat box registration and monitoring programme is now providing
data on box occupancy, timing of seasonal arrivals/departures and parturition,
and disease surveillance.
In Australia, where 46 bat species (or 57%) partially or wholly rely on tree
hollows for roosting and breeding [70], a bat monitoring program at
Melbourne’s Organ Pipes National Park is one of the world’s longest-­running
bat box programmes [71], and it exemplifies how enhancing bat habitat can
raise awareness and appreciation for bats. Since 1992, more than 42 bat boxes
have been installed, monitored, and maintained at this park to compensate for
the lack of natural hollows. Volunteers have been coordinating bat box inspec-
tions and bat assessments since the programme started. Eight species have
been recorded using the boxes and >2000 individuals have been marked. The
research and data have provided important insights into bat ecology and con-
servation, including studies of reproduction, including documentation of dou-
ble-breeding events, survival rates and life history, box occupancy patterns
and design considerations, community dynamics, thermal physiology, and tag
retention rates. Most importantly, this bat box programme has provided peo-
ple with the rare opportunity to see bats up close, fostering an appreciation for
these creatures.

5.1 What to Recommend for the Installation and Proposed Use

of Bat Boxes

So, what universal guidance might be derived for bat boxes? Determining what
roost choices already exist in an area and how to supplement or provide variety is
likely far more important than the design of one box, although modifications that
support passive heating and insulating designs have been proposed and could prove
beneficial in some areas (e.g. [58]). Although there are many publications on styles,
stains, and other box deployment options (e.g. [55]), these may be species- and
88 C. L. Lausen et al.

location-specific, and do not address the real issue of context. It might be that using
many different designs within a large variety of solar exposures may be more stra-
tegic than trying to invent or identify one design and appropriately place a single bat
box to achieve the range of microclimates needed by a bat population (e.g. a mater-
nity colony throughout the reproductive season). However, we recognise that cost
may limit what can be done without collaboration.
Ultimately, a ‘one box does all’ goal is neither achievable nor desirable because
it is likely to appeal to a small subset of species, have narrow temporal use, and pos-
sibly reduce bat fitness. For example, a box stained with a light colour and posi-
tioned to avoid overheating in midsummer will likely be unsuitable in early summer
during gestation [59]. Similarly, an insulated box will retain heat for pups at night
midsummer  but is unlikely to warm up enough from solar incidence  to promote
gestation. Lausen and Barclay [15] found that a maternity colony of approximately
40 big brown bats (Eptesicus fuscus) used more than 70 rock crevice roosts over the
course of the summer. In a forested area of northern Alberta, Canada, Olson and
Barclay [20] identified 135 roost trees used by two colonies of Myotis lucifugus
(approximately 400 bats). The documented pattern of boxes being dominated by
one or a few species may reflect not so much the narrow range of species that will
use boxes (e.g. [60]), as the narrow range of box designs and placements usually
deployed.
Small structural differences in artificial habitat (microhabitat) can dictate suit-
ability of a box as a roost; for example, culverts used by the fishing bat Gould’s
large-footed myotis (Myotis macropus) in Australia differed from unoccupied cul-
verts in the size of holes in the concrete and the presence of crevices [61]. This
highlights the need to consider microhabitat and macrohabitat properties when
planning bat habitat in an urban environment.
It is also important to consider the spatial placement of bat boxes. The distance
between roosts can matter if bats are forced to move young or switch roosts during
daylight when predation risk could be high. Typical distances between succes-
sive  natural day roosts have been reported for some North American bats; e.g.
<200 m for pallid bats (Antrozous pallidus) [62], <110 m for western small-footed
myotis (Myotis ciliolabrum), ~1.25  km for Eptesicus fuscus [63], and ~90  m for
long-eared myotis (Myotis evotis) [19]. In natural situations, crevices may be spa-
tially close so that, if needed, a daytime roost switch would be possible. Successful
use of bat boxes in urban centres may require that the proximity of bat boxes mimics
that of roosts in natural areas.

5.2 Beyond the Box: Installing Other Artificial Roost

Structures to Diversify Available Roost Space

Artificial structures besides bat boxes may also complement existing roosting
opportunities and promote roosting by a greater diversity of bats. Wooden shingles
attached to the outside of buildings as siding/roofing may offer roosting habitat and
6  Bat Boxes as Roosting Habitat in Urban Centres: ‘Thinking Outside the Box’ 89

attract bark-roosting species, such as the silver-haired bat (Lasionycteris noctiva-

gans) and long-legged myotis (Myotis volans; M. Kellner, pers. obs.), that rarely use
bat boxes. Bark mimic structures, made of resin to resemble loose bark, can be
affixed to trees [64]. The bark mimic, BrandenBark™, used in the eastern United
States for the Indiana myotis (Myotis sodalis), has hosted other crevice-roosting bat
species [65]. These structures can be installed on tall poles, in urban environments,
simulating trees where there are none. Where trees exist, roosting habitat can also
be enhanced through modifications that create roosting locations (cavities/crevices),
which may be possible in some urban green spaces. In Australia, mechanically cre-
ated hollows (chainsaw cuts) in tree trunks can mimic natural cavities used by long-­
eared bats (Nyctophilus species) [66]. By structurally and thermally resembling
natural roosts, these hollows may benefit bats [67]. In Costa Rica, sawdust concrete
bat roosts resembling tree hollows have been shown to effectively host frugivorous
and nectivorous bats [68]. Few data exist on the effectiveness of artificial roosts for
foliage-roosting species, but the Ussuri tube-nosed bat (Murina ussuriensis) used
roosts made to mimic the leaves of butterbur (Petasites japonicus) and Japanese
whitebark magnolia (Magnolia obovata) [69]. Although foliage roosts are consid-
ered abundant [11], they may not be in urban environments, so these roosts may be
beneficial here.

6 Conclusion: Urban Planning for Bats

As landscapes continue to urbanise or otherwise change and natural habitats become

increasingly limited, availability of roosts for bats is likely to diminish – hence the
need to plan bat box designs and installations to effectively support urban bats.
Evaluating existing foraging and roosting habitat in the context of a building evic-
tion is necessary to appropriately mitigate for eliminated roosts. A bat box erected
for reasons other than to mitigate an eviction may never become occupied, because
a bat box is but one crevice roost, akin to one tree cavity. As shown by Olson and
Barclay [20], it takes a forest of many tree roosts to meet the needs of one bat col-
ony. We recognise that bat boxes are not insignificant in cost, and can be challeng-
ing to install and maintain; while they are not the only option for artificial roosts,
variable designs and placements of boxes make them an attractive option for replac-
ing lost roosting habitat. Just as our city planning is now occurring in some places
to ensure buildings are safe and near resources that people require, urban landscapes
should also be planned for wildlife, including bats, to ensure the availability of safe
and accessible roosts near suitable food and water resources. There can be immense
value in engaging stewardship groups and other volunteers in planning and imple-
menting urban bat conservation programmes.
90 C. L. Lausen et al.

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Chapter 7
Aerial Habitats for Urban Bats

Lauren A. Hooton, Lauren Moretto, and Christina M. Davy

Abstract  Aerial habitats in cities are understudied but essential for urban, flying
wildlife. Understanding interactions between aerial habitats and wildlife (i.e. aero-
ecology, the study of aerial ecosystems) can identify key foraging and migratory
resources for these species. In an urban context, where urban infrastructures domi-
nate the airspace, an aeroecology lens can inform wildlife-friendly urban planning
and land management. In this chapter, we highlight key knowledge gaps associated
with urban aeroecology of bats by exploring how elements of urban environments
may influence the aerial habitat of bats. We draw on studies from within and outside
cities to consider how bats might navigate characteristics of urban areas that alter
the airspace, including roads and traffic, anthropogenic noise, artificial light, urban
heat islands, air pollution, urban canyon effects, high wind speeds, and windows.
Finally, we summarise potential approaches to mitigate the negative impacts of
these challenges and support aeroconservation of urban bats and other flying
wildlife.

Keywords  Aeroecology · Aeroconservation · Anthropogenic urban infrastructure ·

Urban airspace

L. A. Hooton
Department of Environmental and Life Sciences, Trent University, Peterborough, ON, Canada
L. Moretto
Vaughan, ON, Canada
C. M. Davy (*)
Department of Biology, Carleton University, Ottawa, Ontario, Canada
e-mail: [email protected]

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 95

L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_7
96 L. A. Hooton et al.

1 Introduction

The study of aerial ecosystems (aeroecology; [1–3]) and their conservation (aero-
conservation [4–7]) can inform our understanding of the behaviour and habitat
requirements of flying wildlife, including bats. Bats rely on aerial habitats to access
a range of resources. For example, nectivorous and frugivorous bats commute
through the airspace to access flowering and fruiting trees. Insectivorous bats aerial-­
hawk flying prey, or glean prey off aerial-adjacent surfaces, and some species even
mate in the air [8].
Structural and environmental modifications in urban basoaerial habitats (0–1 km
altitude) [4–6] pose challenges for navigation beyond those faced by bats in non-­
urban habitats. Each species of bat may perceive these challenges differently, and
flight style may determine how much of the airspace that a species uses is affected
by urban infrastructure. For example, ground-level modifications should more
strongly affect the airspace for species that fly close to the ground than for high-­
flying species [8]. Nonetheless, bats must navigate around anthropogenic elements,
including densely arranged buildings of variable heights, windows, transmission
lines, open roads, and vehicles, all of which increase collision risk and alter the
structure of the airspace [5, 6]. Urban airspace is also affected by high noise levels,
air pollution, and intense artificial light at night (ALAN) [4, 8]. Urban canyons (also
called street canyons), created by clusters of tall buildings, can alter conditions in
the atmospheric boundary layer by trapping noise and radiant heat, thereby altering
wind speed and direction, temperature, and ultimately air quality [9]. Redirected
echoes from the smooth surfaces and windows of buildings may also be disorienting
to bats [10].
In this chapter, we explore how the structural and environmental modifications of
the urban airspace might affect urban bats, based on existing literature that has
tested the effects of these modifications in laboratory and field settings (non-urban
and urban). We highlight key knowledge gaps associated with urban aeroecology of
bats and, where sufficient evidence is available to inform potential solutions, pro-
pose actions to support bats that rely on urban aerial habitats.

2 Urban Modifications to Aerial Habitats

Urban bats must deal with a variety of anthropogenic modifications of the airspace,
including dense roads with heavy traffic, intense anthropogenic noise (anthrophony)
and artificial light at night (ALAN), heat islands, air pollution, street canyons that
affect temperature and wind speed, and risk of collision with windows. Each of
these modifications varies along a spectrum with increasing urban densification, and
we consider them in detail below.
7  Aerial Habitats for Urban Bats 97

2.1 Roads and Vehicle Traffic

Given that roads and vehicle traffic often affect the movements of wildlife, includ-
ing bats outside cities [11], how do they respond to roads and traffic in cities? Road
density increases in urban environments, where roads and traffic range from two-­
lane, local roads with light traffic (e.g. residential areas) to multi-lane roads with
heavy and fast-moving traffic (e.g. highways). Research outside cities suggests the
contextual nature of bats’ responses to roads and traffic – these responses seem to
vary with road characteristics and surrounding habitat (e.g. number of lanes, traffic
volume, vehicle noise, surrounding vegetation) and with variation among ecological
traits among bat species. However, research in cities is sparse. Drawing on studies
from non-urban areas, we consider how roads and traffic may affect urban bats and
outline knowledge gaps to be addressed.
Bats may be less willing to cross wide roads compared to narrower, two-lane
roads [11, 12], but roadside vegetation might mitigate road avoidance in cities by
bridging the airspace and buffering disturbances from vehicle traffic below.
Vegetation adjacent to roads can direct bats to cross where it is relatively safer, such
as high above the road or through an underpass [12]. For example, acoustic monitor-
ing of an urban population of northern myotis (Myotis septentrionalis) in Toronto,
Canada, revealed that bats may use a forest corridor under a raised portion of a
14-lane highway to move between patches of preferred, interior habitat [13]. Bats in
residential neighbourhoods in Toronto also cross tree-lined roads across the city
(L. Moretto, pers. obs.). However, implementing roadside vegetation to guide cross-
ings by bats should be well-planned because it can also raise the risk of collisions if
it encourages low-altitude crossings [14]. Data from Brazil indicate that road cross-
ings and vehicle strikes are most frequent where forest and other high-quality bat
habitats intersect with a road, possibly because bats emerge from nearby roosts at
lower altitudes [15].
Traffic noise and vehicle movements also generally disturb bats, interfering with
their commuting and foraging [11, 12, 16–18]. However, most available studies
have not been performed in urban settings, where bat responses may be distinct. In
one laboratory study, greater mouse-eared bats (Myotis myotis) foraged less effi-
ciently in response to playbacks of recorded traffic noise [16, 18]. Traffic noise also
reduced general bat activity in another European study, but playback of ultrasonic
sounds matching the frequencies of echolocation calls affected only one species,
suggesting that traffic noise has additional effects beyond interfering with echoloca-
tion [17].
Demographic and functional traits of bats may partly predict their responses to
roads and traffic and risk of vehicle strikes [11, 17, 19, 20]. Generally, collisions and
road-related evasive manoeuvres increase during swarming, mating, and migration
and for males and juveniles [12]. Species adapted to slow, low-altitude, manoeu-
vrable flight, such as those that glean or forage in clutter, may also be at a greater
risk of collision because they often cross roads at lower altitudes and are less willing
to make long-distance detours around roads [11, 17, 19, 21, 22]. For example,
98 L. A. Hooton et al.

low-flying frugivorous and insectivorous phyllostomids were the most commonly

detected roadkill in Brazil [15]. Conversely, some generalist species that are com-
mon in cities, such as pipistrelles (Pipistrellus spp.), do not exhibit road avoidance
behaviours and thus may be at greater risk of collision with vehicles if they cross
roads more often [23]. Unfortunately, with most knowledge of how traffic affects
bats coming from non-urban contexts, it remains unclear whether urban bats, which
may have habituated to constant traffic, might respond differently.
If some urban bats avoid road crossings, then how can we ‘bridge the gap’ to
enhance connectivity across aerial habitat? Prioritising locations for ‘enhanced con-
nectivity’ should start by mapping the movements of bats, e.g. using radiotelemetry
to identify where bats actually cross roads (see [13, 22]). Once active crossing sites
are discovered, vegetated over- or underpasses can be established to offer options
for safer crossing [24]. For example, tall trees may help promote crossing over
urban neighbourhoods or arterial roads at a safe height [12, 14], while crossing
under elevated roads may be facilitated by continuous vegetation [13].

2.2 Urban Noise

Urban airspaces are acoustically complex and noisy, and the effects of this noise on
bats are not clear. Some research suggests that bats might be able to tolerate urban
noise. Most bats are sensitive to frequencies above 10 kHz, corresponding to calls
used for social communication and ultrasonic calls used for echolocation [25]. Most
anthropogenic sound in urban environments is loudest at frequencies below 2 kHz,
and so is unlikely to interfere with activities that depend on ultrasonic sounds [26–
28] or with high-frequency communication calls. Some bats tolerate and habituate
to urban noise by adapting their activity to the general soundscape. For example, to
deal with urban noise masking prey-generated sounds, some gleaning species may
increase their use of visual cues for foraging [26, 27]. Bats in a noisy airspace may
also adjust their calls; for example, Russo and Ancillotto [28] suggested that lower-
ing the frequencies of social calls [e.g. by Kuhl’s pipistrelles (Pipistrellus kuhlii)] in
an urban area of Italy may reduce call attenuation, as lower-frequency sounds prop-
agate further. In southern Australia, grey-headed flying foxes (Pteropus poliocepha-
lus) appeared to simply tolerate urban noise – vocalisations were similar between
urban and rural colonies [29].
Nevertheless, there may be thresholds of urban noise beyond which tolerance is
limited. In the Australian study of P. poliocephalus, vocalisations at two highly
urban roosts declined or ceased in response to loud noise produced by low-flying
aircraft, despite these colonies’ apparent tolerance for other urban noise and moving
vehicles. In Chicago, United States, the activity of silver-haired (Lasionycteris noc-
tivagans) and big brown bats (Eptesicus fuscus) declined in response to anthrophony
[30]. Specific anthropogenic sounds associated with a greater risk of mortality, such
as traffic noise, may alter bat behaviour [16, 18, 29]. Ultimately, we need to
7  Aerial Habitats for Urban Bats 99

understand interspecific variation in bats’ responses to anthropogenic noise in the

urban airspace before we can develop effective mitigation strategies.

2.3 Urban Light Pollution

Artificial light at night (ALAN) is a recognised threat to global biodiversity [31] and
affects roughly 23% of global land surface [32]. The effect of ALAN on bats varies
with the type of light and species of bat [33–38]. Here, we summarise trends based
on available evidence, which should be considered with the following two caveats.
First, there is a pronounced latitudinal bias in research on ALAN [39], and most of
the research on bat responses to ALAN has focused on temperate zone species.
Second, although we include results from studies in rural areas, we acknowledge
that bats accustomed to urban habitats may respond differently to ALAN.
The spectrum of ALAN is changing as lighting technology and consumer prefer-
ences evolve, and bat species appear to vary in their responses to different wave-
lengths and illuminance [38]. Older technologies, such as low-pressure sodium
(LPS) and high-pressure sodium lights, release narrow-spectrum, yellow/orange
light, whereas mercury vapour lights produce broader-spectrum, whiter light,
including ultraviolet (UV) wavelengths. These are increasingly being replaced by
broader-spectrum, light-emitting diodes (LEDs) and metal halide lights that also
produce UV light [38, 40]. In European and British studies, most pipistrelles seem
to exhibit higher activity at UV-emitting streetlights than at LED streetlights,
whereas activity of Myotis spp. and parti-coloured bats (Vespertilio murinus)
declines near ALAN regardless of wavelength [37, 41, 42]. Noctules (Nyctalus
spp.), serotine bats (Eptesicus serotinus), and soprano pipistrelles (P. pygmaeus)
exhibit inconsistent responses to different wavelengths of ALAN among studies
[34, 37, 42, 43]. In contrast, tropical urban bats in Singapore exhibit no difference
in activity between streets lit by HPS lights and streets retrofitted with LED lights
[43]. Bat activity may also vary with the distribution of light in the airspace: activity
of some species decreases more with vertical than with horizontal illuminance [36].
Artificial lights are associated with global insect declines [31] that pose a long-­
term threat to insectivorous bats, but lights can provide a foraging advantage for
some bat species at the local scale by concentrating insects (e.g. [36, 44, 45]).
Indeed, bat responses to different light spectra may partially reflect insect responses
to the same lights. Lights that emit short wavelengths, particularly UV, typically
attract more insects than lights with longer wavelengths (e.g. LPS streetlights; [31,
36]), so some lights provide better foraging opportunities than others [38]. This may
be especially true for moths ([1, 46]; but see [47]).
Certain species are considered ‘light-tolerant’, but even they may modify their
movements in response to ALAN [36, 38, 48]. Pipistrellus pipistrellus appears to
tolerate lighting in rural areas where illumination is limited [48] but is less likely to
leave tree cover to cross gaps in vegetation in cities, which are brightly lit and have
large gaps [49]. Radio-tracked common noctules (N. noctula) in Berlin, Germany,
100 L. A. Hooton et al.

tolerated ALAN when foraging in areas with abundant water or vegetation but
avoided light when commuting between roosts and foraging areas [50]. In a park
south of Paris, France, activity by Pipistrellus and Nyctalus spp. increased near
streetlights, but the effect varied with illuminance [36], and both species preferred
forest cover over open space as they approached lights, particularly white light [43].
Both fast- and slow-flying species of bats used lit streets to commute in Singapore,
but feeding buzzes were rarely recorded, suggesting that the bats were foraging
elsewhere [51].
Other species may restrict their activity to dark areas where possible. Forest bats
in Sydney, Australia, exhibited higher activity within urban forests than near forest
edges lit by streetlights [33]. In Europe, slow-flying, forest specialists [e.g. Plecotus
sp., some Myotis sp., horseshoe bats (Rhinolophus spp.)], which are adapted to clut-
ter, exhibit light avoidance behaviour, which may reflect a greater perceived risk of
predation. Experiments in non-urban habitats revealed that Myotis and Plecotus sp.
are less active when lights are on than when they are off [34, 35, 43], as also observed
for Myotis bats in an urban habitat [37]. The effect of streetlights on Myotis activity
extends up to 50 m from the lights, even at low illuminance (<1 lux), and persists
after the lights are turned off [36]. Lesser horseshoe bats (R. hipposideros) also
reduce activity and delay emergence in response to ALAN [35, 52, 53]. In Costa
Rica, fast- and slow-flying urban bats both responded negatively to ALAN, suggest-
ing light avoidance [54].
Solutions to mitigate the effects of ALAN on urban bats are similar to those pro-
posed for other nocturnal species and require urban planners to explicitly account
for biodiversity in land management and lighting decisions [48]. Existing lighting
infrastructure can also be made more bat-friendly by decreasing the spectral inten-
sity of LEDs and shifting to lower (yellower) spectra [55]. Of course, any modifica-
tions to street lighting must meet the perceived safety needs of humans. For example,
new lights or retrofits that produce minimal vertical illuminance but enough hori-
zontal illuminance for human use can benefit bats and still meet public safety
requirements [21, 36].

2.4 Urban Heat Islands

Bats experience higher ambient temperatures in cities due to the urban heat island
(UHI) effect, a phenomenon whereby cities are substantially warmer than surround-
ing, non-urban areas. Dark and impervious surfaces absorb radiation, and urban
infrastructure traps heat, while remnant patches of vegetation continue to cool the
air in specific locations, generating strong thermal gradients [56]. As a result, maxi-
mum air temperatures in some cities reach up to 15 °C higher than surrounding rural
areas [57].
The interactive effects of global warming and UHIs on bats may be contextual.
In the temperate zone, bats in UHIs might experience longer active seasons and
warmer roosts than in non-urban areas. Warmer maternity roosts are associated with
7  Aerial Habitats for Urban Bats 101

accelerated juvenile development in some species [58]. However, global warming

may drive air and roost temperatures in some regions above the species’ thermal
tolerance [59, 60], resulting in heat stress and mortality. For example, extreme heat
in the austral summer of 2019–2020 resulted in mass abandonment of pups at flying
fox colonies in Australia and killed more than 72,000 individuals of various species
[61]. Pteropodids also died of heat stress in and around the town of Pongola, South
Africa [62]. These heat-related mortalities are not confined to cities, but UHIs cer-
tainly increase the frequency and severity of heatwaves [56].
Slowing climate change directly benefits bat populations everywhere, while
urban bats will also benefit from urban planning to mitigate UHIs. Current methods
include the use of permeable or reflective pavement, reflective building materials,
and addition of green spaces and green infrastructure [57, 63].

2.5 Urban Canyons

From an urban bat’s perspective, the airspace is characterised by frequent intrusion

of buildings, especially in large urban cores, which often have densely packed sky-
scrapers [9]. In some ways, the urban canyons created by tall buildings mimic natu-
ral canyons; they provide roosting habitat analogous to that in rock crevices of
escarpments. However, most natural canyons form over time by ephemeral or per-
manent rivers that buffer air temperature and provide access to drinking water and
arthropod prey. In contrast, urban canyons rise from busy roads that present a colli-
sion risk to bats (although it is possible that bats can learn to avoid vehicle traffic
more effectively in cities, given the more consistent volume of traffic in cities than
non-urban areas).
High-velocity, turbulent airflow in urban canyons [56] may also pose a challenge
to bats. As wind moves quickly above the top of clusters of tall buildings, some of
the moving air is also pulled down into urban canyons, creating high spatial varia-
tion in wind speed, including downdraught and updraught [64] that could be diffi-
cult for a bat to navigate. We speculate that bats flying at high altitudes (e.g. during
long-distance migrations) could be directed down into urban canyons by wind vor-
tices they may not anticipate, but are not aware of any studies on the behavioural
adaptations of flying wildlife to variable airflow in urban canyons. Even high-flying
species that are well-adapted to navigating comparable wind speeds in natural can-
yons might struggle to navigate between buildings composed largely of smooth
surfaces such as glass, concrete, or steel that they cannot grip when they require rest.
Urban canyons also contribute to UHI effects because wind vortexes trap heat
and air pollution at street level [56], which can be mitigated by incorporating trees
and other vegetation into street design. Hedges and other low vegetation can improve
air quality at street level, and incorporating green walls can improve air quality at
higher altitudes [9]. Tall street trees can also help cool urban canyons but, unlike
hedges, can also concentrate air pollutants at street level as they trap some air below
their canopy [65]. Implementing green roofs and walls on tall structures can improve
102 L. A. Hooton et al.

aerial habitat quality [4] and provide shelter to bats foraging in or migrating through
urban canyons. The effectiveness of these actions has not been evaluated, and post-­
construction monitoring should be conducted to identify and refine building designs
that provide the greatest benefit to urban bats and other flying wildlife.

2.6 Windows

Windows are invisible barriers for flying wildlife (e.g. billions of birds in the United
States die each year from window collisions; [66]), but the limited bat-related data
suggests that windows are not a major threat to bats. Organisations that track wild-
life window collisions in cities rarely report bat-window collisions. For example, at
the time of this writing, the Toronto chapter of the Fatal Light Awareness Program
has recorded >75,000 window strikes for birds since 2000 but <200 for bats (P. Plant,
pers. comm., 2021). Similarly, since 2013, Lights Out Baltimore has reported only
85 bat strikes (L. Jacks, pers. comm., 2021), most during periods of migration.
Although observations of bats and window collisions to date have been passive
or incidental and windows may not pose a substantial threat to bats, a series of
intriguing experiments is revealing how flying bats may perceive windows. At an
obtuse angle of approach, a window’s smooth surface redirects most of a bat’s echo-
location calls away from the bat, which could confuse the bat [10]. Thus, angle of
approach may influence the likelihood of collision. However, bats use visual cues
alongside acoustic cues to improve perception [67, 68], which may help bats to
perceive windows in their flight path and avoid collisions. Unless further data on
bat-window collisions arise to suggest otherwise, it seems unlikely that window col-
lisions pose a real threat to urban bats.

3 Bat-Friendly Stewardship of Urban, Aerial Habitats

Although we have presented potential actions to support urban bats throughout the
chapter, these require robust evaluation before they can be recommended to policy-­
makers, urban planners, and conservation practitioners. We had to draw on many
non-urban studies, but city-dwelling bats may be habituated to urban aerial habitat
modification and respond differently. Accurately generalising the needs of bats in
urban, aerial habitats is also limited by high interspecific variation in bats’ responses
to the risk of vehicle strikes, habitat modification by roads, urban noise and light
pollution, and tolerance of extreme heat. Nevertheless, the potential solutions we
have summarised here overlap with urban habitat management that supports other
urban wildlife and human wellbeing.
Evidence-based stewardship projects to support aerial habitats for other urban
species can be leveraged to test effects on urban bats. Urban planners, developers,
and researchers should collaborate to enable robust experimental designs such as
7  Aerial Habitats for Urban Bats 103

before-after-control-impact studies to quantify bat responses to habitat manage-

ment. Reducing ALAN where possible and incorporating vegetation into urban
infrastructure provide habitat for other wildlife and an opportunity to test how bats
respond to these changes in aerial commuting pathways and foraging habitat. More
specifically, reducing high-intensity, vertical lighting where bats cross roads may
work best when combined with tree planting to reduce perceived gap width. Finally,
any actions to slow climate change are likely to benefit urban bats by reducing UHI
effects and canyon effects.

Acknowledgements  We are grateful to Brendan Samuels (Western University), Paloma Plant

(Fatal Light Awareness Program Canada), and Lindsay Jacks (Lights Out Baltimore) for sharing
information about bat collisions with windows and Allison Fairbrass for helpful discussions about
anthropogenic noise. Two anonymous reviewers and the editor of this chapter provided helpful
comments on an earlier version of this chapter.

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Chapter 8
City Trees, Parks, and Ponds: Green
and Blue Spaces as Life Supports to Urban
Bats

Lauren Moretto, Leonardo Ancillotto, Han Li, Caragh G. Threlfall,

Kirsten Jung, and Rafael Avila-Flores

Abstract  Patches of vegetated habitat within urban areas (“green spaces”) and
water bodies (“blue spaces”) are crucial to support urban wildlife, including bats. In
this chapter, we review the literature to explore how bats use green and blue spaces,
including natural, semi-natural, and manicured vegetated areas, and various water
bodies. We first examine the value of urban green spaces to bats for roosting, forag-
ing, commuting, and refuge from disturbances. We then examine the importance of
blue spaces as sources of drinking water and prey. We also consider how  spatial
arrangements of green and blue spaces across the urban landscape influence use by
bats. Finally, we review approaches of studying green and blue spaces to guide
future research and suggest guidelines for better design and management of these
valuable habitats to support urban bat abundance and diversity.

L. Moretto (*)
Vaughan, ON, Canada
L. Ancillotto
Wildlife Research Unit, Dipartimento di Agraria, Università degli Studi di Napoli Federico II,
Naples, Italy
H. Li
Department of Biology, University of North Carolina at Greensboro, Greensboro, NC, USA
Department of Biology, University of Nebraska Omaha, Omaha, NE, USA
C. G. Threlfall
School of Life and Environmental Science, The University of Sydney,
Sydney, NSW, Australia
K. Jung
Institute of Evolutionary Ecology and Conservation Genomics, University Ulm,
Ulm, Germany
R. Avila-Flores
División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco,
Villahermosa, Tabasco, Mexico

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 107
L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_8
108 L. Moretto et al.

Keywords  Green space · Blue space · Foraging · Drinking · Habitat · Urban

landscape

1 Introduction

Urbanisation fundamentally alters natural environments around the world. Urban

areas become a mosaic of impervious surfaces with patches of semi-natural, vege-
tated habitat when large, interconnected patches of habitat are transformed with
artificial structures. These remaining patches, hereafter “green spaces” [1], include
urban nature reserves and parks, street trees, private lots, and community gardens
(Figs. 8.1 and 8.2). However, they are mostly small, fragmented, heavily manicured,
and dominated by non-native vegetation [1–3] (Fig. 8.2).
Although these green spaces are often heavily transformed, they remain valuable
to wildlife, including bats [4–9]. In this chapter, we explore how various green
spaces may be used by bats in urban environments. In particular, we examine how
green spaces provide critical resources and spaces for roosting, foraging, commut-
ing, and refuge from disturbance. We also investigate the importance of waterbodies

Fig. 8.1  Green spaces provide important resources to support populations of bats in urban areas,
including spaces for roosting, foraging, commuting, and hiding from predators. Large green
spaces, like this urban park in Ulm, Germany, may support the diversity of bats in cities by provid-
ing habitat for urban-sensitive species
8  City Trees, Parks, and Ponds: Green and Blue Spaces as Life Supports to Urban Bats 109

Fig. 8.2  Many green spaces in urban areas are small in size, but nonetheless, they provide valu-
able habitat for urban bats. A city with many small fragments of green space may help to distribute
resources for bats across the landscape

within these green spaces, or “blue spaces”, to bats. We then consider the influence
of spatial, landscape-scale arrangements of green and blue spaces on the use by
bats. Lastly, we review approaches to studying urban green and blue spaces to guide
future research, and we provide recommendations to improve management and
design of urban green and blue spaces to support urban bat populations.
We recognize that bats will perceive green and blue spaces differently from
humans. Understanding this perspective from a sensory and experiential point of
view is a challenging task (especially since bats rely primarily on auditory percep-
tion to experience the world, unlike humans [10]). For example, humans may con-
sider street trees, private gardens, and yards as being different types of green spaces.
Bats may perceive these spaces as general habitat patches with different purposes
(e.g. foraging and roosting) or levels of quality/value (e.g. a street tree may have no
value to a bat due to surrounding disturbance, while trees in parks may provide safe
roosting space). The same “type” of green or blue space (e.g. all street trees) may
also be perceived differently across an urban environment. For example, street trees
that are within or close to other roosting, foraging, or drinking locations may be
preferred to street trees which are further from these sites [11]. The quality, avail-
ability, and functions of resources within green and blue spaces may differ tempo-
rally (e.g. seasonally), which may alter how bats will use these spaces over time. For
instance, trees that are used for summer roosts may not provide adequate roosting
space in the winter months, and tree hollows that are used as maternity roosts may
differ from those used outside of this period [6, 12]. Ultimately, we recognize that
our understanding of bat needs and preferences in urban areas can easily be biased
110 L. Moretto et al.

by human perception. Using existing and emerging knowledge about bat ecology
and behaviour will help to remove human biases. This will benefit  our ability to
understand how bats use the urban environment and better inform management
decisions for bats.

2 Use of Green Spaces by Urban Bats

Urban green spaces vary in their composition (e.g. vegetation types and structure),
management, and use by humans, but research suggests that these green spaces
provide critical resources for bats in urban environments. Below, we describe how
urban bats may use these green spaces.

2.1 Roosting Habitat

Green spaces provide vegetation for roosting and improve the quality of artificial
roosts nearby (e.g. bat boxes). For tree-roosting bats, trees with nooks, crevices, and
large crowns (e.g. old trees or dead trees/snags) provide several spaces for roosting
[6, 11–13]. Unfortunately, these trees are often removed in city centres for aesthetic
or safety reasons (i.e. falling branches/trunks may pose a hazard to people if a tree
is close to streets, public paths and trails, buildings, etc.), but they may be retained
in parks and nature reserves. These larger green spaces have several diverse roosting
structures and can support populations of different bat species [7, 8, 14–16]; both
common and rare bat species have been recorded roosting in urban green spaces [6,
11–13]. Bats that roost in artificial structures, like bat boxes and houses, also prefer
roosting near green spaces. For example, Kubista et al. found that roost site selec-
tion in human houses was positively influenced by the amount of green space nearby
[16]. Green spaces may improve the quality of these artificial roosts by providing
easy access to other resources, such as food and water (see Sect. 4 below).

2.2 Foraging Habitat

Green spaces provide food and foraging spaces for urban bats. Frugivorous and
nectivorous bat species feed on the nectar and fruits from trees and other plants in
urban green spaces [17–20]. In Tuxtla Gutiérrez, southern Mexico, the relative
abundance (number of individuals captured in ground-level mist nets) of Jamaican
fruit bats (Artibeus jamaicensis) in urban parks was positively influenced by the
abundance and quality of fruits in these parks; in particular, quantity of nitrogen
available in fruits was the best predictor of bat abundance [21]. Vegetation in green
spaces also supports populations of prey for insectivorous bats [8, 22, 23]. In urban
8  City Trees, Parks, and Ponds: Green and Blue Spaces as Life Supports to Urban Bats 111

Sydney, Australia, green patches and backyards in areas of the city with nutrient-­
rich soils and moderate vegetation cover supported greater insect biomass and sig-
nificantly greater bat feeding activity than other parts of the city with nutrient-­poor
soils and less vegetation [23]. Similarly, in urban Melbourne, Australia, a positive
relationship was observed between vegetation cover within green spaces, abun-
dance of nocturnal invertebrates, and activity and species richness of insectivorous
bats [24]. Researchers also speculate that green roofs may provide important forag-
ing spaces for insectivorous bats, since they support more insect populations and bat
activity than conventional roofs [25–27].

2.3 Corridors for Commuting and Refuge from Disturbances

Green spaces provide commuting routes for bats and connect roosting and foraging
areas in urban environments. For example, linked tree canopies may help bats com-
mute across urban areas. Studies have recorded bats flying along tree canopies in
urban areas, possibly because they physically bridge habitat, orient commuting
bats, and mitigate disturbances by reducing exposure to artificial lighting and buff-
ering anthropogenic noise [11, 13, 28–37]. However, not all bat species will use
these commuting routes equally; bats may be selective of routes, depending on their
tolerance to anthropogenic disturbance. For example, bat species that opportunisti-
cally forage around street lights [e.g. great fruit-eating bat (Artibeus lituratus)] may
prefer using tree-lined streets as commuting routes while disturbance-sensitive spe-
cies may not [11, 28].
Large urban green spaces may provide refuge from anthropogenic disturbances
for bats. A study of urban forest patches by Haddock et al. found that the dark inte-
rior of urban forest patches provided habitat for light-sensitive species [29]. In
Greensboro, North Carolina, USA, more bat activity was found in peripheral city
parks with less human activity than central city parks with more human activity
[35]. In Melbourne, Australia, urban golf courses in areas of moderate anthropo-
genic activity were extremely important for supporting bat species richness. These
golf courses contained large, old trees, understory vegetation that supported insect
populations, water bodies, and large expanses of dark spaces for foraging [24].

3 Blue Spaces in and around Urban Green Spaces

Urban green spaces often contain blue spaces, such as ponds, streams, fountains,
and artificial pools, which may provide critical resources for urban bats. Despite
being common in urban environments worldwide, their importance to urban bats
has historically been under-examined, but research about blue spaces is increasing
[37–40]. Studies suggest that urban green spaces that contain or are found near blue
spaces support more bat activity when compared to green spaces without or far from
112 L. Moretto et al.

blue spaces [41–44]. Furthermore, characteristics of blue spaces, including water

availability, water quality, and the quality of green space surrounding the water
source, may also influence bats [40–42]. Given this recent research into blue spaces,
we examine the possible value of blue spaces to urban bats.
The primary value of blue spaces to bats is their provision of drinking water,
especially during periods of drought. Bats require regular access to drinking water
due to their morphology (i.e. small size and high surface-to-volume ratio of their
wing membranes), which makes them susceptible to dehydration. Drinking involves
strategic manoeuvring to lap water from the surface, so easily accessible and unclut-
tered blue spaces (i.e. easier to perceive returning echolocation calls) are often pre-
ferred drinking sites (Fig. 8.3). Many urban blue spaces, like ornamental/recreational
ponds and swimming pools, are often free of obstacles and may provide easy access
to drinking water for bats. Bats also prefer drinking from water with fewer or less
potent chemical treatments (e.g. swimming pools with mineral treatments are

Fig. 8.3  Blue spaces in

urban environments
provide sites for foraging
and critical sources of
drinking water for bats in
urban environments. This
brown long-eared bat
(Plecotus auratus) from
Italy manoeuvres close to
the water surface to lap a
drink with its tongue.
Uncluttered blue spaces
can improve access to
drinking water (Photo
credit to Sherri and Brock
Fenton)
8  City Trees, Parks, and Ponds: Green and Blue Spaces as Life Supports to Urban Bats 113

preferred to those with chlorine and salt [45]), though research has yet to address the
effects of these chemicals on urban bats.
Blue spaces are also often structurally complex and seasonally variable, provid-
ing a variety of unique resources for urban bats. Several blue spaces in urban envi-
ronments feature concrete embankments and culverts to direct water flow or prevent
flooding, which may provide artificial roosting habitat for bats [46, 47]. Blue spaces
in recreational areas or private gardens are often surrounded by vegetation or con-
tain aesthetic features, such as fountains and waterfalls, which provide spaces and
resources for foraging.
Blue spaces are important foraging spaces to some species of bats. Insectivorous
bats like big brown bats (Eptesicus fuscus) and Mexican free-tailed bats (Tadarida
brasiliensis) often forage for insect prey above water [8], and blue spaces may sup-
port nectar-yielding flowers for nectivorous bat species. In Melbourne, Australia,
Straka et al. found that water bodies (including ponds) in green spaces supported
abundant populations of nocturnal flying insects, including flies (Diptera) and cad-
disflies (Trichoptera). As a result, these spaces supported greater bat activity than
similarly sized green spaces without blue spaces [42]. Blue spaces may also concen-
trate prey populations for bat species that glean prey from vegetation by hosting
juvenile stages of insects and amphibians on aquatic vegetation. For example, urban
populations of túngara frogs (Engystomops pustulosus) gather at ponds within green
spaces for reproduction, concentrating these population for the frog-eating, fringe-­
lipped bat (Trachops cirrhosus) in urban areas [48, 49]. However, urban blue spaces
that are highly managed or treated with insecticides may reduce the availability and
quality of prey items.
Bats may prefer particular characteristics of blue spaces. Generally, bat activity
is greater around larger blue spaces [41, 42] and around blue spaces with more
riparian vegetation [39, 40, 42]. Irrespective of the size and presence of natural fea-
tures around blue spaces, artificial illumination generally negatively impacts bat
activity in and around blue spaces [40, 41, 50, 51]. Water quality and pollution may
also influence the use of urban blue spaces by bats (e.g. [45]), but more research
about this is required to better understand its effects on bats. Straka et al. found that
bat activity was notably greater at ponds with lower levels of heavy metals in
Melbourne [41], but Naidoo et al. [52] and Kalcounis-Rueppel et al. [53] found that
eutrophic rivers host greater bat richness and activity levels when compared to
nearby unpolluted urban rivers.

4 Spatial Considerations for Green and Blue Spaces

in the Urban Landscape

The spatial organization of patches of green and blue space across an urban land-
scape influences a bat’s use of these spaces [7, 32, 54]. Specifically, bats can be
influenced by the total amount of green and blue space within an urban area (i.e.
composition of patches in an urban area) and the spatial arrangement of these green
and blue spaces (i.e. configuration of patches in an urban area; see [55, 56]). We
114 L. Moretto et al.

explore the effects of both urban green and blue space composition and configura-
tion on bats in this section.
Green and blue space composition in urban environments influences urban bat
activity, abundance, and diversity. Simply, more green or blue space will provide
more resources and potentially easier access to resources (e.g. prey refuge areas).
More resources may attract and/or support larger populations of bats and a greater
diversity of species. Research suggests  that larger green spaces in urban areas,
including large urban parks or golf courses, support greater abundance and diversity
of bats than small green spaces [4, 8, 12, 15, 57, 58]. Although most of these studies
examined the effects of large, unfragmented patches of habitat on bats, a large
amount of fragmented habitat across an urban landscape may still importantly sup-
port bat populations [4, 8, 9, 11, 15].
Recently, researchers are examining the effects of fragmentation alone on urban
bats (e.g. the value of a few large green space patches is compared to several smaller
green space patches with the same total area). For some bat species, if the quality of
many small, fragmented green space patches is high, these patches may contain
enough high-quality resources across an urban area to support populations of these
species [4, 8, 9, 11, 15, 59]. For example, highly mobile insectivorous species, like
molossids, may find that many small, fragmented green spaces distribute pockets of
prey across an urban landscape ([8]; Fig. 8.2). This may improve access to prey and
foraging success. Conversely, other species may require large, unfragmented green
spaces ([59, 60]; Fig. 8.1). For example, in Melbourne, Australia, Caryl et al. found
that many bat species were no longer present in landscapes with medium densities
of houses, irrespective of the total amount of tree cover across the landscape [61].
Therefore, they suggest that fewer large patches of green space may provide better
conservation outcomes for bats in Melbourne than many smaller patches. If this is
not achievable, they recommend that at least 20% of the landscape contain trees, as
below this threshold in tree cover many species no longer occurred.
The configuration, or spatial arrangements, of green and blue spaces across an
urban area also influences species diversity. The presence of a variety of comple-
mentary habitat types in an urban environment could suit the needs of a variety of
species, thereby supporting greater species diversity. For example, Ancillotto et al.
investigated the use of a pond archipelago by an assemblage of four generalist pip-
istrelle species, namely, common pipistrelle (Pipistrellus pipistrellus), soprano pip-
istrelle (P. pygmaeus), Kuhl’s pipistrelle (P. kuhlii), and Savi’s pipistrelle (Hypsugo
savii), in Rome, Italy [40]. They found that all bats were present at ponds with
woodland less than  1 km  away and at ponds adjacent to woodland margins and
hedgerows. The close proximity of complementary habitat types in this study may
have reduced commuting times between roosts to foraging locations, risk of preda-
tion, and exposure to unfavourable weather conditions (e.g. wind, rain). Straka et al.
also found that the amount of vegetation cover in the surrounding 0.5 km [measured
using remote sensing as mean normalized difference vegetation index (NDVI) in the
buffer area] strongly influenced the use of blue spaces by bats [42]. Inversely, there
8  City Trees, Parks, and Ponds: Green and Blue Spaces as Life Supports to Urban Bats 115

is also evidence suggesting that the absence of complementary habitat types in close
proximity negatively affects bats; Lintott et al. found that greater amounts of built-
up area surrounding an urban river negatively affected bat activity up to 3  km
away [39].

5 The Study of Urban Green and Blue Spaces

Continuing to study urban green and blue spaces and their characteristics is impor-
tant to guide future conservation efforts for bats. A common approach to studying
the influence of these spaces involves surveying bat activity and species richness
within different land cover types (e.g. commercial areas, residential areas, large
parks, etc.) across urban environments (e.g. [4, 5, 7, 14, 15, 54]). Results from these
studies may identify green and blue spaces that are most used by species of interest
(e.g. [13, 58, 60]), which can inform management strategies in an urban area.
When green and blue spaces with high bat activity or species richness are identi-
fied, studies often examine characteristics of these spaces in detail to better under-
stand bat habitat and resource needs (e.g. proximity of roost sites to feeding habitats,
food availability, or human disturbance). For example, species not commonly found
in urban areas can be found in large urban parks and nature reserves [12, 57], so
characteristics of these green spaces are closely examined (e.g. light levels, water
quality, tree cover, etc.), and the movements and behaviours of bats across these
spaces are tracked [13, 14, 18, 19, 30, 35]. Alternatively, comparing the characteris-
tics of green/blue spaces to those of non-green/blue space sites may also help to
highlight characteristics of importance to urban bats (e.g. building design, water
courses adjacent to wooded areas, parks without artificial lighting, etc.; see [8, 9]).
Observations of bats using other green or blue spaces not previously considered,
including urban street treelines, private lots, green infrastructure (e.g. green roofs),
urban water ways, and swimming pools, are inspiring research into characteristics
of these spaces and their resources [11, 15, 25–27, 39, 41, 62]. For example, studies
from Australia found that many species use residential gardens and lots, but less so
than other larger or more vegetated spaces [24, 54, 63]. Brownfields (i.e. previously
developed and abandoned sites) may also be used as foraging sites for insectivorous
species, since they may support insect populations, but merit further examination as
they retain pollutants which may harm the health of bats [52, 53]. Although some of
these spaces may be challenging to access for research, such as private lots and resi-
dential properties, they should not be disregarded as they too provide important
resources for urban bats [15, 64, 65].
116 L. Moretto et al.

6 Recommendations for Green and Blue Space Design

and Management to Support Urban Bats

Here, we provide general recommendations for urban green and blue space design
and management to support urban bat populations based on existing knowledge and
expert opinion. However, these recommendations should not replace consideration
of local context and site-/species-specific studies, which will always provide the
best guidance for management action. The use of these spaces by bats is still not
completely understood and will vary between urban environments around the world:
1. Green and blue spaces can provide resources for roosting, foraging, and drink-
ing, corridors for commuting, and refuge from disturbance. Large green and blue
spaces with a diversity of features (e.g. vegetation of various heights, dense for-
est, open spaces, dark spaces, water bodies surrounded by vegetation) should be
prioritized for protection, as they may be able to support greater bat activity and
species richness in urban areas. Specifically, the following features may help to
promote urban bat diversity in green and blue spaces:
• Patches of “interior” habitat (i.e. dark, buffered from anthropogenic distur-
bances such as light and noise, and highly vegetated) may support species
that are less tolerant to disturbance (e.g. edge-sensitive or forest-interior
species).
• Large, older trees should be protected within green spaces when possible
(balanced with removal of hazardous branches or trees for human safety)
since they may provide support to populations of tree-roosting species in
urban environments. Large trees provide several nooks and crevices for roost-
ing and often harbour fruits or prey.
• Blue spaces should contain both uncluttered areas for easier drinking and be
surrounded by vegetation to concentrate prey for bats. Reducing artificial illu-
mination in these spaces may also promote bat activity.
2. Green and blue space use by bats and associated management efforts should be
considered across an urban landscape (not only within a single green or blue
space patch):
• The greatest total amount of green and blue space should be protected in an
urban area. If large, unfragmented green and blue spaces cannot be protected,
several smaller but high-quality patches should be protected.
• Spaces may provide different functions and resources to bats (which may
change seasonally), so a variety of spaces should be close together to improve
access to these resources (e.g. within 1 km; see [15, 40, 58, 60]). For example,
green spaces should contain or be close to blue spaces. This will improve
access to drinking water and may concentrate prey items for urban bats.
8  City Trees, Parks, and Ponds: Green and Blue Spaces as Life Supports to Urban Bats 117

7 Future Research Directions

There is still much to learn about how urban bats use green and blue spaces. Here,
we highlight key knowledge gaps to guide future directions for research:
1. The use of green and blue spaces in private, residential lots should be studied
when possible to better understand how these spaces support bat populations
across an urban landscape (see [15, 64, 65]). For example, while residential lots
may provide important spaces and resources for foraging or commuting, their
value may depend on their proximity to larger patches of roosting habitat or on
the degree of disturbances or threats present at these sites (e.g. backyard lights,
cats and other predators, use of pesticides by residents).
2. The use of brownfields by bats should be explored further. Brownfields may be
used as foraging sites for insectivorous species since they may support insect
populations. However, the concentration of pollutants in brownfields may harm
the health of bats. For instance, bats may consume insects with high concentra-
tions of pollutants or drink from polluted water at these sites.
3. Blue spaces can be highly important to urban bats, but there are still many unan-
swered questions about their influences, including:
• How valuable are blue spaces such as fountains and private swimming pools
to bats? These are common in urban areas, but their use by bats is still poorly
understood [45, 66]. Their function as sources of water for bats should be
explored further given their permanence, especially to urban bat populations
during dry seasons and/or in semiarid environments [66, 67].
• What is the effect of chemically treated or polluted blue spaces (e.g. chlori-
nated swimming pools, polluted storm water ponds) on bat health in the short
and long term?

Acknowledgments  We are grateful to the editor of this chapter and two anonymous reviewers for
the helpful comments and suggestions for revisions.

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Chapter 9
Assessing the Effects of Urbanisation
on Bats in Recife Area, Atlantic Forest
of Brazil

Enrico Bernard, Laura Thomázia de Lucena Damasceno,

Alini Vasconcelos Cavalcanti de Frias, and Frederico Hintze

Abstract  The metropolitan area of Recife has 4.1 million inhabitants and is in one
of the most deforested areas of the Brazilian Atlantic Forest. Here, few forest frag-
ments remain in a large urban matrix. How do bats interact with this complex and
challenging landscape? Focusing on insectivores, we used bioacoustics to (1) assess
which bats use green spaces in Recife, (2) evaluate the effect of intense artificial
light at night (ALAN) on bat activity, and (3) compare molossids’ activity and
behaviour in urban and non-urban areas. Although with fewer species when com-
pared to forested areas, we show that several insectivores can persist in that urban
matrix. However, these species make a heterogeneous use of the landscape: green
spaces were hotspots for bat activity with nearly 2.4 times more activity than non-­
green spaces. We also identified that ALAN from soccer (football) stadiums influ-
ences not only the total activity of insectivores but also their temporal activity
patterns. However, this influence was stadium-specific with no pattern common to
all stadia, pointing to a more complex interaction between species and ALAN. Finally,
we show that urbanisation influences the activity and behaviour of urban molossids.
We found a significant decrease in total activity in the urban environment but found
that urban molossids are active earlier in the night compared to non-urban molos-
sids. Our studies provide evidence of some of the effects of urbanisation on insec-
tivorous bats in a large city among the remains of the Atlantic Forest in Northeastern
Brazil, and we highlight the need for more local research and conservation action.

E. Bernard (*) · L. T. de Lucena Damasceno · A. V. C. de Frias

Laboratório de Ciência Aplicada à Conservação da Biodiversidade, Departamento de
Zoologia, Centro de Biociências, Universidade Federal de Pernambuco, Recife, PE, Brazil
e-mail: [email protected]
F. Hintze
Laboratório de Ciência Aplicada à Conservação da Biodiversidade, Departamento de
Zoologia, Centro de Biociências, Universidade Federal de Pernambuco, Recife, PE, Brazil
Programa de Pós-Graduação em Biologia Animal, Universidade Federal de Pernambuco,
Recife, PE, Brazil

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 123
L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_9
124 E. Bernard et al.

Keywords  Artificial light at night (ALAN) · Bioacoustics · Green urban remnants

· Urban fauna

1 Introduction

Urbanisation is transforming the terrestrial environment markedly [1, 2].

Deforestation, habitat degradation, and fragmentation due to urbanisation are affect-
ing thousands of species. Urban expansion can be particularly harmful when it
occurs in areas rich in biodiversity (i.e. biodiversity hotspots - locations with a high
level of biodiversity and endemism that suffer intense degradation and threat to their
diversity) [3]. Extensive tropical regions around the world are impacted by poorly
planned expansion of their urban centres, amplifying the effects of habitat loss and
degradation and threatening species [4].
Perhaps one of the most extreme examples of the impact that urbanisation can
have on a tropical hotspot is the Atlantic Forest of Brazil, where biodiversity is
becoming critically threatened by extensive human occupation. The Atlantic Forest
harbours about 60% of all endangered species in Brazil [5], but about 70% of the
Brazilian population currently resides in the Atlantic Forest domains [6], and less
than 30% of the original forest remains. This forest mostly consists of second-­
growth forests or areas affected by edge effects [5, 7].
Although occupation predates the colonisation of Brazil (i.e. more than 500 years
ago), the process of urban densification in the Brazilian Atlantic Forest is relatively
recent, having intensified around the 1970s, when rural populations moved to the
cities. This population growth in cities was rapid and poorly planned. This brought
about a new and heterogeneous landscape: the green spaces that remain within cities
are small parks (frequently <10 hectares), plazas, gardens, and a few private or pub-
lic reserves of arboreal environment. As in many parts of the world, urban green
spaces of the Brazilian Atlantic Forest are small, isolated, and distant from each
other, forming green islands within the urban matrix [8].
Urbanisation can, however, generate different responses on different wildlife
groups [9–11]. Some wildlife may be highly disturbed by anthropogenic modifica-
tions and cannot persist in cities, while others may tolerate or obtain benefits from
anthropogenic environments and human interactions within them (i.e. synanthropic
species). The impact of urbanisation on a species is dependent on its traits [8, 12,
13], and different species of bats present different responses to urbanisation (see
[14]). Some bat families and species are highly sensitive to habitat change, and
urbanisation can strongly impact the structure of local communities, causing a
9  Assessing the Effects of Urbanisation on Bats in Recife Area, Atlantic Forest of Brazil 125

decrease in richness and diversity when compared to the original pre-urbanisation

habitats. Structures such as bridges and buildings may provide roosts for some spe-
cies, helping them to adapt to the urban environment [15]. Conversely, species spe-
cialised in using natural roosts are unlikely to persist in cities  if these roosts
are limited [16]. Artificial lights attract insects and may improve prey availability
for light-tolerant species [17, 18]. In contrast, some species avoid illuminated areas
because they are sensitive to artificial light at night (ALAN), and therefore cannot
make use of insect clusters around lights [15, 19].
It can be quite challenging to understand the responses of bats – a speciose and
ecologically diverse group – to urbanisation in biodiversity hotspots. In Brazil, at
least 84 bat species have been recorded in cities [20], representing about 47% of the
country’s 181 described bats [21], and nearly 100 species occur in the entire Atlantic
Forest [22]. However, most of these records are sporadic or from studies of bats and
disease transmission. As such, there is a clear and pressing need for more research
on these bats, given the projected losses of natural forest with future urban expan-
sion in the region.
In this chapter, we present three studies of the effects of urban modification on
bats in the area of Recife, the capital of Pernambuco State, in the Northeastern
Brazilian Atlantic Forest. We focused on insectivorous species using bioacoustics to
(1) assess which species use urban green spaces, (2) evaluate the effect of artificial
light on bat activity, and (3) compare the activity and behaviour of urban- and non-­
urban-­dwelling species.
Recife (8°03′46″S, 34°52′14″W) is Brazil’s third most densely populated metro-
politan area. It consists of 15 municipalities distributed across ca. 3200 km2, with
~4.1 million human inhabitants [23]. The climate is tropical, with average annual
temperature ranging from 24 °C to 26 °C and 1800 and 2000 mm of rain annually
(https://portal.inmet.gov.br).
The history of urbanisation in the region goes back 500 years. Indigenous vil-
lages historically existed in the Atlantic Forest, but the first urban settlements were
established by the Portuguese in the 1530s. Since this colonisation, the region’s
economy has been heavily dependent on extraction of natural resources and sugar-
cane farming. Over time, these activities have driven deforestation and forest degra-
dation, leaving behind small, isolated, and poor-quality habitat patches.
The 15 municipalities are totally inserted in the Atlantic Forest biome and have
~640  km2 of natural remnants or ~19.5% of their total area, varying from 2 to
108 km2 of remnants per municipality (4.8–61.4% of their areas). An inventory of
bat species has never been conducted in Recife’s metropolitan region, but small-­
scale short-term inventories based on mist netting have resulted in records of 12–26
species per site [24], and a tentative list for the area presents at least 59 species in 37
genus and 5 families.
126 E. Bernard et al.

2 Bat Species Richness and Activity in Green Spaces

and Urban Areas in Recife

To examine how green spaces affect insectivorous bats, we measured bat activity at
sampling sites across the region. We used satellite images to select five study sites.
Each site had a green space measuring between 15,239 and 139,457 m2 and a paired
urban area 200 m away. Between September 2012 and January 2013 (five sampling
nights per site), we simultaneously monitored the green space and the urban area for
2 h per night. We recorded bat activity on full-spectrum bat detectors, which we set
up in locations expected to have low human traffic.
We used CallViewer18 [25] to view and analyse files and extract key call param-
eters (i.e. duration, minimum and maximum frequencies, frequency with maximum
energy, and call intensity), which we used to assign search-phase calls to sonotypes
and families, based on published values [26]. For a detailed description of the meth-
odology adopted, see [27].
We analysed 500 files and 1500 min of recordings. We recorded a total of 16
sonotypes (16  in green spaces, 8  in urban areas) belonging to 5 families
(Emballonuridae, Molossidae, Noctilionidae, Phyllostomidae, Vespertilionidae)  –
all but the Phyllostomids are strict insectivores. Compared to the paired urban areas,
green spaces had more bat species and activity (student t: t = 2.53; P = 0.02), but not
more feeding buzzes (t  =  1.81; P  =  0.08) or social calls (t  =  −1.56; P  =  0.13)
(Fig. 9.1). Vespertilionids were more active in green spaces (Chi-square residual test
R = 6.27), while molossids were more active in urban areas (R = 4.71).

Fig. 9.1  Activity of four different bat families recorded in green urban remnants (GR) and outside
them (NR) in the metropolitan area of Recife, Northeastern Brazil. Embal  =  Emballonuridae;
Vesper  =  Vespertilionidae; Molo  =  Molossidae; Phyll  =  Phyllostomidae. Noctilionidae was
recorded but accounted for <1% of the calls and was not represented. Activity is expressed based
on the % of echolocation calls in the analysed files, and one file could contain calls from more than
one family. Therefore, the sum of the percentages could be higher than 100%
9  Assessing the Effects of Urbanisation on Bats in Recife Area, Atlantic Forest of Brazil 127

3 Impact of Artificial Illumination on Bat Activity

Urbanisation increases light pollution, but the ecological impacts already extend
well beyond the urban fringe and increasingly affect species in natural habitats,
including protected areas [28]. These impacts occur because  artificial light can
interfere with species’ ability to access resources; some prey species may avoid
bright areas due to a higher risk of predation, while other predator species may pre-
fer those areas because they may attract more prey – like insects around a street-
light – making easier to locate them [29, 30]. ALAN may modify light-mediated
endocrine regulations, causing shifts in reproduction patterns [11, 36], and may also
disrupt the spatial orientation of nocturnal species, by removing dark areas or creat-
ing artificial shadows and reflexes [30, 31]. Impacts on species appear to differ
among taxa but may ultimately have cascading ecosystem effects that translate into
biodiversity loss [31–33].
Patterns of artificial illumination in cities are complex and heterogeneous with
spatial and temporal variation in the intensity of light. For example, sports stadia
concentrate intense lighting on game nights but are dark when not in use – as such,
they are interesting locations to study ecological impacts of lights [34]. Bats are
suitable study subjects, given that they are strictly nocturnal and may use vision to
find food and detect predators ([30] and others therein).
Given knowledge that many phototactic insects are attracted to certain artificial
lights [15, 30, 34–37], we tested the prediction that bat activity at football (soccer)
stadia is greater on game nights, when lights are on, than on non-game nights, when
they are off, and asked whether the lights otherwise influence bat behaviour.
We selected three stadia, all fitted with 2000-W mercury vapour lights. The sta-
dium Ilha do Retiro is 16,515 m2, can hold 32,983 people, ​​and has 96 reflectors. It
is located next to a river and has swimming pools, tennis courts, shops, car park, and
smaller soccer fields, as well as billboards that are lit every night. It is mainly sur-
rounded by residences and shops (67% in a 500-m buffer). Arruda Stadium, simi-
larly surrounded by residential and commercial buildings (98% in a 500-m buffer),
is 30,000  m2, seats 60,044 spectators, and has 128 reflectors. Finally, Arena
Pernambuco is 24,000 m2, with a capacity of 44,300 people and 360 reflectors, and
is surrounded by forest fragments (51% vegetation and no buildings in a 500-m
buffer).
Between April and September 2018, we acoustically monitored bats on a total of
11 game nights and 41 non-game nights. We worked four times at Ilha do Retiro and
three times at Arruda – at each stadium, we recorded bats on the eve of the game, on
game night, and on the three subsequent nights (i.e. 1 off, 1 lit, 3 off). We obtained
four samples at Arena Pernambuco using the same protocol but instead recorded on
game night and on four subsequent nights (i.e. 1 lit, 4 off). We used full-spectrum
bat detectors, placed under one reflector in the centre of the stadiums, and recorded
from 1 h before sunset to 1 h after sunrise. We used Kaleidoscope (version 4.5.5,
Wildlife Acoustics, Maynard, MA, USA) to process and analyse spectrograms. We
128 E. Bernard et al.

Fig. 9.2  Bat echolocation pulses recorded in three football stadiums (Arena Pernambuco, Arruda,
and Ilha do Retiro) in the metropolitan area of Recife, Northeastern Brazil, between April and
September 2018. Bat pulses were recorded from 16:00 h to 06:00 h along nights with reflectors on
(lit) and off (dark). Diamonds indicate the average number of pulses and bars the interval variation.
Different letters represent statistically significant differences within site pairs

used the number of echolocation calls as a proxy for bat activity and Mann-Whitney
to test for differences between game and non-game nights.
We observed more bat activity on game nights than on non-game nights at Arena
Pernambuco (P = 0.002) and Arruda (P = 0.0167), but not at Ilha do Retiro (P = 0.44)
(Fig. 9.2). We also observed shifts in temporal activity patterns, but not consistent
ones. At Arena Pernambuco, for example, activity patterns were trimodal on non-­
game nights (peaks at ca. 17:30 h, 00:30 h, and 4:30 h) and bimodal on game nights
(peaks at ca. 20:00 h and 04:30 h) (Fig.  9.3). At Ilha do Retiro, bats exhibited a
bimodal pattern on non-game nights (peaks at ca. 17:30 h and 05:00 h) and a tri-
modal pattern on game nights (peaks at ca. 17:00 h, 23:00 h, and 4:30 h). At Arruda,
bat activity was unimodal on non-game nights (peak at ca. 17:30 h) and trimodal on
game nights (peaks at ca. 17:30 h, 21:30 h, and 4:30 h).

4 Molossid Activity and Behaviour in Urban vs.

Non-urban Areas

The family Molossidae accounts for almost one third of the country’s total diversity
of insectivorous bats [21] and is one of the main insectivorous bat families in cities
[14, 18, 27, 38]. Several authors (e.g. [16, 18, 39, 40]) argue that many molossids
9  Assessing the Effects of Urbanisation on Bats in Recife Area, Atlantic Forest of Brazil 129

Fig. 9.3  Bat activity based on the recording of echolocation calls along 19 nights at Arena
Pernambuco Stadium, in Recife, Northeastern Brazil. Echolocation calls were recorded on nights
with reflectors on (red) and off (light blue), and dashed vertical lines mark the intervals where the
lights were on
130 E. Bernard et al.

are adapted to the urban environment. Molossids have a fast flight style well suited
to open areas and with few obstacles [41]. Furthermore, their roosting habits (i.e.
use of fissures or crevices), allow them to take advantage of the many opportunities
provided by anthropogenic structures (e.g. expansion joints of bridges and build-
ings, spaces between tiles, etc.) [15, 39]. However, molossids are still poorly studied
in the Neotropics, because mist nets – the traditional method of capturing bats – are
relatively ineffective for high-flying aerial insectivores like molossids. Here, bio-
acoustics can help fill knowledge gaps about habitat use and activity patterns of
molossid bats in cities.
In our third study, we monitored molossid activity in an urban site in Recife and
in the non-urban, 562-ha Saltinho Biological Reserve (8°43′57″S, 35°10′25″W),
also in the Atlantic Forest. Between December 2017 and December 2018, we set
full-spectrum bat detectors to record in open areas for 4 h (starting 1 h before sun-
set) on calm nights without rain. We visualised spectrograms in Raven Pro 1.5
(Cornell Lab of Ornithology, USA) and assigned calls to species by comparing
recordings with published literature [26]. We used bat activity as a proxy for relative
abundance, following Miller [42], and analysed activity in 10 min intervals within
each night of sampling. Finally, we compared total molossid activity between both
environments using student t-tests (after verifying that our data met the assumption
of normality).
Of 6,866 bat records obtained over 24 h in each environment, 47.8% were from
molossids. Total bat activity in the forest environment (789.7 ± 235.2 records) was
significantly higher (t  =  3.4102; p  =  0.0270) than in the urban environment
(324.3 ± 22.9 records) on all nights (Fig. 9.4). However, whereas molossids clearly
dominated the urban bat assemblage (68–82% of records per night), they only

Fig. 9.4  Activity of molossid and other insectivorous bats in non-urban (Saltinho Reserve, a
562-hectare forest remnant) and urban (Recife) areas, in the northeastern Atlantic Forest of Brazil.
Data based on 24  h of recordings in each habitat along three simultaneous nights between
December 2017 and December 2018
9  Assessing the Effects of Urbanisation on Bats in Recife Area, Atlantic Forest of Brazil 131

Fig. 9.5  Average activity of molossids in relation to the sunset in non-urban (Saltinho Reserve, a
562-hectare forest remnant) and urban (Recife) areas, in the northeastern Atlantic Forest of Brazil.
The x axis represents 10 min time blocks and 0 marks the sunset. The first dashed vertical lines
mark 25% of the recorded activity, and second dashed vertical lines mark 75% of the recorded
activity. Data based on 24 h of recordings in each habitat along three simultaneous nights between
December 2017 and December 2018

accounted for 37–49% of the total bat activity in the reserve. Furthermore, urban
molossids started about 10 min before sunset and were mainly active in the early
part of the night, with 75% of the total activity in the first 25  min after sunset
(Fig. 9.5). In contrast, molossid activity in the reserve started later and was more
homogeneous, with 75% occurring in the first 90 min after sunset.

5 Discussion and Conclusions

Our three studies offer glimpses of some of the effects of urbanisation on insectivo-
rous bats in a large city within Brazil’s Atlantic Forest region. First, although the
urban landscape is more simplified than natural forest, several bat species (repre-
sented by different sonotypes) persist in the city of Recife. However, our results also
132 E. Bernard et al.

suggest that those bats use this urban landscape heterogeneously. As prior studies
[14] have reported, a combination of ecological and behavioural adaptability and
opportunism determines whether a bat species can exploit the diverse anthropogenic
resources in the urban matrix and ultimately tolerate urbanisation. The concept of
“urban adapters” and “urban avoiders” is appropriate and helps to elucidate which
species do well in and which ones are extirpated from urban areas [14, 18]. In our
first study, we recorded 16 sonotypes belonging to 5 bat families in Recife – pre-
sumably, these are all at least somewhat urban “adapted” or tolerant. Yet, green
spaces matter: they supported twice as many species and nearly 2.4 times more bat
activity compared to paired urbanised sites. In fact, green spaces were bat hotspots,
suggesting that urban green spaces are top priorities for bat conservation (see also
[27, 43, 44]).
Our second study revealed that the intense lighting of sports stadia can influence
bats, but contextually in that bat activity increased when lights were on, but only at
two stadia. Furthermore, stadium lights appear to influence temporal activity pat-
terns in a contextual way, which suggests that impacts of artificial light on bats
reflect complex interactions between multiple variables, including species-specific
responses.
All terrestrial (above-ground) life evolved in environments where natural light
regimes vary daily and seasonally in predictable ways, and nocturnal animals are
particularly responsive to alteration of these regimes [45]. Indeed, light is the most
important environmental factor that regulates the activity of bats [46], and artificial
light can alter interactions between species that use very similar resources in a light-
ing gradient [26]. Thus, bats are expected to be affected by artificial light (e.g. [30,
47–49]), but two key points must be considered. First, impacts depend on light
spectra and intensity. Second, bat responses are species-specific. Some insectivores
may benefit by exploiting swarms of phototactic insects at lights, while others avoid
light. In fact, studies ([30] and others therein) document altered feeding patterns of
several bat species resulting from light pollution and that these changes ultimately
act as a species filter and tend to homogenise urban bat faunas. Although we used
sonotype as a proxy for species, identifying acoustic recordings of urban bats to
species is useful to obtain a better understanding of which ones are positively or
negatively affected by urbanisation. Doing so in Neotropical cities becomes increas-
ingly feasible as the number and quality of published reference call libraries increase
(e.g. [26]).
Unfortunately, urban light pollution is not considered a conservation threat (or
even a pressing problem) in many lower- to middle-income countries. In fact, an
increase in lit areas is frequently seen as necessary and beneficial due to the percep-
tion (justified or not; [50]) that lighting reduces crime and improves traffic safety.
However, with mounting evidence that light pollution affects not only urban flora
and fauna but also human health [29, 31, 45, 51], it is worth reducing and mitigating
urban light pollution. Bats could benefit from actions to do so, especially by adopt-
ing bat-friendly lightning [52].
Our third study indicated that urbanisation influences the activity and behaviour
patterns of molossids. Relative to their counterparts in the native Atlantic Forest,
9  Assessing the Effects of Urbanisation on Bats in Recife Area, Atlantic Forest of Brazil 133

urban bats appeared to exhibit reduced activity that was also concentrated in a
shorter interval near the beginning of the night. The observed early foraging activity
by urban molossids may result from several causes, one of which may reflect
responses to possible changes in prey availability. The lower abundance and diver-
sity of insects in urban areas can intensify competition among bats – to avoid com-
petitors, they may anticipate the beginning of foraging [53]. Previous studies of
insectivorous bats, and especially molossids, have found that for them, optimal for-
aging implies timing their activities to those of their prey and predators [18, 36, 37,
54]. For example, artificial lights, by attracting swarms of phototactic insects, may
in turn attract hungry molossids, which spend less time searching for prey and thus
benefit from reduced energy expenditure and greater hunting efficiency [17, 39, 47].
For molossids, this is possible thanks to their fast flight style, which mitigates the
risk of exposure to and capture by visual predators. In addition, molossids may
benefit from reduced competition with slow-flying bats, which tend to avoid brightly
lit areas where they are vulnerable to predation.
Alternatively, urbanisation could affect the foraging behaviour of molossids,
forcing them to move to less urbanised, peripheral areas later in the night, because
the biomass of moths, which are important in their diet, is reduced in bright environ-
ments [16, 17, 39, 55, 56]. This change in the diversity and abundance of potential
prey in illuminated areas could explain why the activity of urban molossids declines
rapidly after the beginning of the night. Both hypotheses should be tested.
Despite their shortcomings (e.g. small sample size, short duration, focus on sin-
gle variables), our three studies offer useful baselines and examples of issues to
address when investigating interactions between Neotropical bats and urban envi-
ronments. Such investigations are worthwhile not only to determine the drivers of
bats’ responses but also to identify strategies to mitigate the negative impacts of
urbanisation on insectivorous bats, whose ecological roles are vital to ecosystem
integrity and the maintenance of biodiversity.

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 Part III
How do Bats and Humans Interact
in Urban Environments? Human
Perceptions, Public Health, and Ecosystem
Services of Bats
Chapter 10
Human Dimensions of Bats in the City

Leonardo Ancillotto, Joanna L. Coleman, Anna Maria Gibellini,

and Danilo Russo

Abstract  Cities are characterised by low amounts of natural habitat, so their human
populations, i.e. urbanites, are expected to be poorly connected to and knowledge-
able about the natural world, despite high biodiversity levels being increasingly
recorded in unconventional, urban habitats. Such disconnection may raise potential
conservation issues for wildlife living in urban areas. Bats are common in cities
around the world and so too, therefore, are interactions between bats and urbanites.
Yet, the elusive habits and peculiar adaptations of bats make these mammals poorly
known and even feared, often as a consequence of long-standing, negative cultural
framing. Here, we review the available literature on the human dimensions of urban
bats. We first present a potential theoretical framework for understanding the drivers
of human-bat relationships and how it applies to the available literature on urban
bats. Next, we present an array of potential real-life contexts in which human-bat
interactions may occur in urban areas worldwide. Such interactions vary in their
nature and context and include visits to zoos, rescue, volunteering, occasional
encounters, and the installation of bat boxes. Finally, we present a focal case study
investigating attitudes towards and knowledge of bats from a tropical city.

Keywords  Attitudes · Bat boxes · Cognitive hierarchy theory · Human-wildlife

conflict · Urbanites

L. Ancillotto (*) · D. Russo

Wildlife Research Unit, Dipartimento di Agraria, Università degli Studi di Napoli Federico II,
Naples, Italy
e-mail: [email protected]
J. L. Coleman
Department of Biology, Queens College at the City University of New York,
Flushing, NY, USA
A. M. Gibellini
Centro Recupero Animali Selvatici WWF di Valpredina, Bergamo, Italy

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 139
L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_10
140 L. Ancillotto et al.

1 Introduction

In this so-called urban century, natural habitats are increasingly replaced by urban
land uses, and the proportion of the human population residing in cities is growing.
The most urbanised areas usually only host remnants of natural habitats and highly
modified wildlife communities in comparison to natural areas [1]. Consequently,
the maintenance and management of urban biodiversity are widely accepted as fun-
damental tasks for land managers, particularly in Western Europe and North
America, with “green” strategies often implemented to conserve urban biodiversity
and manage interactions between urbanites and wildlife (e.g. [2]).
These interactions are diverse in how they are perceived by humans. Some are
arguably unequivocally positive, such as when an attic houses a colony of endan-
gered bats, which otherwise lack suitable roost habitat, and the homeowners are
happy about it and enjoy watching the bats emerge at dusk but otherwise leave them
alone. Some are benign, as when a pedestrian stops momentarily to watch a bat
hunting insects at a streetlamp. Some interactions are unequivocally negative: an
urbanite has an aggressive encounter with a bat and kills it. But often, deeming an
interaction as positive or negative depends on perspective. For example, a group of
people crowds around a roosting bat, enjoying taking photos (positive) while dis-
turbing the bat (negative). Thus, these interactions (and perceptions thereof) are
complex.
These interactions also have potentially significant implications for urban con-
servation because conservation threats to bats (like other wildlife) mostly result
from human behaviours [3, 4], and willingness to conserve (like other pro-­
environmental behaviours) is shaped by our experiences in nature ([5, 6] and others
therein). However, due to the relative scarcity of natural habitats in cities, urbanites
may be less connected to nature than those living in more rural or natural contexts
([5], but see [6, 7]). Consequently, the human-wildlife relationship in cities may be
weak and not based on direct experience, despite the active engagement of people
with urban green spaces, especially for recreational activities and wellbeing.
Bats are elusive mammals, rarely encountered by people generally, except perhaps
when conflicts arise (e.g. when bats occupy spaces in buildings and are thus noticed
by people inhabiting the building) [8] or when a grounded bat is found. Nevertheless,
bats are the most speciose order of mammals in many urban areas, where they often
have large populations [9]. Because bats are ubiquitous in cities, it is fairly common
for urbanites to encounter bats – this makes management of human-bat interactions
a fundamental challenge of bat conservation. Also, recent media representations of
bats as reservoirs of dangerous viral diseases [10] have increased the importance of
understanding human behaviours (and drivers thereof) towards bats.
Studying these interactions and behaviours is an endeavour for human dimension
research. Here, we provide a review of what is known about human dimension
research as it relates to bats and urbanites (including their knowledge, behaviours,
and attitudes towards bats), outlining trends and gaps in this field. We first present a
potential theoretical framework for understanding the drivers of human-bat
10  Human Dimensions of Bats in the City 141

relationships and how this applies to the available literature on the topic of urban
bats. Next, we present an array of potential real-life contexts in which human-bat
interactions may actually occur in urban areas worldwide, with a focal case study
from a tropical city.

2 A Brief Theoretical Framework

The discipline of human dimension research, which falls under the umbrella of
conservation social science, integrates various social sciences (e.g. sociology,
psychology) to understand stakeholders, including urbanites, in wildlife issues [11].
As such, it employs key social-science conceptual frameworks to study human
behaviours (actions performed towards a target object) and their drivers. As an illus-
trative example, let us consider a homeowner who has a colony of bats in their attic
and wishes to get rid of them.
One model, Cognitive Hierarchy Theory, aims to disentangle the cognitive
mechanisms that ultimately produce a given human behaviour [12]. In this example,
it might be hiring an exterminator. Knowledge and behaviours have a hierarchical
structure, i.e. forming a so-called inverted pyramid (Fig. 10.1) [13]. At the base are
general values and norms, which are stable and usually resist modification (e.g. via
education). These underpin values and norms that are much more contextual and
ultimately give rise to the great variety of potential behaviours, which, in contrast to
the base of the pyramid, may be rapidly changed through experience. Norms and
attitudes represent evaluations of target objects and judgements about them in spe-
cific contexts. For example, if “bats” is the object, then a person’s evaluation of bats
should summarise their general attitude towards bats, while changing the object into

Fig. 10.1  The Cognitive Hierarchy model of human behaviour, with examples of potential evalu-
ations of bats in real-life contexts. (Adapted from Vaske and Donnelly [13])
142 L. Ancillotto et al.

“bats in your own house” significantly narrows the context and thus will elicit a
more circumstance-specific evaluation [14].
Two of the most applied frameworks to pro-environmental behaviours, the theo-
ries of Reasoned Action and Planned Behaviour, recognise a person’s intent to per-
form a behaviour (calling an exterminator) as the proximate predictor of whether
they ultimately do so ([15] and others therein). This intention has two direct ante-
cedents: first, the person’s attitudes about the behaviour (perceived likelihood that
hiring an exterminator will effectively get rid of the bats) and, second, their subjec-
tive norms about it (belief as to whether certain important others, such as relatives,
neighbours, etc., would (1) approve of them hiring an exterminator and (2) hire an
exterminator themselves). The Theory of Planned Behaviour further recognises the
role of behavioural control – their actual or perceived ability to perform the behav-
iour (e.g. availability of time and money to hire an exterminator) in modulating the
influences of attitudes and norms ([15] and others therein).
Alternate models may distinguish between the cognitive (knowledge and percep-
tions), normative (involving norms), and affective (emotional) aspects of behaviour
(e.g. [16]). Emotions are classifiable by various schemes, including dichotomised
between positive (e.g. happiness, surprise) and negative (e.g. sadness, fear; [17] and
others therein). Finally, most frameworks acknowledge the importance of other
intrinsic behavioural antecedents (e.g. demographics, ethnicity, education, income,
personality), though often only as indirectly influential ([15] and others therein).

3 Disentangling Values, Attitudes, and Behaviours

Historically, bat-related human-dimension research, both generally and in urban

areas, is relatively scant [18]. Yet, some studies lay the foundations for our under-
standing of how human behaviours are affected by attitudes and how these may
change in different socio-economic contexts that also include urbanites.
A seminal study by Kellert [19] attempted to highlight drivers of negative atti-
tudes towards animals generally, and specifically invertebrates which, like bats, tend
to be unpopular [20]. The authors developed and used a questionnaire to identify the
cognitive bases for negative behaviours and postulated that the public may perceive
these “unloved” animals with fear, antipathy, and aversion, as a result of a gener-
alised fear of the unfamiliar. Where bats are concerned, people may avoid them,
selectively focusing on the fact that they may be reservoirs of diseases, especially
when the media represents them as such [21]. People may dislike bats because (i)
they are morphologically and behaviourally different from people and other species
[21], (ii) many species display erratic flight patterns, and (iii) some species “invade”
human spaces unexpectedly. They may also dislike bats because they are considered
to be negative omens in some folklore, although perhaps mainly in countries where
Western cultures predominate, in contrast to many Asia-Pacific cultures which fea-
ture positive associations with bats [22]. Nevertheless, local belief systems do not
always align with actual practices, i.e. positive cultural framing of bats may also be
10  Human Dimensions of Bats in the City 143

associated with practices detrimental to bat populations (e.g. unsustainable harvest-

ing; [22]). Following Kellert [23], several authors adopted a Bat Attitude
Questionnaire (BAQ) to explore the dimensions of attitudes towards bats [24], dis-
entangling the different roles of myths and knowledge, as well as those of ecologis-
tic, scientistic, and negativistic typologies of human attitudes (see also [25]).
Namely, Boso et al. [24] found that gender, educational level, and religiosity are
significant drivers of attitude polarisation towards bats. Yet, only a few of these stud-
ies actually focused on urbanites or included cities.
A government report from Fort Collins, Colorado [26], directly tackled bat-­
related attitudes, awareness, and knowledge using a questionnaire administered in
2004. The fact that most respondents, who self-reported living in urban and subur-
ban areas, were also aware of bats’ presence and had observed bats regularly (e.g.
in their neighbourhoods) supports the statement that despite having lost significant
fractions of their original faunas, cities may still offer residents the chance to
encounter bats. However, despite being relatively familiar with bats (i.e. given their
direct observations), these respondents were not knowledgeable about bats. For
example, people were not well-acquainted with ecosystem services provided by
bats and were likely to report false information on disease transmission risk. Still,
they tended to hold neutral-to-positive attitudes, with most recognising bats as being
important to ecosystem integrity and, as such, deserving of protection. Yet, urban-
ites reported diverging attitudes towards bats inhabiting their neighbourhoods (posi-
tive) or their yards/households (negative; [25]), once again illustrating the
contextuality of attitudes.
Early education within families and in schools also plays a major role in modify-
ing bat-related  behaviours, and even attitudes. For example, Slovakian primary
school children from urban contexts who knew more about bats held more positive
attitudes towards them, while false beliefs arising from myth and folklore were
associated with negative attitudes [27]. However, a general dislike of bats is not a
strictly urban phenomenon. For instance, when Swiss students were shown images
of wild animals, including the greater mouse-eared bat, Myotis myotis, they strongly
preferred other species over bats, regardless of whether their schools were rural or
urban [28].

4 Encounters Between Bats and Urbanites: A Change

of Attitude?

A more general biophilia (referring to the human urge to affiliate with nature, sensu
[29]) and associated positive feelings towards bats may be driving shifts in attitudes
towards and beliefs about bats. Urbanites’ low familiarity with nature in general,
and bats in particular, makes bats potentially appealing in terms of curiosity and
charisma, especially if human-bat interactions are mediated by experts (or physical
barriers) and are thus perceived as safer. Signs of a shift in attitudes may include the
144 L. Ancillotto et al.

spread of activities such as bat-related tourism in cities, including zoo exhibits and
roost-emergence viewing, bat rescue efforts, and the installation of artificial roosts
(e.g. bat boxes) as activities that bring people closer to bats.
Zoos are important constituents of traditional “green spaces” in many large cities
and, as such, may enhance urbanites’ experiences with – and awareness of – wild-
life. Bats had long been mostly neglected as zoo animals, except for common vam-
pire bats (Desmodus rotundus) and some flying foxes (Pteropus spp.), kept in
several collections around the world as objects of curiosity, or ghost bats
(Macroderma gigas), kept in several Australian zoos. Recently, zoos have added
more bats to their collections and thus increased public attention to these mammals.
As early as 1996, Bat Conservation International reported that 1.6 million people
visited the “Lied Jungle” bat exhibit at the Henry Doorly Zoo, in central Omaha,
Nebraska, USA, within one year of its opening. Similarly, in Europe, the Bat Cave
at Hellabrunn Zoo in Munich, hosting Seba’s short-tailed bats (Carollia perspicil-
lata), opened in 1992. The advent of third-generation walk-through exhibits includ-
ing bats has also improved the ability of zoos to raise awareness of wildlife (and bat)
conservation and promote more positive perceptions of bats [30]. Zoos may also be
excellent experimental settings to assess urbanites’ feelings about bats, provided
that husbandry practices ensure the welfare of individual bats in exhibits. For
instance, children visiting a bat exhibit at the Brookfield Zoo, in Chicago, Illinois,
USA, showed conflicting emotions towards fruit bats, i.e. fear and concern for their
wellbeing [31].
The phenomenon of bats emerging from large colonies at dusk is also increas-
ingly attracting public attention to urban bats. For example, among 17 large roosts
used by Mexican free-tailed bats (Tadarida brasiliensis) in the Southwestern USA,
two urban ones in Texas draw more than 65% of the 242,000 annual visitors to these
roosts [32].
Another frequent type of human-bat interaction in cities occurs when people find
grounded bats, usually injured adults or dependent juveniles that have fallen from
their roosts [33]. In such cases, individual attitudes towards bats are the main pre-
dictor of the outcome, i.e. whether people rescue, ignore, or kill the bat. Despite
generally negative attitudes towards bats being reported in the few studies that have
assessed urbanites, positive behaviours such as rescuing bats in trouble seem rela-
tively common in some cities. Yet, in other urban contexts, negative behaviours may
also be strongly rooted as common habits. For example, the most frequent behav-
iours exhibited by people finding bats in their homes in Brazil were hunting and
removal [34]. As such, wildlife rescue is a quantitatively relevant aspect of the bat-­
human interface (zone of interaction) in cities, suggesting that urbanites may engage
in positive interactions such as rescue regardless of their general attitude. For exam-
ple, each year, the Wildlife Rescue Centre of Rome, Italy, admits more than 300 bats
per year, 95% of which come from Rome’s city centre, leading to 3,548 human-bat
encounters in the last 10 years (pers. obs.), and such rates are comparable with those
in other locales [35, 36]. Such high rates of encounters suggest the important role of
wildlife rescue initiatives in bat conservation, particularly in urban areas.
10  Human Dimensions of Bats in the City 145

Wildlife rescue activities involve two main types of human-bat interactions: (1)
members of the public finding a bat in distress and (2) staff and volunteers advising
people and caring for bats. These interactions differ in the underlying perceptions
and motivations of the people involved and in their potential contributions to con-
servation. In the first case, urbanites are motivated to rescue a bat (or have it rescued
by professionals or volunteers), which presumably indicates a certain degree of gen-
eral biophilia [30], and are usually keen to be advised on how to properly rescue the
bat. Yet, people finding a bat in need of help generally lack knowledge of bats’ basic
biology and needs. For example, they frequently report having provided potentially
harmful foods (e.g. honey, fruit, sugar to insectivores) to a bat before bringing it to
a rescue centre, possibly a result of having viewed viral videos of flying foxes in
Australian rescue centres. More rarely, they wrongly identify a bat as something
else (e.g. bird, mouse or even frog, pers. obs.), a possible sign of disconnection from
nature [37].
Rescue centres play an important role in addressing the poor knowledge and
opinions that urbanites often have of bats. By bringing a bat in need of help to a
centre, people may boost the chances that the bat survives [33] all while being
offered proper support and information about bats that may further raise their appre-
ciation for bats and promote their conservation. For example, the Valpredina Wildlife
Rescue Centre, which is run by the WWF and admits >130 bats annually, represents
an exemplary Italian case of management of the human-bat interface. The centre
hosts a front office (“Sportello pipistrelli” – Life+ Project IPE 018 Gestire 2020)
which, besides providing 24/7 support to people who find bats in trouble, promotes
public involvement in conserving urban bat colonies. For example, staff members
encourage those who rescue bat pups to search for the roost on their property and
become “colony guardians”. When urbanites enrol in the program, they are men-
tored by bat experts, who regularly provide information about bats in general and
how to monitor “their” colonies, i.e. promoting a citizen-based monitoring approach
and conscious cohabitation with bats. Empowering urbanites to protect bat colonies
fosters an emotional bond between people and bats all while representing a durable
way to protect urban roosts.
As for the motivations and attitudes of bat carers and volunteers, they remain
poorly known. The only study to date [35] profiled carers of Australian flying foxes
from a socio-demographic point of view, but only marginally explored their knowl-
edge base and did not strictly focus on urbanites. This study reported that most bat
carers were women between the ages of 30 and 50 years old, but detected no par-
ticular pattern with regard to previous knowledge and motivation to volunteer for
bats. Moreover, volunteers appeared to be motivated by general altruism rather than
by the drive to conserve bats.
Urbanites may also seek out contact with bats on their properties, in addition to
casual encounters or volunteering. In recent years, bat boxes have gained popularity
in urban green spaces. Urbanites set up bat boxes because they anticipate that doing
so will suppress mosquitoes near their homes and/or to provide habitat for bats,
partly thanks to large campaigns that have improved bats’ “image” and increased
urbanites’ connection to bats (pers. obs.). For instance, the Natural History Museum
146 L. Ancillotto et al.

of Florence launched a successful campaign (“Un Pipistrello per Amico”, i.e. “Be a
Bat’s Friend) in 2006 [38]. Its goal was to disseminate accurate information about
the ecological value of bats and foster direct public engagement in bat-conservation
activities. The project involved active cooperation with one of Italy’s main super-
market chains, which sold more than 25,000 inexpensive bat boxes along with a
range of bat-related gadgets. Citizens, schools, institutions, and associations
installed bat boxes and monitored them using a standard data collection form. Bats
colonised 40% of bat boxes, but the operation’s biggest achievement was a general
improvement in bat-related attitudes across Italy, e.g. with bat boxes becoming
objects that were in high demand and commonly sold. Bat box campaigns, like
other citizen science and conservation activities, offer an outstanding but still unde-
rutilised potential to improve bats’ public image and counter negative portrayals
fostered by myths and misinformation. This example also highlights how important
it is for experienced staff to provide supervision throughout projects involving the
design and use of bat boxes, as these may easily become ecological traps if not
properly designed or positioned [39].

Case Study: What Singaporeans Know and Feel About Bats

Here, we provide an example of an investigation into the attitudes and their
antecedents towards bats by urbanites in a densely populated tropical city.
This study, motivated by an interest in bats and belief that conservation must
ultimately change human behaviours (see also [3]), sought to understand pre-
dictors of behaviours towards bats in the understudied context of a large tropi-
cal city, specifically focusing on knowledge and attitudes as antecedents (see
also [40]).
The context was Singapore, a densely populated city-state whose popula-
tion (5.64 million in 2018) is fully urbanised. By the turn of the millennium,
many of Singapore’s original bat species had become locally extinct [41],
with most of the remaining species being locally threatened. Even though
Singapore’s bats need protection to avoid further declines and extinctions,
removing bats (except for flying foxes, which are casual vagrants) is not ille-
gal if one can prove they are damaging property. Based on this policy and lack
of legal protection for resident species, one might infer that bats have no place
in the city [42].
This mixed method study started with two focus group discussions (five
participants each), whose outcomes were used to craft a quantitative survey of
106 Singapore residents, whose demographics were representative of the
city’s general population. Finally, individuals who expressed fear of bats were
interviewed.
When asked what they know about bats, focus group discussion partici-
pants mainly said that bats eat fruit, are nocturnal, and hang upside down.
However, nearly one third of survey respondents described their knowledge as
“low”, even though 79% had encountered live bats (albeit rarely in most

(continued)
10  Human Dimensions of Bats in the City 147

cases). In response to the statement that bats benefit humans, 23.6% agreed –
pollination (32%) and pest control (32%) were the most cited benefits. Fewer
(20.8%) agreed that bats cause problems – 68% of them mentioned health or
disease issues. Finally, the mean score on a knowledge quiz was 7.17/12 – the
most challenging question was the “bats are blind” myth, which 29.2% of
respondents believed.
Three components of attitude were assessed. The first one was affect, and
most of the focus discussion group participants expressed neutral attitudes, no
opinion, or unclear emotions. Roughly equal numbers of survey respondents
said they like (33.3%), dislike (31.1%), and neither like nor dislike (26.4%)
bats – 34.9% said they find bats scary, even in images or videos. Most (62.2%)
said they would not willingly live near bats, and 34.9% cared about their sur-
vival. As for the second, cognitive, component, while 66% of respondents
agreed that bats are part of the environment, most disagreed with statements
that they are attractive (54.7%) or charismatic (57.8%). Still, fewer than half
agreed with any negative characterisations of bats (as unpredictable, disgust-
ing, dangerous, or nuisances). Finally, social attitudes appeared to reflect
societal expectations. In focus group discussions, participants varied in their
level of support for protecting bats, but few were opposed to doing so. Most
survey respondents agreed that bats have the right to exist (76.4%), are an
important part of nature (74.5%), and should be conserved (68.9%), though
only 39.6% said governments should fund this.
Religious or ethnic beliefs about bats were rare (8.5% of survey respon-
dents). Three participants expressed the view of bats as auspicious  – most
Singaporeans are ethnically Chinese, and the Chinese character for bat (fú 蝠)
is a homonym for luck (fú 福). Three viewed bats as God’s creations, two said
all creatures have intrinsic worth, and one said eating bats is haram (forbidden
under Islam).
As to intrinsic predictors of cognitive attitudes, two predicted more posi-
tive ones. One was pet ownership, as in other studies (e.g. [7]), though why is
unclear. Do people keep pets because they are animal lovers, or does owning
pets promote love of animals? The other was positive prior experience (Wald’s
Χ2 = 10.1) – again, the link is unclear. Animal lovers might be more observant
and so report more bat interactions or may be more likely to describe interac-
tions as positive.
The expectation that gender is predictive (based on findings that negative
attitudes towards bats may be more common among females, e.g. [43]) was
not supported by the data, leading to the hypothesis that sex-biased differ-
ences are minimised in a fully urbanised population that sees bats only rarely.
Nor did knowledge of bats predict positive attitudes as it had in other studies
(e.g. [43]). Perhaps low knowledge, as in Singapore, leads to weaker, less
consistent, rather than negative, attitudes (see also [44]).

(continued)
148 L. Ancillotto et al.

In Singapore’s densely built-up city, where bat sightings are rare, most
residents may be effectively “blind to bats” [45]. This may be problematic for
conservation. Upon encountering a familiar object, we retrieve the relevant
affect and beliefs from memory to express an attitude towards it, but for a new
object, we may rely on emotions [46], thus forming attitudes that resist cogni-
tive persuasion [47]. Take, for instance, one interviewee whose fear of bats
started after a bat flew near them. Teaching this person that bats are non-
aggressive and are key to ecosystems could be futile or even backfire, due to
cognitive dissonance [48], and with the negative affect formed first, they
would probably disregard new information [47]. Using affect might change
their mind, though one hurdle remains: we avoid thinking about things we
fear [49]. Conversely, once a positive affect is formed, cognitive persuasion
can reinforce it. Therefore, we suggest that outreach efforts not only present
bats in a way that targets emotions but also (given the prevailing attitude that
bats are not attractive) use aesthetically appealing portrayals rather than live
bats (see also [3]).
Naturally, outreach can usefully present cognitive information on how bats
benefit humans [4], but this approach may not always be contextually appro-
priate. For example, in Singapore’s highly urbanised society, with no major
agricultural sector, ecosystem services by bats do not yield economic benefits
that most locals appreciate. Singapore hosts a diverse bat assemblage, which
may potentially provide several services such as suppression of insect pests
and pollination/seed dispersal of plants consumed by locals, yet such services
are not yet quantified and unlikely to have high economic relevance. Indeed,
when focus group discussion participants asked why bats should be protected
and were told that bats pollinate durians (which are prized fruits in Singapore),
this piqued their interest. Yet one countered, “Singapore does not produce
durians”, implying the fact’s potential irrelevance locally. Still, if most respon-
dents support conserving bats for other reasons and agree that bats are part of
nature, perhaps outreach may be more effective by enhancing nature appre-
ciation generally, rather than focusing on bats per se.

5 New Challenges

As evidenced by the reported examples, the human dimensions of bats in cities is a

research topic with much to be learned. In most cases, knowledge of human behav-
iours towards bats (and their drivers) is anecdotal or based on single case studies at
best. The contribution of social sciences to bat conservation is now widely recog-
nised [50]. What is lacking is the identification and promotion of best practices and
approaches to foster positive behaviours by urbanites towards bats, which, again,
are needed to conserve them [4]. Negative perceptions of bats by urbanites may be
10  Human Dimensions of Bats in the City 149

Fig. 10.2  Rescued bats,

such as this European
free-tailed bat (Tadarida
teniotis) from Italy, offer
great opportunities to take
catchy pictures that
showcase the cute or even
charismatic aspects of bats,
exploiting aesthetics in
shaping people’s attitudes
towards bats. (Photo by
Anna Maria Gibellini)

generally ameliorated by outreach activities that raise their knowledge of bats and
by the efforts of Bat Conservation International (especially those with the capacity
to directly involve people). Initiatives such as the International Year of the Bat and
the International Bat Night (https://eurobats.org/international_bat_night) spread a
globally unified message and allow local bodies and organisations (universities,
agencies, associations, conservationists) to inform and involve urbanites under an
international and authoritative framework. Such efforts may also represent a posi-
tive feedback mechanism to bat monitoring and conservation, as also suggested by
the recent rise of volunteer-based monitoring schemes [51]. Experimental evidence
strongly suggests an important role of aesthetics and direct experience, in addition
to scientific information, in shaping people’s attitudes towards bats [24], increasing
the educational role of zoo collections and rescue centres (Fig. 10.2) as fundamental
opportunities for urbanites to directly experience bats. Moreover, outreach actions,
such as the applications of informative, aesthetically appealing panels at urban bat
roosts, may facilitate acceptance of bats in buildings by urbanites, decreasing the
risk of conflict and/or consequent damage to urban bats, as already evidenced in
other contexts and taxa [52].
The role of bat conservationists has become even more important recently, given
the need for outreach to mitigate the increase in negative attitudes and persecution
stemming from media portrayals of bats in relation to the COVID-19 pandemic [50,
53]. With many bats, including species that occur in cities, being threatened, it is
vital to provide efficient tools and consistent strategies to promote peaceful coexis-
tence between bats and humans and public support for bat conservation.
150 L. Ancillotto et al.

Bat-related human dimension research is young and emerging, lacking system-

atic efforts to unify approaches and depict global trends until recently (e.g. [50], but
see [54]). This situation presents many research opportunities to both social scien-
tists and conservationists. One such opportunity is to address the relative lack of
studies focusing specifically on the urban context – a worthwhile endeavour in the
urban century, when more than half of all people already live in cities, which will
house over two thirds of humanity by 2050. Fostering positive bat-related attitudes
and norms among urbanites, e.g. by addressing the underlying cognitive and emo-
tional drivers, may usefully help reduce persecution and other behaviours that may
be detrimental to bat conservation.
We encourage human dimensions researchers delving into this area to engage in
rigorous studies grounded in social sciences. Most fundamentally, studies should
involve social scientists meaningfully and from the outset – thereby increasing the
likelihood that appropriate conceptual frameworks and methodologies are applied
and best social science practices are followed (see also [18]).

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Chapter 11
Urban Bats, Public Health,
and Human-­Wildlife Conflict

Christina M. Davy, Arinjay Banerjee, Carmi Korine, Cylita Guy,

and Samira Mubareka

Abstract  Coexistence of humans and bats in cities requires mitigation of two key
sources of human-bat conflict: risk of zoonotic disease transmission and human
concerns about cleanliness. Bats can transmit infectious diseases to humans, and
mitigating this risk is an important challenge for both public health and bat conser-
vation. Bat colonies in buildings (or adjacent to buildings) are often categorised as
“nuisance wildlife” even when disease risk is low. These colonies can be noisy and
create guano deposits that can be substantial and unsightly. Colonies of fruit bats
may also feed on fruit grown for human consumption. In this chapter, we review
perceived public health concerns around human-bat cohabitation and the factors
that can increase or reduce the risk of disease transmission from urban bats to
humans. We briefly review the importance of human dimensions in assessing the
risk of zoonotic spillover and other bat-human conflict. We use two case studies
(Boxes 11.1 and 11.2) to illustrate the implications of urban bats for human-wildlife
conflict and public health: one on guano deposition by Egyptian fruit bats (Rousettus
aegyptiacus) and the other on the risk of rabies exposure for humans cohabiting

C. M. Davy (*)
Department of Biology, Carleton University, Ottawa, ON, Canada
e-mail: [email protected]
A. Banerjee
Vaccine and Infectious Disease Organization, Department of Veterinary Microbiology,
University of Saskatchewan, Saskatoon, SK, Canada
Department of Biology, University of Waterloo, Waterloo, ON, Canada
C. Korine
Mitrani Department of Desert Ecology, Ben-Gurion University of the Negev,
Midreshet Ben-Gurion, Israel
C. Guy
Toronto, ON, Canada
S. Mubareka
Sunnybrook Research Institute and Department of Laboratory Medicine and Pathobiology,
University of Toronto, Toronto, ON, Canada

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 153
L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_11
154 C. M. Davy et al.

with big brown bats (Eptesicus fuscus). Finally, we briefly consider key priorities
for studies of bat-­borne disease transmission in cities.

Keywords  Zoonoses · Spillover · Wildlife disease · Synanthropy · Bat-­

borne viruses

1 Urban Bats and Zoonotic Diseases

Spillover of known and novel zoonotic diseases poses a major threat to global pub-
lic health and world economies [1]. The risk of spillover is highest in regions with
high mammalian diversity (typically tropical forest biomes) where land use and
land cover changes drive the loss of wildlife habitat [2, 3]. In these regions, diverse
wildlife species are also traded in live animal markets, where many species of live-
stock and/or wildlife may be brought from different jurisdictions and are often co-­
housed under stressful and crowded conditions [4]. Finally, urbanisation, the most
dramatic form of land cover change, has been associated with increased spillover [5,
6]. Urbanisation increases contact between humans and wildlife because synan-
thropic species (wildlife that benefit from living near humans) typically rely on
anthropogenic habitats (including buildings). Thus, urban expansion and intensifi-
cation are explicitly associated with increased spillover risk from synanthropes,
which include many species of bat [5, 6].
The number and severity of recent spillover events involving bats (e.g. severe
acute respiratory syndrome coronavirus (SARS-CoV), Middle East respiratory syn-
drome coronavirus (MERS-CoV), Marburg virus (MARV), and Hendra virus (HeV)
[3, 7]) illustrate the public health relevance of bat-borne pathogens. Horseshoe bats
(Rhinolophus spp.) are reservoir hosts of close relatives of SARS-CoV-2 (the caus-
ative agent of COVID-19): SARS-CoV-2-related viruses have been identified in
samples collected from wild R. pusillus, R. stheno, R. affinis, and R. malayanus [8].
Despite a flurry of research activity, the precise evolutionary and intermediate hosts
of SARS-CoV-2 and mechanisms of spillover to humans remain enigmatic at the
time of writing [8, 9].
Bats’ physiological and immune adaptations often allow them to tolerate chronic,
persistent viral infections [3, 10], although pathogen diversity varies interspecifi-
cally and geographically. Natural and experimental infections of bats with viruses
rarely cause clinical signs of disease, even when co-infected with multiple viruses
that are pathogenic to humans or livestock [11, 12]. The bats’ adaptations make
them reservoir hosts for a multitude of viruses that may cause illness if they spill
over to other mammals [13]. Pathogen diversity tends to be higher in bat species that
live longer and form larger colonies and may be higher in species with broad geo-
graphic distributions in the Eastern Hemisphere [14]. However, rigorous compari-
sons are limited by geographically uneven pathogen surveillance to date, and
bat-borne pathogens (and hence spillover risk) also occur in regions with low bat
diversity [e.g. 15].
11  Urban Bats, Public Health, and Human-Wildlife Conflict 155

Disease caused by emerging bat-borne viruses, such as the coronaviruses that

cause SARS, MERS, and COVID-19, is driven by dysregulation of the host immune
response, including dampened antiviral and exaggerated pro-inflammatory
responses [3]. Studies of selected bat species reveal adaptations to control both
virus-mediated modulation of the bats’ antiviral defensive responses and the inflam-
matory responses typically mounted following viral infections [3]. Indeed, under-
standing the adaptations that allow bats to tolerate viruses that cause severe disease
in other mammals may lead to the discovery of new therapeutic targets in other
mammals, including humans and livestock.
Despite their remarkable immune responses, urban bats can still transmit patho-
gens, and understanding the urban ecology of viral spillover can help predict and
mitigate disease transmission to people, livestock, and other urban wildlife. Urban
bats may face increased physiological stress or pathogen exposures compared to
their non-urban counterparts, and both factors may increase spillover risk. For
example, little red flying foxes (Pteropus scapulatus) that are nutritionally or repro-
ductively stressed have higher levels of Hendra virus replication [16]. Similarly,
little brown bats (Myotis lucifugus) co-infected with Myotis lucifugus coronavirus
(MyL-CoV) and the fungus Pseudogymnoascus destructans, which causes white-­
nose syndrome in hibernating bats, shed greater coronavirus loads than singly
infected bats [17]. It remains unclear how well such studies can be generalised
among urban and non-urban contexts, and future research should directly test
anthropogenic stressors that may affect viral replication in bats, facilitating increased
virus shedding and thus spillover into other mammals.

2 Health Risks of Bat-Human Cohabitation: To Humans

and to Bats

In urban settings, as elsewhere, several factors determine interspecific pathogen

transmission. These factors fall broadly into two categories: (1) drivers of exposure
to an infectious pathogen, which is an essential first step for infection, and (2) bio-
logical determinants of infection. Here, we use different scenarios to highlight how
exposure and host-pathogen biology contribute to spillovers and pose risks to human
and wildlife health, with an emphasis on conditions common in cities. These sce-
narios focus on viruses because bat-human transmission of bacterial and fungal
pathogens remains poorly understood [18]. Nevertheless, the principles we discuss
apply to all zoonoses.
Exposure is determined largely by the human-animal interface. This interface
may be narrow and sustained, with intense exposure to one reservoir or intermediate
host (e.g. certain agricultural settings where camel producers are exposed to MERS
[19]). The interface may also be broader and more intermittent (e.g. incursions into
forests due to socio-economic necessity or geopolitical conflict resulting in human
exposures to Ebola virus). Some exposures are easy to identify; others are difficult
156 C. M. Davy et al.

to detect but can be assessed retrospectively. For example, occupational exposures

to filoviruses increase the risk of seropositivity. The adjusted odds ratio for sero-
positivity can be as high as 3.4 for miners who share their workspace with bats in
areas where Marburg is endemic, compared to community controls [20]. In this
example, close, sustained, and frequent contact with reservoir species in a poorly
ventilated space likely contributes to high rates of exposure, seropositivity, and out-
breaks. Other forms of exposure are more complex and multifactorial, as demon-
strated for Nipah and Hendra viruses. Reduced connectivity among urban bat
populations may reduce viral transmission, apparently decreasing exposure risk,
while also generating populations of susceptible bats that ultimately drive more
intense outbreaks when a virus is reintroduced locally [21].
Habitat loss associated with urbanisation also brings high densities of suscepti-
ble humans into direct contact with wild animals that have nowhere else to go.
Planting of mango orchards in recently deforested areas placed bats (island flying
foxes, Pteropus hypomelanus), pigs, humans, and Nipah virus in close proximity,
leading to spillover events [22]. Although this example is from a rural area of
Malaysia, similar processes during urbanisation could increase exposure risk for
urbanites.
Where exposures occur, spillover risk varies with biological determinants such
as host susceptibility (whether the host can become infected by the pathogen) and
host competence (whether the infected host can transmit the pathogen to another
susceptible host). For example, feline coronaviruses (FCoV), which are ubiquitous
pathogens of domestic cats (Felis catus), do not spill over into humans despite con-
stant, widespread exposure. It appears there are biological barriers to spillover,
probably because humans do not have homologous cell attachment and entry deter-
minants to which both FCoV biotypes can attach [23]. Similar biological transmis-
sion bottlenecks seem to prevent human infection by bat-borne coronaviruses
(alphacoronaviruses and betacoronaviruses) [24]. However, growing human impacts
on bat habitat by urban and agricultural development expand the interface between
humans, livestock, and bats [2], increasing the probability of exposure to a corona-
virus strain that can attach to and enter human cells. Such exposures can lead to
spillover, and if humans are competent hosts for the particular virus, cities provide
ideal conditions for sustained person-to-person transmission.
In cities, probabilities of both exposure and spillover increase because of high
human populations and the increased likelihood that people will encounter synan-
thropic species that can transmit pathogens to them. Integration of epidemiological
and biological data into risk assessment tools can also be adapted to support urban
surveillance of bat disease. Recent, relevant initiatives include genome-based zoo-
notic risk assessment [25] and the web tool SpillOver [26], which integrates avail-
able scientific evidence with expert opinion to predict risk. Host surveillance can
also be prioritised based on validated models. For example, ecological trait-based
models recently revealed 47 previously unrecognised bat hosts of betacoronavi-
ruses [27].
When bats and humans share buildings, they also share potential health risks.
Given the new, global distribution of SARS-CoV-2, COVID-19 hotspots also
11  Urban Bats, Public Health, and Human-Wildlife Conflict 157

represent areas of greater potential risk of spillback (anthropozoonosis or reverse

zoonosis) to synanthropic bats that roost in buildings and therefore share air with
humans in enclosed spaces. The SARS-CoV-2 virus has spilled back from humans
into other mammals, including farmed European mink (Mustela vison) and
American mink (Neovison vison), domestic cats, and some livestock and zoo ani-
mals [3]. At the time of writing, a range of wild species are confirmed as competent
hosts for ancestral SARS-CoV-2 [e.g. 28–32]. However, host competence has only
been experimentally confirmed in Egyptian fruit bats [Rousettus aegyptiacus; 33]
and was refuted in big brown bats [Eptesicus fuscus 34], both of which often share
space with humans.
Although in vivo experimental infections with SARS-CoV-2 have not yet been
performed on other bat species, host susceptibility can also be inferred from studies
of the receptor angiotensin-converting enzyme 2 (ACE2), which interacts directly
with the viral spike protein [26]. A study of 46 bat species representing the major
phylogenetic clades in Chiroptera used virus-host receptor binding and infection
assays to examine ACE2 orthologues [33]. Synanthropic bats were no more suscep-
tible than non-synanthropes to SARS-CoV or SARS-CoV-2, and host susceptibility
was not phylogenetically constrained, but varied among congeners. Analyses of
ACE2 in mammals have also been used to predict host capacity to transmit SARS-­
CoV-­2 back to humans, suggesting low risk for E. fuscus but high risk for several
Rhinolophus spp. and some flying foxes (Pteropus spp.) [34]. Unfortunately, emerg-
ing SARS-CoV-2 variants of concern (VOCs) have demonstrated expanded host
tropism. For example, ancestral SARS-CoV-2 did not infect mice efficiently, but the
beta VOC does [35–37]. In addition, both delta- and omicron-like SARS-CoV-2
isolates have been identified in white-tailed deer [Odocoileus virginianus; 32].
Indeed, the ability of SARS-CoV-2 VOCs to infect bat species, including E. fus-
cus and R. aegyptiacus, remains unknown. Nearctic bats carry a range of alphacoro-
naviruses, but did not evolve alongside betacoronaviruses such as SARS-CoV-2,
prompting speculation that these bats may be particularly vulnerable to
Betacoronavirus infection [38]. This hypothesis was not supported by ACE2 analy-
ses, which found no association between host susceptibility to SARS-CoV-2 and a
species’ distribution [33]. Taken together, these studies indicate that the risk of
SARS-CoV-2 spillback from humans to synanthropic bats should be assessed on a
species-specific basis and re-examined periodically to account for emerging VOCs.
Finally, the urban wildlife trade raises added risks of pathogen spillover. Many
cities contain some form of wildlife market, where urbanites can purchase live ani-
mals and their parts for various uses including food, medicine, souvenirs, and the
pet trade [4]. The ethics of wildlife trade are complex and outside the scope of this
chapter. However, the trade involves bringing many wild animals together for sale,
exposing diverse species to each other’s pathogens, and housing them under stress-
ful and crowded conditions that will likely suppress immune function [39]. The risk
to human health is well-documented [40], but the associated risks of spillover to
free-ranging urban bats and other urban wildlife deserve further study.
158 C. M. Davy et al.

3 Nuisance Wildlife or Welcome Guest?

Some cultures consider bats to embody luck and good fortune and tolerate or even
celebrate bat roosts in buildings [41]. Other cultures consider bats to be nuisance
wildlife or associated with misfortune. The human dimension aspects of urban bats
are beyond the scope of this chapter, but we revisit them briefly here because human
attitudes and behaviours towards urban bats and other wild animals are key drivers
of human-wildlife conflict and the risk of zoonotic spillover. Urbanites’ reluctance
to host or live alongside colonies of bats may derive from the unsightly nature of
guano deposits in attics or on exterior walls, the stigma associated with living with
perceived pests, or concern about disease transmission [41, 42]. Thus, urban bat
colonies may be subject to intentional killing under the guise of wildlife control or
pest extermination, even when disease transmission is unlikely [43]. Prior to 2000,
intentional killing of “nuisance” bats roosting in buildings was a common source of
bat mortality in North America and Europe [44], and this threat remains unre-
solved [42].
Bat-borne pathogens, such as bat rabies, Australian bat lyssavirus, filoviruses,
and paramyxoviruses, pose real risks to human health [45]. As such, ensuring that
urbanites appreciate the risks of direct contact with bats is key to building bat-­
friendly cities while protecting human health [e.g. 49]. The emergence of COVID-19
has complicated this messaging as media coverage of the origins of COVID-19 has
created inaccurate perceptions of disease risk from bats, leading to increased perse-
cution of bats [47]. For example, a survey of residents of Arkansas, United States,
found that strong negative perceptions of local bat species were associated with the
belief that bats transmit SARS-CoV-2, even though local species are not implicated
in the origins of COVID-19. In contrast, respondents were less concerned about
rabies, which persists in populations of many urban and non-urban Nearctic
bats [48].
Outreach may improve public awareness of bat diversity and the need for bat
conservation. For example, a study of bat pollinators of durian (Durio spp.) suggests
an economic incentive to conserve bats by demonstrating the ecosystem service
they render [49]. Such examples are more difficult to find in cities, where ecosystem
services provided by bats are less clear. However, outreach can help reduce spillover
risk by informing urbanites about the risks of direct contact with bats, such as rabies
in building-roosting E. fuscus in cities in the United States [48] or filoviruses in tree-­
roosting straw-coloured fruit bats (Eidolon helvum) in Ghanaian cities [46].
Importantly, outreach must be informed by culturally relevant social science meth-
odology that considers the drivers of bat persecution or protection [41, 42, 47].
11  Urban Bats, Public Health, and Human-Wildlife Conflict 159

Box 11.1: Case Study – Fighting over Fruit and Faeces; The Case of
Rousettus aegyptiacus
Spillover risk, actual or perceived, is not the only driver of human-bat conflict
in cities. Competition for resources can also lead to conflict, as in the case of
R. aegyptiacus. This bat occurs across the tropical and subtropical areas of
Africa and the Eastern Mediterranean [50]. It is abundant in non-urban and
urban habitats, including large cities, such as Cairo, Egypt, and Cape Town,
South Africa. This species’ cosmopolitan distribution, ability to successfully
reproduce and thrive in urban habitats, and habit of feeding on fleshy fruits,
including commercial crops [51], may all lead to major conflicts with humans.
Rousettus aegyptiacus are considered agricultural pests [51], and in some
cities, they are also considered urban “pests” because they feed on fruit in
urban gardens, dirty the walls of buildings with their guano [52], and are con-
sidered potential sources of human disease. Rousettus aegyptiacus is not
thought to be a competent host for Nipah virus or the five known Ebolaviruses
[7, 53], but like other pteropodids, these bats are potential reservoirs for coro-
naviruses [33], and they can carry Marburg virus [12]. As of this writing, we
are not aware of confirmed cases of pathogen transmission from R. aegyptia-
cus to humans despite widespread overlap between humans and this species
of bat, particularly in cities. Nevertheless, the perceived risks of competition
for fruit crops and pathogen transmission have spurred culling of R. aegyptia-
cus populations by shooting and cave fumigation, leading some countries to
enact legislation to protect this species [54]. For example, Israel banned cave
fumigation in 1985, and R. aegyptiacus is legally protected by the law in
Israel, Cyprus, and Turkey and is explicitly protected by the Agreement on the
Conservation of Bats in Europe (https://www.eurobats.org/about_eurobats/
protected_bat_species).
In this case study, we discuss two non-harmful ways in which conflict
between humans and R. aegyptiacus can be mitigated; (1) by reducing dam-
age to urban fruit crops, and (2) by  discouraging colonies from settling
in locations where unsightly guano deposits create a nuisance for urbanites
and a potential disease risk [54].
Tree-Covering and Pruning to Prevent Fruit Damage
Tree covering is probably the most effective and bat-friendly method to avoid
fruit damage in commercial orchards and can also be applied to urban fruit
trees. Covering urban trees with woven, unframed nets that have a mesh size
<2 mm or even <5 mm [54, 55] can protect fruit while preventing tangling by
birds, lizards, and bats. On small or easily accessible trees, fruit protection
bags may be also used [55]. When a tree is too tall to cover, it can be pruned
to enable direct protection with netting, or alternate, indirect methods can be
used to discourage the bats. For example, Rousettus aegyptiacus tend to carry
fruit from the fruiting tree to temporary feeding roosts 5–30  m away (pine

(continued)
160 C. M. Davy et al.

Box 11.1 (continued)

trees and other non-fruiting species [56]). Pruning these feeding roosts may
also discourage bats from visiting the nearby fruiting tree. Finally, new neigh-
bourhoods or city gardens can be planned with trees that do not bear fleshy
fruit planted near buildings, to avoid attracting frugivores [57], and fruiting
trees planted in locations farther from buildings.
Bat Deterrent Devices to Prevent Fruit Damage or Guano Deposition
Rousettus aegyptiacus can also be repelled from consuming fruit near the
fruiting tree or defecating on exterior walls and cars using acoustic, visual, or
chemical deterrents. Audible and ultrasonic acoustic deterrents differ with
respect to the frequency and amplitude of sound they emit, the beam of the
speaker, and the cost, but they may repel pteropodids and other frugivores [52,
58]. Ultrasonic deterrents typically operate across short distances because the
sounds they produce attenuate quickly, and their effectiveness is unclear [54].
Playback of sounds audible to humans (e.g. gunshots and the sound of dis-
tressed bats) has also been used to deter pteropodids [54], but playback of
loud, distressing noises is inappropriate in urban settings. Rousettus aegyptia-
cus can also habituate to the sounds of acoustic deterrents, so the efficiency of
these devices may also be short-lived.
Chemical deterrents can include smoke, which may temporarily repel bats
from fruiting trees, and strong odours, which may be taxon-specific or are
generally unpleasant [54]. These are clearly not well suited to urban contexts
as they would also be unpleasant or unsafe for urbanites. Visual deterrents
based on lighting [54] may also be difficult to implement in cities because
background light levels in cities tend to already be higher than in non-urban
areas and because lights that would deter fruit bats may also be unpleasant for
humans. Urban R. aegyptiacus may also be less impacted by light-based
deterrents as they are already habituated to artificial light at night.
Well-designed experiments are needed to better understand the potential
effects of such deterrents on the foraging behaviour of the fruit bats [e.g. 59],
as well as on humans and other urban animals. However, these may be better
suited to non-urban contexts, as the available acoustic, chemical, and visual
deterrents are not taxon-­specific and are likely to inadvertently impact urban
humans, domestic animals, and wildlife, as well as R. aegyptiacus. Thus, dis-
couraging bats by netting and pruning fruiting trees (as described above) may
be the most appropriate mitigation in urban areas.
11  Urban Bats, Public Health, and Human-Wildlife Conflict 161

Box 11.2: Case Study – Eptesicus fuscus as House Guests

Eptesicus fuscus are widely distributed in North America, where they are rela-
tively common in cities and often form large colonies in buildings [60]. They
are typically excellent house guests – they prefer not to use the same space as
human inhabitants, and it is not uncommon for people to be unaware that they
share a building with bats. Still, E. fuscus roosts pose potential disease risks
to humans in at least two ways. First, large accumulations of guano can enable
growth of Histoplasma capsulatum var. capsulatum, a soil-associated endemic
and dimorphic fungus that can cause histoplasmosis when microconidia are
inhaled [43]. Second, E. fuscus can carry rabies virus (RABV) in North
America [61] and transmit rabies to humans through direct bat-human contact
and through intermediate hosts (wild and domestic mesocarnivores). The risk
of exposure to both diseases is minimised when urbanites understand how
they are transmitted and how to avoid them.
Mitigating Risk of Histoplasmosis in Homes Shared with E. fuscus
Guano deposits in enclosed, dry spaces such as attics can provide suitable
growth conditions for H. capsulatum. Microconidia are aerosolised when
guano is disturbed (e.g. while removing deposits), which increases inhalation
risk [43, 62]. This fungus is not a bat-guano specialist; it can also grow on
other nitrogen sources, including droppings of domestic poultry [63]. Thus,
histoplasmosis risk is not limited to cohabitation with (or exposure to) bats.
Nevertheless, people living with any large colony of bats that create contained
guano deposits should be informed about histoplasmosis so they can take
appropriate precautions.
Fortunately, minimising exposure to H. capsulatum is relatively straight-
forward. Removing guano deposits from enclosed spaces regularly (annually)
can prevent build-up of large amounts of guano. Building-roosting E. fuscus
typically select enclosed interior spaces, such as attics, that humans rarely
enter, which effectively isolates their guano deposits from the rest of the
home. When entering these spaces, humans can wear respirators to prevent
inhalation of H. capsulatum spores as the deposits are disturbed [64]. Ideally,
guano removal is (1) performed by professionals who have effective personal
protective equipment and (2) completed in the winter, after resident bats have
moved elsewhere to hibernate. This can minimise direct human-bat contact
and thus reduce the risk of transmission of other diseases, including rabies.
Transmission of Rabies by Eptesicus fuscus: Low Probability, High Stakes
The rabies virus (RABV) belongs to the family Rhabdoviridae and genus
Lyssavirus and causes fatal encephalitis in infected mammals. Rabies causes
tens of thousands of human deaths globally each year, most of which occur in
Asia and Africa and result from bites by infected dogs [45]. The situation in
North America is very different – cases in humans are rare but are overwhelm-
ingly associated with bat-borne strains of RABV [15, 65].

(continued)
162 C. M. Davy et al.

Box 11.2 (continued)

Eptesicus fuscus is one of the most commonly submitted species for rabies
testing in North America because, thanks to its building-roosting habit, it is
encountered more often than most other species of bat. The incidence of
RABV in E. fuscus appears low: a mere 3.6% of 62,997 E. fuscus tested from
2010 to 2015 in the United States were carrying the virus [65]. However, this
sample is not representative (i.e. individual E. fuscus that are tested for rabies
have already behaved atypically enough to be sent for testing), so true popula-
tion prevalence is likely much lower. These data can be further parsed by
RABV strain as the various strains of bat-borne RABV are not evenly repre-
sented in human cases.
Spillover of rabies from Nearctic bats is not clearly associated with synan-
thropic species of bats. The most commonly implicated strains in human
cases of bat rabies in North America are associated with silver-haired bats
(Lasionycteris noctivagans), tricolored bats (Perimyotis subflavus), and
Brazilian free-tailed bats (Tadarida brasiliensis). The first two species are
rarely synanthropic and infrequently encountered by humans. However,
strains from these species could be transmitted by synanthropes such as
E. fuscus. Of 232 RABV sequences isolated from E. fuscus in Canada, 5 were
assigned to strains associated with other bat species [61]. Isolates from E. fus-
cus submitted for rabies testing in the United States provide further evidence
for occasional spillover: 94.8% of 116 genotyped samples belonged to strains
associated with E. fuscus, but the rest originated in other species [65]. Limited
genotyping of RABV strains from rabies-positive bats limits conclusions
about the rate of RABV spillover among bat species [65], but RABV strains
from other species can clearly spill over to E. fuscus, which can transmit these
strains directly to humans, and to domestic or wild mammals that can also
transmit to humans. The apparently low rate of spillover is intriguing, because
strains associated with E. fuscus are rarely transmitted to humans despite their
abundant urban colonies [65, 66].
Minimising the risk of RABV transmission between E. fuscus and humans
is critical, because human rabies is almost always fatal [15]. One mitigation
strategy is public education. First, people must be instructed never to handle
bats with bare hands. When bats enter the parts of a building used by humans,
leaving doors and windows open usually allows the bats to leave of their own
accord. If a bat is acting strangely or simply does not leave, it may be safely
picked up while wearing thick leather work gloves, or gently scooped up
using a dustpan and container, and released outside. Finally, the public should
be informed that bites from E. fuscus (and many other species) can be practi-
cally invisible even if the teeth have broken the skin. If a bite occurs, or a bat
enters a room where someone is sleeping or incapacitated, and a bite may
have occurred unnoticed, medical attention should be sought immedi-
ately [15].
11  Urban Bats, Public Health, and Human-Wildlife Conflict 163

4 Reducing Risk of Zoonotic Spillovers from Urban Bats

Cities bring together high densities of humans, domestic animals, and wildlife ani-
mals [5, 21], bringing urban bats into contact with a myriad of pathogens they may
not encounter in non-urban areas. Conversely, humans sharing buildings or green
spaces with urban bats may be exposed to bat-borne pathogens, whether directly or
indirectly through contact with bats, bat guano, or domestic animals that may be
intermediate hosts [22]. Clarifying these transmission pathways can identify expo-
sure hotspots and inform mitigation to reduce spillover risk [2].
Effective, humane deterrents for bat species that are perceived as nuisances or
pests could reduce human-bat contact, but public education may provide a more
effective solution by helping people to appreciate living with bats [42]. Of course,
to safely live with bats (or any urban wildlife), people must know about potential
public health risks and how to mitigate them. An essential message is that eradicat-
ing or culling bats is unlikely to reduce, and can even exacerbate, risks of disease
transmission [42]. Conservation of bats in cities, with a focus on outreach and risk
mitigation (rather than eradication), is therefore a public health imperative.
Future research should continue to untangle disease dynamics among urban bats,
recognising that bat-borne pathogens can pose a risk to human health, while human-­
to-­bat spillover (e.g. potential spillback of SARS-CoV-2) or human-mediated trans-
mission of other pathogens to bats (e.g. dispersal of P. destructans) can pose a threat
to bat health. There are challenges in advancing this work, and we highlight two in
particular. First, procedural variation among surveillance studies can limit the power
of systematic reviews or meta-analyses to detect temporal or spatial trends.
Standardising detection methods, assay interpretation, and diagnostic criteria for
diseases among studies will increase the long-term impact of surveillance. For
example, studies exploring whether bats are a principal reservoir for Ebola virus are
highly heterogeneous in sample type, assay (molecular or serological), and taxo-
nomic and demographic representation (species, sex, age), and are frequently based
on small sample sizes with limited statistical power. Establishing best practices
would facilitate inter-study comparison and enable more powerful meta-analyses.
An example of how this could be done on a global scale comes from surveillance for
avian influenza in wild birds (http://www.fao.org/AVIANFLU/en/manuals.html),
but this approach involves establishing reference centres instead of relying on spo-
radic and variable research protocols. Minimum metadata sets that include host
traits and ecological context are essential, as demonstrated in a recent study that
used ecological trait-based models to reveal previously unrecognised bat hosts for
betacoronaviruses [27].
The importance of standardised surveillance intensity and effort is also illus-
trated by our case study of RABV prevalence in E. fuscus. Rabies is deadly in
humans, and bat rabies is linked to most human cases in North America [15]. Yet,
big knowledge gaps include prevalence of the various strains in E. fuscus (current
sampling is not representative) and the factors driving spillover among bat species.
Standardised, long-term surveillance of existing pathogen diversity can characterise
164 C. M. Davy et al.

temporal and regional variation in prevalence of zoonoses and their causative agents
and identify the drivers of outbreaks and spillovers.
Finally, although surveillance studies provide an essential baseline, research
should also explicitly address the gap between identifying existing pathogen diver-
sity and understanding the drivers of bat-human spillover in the urban context [2,
67]. This requires sustained investment in coordinated, long-term, collaborative
approaches that include community organisations, academic and government scien-
tists, public health agencies, and social scientists, as well as wildlife rehabilitators,
zoos, non-governmental organisations (NGOs), and community science initiatives.
Such a comprehensive, One Health framework can not only benefit public and ani-
mal health but also raise awareness of the interconnectedness of bats, humans, and
the biosphere, and of the benefits of coexistence.

Acknowledgements  We thank two anonymous reviewers and the editor of this chapter for their
helpful comments and suggestions.

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Chapter 12
Ecosystem Services by Bats in Urban Areas

Danilo Russo, Joanna L. Coleman, Leonardo Ancillotto, and Carmi Korine

Abstract  Preserving biodiversity and the ecosystem services (ES) it provides is

vital to sustainability. With over half of all people living in cities, urban ES play an
especially important role. Bats are the most speciose mammalian group in many
cities and may provide a variety of important ES. This chapter explores the available
literature and provides unpublished information on bats’ urban ES, covering insec-
tivory, pollination, seed dispersal, and bat-related tourism.
We found that although research interest in bat-mediated ES has grown consider-
ably, ES by urban bats have been relatively neglected. Twenty-two studies on vari-
ous continents that used molecular identification of prey remains in bat droppings
revealed a substantial consumption of urban pests, including ‘nuisance’ insects,
such as drain flies and mosquitos, and species that bite or induce allergic reactions.
Bats also consume the same species of mosquitos that are vectors of the West Nile
virus and malaria, phlebotomine sandflies that transmit leishmaniasis, as well as
insects that damage stored products. Ecosystem services rendered by phytophagous
bats (pollination and seed dispersal) in urban areas are poorly known but potentially
important. However, urbanisation might hinder the movement of bats and thus limit

Supplementary Information The online version contains supplementary material available at

[https://doi.org/10.1007/978-­3-­031-­13173-­8_12].

D. Russo (*) · L. Ancillotto

Laboratory of Animal Ecology and Evolution (AnEcoEvo), Dipartimento di Agraria,
Università degli Studi di Napoli Federico II, Portici, Naples, Italy
e-mail: [email protected]
J. L. Coleman
Department of Biology, Queens College at the City University of New York,
Flushing, NY, USA
C. Korine
Mitrani Department of Desert Ecology, Ben-Gurion University of the Negev,
Midreshet, Ben-Gurion, Israel

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 167
L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_12
168 D. Russo et al.

the provision of such ES. The few studies available fail to prove that phytophagous
bats in urban areas mediate plant recruitment, yet there is some anecdotal evidence
that they do. Urban bats also provide cultural ES, such as bat-related tourism, which
in some cases generate considerable revenue. We highlight a significant gap in
research on urban ES by bats that must be filled given its expected importance. We
call for studies to document and quantify such ES, especially studies that adopt
rigorous methods, such as DNA metabarcoding in faecal analysis, exclosure experi-
ments to study insect suppression, or bat-mediated pollination, and studies that pro-
vide evidence of the role of bats in increasing fruit set and/or plant recruitment.
Raising awareness of bat-mediated urban ES might help convince the public that
bats are essential components of urban biodiversity and are worth conserving.

Keywords  Biodiversity · Chiroptera · Cities · Ecosystem services · Insectivory ·

Pollination · Seed dispersal

1 Introduction

Ecosystem services (ES), here defined as the benefits provided to people by ecosys-
tems and their components, bear a value that is well-recognised at national and
international scales. Preserving biodiversity, i.e., the source of ES, and its provi-
sions is therefore regarded as a top priority in sustainability policy [1]. Although
only ca. 3% of global land is classified as urban, more than half of all people live in
cities, a fraction that is projected to rise to two-thirds by 2050 [2]. This trend under-
scores the increasing importance of urban landscapes to humankind. Although con-
version of natural and semi-natural habitats to urban land uses is seen as a major
cause of loss of ES [2], there is growing research interest in ES provided by urban
biodiversity [3].
Although many mammal species are threatened by urbanisation, some tolerate,
or even thrive in, urban habitats [4]. Within urban mammal communities, bats are an
important group, with several species that persist not only in remnants of natural
habitats but also in the most built-up areas, where they may roost in buildings or
forage near streetlamps [5]. These include many bat species, which, like other wild-
life, may provide both ES and ecosystem disservices [ED; 6]. Whereas ED, such as
conflicts caused by the presence of bats in buildings and sometimes zoonoses (dis-
eases that originate in non-human animals), are well-­known [7], there is less knowl-
edge of the role of bats as providers of urban ES.
In this chapter, we provide a state-of-the-art picture of ES delivered by urban
bats by analysing the available literature and complementing it with unpublished
information on bat pollination in Southeast Asia. The specific ES we address are
insectivory, pollination, and seed dispersal by bats and the economic and cultural
benefits of bat-related tourism.
To assess the representation of bats in the literature on urban ecosystem services
(UES), we performed a Web of Science (WoS) search, with ‘urban’ AND
12  Ecosystem Services by Bats in Urban Areas 169

‘ecosystem service’ as topics (Appendix 1). Of 830 relevant records (identified by

scanning all titles and abstracts), 99.5% were published since 2005, i.e., the same
year as the Millennium Ecosystem Assessment, which popularised the term ‘eco-
system service’. Interest has risen exponentially since then and is dominated by
China (which accounts for more than one-third of all authors and study sites), fol-
lowed by the United States (24% of all authors, 14% of study sites). Only 31 studies
were done in sub-Saharan Africa, which is urbanising faster than any other region
[8]. Most research aims to map the distribution of/change in ES, analyse policy
related to UES, valuate UES, or assess human perceptions of UES. Where direct,
animal-­mediated ES are concerned, nearly all studies focus on insect pollinators,
with only one study [9] on bats.
A similar WoS search but with ‘bats’ AND ‘ecosystem service’ as topics
(Appendix 2) identified 114 relevant records. Again, research interest has grown
exponentially since 2005. Studies of specific bat-mediated ES mainly focus on bats
as pest control agents – as may be expected given that most bats are insectivorous
[10]. Seed dispersal is the next most assessed ES, followed by pollination. In this
case, the geographical bias pertains to authorship only, with 38% of authors based
in the United States, followed by the United Kingdom and Germany, each with
more than 15% of authors. Most study localities (71%) have been in areas of high
biodiversity and many bat species, i.e. the tropics and subtropics, but only ten stud-
ies included urban sites.
Of course, this literature search does not reveal the full scope of work on ES by
urban bats – records are limited to those with ‘ecosystem service’ in the topics. As
described below, searching for ‘urban’ AND ‘pollination’ AND ‘bats’, for example,
yields a different set of records, including some from cities. Still, it is fair to say that
urban bats have been largely overlooked as providers of ES. This oversight may seem
surprising considering that among mammal orders, Chiroptera is the most speciose
one in many cities [4, 5]. Furthermore, by virtue of their unmatched dietary diversity
and long-distance foraging behaviours, their importance as providers of ES is sub-
stantial if undervalued [11]. To help fill this gap, we explore ES provided by bats in
urban areas, presenting the latest knowledge and highlighting research directions.

1.1 Insectivory

Insectivorous bats in natural and semi-natural habitats supply key intermediate (reg-
ulating) ES, such as the suppression of pest arthropods (Fig. 12.1a). The importance
of these services by bats across agricultural landscapes is well-understood [12] and
has been economically valuated [13]. In contrast, very little information is available
about the importance of these services in urban areas. Nevertheless, what informa-
tion does exist suggests that the benefits may be considerable.
For instance, the role of bats as predators of mosquitos may be locally important
[14] (Figs. 12.2 and 12.3) and substantially reduce egg production [15], suggesting
that bats exert top-down regulation on mosquito populations, and do not merely
170 D. Russo et al.

Fig. 12.1  Urban-relevant ecosystem services rendered by bats: (a) A greater mouse-eared bat
(Myotis myotis) – a species known to occur in urban areas – feeding on a rose chafer (Cetonia
aurata), a horticultural pest (photo by Merlin Tuttle). (b) A dog-faced fruit bat (Cynopterus
brachyotis) flying off with the fruit of a yellow stem fig (Ficus fistulosa) in Singapore, potentially
acting as a seed disperser (photo by Chan Kwok Wai). (c) The emergence of Mexican free-tailed
bats (Tadarida brasiliensis) from the Congress Avenue Bridge in Austin, Texas, USA, draws
onlookers each night and is the city’s most popular attraction (photo by Merlin Tuttle). (d) A cave
nectar bat (Eonycteris spelaea) foraging on the nectar of a banana (Musa sp.) flower in Singapore
and thus potentially acting as a pollinator (photo by Nick Baker)

suppress them. Bats might thus help mitigate the transmission of mosquito-borne
diseases in cities [15], including some that cause significant morbidity and mortality
among urbanites worldwide.
Bats also consume other perceived pests. These include chironomids [14; present
analysis (Figs. 12.2 and 12.3)], which cause economic damage, nuisance, and health
issues in cities [16], and moths, e.g., the oak processionary (Thaumetopoea proces-
sionea) [17], whose caterpillars, besides damaging trees, release urticating hairs
that irritate people and domesticated animals. Finally, Gould’s wattled bats
(Chalinolobus gouldii) in Perth, Australia, were recently found to consume hun-
dreds of insect species, but especially lepidopterans, 40% of which are deemed
pests [9]. Otherwise, studies of ES rendered by insectivorous bats in cities are prac-
tically non-existent. We present the first analysis of urban pests from studies on the
diets of bats from various continents.
Previous work adopting morphological analysis of food remains in bat droppings
provides limited evidence of pest consumption because insect fragments large
enough to offer sufficient taxonomic resolution are rare, especially for moths, which
comprise many agricultural pests [12]. However, modern molecular techniques are
highlighting that urban bats deliver this important ES.  For instance, using DNA
12  Ecosystem Services by Bats in Urban Areas 171

Blattodea (0.9)
Dermaptera (1.8)
Hemiptera (1.8)

0.2 ae
No
ctu

(2 icid
)
ida

l
Cu
e(

Co (7.9)
Pyr 4.4

leo
alid )
ae (

pte
3.5)

ra

Oecop
horida
e (2.6)
Tineidae (2.6) 
        
Muscidae


(8.8)

  
(1 1.4) Tip


her


ul
Ot
  (8. idae
8)
Ot

Ca
Other
h

llip
Li

Scath
er

Ptinidae (2.6)
Tabanidae (2.6
m

ho
(7

o
.9)

rid
n

opha
iidae

ae
(6.
gida
(2.6)

1)
e (3.5
)

Fig. 12.2  Classification of 114 insect species (1008 records) identified as urban pests and docu-
mented in the diets of bats (n = 22 publications) into orders and families. Numbers in parentheses
are percentages of species in each taxon

Fig. 12.3 Relationships
with humans of insect
species (n = 114) occurring
in the diet of the bats taken
from 22 publications and
identified as urban pests.
Only occurrence
frequencies >2.5% are
shown. The numbers in
parentheses are
percentages
172 D. Russo et al.

metabarcoding, Aguiar et al. [18] recently analysed faecal samples from five house-­
dwelling bat species in Brazil and determined that more than half of the 83 molecu-
lar taxonomic units were from pest insects.
We adopted a conservative approach to evaluating the possible ES of urban bats,
by collecting data on diets of insectivorous bats from 22 studies that used DNA
metabarcoding to identify insects at least to the level of genus. These studies con-
cerned Australia, Africa, Europe, Asia, and the Neotropics and included 1008 records
of insects. We used a handbook [19] and online databases (CABI, 2019: Invasive
Species Compendium: https://www.cabi.org/isc/ and Plant Pest of the Middle East:
(http://www.agri.huji.ac.il/mepests/) to delineate five groups of insect taxa based on
their relationships with humans, as proposed by the literature: (1) agricultural pests,
which also include known pests of plants in urban habitats, (2) storage pests, (3)
potential disease vectors, (4) nuisance pests, and (5) neutral association (non-pests).
We considered categories 2–4 as primarily urban pests, even though some agricul-
tural pests also cause problems in urban green spaces (e.g. gardens, parks).
We could not unambiguously categorise 8.1% (82) of species due to a lack of
information on their ecology and biology. Our analysis revealed that 46.2%
(n = 465), 32.5% (n = 328), and 13.1% (n = 114) of insect species were categorised
as natural pests, agricultural pests, and urban pests, respectively. Nearly half (45.6%)
of the categorised insects in our database are pests in agricultural or urban habitats.
Documented taxa of urban pests consumed by bats belonged to 44 families, in 6
orders (especially Diptera and Lepidoptera), with the most frequently consumed
families being Culicidae, Muscidae, and Tipulidae (Fig. 12.2).
Urban arthropods in the database included species whose pest status we classi-
fied into four broad categories (Fig. 12.3). More than one-third could be considered
species whose bites are painful or provoke allergic reactions and ‘nuisance’ insects,
such as drain flies (Psychodidae) and mosquitos (Culicidae), which can become
pests in anthropogenic aquatic habitats such as sewage treatment facilities. One-­
quarter of the species are documented pests of various plants (trees, shrubs, crops)
that are cultivated in urban green spaces and their surroundings. One-fifth of species
are disease vectors, including species of mosquitos that transmit West Nile virus and
malaria and phlebotomine sandflies (Psychodidae) that transmit leishmaniasis. The
rest (15%), mainly moths and beetles, are species known to damage stored products
including foodstuffs, household materials, or woollen clothing.

1.2 Pollination and Seed Dispersal

Phytophagous bats in the Old World (Pteropodidae) and New World (Phyllostomidae)
tropics and subtropics are key pollinators and seed dispersers for many plant species
(Fig. 12.1b, d). In several cases, bats are the only animals known to fulfil these eco-
logical roles. Approximately 500 plant species rely solely on bats for pollination,
exemplified by tight mutualisms, such as those between Heliconia solomonensis
and Woodford’s fruit bat (Melonycteris woodfordi) in the Solomon Islands or
12  Ecosystem Services by Bats in Urban Areas 173

Centropogon nigricans and the tube-lipped nectar bat (Anoura fistulata) in Ecuador
[see also 20]. Although plants’ relationships with seed-dispersing bats are rarely
exclusive (obligate), the seeds of hundreds of plant species are dispersed by bats
[21]. Thus, bats are vital mediators of outcrossing and succession, perhaps espe-
cially where, thanks to their long-distance foraging behaviour, they disperse plants
in degraded landscapes that may have lost other animal dispersers [see also 22 and
others therein].
However, the above ecological roles of bats only equate to ES if there is a quan-
tifiable (ideally, valuated) benefit to humans, and convincing demonstrations that
phytophagous bats provide ES are scarce generally, let alone in cities [see also 22].
A Web of Science search (on 20 December 2020; Appendix 3), with ‘urban’ AND
‘pollination’ AND ‘bats’ in the topics, yielded eight unique, relevant records (after
discarding those that were doubled or on other topics). We found one more record
opportunistically from citations within these records or our knowledge of the litera-
ture. A similar search on the same date (substituting ‘seed’ for ‘pollination’) yielded
19 records. Of these papers, one on pollination and five on seed dispersal generated
no useful knowledge on hypothesised or realised ES and/or were not about urban
bats. Thus, it is evident that links between urbanisation and ES by phytophagous
bats are still poorly understood and represent a research frontier.
Research on the role of urban bats as pollinators and seed dispersers is worth
pursuing. If bats are important agents of dispersal for plants in cities, then they are
indirectly implicated in the ES rendered by urban plants, including providing food,
fibre, and wildlife habitat, carbon sequestration, mitigating urban-related abiotic
changes (e.g., urban heat islands, pollution, altered hydrology), and improving
human-nature relationships [see also 3]. However, urbanisation could also under-
mine these ES via extreme habitat fragmentation and the prevalence of artificial light
and noise pollution, all of which could hinder movement by bats [see also 23]. For
example, for urban calabash trees (Crescentia cujete), which are only pollinated by
Pallas’s long-tongued bat (Glossophaga soricine), outcrossing declines with distance
between individuals on a campus in Recife, Brazil – a finding interpreted as being
indicative of reduced habitat connectivity for bats [23]. However, pinpointing exactly
which urban attributes limit connectivity (e.g., impervious cover, light, noise) should
be done through spatial, landscape-scale analyses and/or experimental manipulation.
Yet, adequate spatial (or temporal) replication and experimentation are rare
among studies of ES by urban phytophagous bats. Rather, most studies have
documented diet and/or foraging behaviour in one or a few sites, using morpho-
logical identification of plant parts collected from fur and/or faeces or direct
observation. Ecosystem services provided by bats have then been inferred based
on which plants bats eat or visit. Such studies often find that urban bats have
broad diets and/or readily eat exotic species [e.g. 24–28, and others therein] –
tendencies also revealed by spatially replicated, urban-gradient studies in
Southeast Asia [29, 30] and a systematic review of studies on diets of great fruit-
eating bats (Artibeus lituratus) in Brazil [31]. By promoting increased dietary
generalism and making exotic plants more available to bats, urbanisation may
produce a loss of plant species that exhibit bat pollination syndrome, as shown
174 D. Russo et al.

by studies of floral resources (e.g. in Thailand [29] and Brazil [32]), and raise
competition among native plant species for effective agents of dispersal [33].
These native plants may have high conservation value and/or deliver important
ecosystem services.
Experimental work demonstrates that the consumption of seeds by urban fruit
bats does not hinder or even improves germination outcomes [e.g. 34, 35]. For
example, in Singapore, the lesser dog-faced fruit bat (Cynopterus brachyotis) for-
ages on 33 species, including heritage trees and pioneer plants (Fig.  12.1b), and
seeds remain viable after gut passage [30]. Moreover, this bat species moves seeds
well away from parent plants. These findings suggest a role in dispersing plants of
conservation and/or cultural importance.
However, the above-mentioned studies do not prove that urban fruit bats
mediate plant recruitment because they do not document the location of the seed
rain and/or the fate of seeds. One study [36] found more tree seedlings beneath
sacred figs (Ficus benghalensis) in settlements than in open or riparian areas
and showed that these figs attract visits by Indian flying foxes (Pteropus gigan-
teus). But they attract birds too. As such, it remains unclear which animal spe-
cies are effectively dispersing seeds. Likewise, studies of flower-visiting urban
bats have not documented whether these visits lead to successful pollination.
Therefore, evidence that urban bats are effective pollinators or seed dispersers
needs strengthening.
Yet, there is some anecdotal evidence of bat pollination constituting an effec-
tive ES. In Singapore (as throughout Southeast Asia), durian (Durio spp.) is con-
sidered the ‘King of Fruits’, though it is all imported, mainly from Malaysia [37].
The fruit is so prized that each year, mainstream media publish articles on current
and forecasted prices to help locals find the best deals. But instead of buying
durian, some locals collect fallen fruits in parks or on other public land, even
though doing so is illegal. Bats are the main pollinators of wild and semi-wild
durian, and the most effective species, the cave nectar bat, Eonycteris spelaea
[e.g. 38, 39], is locally common – the large roost mentioned by Leong and Chan
[40] contained >1,400 individuals in 2015 and is <1 km from one of Singapore’s
few durian groves (unpubl. data). In such groves, durians develop without hand
pollination  – which points to the role of animal pollinators, almost certainly
E. spelaea – and are eaten by locals.
Urban phytophagous bats may also provide ecosystem disservices, although
the distinction between ‘services’ and ‘disservices’ is subjective. For example,
in Singapore, C. brachyotis eats and moves seeds of the Jamaican cherry
(Muntingia calabura) [30], an exotic species deemed invasive, but whose fruits
are eaten by several native birds (pers. obs.). Thus, a birder who enjoys watch-
ing these birds might disagree with a conservationist as to whether this ecologi-
cal role is welcome.
12  Ecosystem Services by Bats in Urban Areas 175

1.3 Bat Tourism

Urban bats may provide cultural ecosystem services, which are defined as the
nonmaterial benefits (e.g., recreation, spirituality, etc.) that humans derive from
biodiversity. For instance, Mexican free-tailed bats (Tadarida brasiliensis) roost
under the Congress Avenue Bridge in Austin, Texas, USA (Fig. 12.1c), and the
opportunity to watch their nightly emergence draws more than 242,000 visitors
per year, generating a conservatively estimated revenue of 6.5 million USD [41].
Bat-related tourism may also have positive knock-on repercussions for the con-
servation of bats and biodiversity generally. Bat tourism may raise public aware-
ness of the importance of bats and enhance support for conservation, especially
among urbanites, whose dissociation from nature may adversely affect environ-
mental governance and sustainable urbanisation [3]. For example, visiting a bat
cave sanctuary in the Philippines was found to increase visitors’ willingness to
conserve [42]. And each year, a bat centre in the town of Barrea, Abruzzo, Italy,
receives thousands of tourists who come to watch the televised activity of a large
maternity colony of greater horseshoe bats (Rhinolophus ferrumequinum) in a
building [43]. In summer 2020 alone, an estimated 12,000 people visited the bat
centre (A. Scarnecchia, pers. comm.). This case demonstrates how it is possible
to protect a major bat colony while also providing economic benefits to locals,
education, and enjoyable experiences to tourists as well as behavioural research
[43]. Bat tourism may also involve bat exhibits, festivals, and interactive inter-
faces that allow the public to engage with and learn about urban bats (e.g., bat
walks, listening to echolocation calls, public bat surveys, etc.) – such activities
may successfully engage urbanites and improve their knowledge and perspec-
tives of bats [44].

2 Conclusions

Cities are now home to most of humanity, i.e., the beneficiaries of ES. This is
especially true in the world’s most rapidly urbanising nations, which are also
the lowest-­income ones [8] and where urbanites may therefore be most reliant
on ES [45]. Therefore, understanding the ES rendered by urban bats can have
major economic and sustainability implications. Our comprehensive review of
the literature highlights a lack of research attention to the ES (and ED) ren-
dered by urban bats. This is striking because cities that have lost large fractions
of their pre-settlement bat faunas may still retain several species that have
diverse functional traits and are often abundant – key attributes that underpin
ES [46].
Evidence from non-urban habitats speaks to the potentially large value of these
urban ES, which is expected to grow in the urban century. For instance, as rural-to-­
urban migration and the environmental crisis compromise conventional agriculture,
176 D. Russo et al.

urban farming becomes more important and stands to improve not only food secu-
rity but also nutrition and income for urbanites [47]. The plants best suited to urban
agriculture [e.g. Brassica spp.; 47] are not pollinated by bats but do provide a forag-
ing habitat for certain bats, e.g. Kuhl’s pipistrelle (Pipistrellus kuhlii), especially
near human settlements [48].
Another key trend is the confluence of urbanisation and climate change
exacerbating the risk of certain vector-borne diseases. The role of bats in miti-
gating this risk is exemplified by the case of dengue fever (the world’s fastest-
growing vector-­borne disease) – whose causative agent is a virus transmitted
by Aedes mosquitos (especially A. aegypti) that mainly occur in cities and
whose range should expand with climate change [49]. Here, bats may provide
a two-pronged ES. First, they could suppress the vectors – indeed, urban bats
do consume mosquitos [9]. Second, bats, especially commensal species, appear
to be dead-end hosts for the virus [50], thereby potentially reducing total infec-
tion pressure.
In this century, there is also a growing emphasis on biophilic cities to mitigate
numerous urban-related abiotic changes, promote urban sustainability and resil-
ience, and enhance urbanites’ access to nature [3 and others therein]. Urban bats
play key roles in these initiatives, as evidenced above. They pollinate and disperse
seeds of cultivated and wild plant species, consume horticulturally important insect
pests, and offer people the chance to observe wildlife.
However, most of the evidence for bat-mediated ES comes from non-urban
systems, leaving a large research gap. Therefore, we call for rigorous studies in
cities to document, quantify, and valuate these services, including the use of
DNA metabarcoding techniques for faecal analysis that are exclusively designed
for urban bats [as done by 18]. Ideally, studies focusing on pollination (and/or
insect control) will involve experimentation (e.g., exclosure tests) to isolate the
roles of bats from those of other animals and address potential confounders [see
also 12]. Investigations of pollination and/or seed dispersal should ideally dem-
onstrate that the involvement of bats ultimately increases fruit set and/or plant
recruitment. Moreover, the cultural ES rendered by urban bats should be explored
using established social science frameworks and techniques, despite ongoing
challenges as far as defining categories of cultural ES and identifying the most
appropriate methods to evaluate them [51].
As we approach global tipping points of biodiversity loss and climate change,
the importance of garnering human support for sound conservation cannot be
overstated. With most policy decisions made by urbanites (who also constitute
most of humanity), there is an urgent need to increase public appreciation for
bats (like all components of biodiversity) so that people will act swiftly and
meaningfully to protect them. We argue not that raising awareness of bat-medi-
ated urban ES is enough to accomplish this goal, but rather than doing so at least
stands to persuade most people, whose motivations to conserve are grounded in
utilitarian ethics.
12  Ecosystem Services by Bats in Urban Areas 177

Appendices

Appendix 1

Results of a Web of Science (WoS) search of the literature with ‘urban’ AND ‘eco-
system service’ as topics, performed on 5 May 2021.
The worksheet ‘WoS savedrecs’ displays raw results, with references sorted by
year before assigning them unique serial numbers (column A).
We obtained country data (column D) for the worksheet ‘Study locations’ by
scanning abstracts and (where the location was not evident from abstracts) papers to
ascertain where the research was conducted.
The ‘ES categories’ worksheet classifies references into 16, author-defined,
types of ecosystem services (row 1) that were investigated.
The ‘WoS categories’ and ‘Research areas’ worksheets contain the WoS graphi-
cal outputs depicting the 25 most common subject categories and research areas
(defined by WoS), respectively.
The worksheet entitled ‘years’ contains a chart depicting growth in the literature
over time, i.e. publications per year, with a best-fit exponential trend line and the
associated R2 value – the data to construct this chart come from column N of the
‘WoS savedrecs’ worksheet.
The worksheets entitled ‘Authors’ and ‘WoS countries (authors)’ contain the
graphical outputs from WoS, depicting the 25 most commonly represented authors
and national affiliations of authors, respectively.

Appendix 2

Results of a Web of Science (WoS) search of the literature with ‘bats’ AND ‘ecosys-
tem service’ as topics, performed on 5 May 2021.
The worksheet ‘WoS ES + bats complete’ displays the raw results, with refer-
ences, ordered the same way that WoS returned records.
The worksheet entitled ‘WoS ES + bats refined’ only lists the 114 records that we
established were relevant after scanning the abstracts and/or papers. We assigned
each paper a dichotomised score indicating whether it investigated ecosystem ser-
vices in an urban context (1) or not (0), in column D, and identified the locality
(column E) where the research was done. Columns T through AA classify records
into the six typical categories of bat-mediated ecosystem services that were
investigated.
The ‘Localities’ worksheet is where we tabulated the locality data mentioned
above to establish the geography of the research. The ‘WoS categories’ and
‘Research areas’ worksheets contain the WoS graphical outputs depicting the 25
most common subject categories and research areas (defined by WoS), respectively.
178 D. Russo et al.

The worksheet entitled ‘years’ contains a chart depicting growth in the literature
over time, i.e. publications per year, with a best-fit exponential trend line and the
associated R2 value – the data to construct this chart come from column L of the
‘WoS ES + bats refined’ worksheet.
The worksheets entitled ‘Authors’ and ‘WoS countries (authors)’ contain the
graphical outputs from WoS, depicting the 25 most represented authors and national
affiliations of authors, respectively.

Appendix 3

Results of literature searches related to three types of ecosystem services rendered

by bats.
The worksheets entitled ‘Urban + pollination + bats’ and ‘Urban + seed + bats’
list records returned by Web of Science (WoS) during topic searches performed on
20 December 2020, plus others identified opportunistically (from citations within
these records or our knowledge of the literature). The records in red font in the
‘Urban + seed + bats’ worksheet are redundant, i.e. also returned by the WoS search
of urban AND pollination AND bats in the topics.
The worksheet entitled ‘Urban + insect + bats + control’ lists records returned by
a WoS search of these terms in topics performed on 5 May 2021.

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Chapter 13
The Big Picture and Future Directions
for Urban Bat Conservation and Research

Krista J. Patriquin, Lauren Moretto, and M. Brock Fenton

Abstract  Urbanisation modifies natural environments, creating light, noise, air,

and water pollution, which may impact bat physiology, ecology, and behaviour. The
vast variation in the physical and behavioural characteristics of bats makes it diffi-
cult to predict how each species will be affected by urbanisation. It appears that
urban-dwelling bats commonly present general physiological and behavioural
adaptations to urban environments: an “urban syndrome”. Like other urban-­dwelling
mammals, bats may also move into and out of urban areas to feed, roost, and hiber-
nate. However, the impacts of urban living on the survival and reproductive success
of the few urban bats studied to date remain equivocal as responses are species-­
specific. In some instances, bat fitness appears to be higher in urban areas. In other
instances, fitness is reduced in urban areas, suggesting they may be ecological traps
for some bats. Additional species-specific research and tracking could improve our
knowledge of urban-dwelling bats, which could better inform management actions
that support bats. This could be supplemented by establishing clear definitions of
urban environments and gradients of urbanisation across studies.

Keywords  Urban syndrome · Urban mammals · Conservation action · Research

directions · Urban gradient

K. J. Patriquin (*)
Department of Biology, Saint Mary’s University, Halifax, NS, Canada
e-mail: [email protected]
L. Moretto
Vaughan, ON, Canada
M. B. Fenton
Department of Biology, University of Western Ontario, London, ON, Canada

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 181
L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8_13
182 K. J. Patriquin et al.

1 Urban Bats: Adaptation or Tolerance?

Urbanisation imposes several stressors on bats, such as light, noise, air, and water
pollution, and changes to roosting and foraging resources [[1] (see Chaps. 1, 6, 7, 8,
and 9)]. These stressors can affect habitat use, reproductive success, and survival.
However, responses of bats to urbanisation cannot be easily generalised [2], as they
may vary within and among species due to differences in energetic and thermal
demands associated with age, sex, and reproductive condition (see Chap. 1).
Nevertheless, urban bats are generally flexible in traits relating to roosting, diet,
echolocation, and social structure (see Chaps. 1, 3, 5, 6, 7, and 9). Together, these
traits may comprise an “urban syndrome” (see Chap. 1).
It is unclear if an urban syndrome is adaptive for bats. Adaptive traits promote an
individual’s survival and lifetime reproductive success, but there is limited evidence
of fitness benefits gained by urban-dwelling bats. Bats may be at higher risk of mor-
tality as they fly through cities to feed in patches of green space (see Chaps. 1, 3, 7,
8, and 9). Bats roosting in artificial structures may succumb to overheating (see
Chap. 6), which can also affect bats roosting in the open during extreme heat events
(Chap. 7). Urban bats may also carry greater parasite burdens than non-urban-­
dwelling bats, which may affect body condition, survival, and reproductive success,
but these relationships vary with host species, demographics, season, and parasite
species (see Chap. 4). With a few exceptions [e.g. Kuhl’s pipistrelle (Pipistrellus
kuhlii)], reproductive success in studied urban colonies is either lower than, or does
not differ from, that in non-urban colonies (see Chap. 5). It is worth noting, how-
ever, that offspring may be weaned earlier in urban areas, which could improve
juvenile survival and population recruitment [3–5]. At the population level, urban-
isation can lead to reduced population genetic diversity that then puts populations at
risk of extirpation because they are less resilient to change ([5], see Chap. 2). For
bats, the consequences of living in urban areas are not straightforward and may not
be as beneficial as purported. Instead, urban areas may be ecological traps (e.g. see
Chaps. 5 and 6) where bats that appear equipped to live there may suffer fitness
costs and even extirpation. To establish if urban areas are ecological traps, studies
should determine if bats are attracted to these areas despite reduced fitness.

2 How Do Bats Compare to Other Mammals in Their

Response to Urbanisation?

Bats are among the most common mammals in urban environments [5], possibly
because flight allows them to move among isolated habitat patches more easily than
less mobile mammals like terrestrial carnivores or arboreal species [6–9]. For exam-
ple, fruit bats [e.g. Egyptian fruit bats (Rousettus aegyptiacus)] target stands of fruit
trees in urban areas that are often more densely concentrated, more diverse, and
more productive compared to stands of non-urban fruit trees [10]. Mobility could
13  The Big Picture and Future Directions for Urban Bat Conservation and Research 183

also allow species that are typically sensitive to habitat loss and degradation, such
as tricolored bats (Perimyotis subflavus) and various species of mouse-eared bats
(Myotis spp.), to obtain some of the resources they need in urban areas while seek-
ing other resources beyond a city’s limits [9, 11–15] (see Chap. 8). Additionally,
flight may allow bats to navigate around urban stressors like traffic and artificial
lights, just as subterranean mammals use burrows to escape disturbance [5, 6, 8].
While flight may allow bats to access habitat patches in urban environments, it
may also pose trade-offs in adapting to urban living. Flight limits how much weight
bats can carry and is energetically demanding, which constrains how much energy
bats can devote to offspring production and care [16, 17]. Bats therefore produce
few offspring (typically one annually) that develop slowly (3–4  months) but are
long-lived [7, 16, 17], whereas most small urban-dwelling mammals produce rela-
tively large litters with shorter lifespans [5]. Because they have longer generation
times, species like bats with slow life histories are often slower to adapt to changes
in their environment [5]. This might explain why, despite their incredible diversity
of more than 1400 species, only 6.5% of bat species have been documented in urban
areas [5]. By contrast, less diverse taxa like hyraxes (Hyracoidea), carnivores
(Carnivora), and insectivores (Eulipotyphla) with faster life histories have relatively
higher representation in urban environments with 20%, 10.6%, and 9.5% urban spe-
cies in each order, respectively [5].
Species that persist in urban environments typically possess traits like the ability
to produce larger litter sizes, flexibility in weaning age, and behavioural flexibility
that predispose them to respond to urban stressors and possibly offset higher mortal-
ity rates in urban environments [5]. The small percentage of bat species studied in
urban areas provides equivocal support for this argument (e.g. see Chap. 3). Just as
primates found in urban environments typically produce more offspring (twins)
than non-urban primates, bat species commonly found in urban environments also
produce larger litters than non-urban bats [e.g. two pups (noctule bats, Nyctalus
spp., and pipistrelle bats, Pipistrellus spp.) and up to four pups (hairy-tailed bats,
Lasiurus spp.) [5]]. That said, some commonly cited “synanthropic” bat species
such as little brown myotis (Myotis lucifugus [18]), big brown bats (Eptesicus fus-
cus [19]), and greater short-nosed fruit bats [Cynopterus sphinx (see Chap. 5)] may
have lower reproductive success (but note the trends are not always straightforward)
when compared to populations of non-urban conspecifics. It is difficult to determine
age at weaning for bats because volant juveniles may continue to nurse, but timing
of parturition and age at volancy could be suitable proxies. Parturition is earlier in
urban P. kuhlii compared to non-urban conspecifics, which the authors suggest may
improve recruitment by increasing juvenile survival and allowing females to breed
in their first year [3]. Timing of weaning/fledging was not recorded in this study;
thus, it is not clear if earlier parturition also means earlier fledging. In some years,
weaning occurs later resulting in a longer lactation period in urban M. lucifugus
compared to conspecific non-urban populations [18], which is consistent with
urban-dwelling carnivores and rodents and may facilitate brain development and
learning [5].
184 K. J. Patriquin et al.

Mammals, including bats, may overcome some of the challenges of urban living
through behavioural flexibility that allows them to tolerate risk and disturbance bet-
ter than their non-urban equivalents [5, 9]. Generalist bat species, like molossid
species and E. fuscus, have adjusted to habitat loss by living in artificial structures
and foraging in a variety of patches of green space [[15] (see Chaps. 3, 6, and 8)].
Just as diet diversity has allowed a variety of carnivores (Carnivora) and ungulates
(Cetartiodactyla) to persist in urban environments [5], urban R. aegyptiacus have
broader diets that include the diverse fruits typically planted in urban areas and not
found in the diets of rural conspecifics [10]. By contrast, specialists [e.g. P. subfla-
vus and northern myotis (M. septentrionalis)] only occur in urban areas where they
can access patches of high-quality habitat [1, 11–15, 20]. Santini et al. speculated
that behavioural plasticity is related to relatively larger brains typical of many
urban-dwelling mammals, including bats [5].

3 Impacts of Urban Environments on Hibernation

and Migration

Like many mammals, bats in seasonal, semi-tropical, or temperate habitats face

periods of reduced food availability and increased thermoregulatory costs due to
changes in ambient conditions. In response, some urban-dwelling mammals (e.g.
rodents, hedgehogs, and some carnivores) build up fat stores and cache food to
remain active during these periods, while others, including bats, rely on accumu-
lated fat stores for hibernation and migration [21–23]. Arousal from hibernation is
energetically expensive and may be triggered by human disturbance [21], so bats
hibernating in urban areas (e.g. E. fuscus, in buildings) may be more subject to dis-
turbance than those hibernating in rural areas. Bats can minimise these risks by
migrating short distances to hibernacula outside urban areas or longer distances to
winter roosts [24]. Occupation of urban areas may therefore be seasonal for many
bat species.
Migration and hibernation  phenologies are being disrupted by climate change
and urban heat islands (UHIs), which are also interacting to affect local weather
patterns (e.g. temperature and precipitation) so that urban winters are now warmer
compared to adjacent rural areas (e.g. [25]). As a result, urban populations of some
highly mobile animals that normally migrate, including several birds [e.g. American
goldfinch (Spinus tristis), European starling (Sturnus vulgaris), evening grosbeak
(Coccothraustes vespertinus), and purple finch (Haemorhous purpureus)], now live
in urban areas year-round [26]. Recent reports from Europe suggest the same may
be true for bats (e.g. Nyctalus spp.) that normally migrate long distances but are now
detected year-round in some urban areas [27]. Whether the same is true of other
urban bats remains to be tested. The fitness consequences of these shifts have also
yet to be examined but warrant careful examination.
13  The Big Picture and Future Directions for Urban Bat Conservation and Research 185

4 How Can We Support Urban Bats?

There are measures we can take to reduce the challenges faced by urban-dwelling
bats, although some of the available tools have not yet been rigorously evaluated.
Incorporating more green spaces into urban areas, including forested parks, tree-­
lined roads, and blue spaces, would buffer urban noise, offset UHIs, create commut-
ing corridors, and provide possible roosting and foraging habitat (see Chaps. 7 and
8). Bat boxes can potentially replace lost natural and artificial roosts and enhance
existing habitat (see Chap. 6). The use of diverse green space configurations and bat
box designs should be investigated to accommodate foraging and roosting needs for
a variety of species (see Chaps. 6, 7, and 8). In some countries, federal and munici-
pal efforts are in place to improve urban canopy cover by limiting loss of existing
trees and planting new ones [28], which could benefit bats. However, most targets
involve planting young trees, which offer fewer benefits to bats that typically roost
in, and forage among, older, mature trees. Citizen engagement is also key to sup-
porting urban bat populations, but the most effective pathways to engagement
depend on cultural context (see Chap. 10). Although most negative perceptions of
bats are unfounded, there is legitimate concern around disease transmission (see
Chap. 11). Educating the public about how to limit risks and the value of urban-­
dwelling bats is therefore key to supporting bat conservation in urban areas (see
Chaps. 10, 11, and 12). Fortunately, there is some demand for more natural green
spaces in cities so that meeting these demands may coincidentally support the needs
of urban-dwelling bats. For example, a survey of 25,000 park staff from 27 Canadian
cities revealed that 70% of cities are seeing higher demands for more natural green
spaces to support biodiversity [28]. There are also an increasing number of conser-
vation and stewardship efforts in Australia, Europe, and North America targeting
urban bats specifically, including providing replacement habitat for bats upon evic-
tion, public education, and other community-wide efforts such as citizen science or
volunteering opportunities (see Chaps. 6, 10, 11, and 12). The question remains if
these measures will translate to fitness benefits (i.e. survival and reproductive suc-
cess) for bats and how this might vary across species. By contrast, bats are often
considered a nuisance and receive little conservation support in much of the south-
ern hemisphere, which may account for the relative dearth of work investigating
urban-dwelling bats in these areas (see Chap. 10; [29]).

5 Future Directions for Research and Defining

Urban Environments

Given the varied responses of bats to urbanisation, more studies are needed in
regions underrepresented in the ecological literature, like much of the southern
hemisphere. Future studies should present long-term, comparative data across spe-
cies, as well as between urban and non-urban populations, and specific demographic
186 K. J. Patriquin et al.

groups within a population – including more detailed accounts of reproductive phe-

nology. We also need measures of individual and lifetime reproduction, along with
estimates of genetic diversity, to determine if urban areas are stable environments
for bats or act as ecological traps. More studies of bat responses across an urban
gradient (along with better defining “urban” – see below) would help predict bat
responses to urban sprawl. A meta-analysis of five studies found bat activity was
much lower in “intermediate” urban developments [1], where parasite loads also
appear to be higher (see Chap. 4). We also need specific data about movements and
patterns of habitat use across a large sample of individual bats, both urban and
non-urban.
Captures in mist nets or harp traps, as well as traditional radio-tracking and
acoustic monitoring, typically offer a snapshot of habitat use by bats but do not
provide the fine details we need about what aspects of habitats are vital to bats.
However, when used together, they can provide surprising details about habitat
needs, as seen for the 7-g M. septentrionalis found roost-switching among mature
trees in a 348-ha urban woodlot, as well as foraging in the woodlot and in a marsh
<1 km away [20]. Automated telemetry across a network of receiving towers, such
as the Motus Wildlife Tracking System, offers great potential for more detailed
accounts of habitat use, including the 28 bat species currently being tracked (for
more, visit Motus). GPS tracking systems, such as ATLAS and Icarus, provide
nearly real-time tracking of animals and have provided detailed insight into the
movements of R. aegyptiacus, revealing their use of cognitive maps (i.e. mental
representations of space) to locate food and roost resources in an urban area and
adjacent rural areas [30, 31]. Precise details of habitat use may provide a clear indi-
cation of how different urban stressors influence bats and how this could vary among
species.
Where possible, explicit definitions of “urban” would be helpful as they are often
absent from studies or inconsistent among studies, creating ambiguity and limiting
potential for meaningful comparisons. Urban environments are often defined by
“extreme” habitat modification created by impervious or built-up land, resulting in
habitat loss, degradation, and fragmentation, as well as reduced biodiversity [1, 15].
How we define “urban” influences how we identify the boundaries between urban
and non-urban environments, as well as estimates of urban population numbers (for
a more detailed discussion, visit Urbanization - Our World in Data). Certainly, this
is less concerning for qualitative comparisons across studies or for comparisons of
populations or species within a single study. However, clearer definitions are needed
if we are to compare responses across urban gradients and across taxa. Clear defini-
tions are also needed when making predictions about how wildlife will respond to
urbanising areas and to inform best practices for management. Similar consider-
ations should be given to defining “green” or “natural” spaces in studies where these
labels are used to denote a particular habitat type for comparison of bat diversity,
activity, or fitness.
13  The Big Picture and Future Directions for Urban Bat Conservation and Research 187

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Index

A Cognitive Hierarchy Theory, 141

Aeroconservation, 96 Community-driven conservation, 87
Aeroecology, 96 Conservation action, 69
Anthropogenic urban infrastructure, 96 Cynopterus brachyotis, 23–28, 170, 174
Artificial light at night (ALAN), 5, 6, 96, 99,
100, 103, 125, 127, 160
Artificial roosts, 10, 76–78, 86, 88, 89, 110, D
144, 185 Drinking, 4, 7, 13–15, 55, 101, 109,
Attitudes, 140–143, 148–150, 158 112, 116

B E
Bat-borne viruses, 155 Ecosystem services, 143, 148, 158, 168–178
Bat box, 76–89, 110, 144–146, 185 Ectoparasites, 44, 46–53, 57
Bat house, 76 Endoparasites, 44, 46, 53–57
Behavioural plasticity, 34, 184
Bioacoustics, 125, 130
Biodiversity, 20, 23, 26, 46, 47, 53, 57, 62, 68, F
69, 99, 100, 124, 125, 127, 133, 140, Fast-flying bats, 34, 39
168, 169, 175, 176, 185, 186 Foraging, 4–15, 23, 33–40, 44, 46, 54, 56, 57,
Blue space, 108–117, 185 69, 82, 89, 97–100, 102, 103, 108–117,
Bottleneck, 26, 27, 156 133, 160, 169, 170, 173, 176,
182, 184–186

C
Chiroptera, 21, 157, 169 G
Cities, 4, 5, 7–10, 12, 14, 15, 23, 34–36, 38, Genomic diversity, 23, 24
44–46, 48–50, 52, 53, 56–58, 64, 76, Green space, 9, 23, 101, 108–116, 124–126,
83, 97–102, 108–117, 124, 125, 127, 132, 140, 144, 145, 163, 172, 182,
128, 130–132, 140–150, 155–161, 163, 184, 185
169, 170, 173, 175, 176, 182, 183, 185 Green urban remnants (GR), 126

© The Editor(s) (if applicable) and The Author(s), under exclusive license to 189
Springer Nature Switzerland AG 2022
L. Moretto et al. (eds.), Urban Bats, Fascinating Life Sciences,
https://doi.org/10.1007/978-3-031-13173-8
190 Index

H Research directions, 117, 169

Habitat, 4–10, 12, 14, 20–22, 26–28, 33, 35, Roost energetics, 10, 12
44, 50, 53–58, 62–69, 76–89, 96–103,
108–111, 113–117, 124, 125, 127, 130,
131, 140, 145, 154, 156, 159, 168, 169, S
172, 173, 175, 176, 182–186 Seed dispersal, 148, 168, 169, 172–176
Human-wildlife conflict, 154–164 Social system, 37, 38, 40, 62, 63, 68
Spillover, 154–159, 162–164
Stress physiology, 4–15
I Synanthropes, 45, 154, 157, 162
India, 64
Insectivory, 11, 13, 168–172
U
Urban airspace, 96, 98, 99
L Urban exploiters, 34
Lesser short-nosed fruit bat, 23, 25, 27 Urban fauna, 132
Urban gradient, 46, 50, 58, 173, 186
Urbanisation, 4–7, 20–23, 26–28, 33, 34, 40,
M 44–57, 62–64, 68, 69, 124–133, 154,
Molossidae, 9, 34, 126, 128 156, 168, 173, 175, 176, 182–185
Urbanites, 140–146, 148–150, 156–161, 170,
175, 176
N Urban landscapes, 37, 39, 63, 69, 82, 89, 113,
Noise and light pollution, 4, 49, 102, 182 114, 116, 117, 131, 132, 168
Urban mammals, 168
Urban syndrome, 182
O
Overheating, 76, 83–86, 88, 182
V
Vectors, 47, 50, 54, 172, 176
P
Pollination, 28, 147, 148, 168, 169,
172–176, 178 W
Preadaptation, 4, 9, 13, 15, 34, 37, 39 Water balance, 4, 10, 13–15
Wildlife disease, 154, 155, 158

R
Reproductive success, 8, 63, 64, 68, 69, 76, Z
78, 79, 81, 182, 183, 185 Zoonoses, 46, 47, 155, 164