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13
Chapter 2
Urbanisation and Its Effects
on Bats—A Global Meta-Analysis
Kirsten Jung and Caragh G. Threlfall
© The Author(s) 2016
C.C. Voigt and T. Kingston (eds.), Bats in the Anthropocene: Conservation
of Bats in a Changing World, DOI 10.1007/978-3-319-25220-9_2
Abstract Urbanisation is viewed as the most ecologically damaging change to
land use worldwide, posing significant threats to global biodiversity. However,
studies from around the world suggest that the impacts of urbanisation are not
always negative and can differ between geographic regions and taxa. Bats are a
highly diverse group of mammals that occur worldwide, and many species per-
sist in cities. In this chapter, we synthesise current knowledge of bats in urban
environments. In addition, we use a meta-analysis approach to test if the general
response of bats depends on the intensity of urbanisation. We further investigate
if phylogenetic relatedness or functional ecology determines adaptability of spe-
cies to urban landscapes and if determining factors for urban adaptability are con-
sistent worldwide. Our meta-analysis revealed that, in general, habitat use of bats
decreases in urban areas in comparison to natural areas. A high degree of urbani-
sation had a stronger negative effect on habitat use compared to an intermediate
degree of urbanisation. Neither phylogenetic relatedness nor functional ecology
alone explained species persistence in urban environments; however, our analy-
sis did indicate differences in the response of bats to urban development at the
family level. Bats in the families Rhinolophidae and Mormoopidae exhibited a
negative association with urban development, while responses in all other fami-
lies were highly heterogeneous. Furthermore, our analysis of insectivorous bats
K. Jung (*)
Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm,
Ulm, Germany
e-mail: kirsten.jung@uni-ulm.de
C.G. Threlfall (*)
School of Ecosystem and Forest Sciences, University of Melbourne,
Melbourne, Australia
e-mail: caragh.threlfall@unimelb.edu.au
14 K. Jung and C.G. Threlfall
revealed that the adaptability of individual families, e.g. Emballonuridae and
Vespertilionidae, to urbanisation is not consistent worldwide. These results sug-
gest that behavioural and/or morphological traits of individual species may better
determine species’ adaptability to urban areas, rather than phylogenetic or func-
tional classifications, and that driving factors for species adaptability to urban
areas might be regionally divergent. We thus argue that future research should
focus on behavioural and morphological traits of bats, to assess if these determine
urban adaptability in this species-rich group of mammals.
2.1 Introduction
2.1.1 The Urban Context
Urbanisation results in extreme forms of land use alteration (Shochat et al. 2006;
Grimm et al. 2008). In the last century, the human population has undergone a
transition in which the majority of people now live in urban rather than rural areas
(UNPD 2012). The rate of change at which urban areas are evolving due to natural
population growth is dramatic, including significant rural-to-urban migration and
spatial expansion (Grimm et al. 2008; Montgomery 2008; UN 2012; McDonnell
and Hahs 2013). In the last 50 years, the global human population in urban
areas increased from 2.53 to 6.97 billion people (UNPD 2012). Yet human pres-
sure resulting from urbanisation is not uniformly distributed on the planet. While
urbanisation in the developed countries is slowing down slightly, it is increasing
rapidly in developing countries of Asia, Africa, Latin America and the Caribbean,
many of which harbour hotspots of biodiversity (Myers et al. 2000). In addition,
over half of the urban population growth is projected to occur in smaller towns
and cities (UN 2012). This implies that urbanisation is not a locally concentrated
event, it is rather a fundamentally dispersed process and a happening worldwide
(McDonald 2008).
The ecological footprint of cities reaches far beyond their boundaries
(McGranahan and Satterthwaite 2003; McDonald and Marcotullio 2013). Effects
of cities operate from local (e.g. through urban sprawl) to global scales (e.g.
through greenhouse gas emission) (McDonald et al. 2008), and act both directly,
through expansion of urban areas, and indirectly through growth in infrastructure
and changes in consumption and pollution (McIntyre et al. 2000; Pickett et al.
2001). Apart from the obvious loss in natural area, expansion of cities also impacts
the surrounding rural and natural habitats through increased fragmentation, and
edge effects with increasing temperature and noise levels, which together intro-
duce new anthropogenic stressors on fringe ecosystems (Grimm et al. 2008) and
nearby protected areas (McDonald et al. 2008; McDonald and Marcotullio 2013).
However, despite the radical land transformation and habitat loss incurred through
urbanisation, many species (native and introduced) can still persist in urban envi-
ronments and some even experience population increases (McKinney 2006). This
15
2 Urbanisation and Its Effects on Bats—A Global Meta-Analysis
suggests that urban landscapes can actually provide suitable habitat for a variety of
species, albeit an anthropogenically altered habitat. Nevertheless, our understand-
ing of what constitutes a suitable habitat in urban areas and what determines a spe-
cies’ adaptability to an urban environment is currently very limited.
Generally, urban areas are characterised by high quantities of impervious sur-
faces (McKinney 2002). There are however many additional physical and chemi-
cal changes incurred via the process of urbanisation (McDonnell and Pickett
1990), such as increased pollution, eutrophication, increased waste generation,
altered hydrology (Vitousek et al. 1997; Grimm et al. 2008), increased urban noise
(e.g. Slabbekoorn and Ripmeester 2008) and artificial light (Longcore and Rich
2004). Urban areas can provide a more thermally stable environment via the urban
heat island effect (e.g. Zhao et al. 2006); less radiation is reflected during the day
and more heat is trapped at night, which can increase minimum temperatures in
cities (Grimm et al. 2008). The changed climate profile of cities can benefit some
species by making the area more inhabitable year round. In addition, the planting
of attractive introduced and native plant species throughout the suburbs and along
city roads also changes the resources available to fauna, for example by provid-
ing nectar or fruits throughout the year. Altogether these changes can impact local
species assemblages within cities and regional biodiversity beyond the municipal
boundaries (Grimm et al. 2008).
Anthropogenic changes in urban ecosystems typically occur at rates drastically
faster than long-lived organisms are capable of adapting to, and thus disrupt eco-
logical processes that historically governed community structure (Duchamp and
Swihart 2008). However, generalisations about the negative effects of urbanisation
should not overlook biologically meaningful differences in how taxa respond to
human land use (Dixon 2012). Some wildlife species are able to adjust to a life in
urban areas. Among vertebrates, a range of birds are relatively abundant in urban
environments and bird species richness may peak at intermediate levels of urbani-
sation because of increased heterogeneity of edge habitats (Blair 2001; McKinney
2002) and changes in resource availability due to provision of artificial feed-
ing stations (Sewell and Catterall 1998). In contrast, only a few mammals have
been documented as successful species in urban areas (Macdonald and Newdick
1982; Septon et al. 1995; Luniak 2004). For example, the grey-headed flying fox
(Pteropus poliocephalus) has established a year-round camp in urban Melbourne,
Australia, an area outside of its normal climatic range. Warmer temperatures from
the urban heat effect, enhanced precipitation from local irrigation and year-round
food resources appear to have facilitated the colony’s arrival and persistence
(Parris and Hazell 2005). Many animals, however, disappear from cities because
they depend on habitat features that no longer exist (Gilbert 1989; McKinney
2002; Luniak 2004; Haupt et al. 2006; McDonnell and Hahs 2008). Declining spe-
cies often suffer from increased habitat isolation, or face competition from inva-
sive and more dominant species (McDonald and Marcotullio 2013). Some species
in urban areas also suffer from additional stress (Isaksson 2010), increased infec-
tion and parasitism rates (Giraudeau et al. 2014) and reductions in potential repro-
ductive success (Chamberlain et al. 2009). Urbanisation can also trigger a change
16 K. Jung and C.G. Threlfall
in behaviour (Ditchkoff et al. 2006; Grimm et al. 2008). For example, urban
noise alters the pitch at which some birds call (Slabbekoorn and Peet 2003), and
affects activity patterns of larger vertebrates (Ditchkoff et al. 2006). Furthermore,
increased artificial lighting can potentially disturb the circadian rhythms of noctur-
nal animals and interfere with the navigation of migrating species (Longcore and
Rich 2004; Hölker et al. 2010; see Rowse et al., Chap. 7 this volume).
2.1.2 Urban Wildlife
Persistence of wildlife in urban environments may be linked to opportunism and
a high degree of ecological and behavioural plasticity (Luniak 2004). In contrast,
species that decline in response to urbanisation are often habitat and resource
specialists (McKinney and Lockwood 1999; Jokimäki et al. 2011). Typically this
results in altered assemblage structures in urban environments, often with a few
highly abundant species, which account for a much higher proportion of the whole
community in urban environments than in surrounding wild lands (Shochat et al.
2006). In addition, many native species are replaced by non-native, weedy or pest
species (McKinney 2002). The resulting mix of introduced and native species in
urban areas can lead to novel species interactions and altered ecosystem function-
ing (Hobbs et al. 2006). Often these non-native and introduced species are the
same species across cities throughout the world. Thus, the flora and fauna of cities
are becoming increasingly homogeneous (Hobbs et al. 2006; Grimm et al. 2008),
however recent evidence suggests that many cities still retain several endemic spe-
cies (Aronson et al. 2014).
Multi-scaled and multi-taxa investigations are required to provide detailed
information about urban biodiversity (Clergeau et al. 2006). To date, urban ecolo-
gists have focused on few taxa, examining the response of conspicuous species
to an urbanisation gradient (McDonnell and Hahs 2008). Population- and assem-
blage-level responses to urbanisation have been examined most prolifically for
highly diverse and mobile bird taxa (McKinney 2002; McDonnell and Hahs 2008).
Unfortunately, our understanding of how other wildlife, including bats, respond
to the complex process of urbanisation is still limited (Barclay and Harder 2003).
Research conducted to date provides a general indication that many bats may be
declining due to urbanisation, however an understanding of the processes driving
these patterns remains largely unknown.
2.1.3 Bats in Urban Environments
Bats likely form the most diverse group of mammals remaining in urban areas
(van der Ree and McCarthy 2005; Jung and Kalko 2011). Of the studies con-
ducted in urban landscapes to date, many show that overall bat activity and
17
2 Urbanisation and Its Effects on Bats—A Global Meta-Analysis
species richness are greatest in more natural areas, and decreases with increas-
ing urban influence (Kurta and Teramino 1992; Walsh and Harris 1996; Gaisler
et al. 1998; Legakis et al. 2000; Lesiñski et al. 2000). However, certain bat species
may better be able to adapt to urban landscapes (Avila-Flores and Fenton 2005;
Duchamp and Swihart 2008). Coleman and Barclay (2011), however, cautioned
that most researchers have worked in forested regions directing less attention to
other biomes, including grasslands. They argue that because urban tree cover is
fairly constant (<30 %) in all cities (McKinney 2002), urbanisation in tree-rich
regions implies deforestation and thus reduced tree cover may cause the nega-
tive effect of urbanisation. In contrast, urban areas within grassland regions might
enhance structural heterogeneity and thus benefit species richness and relative
abundance patterns (see Coleman and Barclay 2011 for more details). This is in
accordance with the results of Gehrt and Chelsvig (2003, 2004) investigating the
response of bats in and around the highly populated city of Chicago, USA. Here
species diversity and occurrence were higher in habitat fragments within urban
areas than in similar fragments in rural areas (Gehrt and Chelsvig 2003, 2004).
However the large, forested parks in the region may offset the habitat loss caused
by urbanisation, and hence they mitigate any negative impacts to bats at the
regional scale.
The majority of studies on bats in urban environments come from the temper-
ate regions of Europe and North America. Many studies focus on the response of
bats to differently structured areas within the urban environment including historic
and newly built city districts (Gaisler et al. 1998; Legakis et al. 2000; Guest et al.
2002; Dixon 2012; Hale et al. 2012; Pearce and Walters 2012), illuminated and
non-illuminated areas (Bartonicka and Zukal 2003), industrial areas (Gaisler et al.
1998) small and larger parklands (Kurta and Teramino 1992; Fabianek et al. 2011;
Park et al. 2012) and areas that receive waste water (Kalcounis-Rueppell et al.
2007). Most of these studies report relatively high bat activity and species richness
in areas with remaining vegetation such as older residential areas, riverine habitats
or parklands. Certain bat species appear to thrive in these urban environments, and
success has been linked to species-specific traits (Duchamp and Swihart 2008). In
particular, bat species with high wing loadings and aspect ratios, so presumed to
forage in open areas (Norberg and Rayner 1987), which also roost primarily in
human structures appeared to adjust to urban environments, provided that there is
sufficient tree cover (Dixon 2012). Many of these studies imply that protecting and
establishing tree networks may improve the resilience of some bat populations to
urbanisation (Hale et al. 2012). Population- and assemblage-level responses along
gradients of urbanisation reveal that generally foraging activity of bats seems to
be higher in rural and forested areas than in urban areas (Geggie and Fenton 1985;
Kurta and Teramino 1992; Lesiñski et al. 2000). However, it is important to note
that some species might be highly flexible in their habitat use. The European bat
Eptesicus nilsonii, for example, spends a much higher proportion of its foraging
time in urban areas after birth of the juveniles than before (Haupt et al. 2006). This
raises the importance of repeat observations during different seasons when investi-
gating the response of bats to urbanisation.
18 K. Jung and C.G. Threlfall
In the Neotropics, most studies concerning bats and environmental disturbance
have concentrated on fragmentation effects due to logging or agricultural land use
(e.g. García-Morales et al. 2013). Persistence of bats in fragmented landscapes
has been associated with edge tolerance and mobility in phyllostomids (Meyer
and Kalko 2008), and the predominant use of open space as foraging habitat for
aerial insectivorous bats (Estrada-Villegas et al. 2010). Of the few studies focus-
ing on urban areas, most report an overall decrease in species richness and rela-
tive abundance of bats in urban areas (Avila-Flores and Fenton 2005; Siles et al.
2005; Pacheco et al. 2010; Jung and Kalko 2011) compared to forested areas.
Predominantly, insectivorous bats seem to remain in large urban environments
(Bredt and Uieda 1996; Filho (2011). Of these, it is typically members of the
Molossidae, which are known to forage in the open spaces above the tree canopy
that seem to tolerate and potentially profit from highly urbanised areas (Avila-
Flores and Fenton 2005; Pacheco et al. 2010; Jung and Kalko 2011). In addition,
many buildings in cities provide potential roost sites that resemble natural crev-
ices (Burnett et al. 2001; Avila-Flores and Fenton 2005) and are known to be read-
ily occupied by molossid bats (Kössl et al. 1999; Scales and Wilkins 2007). In a
smaller urban setting in Panama, where mature forest meets very restricted urban
development, a high diversity of bats occurs within the town and bats frequently
forage around street lights (Jung and Kalko 2010). Nevertheless, even in such a low
impact urban setting some species of the bat assemblage such as Centronycteris
centralis revealed high sensitivity and were never recorded within the town, albeit
foraging frequently in the nearby mature forest (Jung and Kalko 2010).
Recent investigations from large metropolitan urban centres in Australia show
suburban areas can provide foraging habitat for bats (Rhodes and Catterall 2008;
Threlfall et al. 2012a), and support greater bat activity and diversity than more
urban and even forested areas (Hourigan et al. 2010; Basham et al. 2011; Threlfall
et al. 2011, 2012b; Luck et al. 2013). However, studies from regional urban cen-
tres in Australia suggest that any urban land cover, even if low-density residential,
can decrease bat activity and species richness (Hourigan et al. 2006; Gonsalves
et al. 2013; Luck et al. 2013), and can deter some species of clutter-tolerant bats
altogether (Gonsalves et al. 2013; Luck et al. 2013). Evidence also suggests that
species adapted to open spaces and edges, such as those within the molossid fam-
ily, do not display the same response to urbanisation in small regional versus
large metropolitan urban centres, indicating subtle behavioural differences among
species with similar ecomorphology (Luck et al. 2013; McConville et al. 2013a,
b). The few studies that have investigated species-specific foraging and roosting
requirements, suggest that although bats display high roost site fidelity within
urban areas (Rhodes and Wardell-Johnson 2006; Rhodes et al. 2006; Threlfall
et al. 2013a), species differ in their ability to forage successfully on aggregations
of insects across the urban matrix, reflecting variation in flight characteristics
and sensitivity to artificial night lighting (Hourigan et al. 2006; Scanlon and Petit
2008; Threlfall et al. 2013b).
Asian bat assemblages comprise a variety of frugivore and insectivore bat spe-
cies; however, there is limited information on urban impacts to bats in this region
19
2 Urbanisation and Its Effects on Bats—A Global Meta-Analysis
of the world. Many roosting and foraging resources for frugivore species such as
Cynopterus and Pteropus species are provided by exotic trees that grow easily in
urban centres in Asia, for example Ficus, Livistona and Syzygium species, which
have been studied in Hong Kong (Corlett 2005, 2006), India (Caughlin et al. 2012)
and Japan (Nakamoto et al. 2007). Frugivore species in these systems provide crit-
ical seed dispersal services and can play a role in regeneration and pollination of
some tree species (Mahmood-ul-Hassan et al. 2010; Caughlin et al. 2012). Radio-
tracking studies show that some bat species roost in forested areas (Nakamoto et al.
2012) or in-built structures (Nadeem et al. 2013), however many frugivore species
appear to profit from the density of planted exotic vegetation and both frugivore
and insectivore bats can benefit from increased foraging resources in urban areas
(Corlett 2005; Nakamoto et al. 2007; Utthammachai et al. 2008; Caughlin et al.
2012; Nakamoto et al. 2012). However, it appears that Asian bats, particularly large
pteropodids, are also under threat from direct human impacts via hunting (Thomas
et al. 2013), in addition to human land use alteration, and hence, any impact of
urbanisation may be confounded by direct human impacts. However, increasing
land use change and growing urban populations have been stated as a likely cause of
dramatic declines of many bat species (including pteropodids) in Singapore (Pottie
et al. 2005; Lane et al. 2006), where it is suggested the reported declines may reflect
the declining status of bats in Southeast Asia more broadly (Lane et al. 2006). The
only study to our knowledge that has examined bat species distribution in relation to
increasing urbanisation was conducted in Pakistan, where greater bat capture success
was recorded in urban areas in comparison to suburban and rural areas (Nadeem
et al. 2013), and in line with other studies worldwide, the urban bat assemblage was
dominated by a few common species. However, it is unclear whether these results
were influenced by trapping success, and as such, should be interpreted cautiously.
The co-location of biodiversity and high human population densities raises the
importance of conservation-related studies in urban areas where anthropogenic
growth directly interacts with the highest levels of biodiversity (Rompré et al.
2008). In these landscapes, it is especially important to identify the underlying
mechanisms determining the potential of different species to adjust to urban envi-
ronments. Currently, our general understanding of what influences a species suc-
cess and details of urban foraging and roosting habitat selection is incomplete. Yet,
arguably the conservation of species such as bats in urban areas dependents upon
this knowledge (Fenton 1997).
2.2 Evidence-Based Evaluation of the Effect
of Urbanisation on Bats Worldwide Using
a Meta-Analysis
Within this book chapter, we were in particular interested in the general conclu-
sions concerning the potential of bats to adjust to urban environments. We thus
synthesised pre-existing data of published literature with a focus on bats in urban
20 K. Jung and C.G. Threlfall
versus natural environments in a worldwide meta-analysis. Meta-analysis has been
previously used in ecology and conservation because results can lead to evidence-
based environmental policies.
Here, we investigated the general response of bats to urbanisation and tested
whether this is consistent across cities differing in the intensity of urban devel-
opment. In addition, we address the question of whether adaptability of spe-
cies to urban landscapes correlates with phylogeny or rather functional ecology.
Functional ecology of species can be linked to species traits, where traits refer
to morphological, behavioural or physiological attributes of species (Violle et al.
2007). Using such functional traits can improve understanding of and help predict
how species respond to environmental change (Didham et al. 1996; Flynn et al.
2009), such as increasing urbanisation. A key challenge is to develop frameworks
that can predict how the environment acts as a filter by advantaging or disadvan-
taging species with certain traits. Urbanisation has been demonstrated to select
for, or against, species with specific response traits within flora and fauna com-
munities, including remnant grasslands (Williams et al. 2005), bat communities
(Threlfall et al. 2011) and bird communities (Evans et al. 2011). To more fully
understand and predict the impact of increasing urban land cover on urban bat
communities, the identification and investigation of traits across a variety of stud-
ies in urban landscapes worldwide may prove useful. To do this, we investigated
the response of bats to urbanisation using a functional ecology approach and fur-
ther investigated if these mechanisms are consistent worldwide and thus separately
analysed the compiled literature for America (North and South America com-
bined) versus Europe, Asia and Australia. Based on previous studies in urban and
other human disturbed landscapes, we expected that predominant food item (fruits,
nectar and insects), foraging mode (aerial, gleaning) and foraging space (narrow,
edge and open, following Schnitzler and Kalko (2001)) may impact upon a spe-
cies ability to adapt to urban environments, as suggested by (e.g. Avila-Flores and
Fenton 2005; Jung and Kalko 2011; Threlfall et al. 2011)
2.2.1 Data Acquisition and Meta-Analysis
We used the Web of Knowledge (Thomson Reuter) to search for publications con-
taining the following key words “bats” AND, “urban”, “urbanis(z)ation”, AND
“gradient”, “community”, “assemblage”, “species composition”. This resulted in
99 studies reporting bat responses to urbanisation. In addition, we searched the
reference list of these publications for further relevant articles. We compiled all
studies focusing on bats in urban areas in our primary dataset. This selection
also including different bat inventory methods such as acoustic monitoring, mist
net and harp trap sampling as well as visual observations and roost surveys. In
many of these articles however, quantitative data on bats were missing, sampling
effort was not standardised, or studies did not reciprocally sample bats in urban
versus natural areas. We excluded all of these studies from our final dataset, as it
21
2 Urbanisation and Its Effects on Bats—A Global Meta-Analysis
was impossible to calculate a standard effect size of urbanisation. We thus only
included studies into our final meta-analysis that reported species-specific data
on capture success, roosting individuals, occurrence counts or activity per sam-
pling time in both urban and natural areas (Table 2.1). In a few cases, we extracted
data from graphs. We considered all of these measures as indicators of the rela-
tive intensity of habitat use and thus assumed comparability of these datasets and
hence eligibility to be combined in a meta-analysis. Our final data set for the meta-
analysis consisted of 23 articles (Table 2.1) and 96 bat species. Within this dataset
we discriminated between studies with high (N = 5) and intermediate intensity
(N = 5) of urbanisation following the individual authors’ statements in their arti-
cles (Table 2.1). Our designation of ‘high’ and ‘intermediate’ was qualitative and
based on descriptions of the urban study area from the original papers. For exam-
ple, Avila-Flores and Fenton (2005) state that their study area of Mexico City is
one of the “largest and most populated cities in the world”, hence we assigned
this study a ‘high’ urban intensity. Gonsalves et al. (2013) state that no quantifica-
tion of urban intensity was made in their study, however they suggest that hous-
ing density in their study area was low and could be classified as suburban, hence
we assigned this study an ‘intermediate’ urban intensity. This classification is by
no means comprehensive, however we believe for comparative purposes these two
classifications give some indication and context of the intensity of urban devel-
opment in the study area for each study used. Some articles (N = 13) reported
the response of bats to multiple intensities of urbanisation; here we extracted data
on the highest, the lowest and the intermediate degrees of urbanisation. Data from
urban parks, suburbia or small towns we considered as intermediate degrees of
urbanisation.
For each species reported in an article we compared the relative intensity of
habitat use in urban (treatment group) versus natural areas (control group) and cal-
culated the log odds ratio as a standardised effect size (Rosenberg et al. 2000).
A positive log odds ratio > 0 indicated species that showed a higher intensity of
habitat use in urban areas, while a negative log odds ratio < 0 indicated higher
intensity of habitat use in natural areas. For multiple reports on a species’ response
to urbanisation in distinct articles we averaged the log odds ratios to avoid pseu-
doreplication. Species with incomplete identifications were deleted from the data-
set, except for Mormopterus species 2 (Australia) which has not yet been formally
named (Adams et al. 1988) and Eumops sp. (Panama) which most likely includes
the two species Eumops glaucinus and Eumops auripendulus (Jung and Kalko
2011). For our analysis we thus considered each bat species (N = 96) as a study
case for our final meta-analysis models. For all statistical analysis, we used the
statistical software package R Version 2.1.4. (R Development Core Team 2011),
package “metafor” (Viechtbauer 2013) (version 1.6-0).
In a first approach, we focused on the general response of bats to urbani-
sation and investigated if the overall response of bats depends on the degree of
urbanisation. Hereby we distinguished between high and intermediate intensity of
urbanisation (see above) and calculated log odds ratios for the respective contrast
to natural areas. We then conducted a random effect model meta-analysis for the
22 K. Jung and C.G. Threlfall
Table 2.1 List of publications included in the meta-analyses
Reference Country Urban
intensity
Study type N species
urban
N species
suburban
N species
forest
Survey
method
Considered habitat
types
Avila-Flores and Fenton
(2005)
Mexico High Urban gradient 2 3 4 Acoustic
monitoring
Residential areas,
large parks, forest
Basham et al. (2010) Australia Intermediate Urban/forest NA 11 13 Acoustic
monitoring
Backyards, natural
bushland
Bihari (2004) Hungary High Urban/forest 1 NA 1 Roost survey Residential area,
forested park
Chirichella (2004) Italy High Urban gradient 1 1 1 Public survey Urban, suburban,
forest
Duchamp et al. (2004) USA High Urban/forest 2 NA 2 Captures/
telemetry
Urban, woods
Fabianek et al. (2011)Canada Intermediate Urban gradient NA 3 3 Acoustic
monitoring
Urban parks < 100 ha,
urban parks > 100 ha
Gaisler et al. (1998)Czech
Republic
High Urban gradient 2 2 2 Acoustic
monitoring
Historical city centre,
old suburbs, outskirts
Gehrt and Chelsvig (2004)USA High Urban gradient 5NA 4 Acoustic
monitoring
Urban index: 0
(urban) urban index:
−5 (rural)
Gonsalves et al. (2013)Australia Intermediate Urban/forest NA 9 13 Acoustic
monitoring
Small urban, forest
Hale et al. (2013) United
Kingdom
High Urban gradient 2 2 2 Acoustic
monitoring
Dense urban, subur-
ban, rural
Haupt et al. (2006)Germany High Urban/forest 1 NA 1 Captures/
telemetry
Urban areas, forest
(before and after birth
of juveniles
Hourigan et al. (2006)Australia Intermediate Urban gradient NA 8 8 Acoustic
monitoring
Intermediate suburbs,
woodland
Hourigan et al. (2010)Australia High Urban gradient 13 13 13 Acoustic
monitoring
High and low-density
residential, bush land
(continued)
23
2 Urbanisation and Its Effects on Bats—A Global Meta-Analysis
Given are the reference, the country where the study was carried out, the urban intensity (large or small) the study type (gradient, paired design), the number
of bat species reported by each author for each habitat type, the survey methodology of the original data and the considered habitat types included in the
meta-analysis. NA indicates that the corresponding study had no record of bats for the specified habitat type
Table 2.1 (continued)
Reference Country Urban
intensity
Study type N species
urban
N species
suburban
N species
forest
Survey
method
Considered habitat
types
Jung and Kalko (2010)Panama Intermediate Urban/forest NA 21 22 Acoustic
monitoring
Small town, forest
Jung and Kalko (2011)Panama High Urban gradient 16 21 25 Acoustic
monitoring
Urban, small town,
forest
Kurta and Teramino
(1992)
USA High Urban/forest 4 NA 5 Captures Urban/rural
Lesinski et al. (2000) Poland High Urban gradient 3 3 3 Acoustic
monitoring
Central,
suburban(III),
suburban(V)
Nadeem et al. (2013)Pakistan High Urban gradient 4 4 3 Roost surveys Urban, suburban,
rural dwelling
Pottie et al. (2005)Malaysia/
Singapore
High Urban gradient 5 5 12 Roost sur-
veys/captures/
acoustic
monitoring
City/urban, suburban,
primary forest
Silva et al. (2005) Brazil High Urban gradient 7 8 9 Acoustic
monitoring
Small farm, campus
Funcesi, forest
Threlfall et al. (2011,
2012)
Australia High Urban gradient 10 15 7 Acoustic
monitoring
Urban, suburban,
forest
Utthammachai et al.
(2008)
Thailand High Urban gradient 1 1 1 Acoustic
monitoring
Forest patch, village/
others, urban
Walters et al. (2007) USA High Urban/forest 1 1 1 Captures Woodlots, low-
density residential,
commercial lands
24 K. Jung and C.G. Threlfall
effect of high and intermediate urban development, respectively. Random effect
models provide an unconditional inference of a larger set of studies from which
only a few are included in the meta-analysis and assumed to be a random sample
(Viechtbauer 2010). We compared both models based on the reported effect size
and assessed the proportion of heterogeneity of bat responses between high and
intermediate urban development (τ2 highly urban- τ2 small urban/τ2 highly urban).
In a second approach, we pooled data from high and intermediate urbanisation
categories to investigate if the potential of bats to adjust to urban environments is
determined by phylogeny or rather functional ecology using a mixed model meta-
analysis. For this analysis we classified bats according to their taxonomic family
and genus, their predominant food item (fruits, nectar and insects), foraging mode
(aerial, gleaning) and foraging space (narrow, edge and open, following Schnitzler
and Kalko (2001)) and included these classifications as moderators in our mixed
model meta-analysis. We further investigated in detail how each of the categori-
cal moderators influences effect size. Further, focusing on aerial insectivores, the
majority of study cases in our dataset, we then investigated if moderators influ-
encing the adaptability to urban areas are consistent between North and South
America versus Europe, Asia and Australia. P-levels for all models were assessed
using a permutation test with 1000 randomizations. In none of our models did the
funnel plot technique (Viechtbauer 2013) reveal any significant publication bias or
asymmetry in our dataset (function: regtest, package metaphor).
2.2.2 High Versus Lower Levels of Urbanisation
Our random effect meta-analysis revealed that in general, urbanisation negatively
affects bats, and areas with high (deviance = 453.14, z-value = −3.9, p < 0.001)
and intermediate (deviance = 439.73; z-value = −2.4, p < 0.05) degrees of urban
development reveal significantly lower intensity of habitat use across species com-
pared to natural areas (Fig. 2.1). A high degree of urbanisation had a stronger
negative effect on the general intensity of habitat use (estimate: −1.47) than an
intermediate degree of urban development (estimate: −0.79). However, in both
high and intermediate urban development, we found significant variation in the
Effect size
-2,0 -1,5 -1,0 -0,5 0,0 0,5
Urbanisation (high)
Urbanisation (intemediate) -0.79 [-1.44, -0.13]
-1.47 [-2.19, -0.73]
Fig. 2.1 Effect sizes of relative intensity of habitat use by bats in high and intermediate urban
development, compared to natural areas. Solid symbols indicate the mean effect size (log odds
ratio) and whiskers indicate the estimated standard error. Values of the estimated effect size,
including the 95 % confidence intervals are listed on the right side of the figure
25
2 Urbanisation and Its Effects on Bats—A Global Meta-Analysis
effect sizes (high urban development: Q(df=84) = 641.2, p < 0.0001; intermedi-
ate urban development Q(df=85) = 989.9, p < 0.0001), indicating a high variabil-
ity in the response of bat species to urbanisation. This species-specific variability
in the intermediate degree of urbanisation (τ2 = 7.74) accounted for 21 % of the
variability in the areas with high urban development (τ2 = 9.80). This suggests that
although intermediate urban development clearly has a negative influence on bats it
still permits the use of this habitat by more species showing fewer extremes in the
species-specific response to urbanisation, compared to high urban development.
2.2.3 Phylogeny Versus Functional Ecology
Neither phylogeny (QM(df=3) = 11.57, p > 0.05) nor functional ecology
(QM(df=3) = 12.18, p > 0.05) explained the heterogeneity in bat response to
urbanisation. However, a different pattern emerged when investigating the effect
of single moderators in detail. Response to urbanisation differed between fami-
lies (QM(df =10) = 32.4, p = 0.05) with bat species in the Rhinolophidae being
negatively affected by urban development (p < 0.01). In addition, bat species in
the Mormoopidae tended to respond negatively towards urbanisation, as the 95 %
confidence interval did not overlap with zero. All other families revealed a high
heterogeneity in the response to urbanisation. Effect size was neither genera—
(QM(df=46) = 81.4, p > 0.05) nor species-specific (QM(df=86) = 99.7, p > 0.05).
Effect size
-4 -3 -2 -1 0123
Frugivore
Insectivore
Nectarivore
Edge space
Narrow space
Open space
Aerial
Gleaning
-0.99 [-3.44, 1.47]
-1.16 [-1.83, -0.43]
-0.16 [-4.44, 4.12]
-0.96 [-1.81, -0.10]
-2.55 [-4.18, -0.92]
-0.72 [-1.84, 0.40]
-1.05 [-1.73, -0.37]
-1.62 [-3.44, 0.21]
Fig. 2.2 Effect of urbanisation (log odds ratio and the estimated standard error) on relative
intensity of habitat use in relation to the predominant food item (a), foraging space (b), and
forag ing mode (c). Solid symbols indicate the mean effect size (log odds ratio) and whiskers
indicate the estimated standard error. Values of the estimated effect size, including the 95 % con-
fidence intervals are listed on the right side of the figure
26 K. Jung and C.G. Threlfall
None of the functional classifications, food item, foraging mode and foraging
space, revealed a significant association with the persistence of bats in urban areas.
However narrow space foragers (estimate −2.55 ± 0.83, p = 0.06) revealed a ten-
dency to be associated with natural areas (Fig. 2.2).
Europe, Asia, Australia
Effect size
-10 -8 -6 -4 -2 024
Emballonuridae
Megadermatidae
Miniopteridae
Molossidae
Nycteridae
Rhinolophidae
Vespertilionidae
RE Model
1.50 [-1.53, 4.52]
-3.22 [-9.50, 3.05]
1.42 [-6.78, 3.95]
-0.71 [-3.13, 1.70]
-2.20 [-8.56, 4.16]
-6.59 [-9.84,-3.33]
-0.00 [-1.17, 1.17]
-0.64 [-1.68, 0.39]
North- and South America
Effect size
-8 -6 -4 -2 024
Emballonuridae
Molossidae
Mormoopidae
Noctiliondae
Vespertilionidae
RE Model
-2.90 [-4.35, -1.44]
-0.74 [-1.86, 0.38]
-3.69 [-6.27, -1.11]
1.50 [-1.86, 4.86]
-2.01 [-3.28, -0.75]
-1.73 [-2.50, -0.96]
(a)
(b)
Fig. 2.3 Response of insectivorous bat families to urbanisation in a North and South America
and b Europe, Asia and Australia. A negative effect size reflects a higher association with nat-
ural areas, a positive effect size an association with urban areas. Depicted are the mean effect
sizes (log odds ratio) and the estimated standard errors by family. Values of the estimated effect
size, including the 95 % confidence intervals are listed on the right side of the figure. The overall
effect of urbanisation on insectivorous bats, based on the random effect model (RE Model), is
given at the bottom of the respective figure
27
2 Urbanisation and Its Effects on Bats—A Global Meta-Analysis
2.2.4 Contrasting the Effects between North
and South America and Europe, Asia
and Australia Focusing on Insectivores
The general response of insectivorous bats differed between the Americas and
Europe, Asia and Australia. While insectivorous bats in the Americas revealed a
significant negative response to urbanisation (deviance = 171.18, z-value = −4.4,
p < 0.001) the overall response of insectivorous bats to urbanisation in Europe,
Asia and Australia was insignificant (deviance = 258.9, z-value = −1.2, p > 0.05,
Fig. 2.3a, b).
However, in both the Americas (QM(df=5) = 35.1, p < 0.05) and Europe, Asia
and Australia (QM(df=7) = 18.7, p < 0.05) the response to urbanisation differed sig-
nificantly across families. Interestingly this family-level response was inconsistent
between the Neo- and Paleotropics. While Neotropical bats in the Emballonuridae
showed a strong tendency to be associated with natural areas (estimate:
−2.9 ± 0.7, p = 0.06), emballonurids in the Paleotropics (estimate: 1.5 ± 1.5,
p > 0.05) occurred frequently in urban areas. We found a similar trend in the glob-
ally distributed family of Vespertilionidae, which showed a higher association
with natural areas in the Americas (estimate: −2.0 ± 0.6, p > 0.05) but did not
reveal any clear association in Europe, Asia and Australia (estimate: −0.0 ± 0.6,
p > 0.05) (Fig. 2.3a, b).
2.3 Adaptability of Species to Urban Areas: General
Trends, Species-Specific Differences and Future
Research
Urban areas can provide suitable habitat for a variety of species, albeit an anthro-
pogenically altered habitat (McKinney 2006). However, our general understanding
of what influences a species’ success in urban environments is limited. Arguably
the conservation of species such as bats in urban areas is dependent upon this
knowledge (Fenton 1997). Within this book chapter, we reviewed the existing lit-
erature on bats in urban areas. In addition, we combined published data in a meta-
analysis to evaluate and derive general patterns in the response of bats to urban
development.
Our meta-analysis revealed that, in general, habitat use of bats decreases in
urban areas. A high degree of urbanisation had a stronger negative effect on
overall habitat use of bats compared to an intermediate degree of urban develop-
ment. However, habitat use in intermediate urban development was much lower
compared with natural areas. This is alarming, as it is generally thought that
small towns and suburban landscapes could potentially provide suitable habitat
for a wide range of species (McKinney 2006), including bats. The combination
28 K. Jung and C.G. Threlfall
of habitats with different complexity in smaller urban developments should lead
to greater complementarity at a local scale and should favour species diversity
and abundance. Some of the publications in our meta-analysis dataset indeed
report a higher bat diversity, activity (Hourigan et al. 2010; Threlfall et al. 2011,
2012b) and feeding activity (Jung and Kalko 2011; Threlfall et al. 2012a) at
intermediate levels of disturbance compared to natural or urban habitats. Other
studies reported that any urban land cover, even if low-density residential, can
decrease bat activity and species richness (Hourigan et al. 2006; Gonsalves
et al. 2013; Luck et al. 2013), and even deter individual species (Jung and Kalko
2010; Gonsalves et al. 2013; Luck et al. 2013). Altogether, this strongly sug-
gests regional differences in the intensity of urban development and points
towards an interacting effect of the surrounding landscape (see Coleman and
Barclay 2011).
Results from recent urban bat studies suggest that bats of some families (e.g.
molossids Jung and Kalko 2011) are better pre-adapted for life in an urban envi-
ronment compared to others (e.g. rhinolophids Stone et al. 2009; Threlfall et al.
2011). Our analysis also indicated a family-specific effect of urbanisation and con-
firmed the negative response of Rhinolophidae to urban development across the
Old World. However, the responses of Molossidae and Vespertilionidae, which are
known to frequently roost in man-made structures in North and South America,
did not reveal consistent associations with either urban or natural areas across con-
tinents. This might be due to the high morphological and behavioural heterogene-
ity within these families. We believe that the likely explanation for our results is
that the response to urbanisation is dictated by the behavioural and morphological
traits of species, regardless of geographic region or phylogeny. In particular, spe-
cies foraging in open space seem to persist in urban areas, as due to their wing
morphology (high aspect ratio and wing loading) they might be able to commute
large distances between roosting sites and feeding areas (Jung and Kalko 2011).
Thus traits predicting species mobility have been associated with urban tolerance
(Jung and Kalko 2011; Threlfall et al. 2012a), and the ability to forage around
street lights (see Rowse et al., Chap. 7 this volume). In addition, traits that allow
for flexible roost and foraging strategies confer an advantage for urban-tolerant
species. Our current results support these findings and thus suggest that adaptabil-
ity of bats to urban environments (or disturbance in general) might be correlated
with, and reflected by, species behavioural flexibility. Advancement of knowledge
in this area will assist with conservation efforts of bat species globally, and poten-
tially allow development of a predictive framework for assessing the impacts of
urban development on bats.
Open Access This chapter is distributed under the terms of the Creative Commons
Attribution Noncommercial License, which permits any noncommercial use, dis-
tribution, and reproduction in any medium, provided the original author(s) and
source are credited.
29
2 Urbanisation and Its Effects on Bats—A Global Meta-Analysis
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