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Urbanisation and Its Effects on Bats—A Global Meta-Analysis

  • Kirsten JungEmail author
  • Caragh G. ThrelfallEmail author
Open Access
Chapter

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 persist 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 species to urban landscapes and if determining factors for urban adaptability are consistent 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 urbanisation 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 analysis 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 families were highly heterogeneous. Furthermore, our analysis of insectivorous bats revealed that the adaptability of individual families, e.g. Emballonuridae and Vespertilionidae, to urbanisation is not consistent worldwide. These results suggest that behavioural and/or morphological traits of individual species may better determine species’ adaptability to urban areas, rather than phylogenetic or functional 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.

Keywords

Urban Environment Urban Development Natural Area Urban Landscape Urban Land Cover 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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 pressure 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 introduce 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 environments and some even experience population increases (McKinney 2006). This suggests that urban landscapes can actually provide suitable habitat for a variety of species, albeit an anthropogenically altered habitat. Nevertheless, our understanding of what constitutes a suitable habitat in urban areas and what determines a species’ adaptability to an urban environment is currently very limited.

Generally, urban areas are characterised by high quantities of impervious surfaces (McKinney 2002). There are however many additional physical and chemical 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 providing 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 ecological 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 urbanisation because of increased heterogeneity of edge habitats (Blair 2001; McKinney 2002) and changes in resource availability due to provision of artificial feeding 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 species often suffer from increased habitat isolation, or face competition from invasive and more dominant species (McDonald and Marcotullio 2013). Some species in urban areas also suffer from additional stress (Isaksson 2010), increased infection and parasitism rates (Giraudeau et al. 2014) and reductions in potential reproductive success (Chamberlain et al. 2009). Urbanisation can also trigger a change 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 nocturnal 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 functioning (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 species (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 ecologists have focused on few taxa, examining the response of conspicuous species to an urbanisation gradient (McDonnell and Hahs 2008). Population- and assemblage-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 conducted in urban landscapes to date, many show that overall bat activity and species richness are greatest in more natural areas, and decreases with increasing 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 negative 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 temperate 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 investigating the response of bats to urbanisation.

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 focusing on urban areas, most report an overall decrease in species richness and relative 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 crevices (Burnett et al. 2001; Avila-Flores and Fenton 2005) and are known to be readily 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 centres 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 family, 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 species; however, there is limited information on urban impacts to bats in this region 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 critical 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 environments. Currently, our general understanding of what influences a species success and details of urban foraging and roosting habitat selection is incomplete. Yet, arguably the conservation of species such as bats in urban areas is dependent 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 conclusions 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 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 development. In addition, we address the question of whether adaptability of species 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 disadvantaging species with certain traits. Urbanisation has been demonstrated to select for, or against, species with specific response traits within flora and fauna communities, 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 studies in urban landscapes worldwide may prove useful. To do this, we investigated the response of bats to urbanisation using a functional ecology approach and further investigated if these mechanisms are consistent worldwide and thus separately analysed the compiled literature for America (North and South America combined) 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 species 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 containing 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 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 sampling 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 relative 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 articles (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 example, 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 quantification of urban intensity was made in their study, however they suggest that housing 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 development 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.
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

5

NA

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, suburban, 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

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 surveys/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

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

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 calculated 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 pseudoreplication. Species with incomplete identifications were deleted from the dataset, 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 urbanisation 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 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 categorical moderators influences effect size. Further, focusing on aerial insectivores, the majority of study cases in our dataset, we then investigated if moderators influencing 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 compared 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 sizes (high urban development: Q (df=84) = 641.2, p < 0.0001; intermediate urban development Q(df=85) = 989.9, p < 0.0001), indicating a high variability in the response of bat species to urbanisation. This species-specific variability in the intermediate degree of urbanisation (τ 2 = 7.74) accounted for 21 % of the variability in the areas with high urban development (τ 2 = 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.
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

2.2.3 Phylogeny Versus Functional Ecology

Neither phylogeny (Q M(df=3) = 11.57, p > 0.05) nor functional ecology (Q M(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 families (Q M(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—(Q M(df=46) = 81.4, p > 0.05) nor species-specific (Q M(df=86) = 99.7, p > 0.05).

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 tendency to be associated with natural areas (Fig. 2.2).
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 foraging 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 % confidence intervals are listed on the right side of the figure

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).
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 natural 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

However, in both the Americas (Q M(df=5) = 35.1, p < 0.05) and Europe, Asia and Australia (Q M(df=7) = 18.7, p < 0.05) the response to urbanisation differed significantly 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 globally 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 anthropogenically 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 dependents upon this knowledge (Fenton 1997). Within this book chapter, we reviewed the existing literature 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 development. 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 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 suggests 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 environment 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 confirmed 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 continents. This might be due to the high morphological and behavioural heterogeneity 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, species 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 adaptability 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 potentially allow development of a predictive framework for assessing the impacts of urban development on bats.

References

  1. Adams M, Reardon T, Baverstock P, Watts C (1988) Electrophoretic resolution of species boundaries in Australian microchiroptera. IV. The Molossidae (Chiroptera). Aust J Biol Sci 41(3):315–326Google Scholar
  2. Aronson MFJ, La Sorte FA, Nilon CH, Katti M, Goddard MA, Lepczyk CA, Warren PS, Williams NSG, Cilliers S, Clarkson B, Dobbs C, Dolan R, Hedblom M, Klotz S, Kooijmans JL, Kühn I, MacGregor-Fors I, McDonnell M, Mörtberg U, Pyšek P, Siebert S, Sushinsky J, Werner P, Winter M (2014) A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc R Soc B Biol Scie 281(1780):20133330Google Scholar
  3. Avila-Flores R, Fenton B (2005) Use of spatial features by foraging insectivorous bats in a large urban landscape. J Mammal 86(6):1193–1204CrossRefGoogle Scholar
  4. Barclay RMR, Harder LD (2003) Life histories of bats: life in the slow lane. In: Kunz TH, Fenton B (eds) Bat ecology. The University of Chicago Press, Chicago, pp 209–253Google Scholar
  5. Bartonicka T, Zukal J (2003) Flight activity and habitat use of four bat species in a small town revealed by bat detectors. Folia Zool 52(2):155–166Google Scholar
  6. Basham R, Law B, Banks PB (2011) Microbats in a ‘leafy’ Sydney urban landscape: are they persisting, and what factors influence their presence? Austral Ecol (in press)Google Scholar
  7. Blair RB (2001) Birds and butterflies along urban gradients in two ecoregions of the U.S. In: Lockwood J, McKinney L (eds) Biotic homogenization. Kluwer, Norwell, pp 33–56Google Scholar
  8. Bredt A, Uieda W (1996) Bats from urban and rural environments of the Distrito Federal, mid-western Brazil. Chiroptera Neotropical 2(2):54–57Google Scholar
  9. Burnett SE, Jennings JB, Rainey JC, Best TL (2001) Molossus bondae. Mamm Species 668:1–5CrossRefGoogle Scholar
  10. Caughlin TT, Ganesh T, Lowman MD (2012) Sacred fig trees promote frugivore visitation and tree seedling abundance in South India. Curr Sci 102(6):918–922Google Scholar
  11. Chamberlain DE, Cannon AR, Toms MP, Leech DI, Hatchwell BJ, Gaston KJ (2009) Avian productivity in urban landscapes: a review and meta-analysis. Ibis 151(1):1–18CrossRefGoogle Scholar
  12. Clergeau P, Jokimäki J, Snep R (2006) Using hierarchical levels for urban ecology. Trends Ecol Evol 21(12):660–661CrossRefPubMedGoogle Scholar
  13. Coleman JL, Barclay RMR (2011) Influence of urbanization on demography of little brown bats (Myotis lucifugus) in the prairies of North America. PLoS ONE 6(5):e20483PubMedCentralCrossRefPubMedGoogle Scholar
  14. Corlett RT (2005) Interactions between birds, fruit bats and exotic plants in urban Hong Kong, South China. Urban Ecosyst 8(3):275–283CrossRefGoogle Scholar
  15. Corlett RT (2006) Figs (Ficus, Moraceae) in Urban Hong Kong, South China. Biotropica 38(1):116–121Google Scholar
  16. Didham RK, Ghazoul J, Stork NE, Davis AJ (1996) Insects in fragmented forests: a functional approach. Trends Ecol Evol 11(6):255–260CrossRefPubMedGoogle Scholar
  17. Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosyst 9(1):5–12CrossRefGoogle Scholar
  18. Dixon MD (2012) Relationship between land cover and insectivorous bat activity in an urban landscape. Urban Ecosyst 15(3):683–695CrossRefGoogle Scholar
  19. Duchamp J, Swihart R (2008) Shifts in bat community structure related to evolved traits and features of human-altered landscapes. Landscape Ecol 23(7):849CrossRefGoogle Scholar
  20. Estrada-Villegas S, Meyer CFJ, Kalko EKV (2010) Effects of tropical forest fragmentation on aerial insectivorous bats in a land-bridge island system. Conserv Biol 143:597–608CrossRefGoogle Scholar
  21. Evans KL, Chamberlain DE, Hatchwell BJ, Gregory RD, Gaston KJ (2011) What makes an urban bird? Glob Change Biol 17(1):32–44CrossRefGoogle Scholar
  22. Fabianek F, Gagnon D, Delorme M (2011) Bat distribution and activity in Montréal Island green spaces: responses to multi-scale habitat effects in a densely urbanized area1. Ecoscience 18(1):9–17CrossRefGoogle Scholar
  23. Fenton B (1997) Science and the conservation of bats. J Mammal 78(1):1–14CrossRefGoogle Scholar
  24. Filho HO (2011) Urban bats: aspects of ecology and health. In: Robinson WH, de Carvalho Campos AE (eds) Proceedings of the seventh international conference on urban pests, Instituto Biológico, São Paulo, BrazilGoogle Scholar
  25. Flynn DFB, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, Simpson N, Mayfield MM, DeClerck F (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12(1):22–33CrossRefPubMedGoogle Scholar
  26. Gaisler J, Zukal J, Rehak Z, Homolka M (1998) Habitat preference and flight activity of bats in a city. J Zool 244(3):439–445CrossRefGoogle Scholar
  27. García-Morales R, Badano EI, Moreno CE (2013) Response of Neotropical bat assemblages to human land use. Conserv Biol 27(5):1096–1106CrossRefPubMedGoogle Scholar
  28. Geggie J, Fenton B (1985) A comparison of foraging by Eptesicus fuscus (Chiroptera: Vespertilionidae) in urban and rural environments. Can J Zool 83:263–265CrossRefGoogle Scholar
  29. Gehrt SD, Chelsvig JE (2003) Bat activity in an urban landscape: patterns at the landscape and microhabitat scale. Ecol Appl 13(4):939–950CrossRefGoogle Scholar
  30. Gehrt SD, Chelsvig JE (2004) Species-specific patterns of bat activity in an urban landscape. Ecol Appl 14:625–635CrossRefGoogle Scholar
  31. Gilbert OL (1989) The ecology of urban habitats. Chapman & Hall, LondonCrossRefGoogle Scholar
  32. Giraudeau M, Mousel M, Earl S, McGraw K (2014) Parasites in the city: degree of urbanization predicts poxvirus and coccidian infections in house finches (Haemorhous mexicanus). PLoS ONE 9(2):e86747PubMedCentralCrossRefPubMedGoogle Scholar
  33. Gonsalves L, Lamb S, Webb C, Law B, Monamy V (2013) Do mosquitoes influence bat activity in coastal habitats? Wildlife Research 40(1):10–24CrossRefGoogle Scholar
  34. Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, Briggs JM (2008) Global change and the ecology of cities. Science 319(5864):756–760CrossRefPubMedGoogle Scholar
  35. Guest P, Jones KE, Tovey J (2002) Bats in greater London: unique evidence of a decline over 15 years. Br Wildl 14:1–5Google Scholar
  36. Hale JD, Fairbrass AJ, Matthews TJ, Sadler JP (2012) Habitat composition and connectivity predicts bat presence and activity at foraging sites in a large UK conurbation. PLoS ONE 7(3):e33300PubMedCentralCrossRefPubMedGoogle Scholar
  37. Haupt M, Menzler S, Schmidt S (2006) Flexibility of habitat use in Eptesicus nilssonii: does the species profit from anthropogenically altered habitats? J Mammal 87(2):351–361CrossRefGoogle Scholar
  38. Hobbs RJ, Arico S, Aronson J, Baron JS, Bridgewater P, Cramer VA, Epstein PR, Ewel JJ, Klink CA, Lugo AE, Norton D, Ojima D, Richardson DM, Sanderson EW, Valladares F, Vilà M, Zamora R, Zobel M (2006) Novel ecosystems: theoretical and management aspects of the new ecological world order. Glob Ecol Biogeogr 15(1):1–7CrossRefGoogle Scholar
  39. Hölker F, Wolter C, Perkin EK, Tockner K (2010) Light pollution as a biodiversity threat. Trends Ecol Evol 25(12):681–682CrossRefPubMedGoogle Scholar
  40. Hourigan CH, Johnson C, Robson SKA (2006) The structure of a micro-bat community in relation to gradients of environmental variation in a tropical urban area. Urban Ecosyst 9:67–82CrossRefGoogle Scholar
  41. Hourigan CL, Catterall CP, Jones D, Rhodes M (2010) The diversity of insectivorous bat assemblages among habitats within a subtropical urban landscape. Austral Ecol 35:849–857CrossRefGoogle Scholar
  42. Isaksson C (2010) Pollution and its impact on wild animals: a meta-analysis on oxidative stress. EcoHealth 7(3):342–350CrossRefPubMedGoogle Scholar
  43. Jokimäki J, Kaisanlahti-Jokimäki M-L, Suhonen J, Clergeau P, Pautasso M, Fernández-Juricic E (2011) Merging wildlife community ecology with animal behavioral ecology for a better urban landscape planning. Landscape Urban Plann 100(4):383–385CrossRefGoogle Scholar
  44. Jung K, Kalko EKV (2010) Where forest meets urbanization: foraging plasticity of aerial insectivorous bats in an anthropogenically altered environment. J Mammal 91(1):144–153CrossRefGoogle Scholar
  45. Jung K, Kalko EKV (2011) Adaptability and vulnerability of high flying Neotropical aerial insectivorous bats to urbanization. Divers Distrib 17(2):262–274CrossRefGoogle Scholar
  46. Kalcounis-Rueppell MC, Payne VH, Huff SR, Boyko AL (2007) Effects of wastewater treatment plant effluent on bat foraging ecology in an urban stream system. Biol Conserv 138(1–2):120–130CrossRefGoogle Scholar
  47. Kössl M, Mora E, Coro F, Vater M (1999) Two-toned echolocation calls from Molossus molossus in Cuba. J Mammal 80(3):929–932CrossRefGoogle Scholar
  48. Kurta A, Teramino JA (1992) Bat community structure in an urban park. Ecography 15:257–261CrossRefGoogle Scholar
  49. Lane DJW, Kingston T, Lee BPYH (2006) Dramatic decline in bat species richness in Singapore, with implications for Southeast Asia. Biol Conserv 131(4):584–593CrossRefGoogle Scholar
  50. Legakis A, Papdimitriou C, Gaetglich M, Lazaris D (2000) Survey of bats of the Athens metropolitan area. Myotis 38:41–46Google Scholar
  51. Lesiñski G, Eb Fuszara, Kowalski M (2000) Foraging areas and relative density of bats (Chiroptera) in differently human transformed landscapes. Z Säugetierkunde 65:129–137Google Scholar
  52. Longcore T, Rich C (2004) Ecological light pollution. Front Ecol Environ 2(4):191–198CrossRefGoogle Scholar
  53. Luck GW, Smallbone L, Threlfall C, Law B (2013) Patterns in bat functional guilds across multiple urban centres in south-eastern Australia. Landscape Ecol 28:455–469CrossRefGoogle Scholar
  54. Luniak M (2004) Synurbization—adaptation of animal wildlife to urban development. In: Shaw WW, Harris LK, VanDruff L (eds) Proceedings 4th international urban wildlife symposium. University of Arizona, Tucson, USA, pp 50–55Google Scholar
  55. Macdonald DW, Newdick MT (1982) The distribution and ecology of foxes, Vulpes vulpes (L.) in urban areas. In: Bornkamm R, Lee JA, Seaward MRD (eds) Urban ecology. Oxford University Press, Oxford, pp 123–138Google Scholar
  56. Mahmood-ul-Hassan M, Gulraiz TL, Rana SA, Javid A (2010) The diet of Indian flying-foxes (Pteropus giganteus) in urban habitats of Pakistan. Acta Chiropterologica 12(2):341–347CrossRefGoogle Scholar
  57. McConville A, Law B, Penman T, Mahony M (2013a) Contrasting habitat use of morphologically similar bat species with differing conservation status in south-eastern Australia. Austral Ecol 39(1):83–94Google Scholar
  58. McConville A, Law BS, Mahony MJ (2013b) Are regional habitat models useful at a local-scale? A case study of threatened and common insectivorous bats in south-eastern Australia. PLoS ONE 8(8):1–10CrossRefGoogle Scholar
  59. McDonald RI (2008) Global urbanization: can ecologists identify a sustainable way forward? Front Ecol Environ 6(2):99–104CrossRefGoogle Scholar
  60. McDonald R, Marcotullio P (2013) Global effects of urbanization on ecosystem services. In: Elmqvist T, Fragkias M, Goodness J et al (eds) Urbanization, biodiversity and ecosystem services: challenges and opportunities. Springer, DordrechtGoogle Scholar
  61. McDonald RI, Kareiva P, Forman RTT (2008) The implications of current and future urbanization for global protected areas and biodiversity conservation. Biol Conserv 141(6):1695–1703CrossRefGoogle Scholar
  62. McDonnell MJ, Hahs AK (2008) The use of gradient analysis studies in advancing our understanding of the ecology of urbanizing landscapes: current status and future directions. Landscape Ecol 23(10):1143–1155CrossRefGoogle Scholar
  63. McDonnell M, Hahs A (2013) The future of urban biodiversity research: moving beyond the ‘low-hanging fruit’. Urban Ecosyst 16(3):397–409CrossRefGoogle Scholar
  64. McDonnell MJ, Pickett STA (1990) Ecosystem structure and function along urban-rural gradients: an unexploited opportunity for ecology. Ecology 71(4):1232–1237CrossRefGoogle Scholar
  65. McGranahan G, Satterthwaite D (2003) Urban centers: an assessment of sustainability. Annu Rev Environ Resour 28:243–274CrossRefGoogle Scholar
  66. McIntyre NE, Knowles-Yánez K, Hope D (2000) Urban ecology as an interdisciplinary field: differences in the use of “urban” between the social and natural sciences. Urban Ecosyst 4(1):5–24CrossRefGoogle Scholar
  67. McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52(10):883–890CrossRefGoogle Scholar
  68. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127(3):247–260CrossRefGoogle Scholar
  69. McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14(11):450–453CrossRefPubMedGoogle Scholar
  70. Meyer CFJ, Kalko EKV (2008) Assemblage-level responses of phyllostomid bats to tropical forest fragmentation: land-bridge islands as a model system. J Biogeogr 35(9):1711–1726CrossRefGoogle Scholar
  71. Montgomery MR (2008) The urban transformation of the developing world. Science 319(5864):761–764CrossRefPubMedGoogle Scholar
  72. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  73. Nadeem MS, Zafar S, Kayani AR, Mushtaq M, Beg MA, Nasir MF (2013) Distribution and roosting habitats of some Microchiropteran bats in Rawalpindi District, Pakistan. Pak J Zool 45(2):565–569Google Scholar
  74. Nakamoto A, Kinjo K, Izawa M (2007) Food habits of Orii’s flying-fox, Pteropus dasymallus inopinatus, in relation to food availability in an urban area of Okinawa-jima Island, the Ryukyu Archipelago, Japan. Acta Chiropterologica 9(1):237–249CrossRefGoogle Scholar
  75. Nakamoto A, Kinjo K, Izawa M (2012) Ranging patterns and habitat use of a solitary flying fox (Pteropus dasymallus) on Okinawa-jima Island, Japan. Acta Chiropterologica 14(2):387–399CrossRefGoogle Scholar
  76. Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philos Trans R Soc Lond B Biol Sci 316(1179):335–427CrossRefGoogle Scholar
  77. Pacheco SM, Sodré M, Gama AR, Bredt A, Cavallini EM, Sanches Marques RV, Guimarães MM, Bianconi G (2010) Morcegos Urbanos: Status do Conhecimento e Plano de Ação para a Conservação no Brasil. Chiroptera Neotropical 16(1):629–647Google Scholar
  78. Park KJ, Mochar F, Fuentes-Montemayor E (2012) Urban biodiversity: successes and challenges: bat activity in urban green space. Glasg Naturalist 25(4)Google Scholar
  79. Parris KM, Hazell DL (2005) Biotic effects of climate change in urban environments: the case of the grey-headed flying-fox (Pteropus poliocephalus) in Melbourne, Australia. Biol Conserv 124(2):267–276CrossRefGoogle Scholar
  80. Pearce H, Walters CL (2012) Do green roofs provide habitat for bats in urban areas? Acta Chiropterologica 14(2):469–478CrossRefGoogle Scholar
  81. Pickett STA, Cadenasso ML, Grove JM, Nilon CH, Pouyat RV, Zipperer WC, Costanza R (2001) Urban ecological systems: linking terrestrial ecological, physical, and socioeconomic components of metropolitan areas. Ann Rev Ecol Syst 32:127–157CrossRefGoogle Scholar
  82. Pottie SA, Lane DJW, Kingston T, Lee BPYH (2005) The microchiropteran bat fauna of Singapore. Acta Chiropterologica 7(2):237–247CrossRefGoogle Scholar
  83. Rhodes M, Catterall C (2008) Spatial foraging behaviour and use of an urban landscape by a fast-flying bat, the Molossid Tadarida australis. J Mammal 89(1):34–42CrossRefGoogle Scholar
  84. Rhodes M, Wardell-Johnson G (2006) Roost tree characteristics determine use by the white-striped freetail bat (Tadarida australis, Chiroptera: Molossidae) in suburban subtropical Brisbane, Australia. Austral Ecol 31:228–239CrossRefGoogle Scholar
  85. Rhodes M, Wardell-Johnson GW, Rhodes MP, Raymond BEN (2006) Applying network analysis to the conservation of habitat trees in urban environments: a case study from Brisbane. Australia. Conservation Biology 20(3):861–870CrossRefPubMedGoogle Scholar
  86. Rompré G, Robinson WD, Desrochers A (2008) Causes of habitat loss in a neotropical landscape: the Panama Canal corridor. Landscape and Urban Planning 87(2):129–139CrossRefGoogle Scholar
  87. Rosenberg MS, Adams DC, Gurevitch J (2000) Metawin: manual of statistical software for meta-analysis. Sinauer, SunderlandGoogle Scholar
  88. Scales J, Wilkins KT (2007) Seasonality and fidelity in roost use of the mexican free tailed bat Tadarida brasiliensis in an urban setting. Western North American Naturalist 67(3):402–408CrossRefGoogle Scholar
  89. Scanlon AT, Petit S (2008) Effects of site, time, weather and light on urban bat activity and richness: considerations for survey effort. Wildlife Research 35(8):821–834CrossRefGoogle Scholar
  90. Schnitzler H-U, Kalko EKV (2001) Echolocation by insect-eating bats. Bioscience 51(7):557–569CrossRefGoogle Scholar
  91. Septon G, Marks JB, Ellestad T (1995) A preliminary assessment of peregrine Falcon Falco peregrinus recovery in the Midwestern North America. Acta Ornithologica 30:65–68Google Scholar
  92. Sewell SR, Catterall CP (1998) Bushland modification and styles of urban development: their effects on birds in south-east Queensland. Wildlife Research 25(1):41–63CrossRefGoogle Scholar
  93. Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21(4):186–191CrossRefPubMedGoogle Scholar
  94. Siles L, Peñaranda D, Pérez-Zubieta JC, Barboza K (2005) Los murciélagos de la ciudad de Cochabamba. Revista Boliviana Ecologia 18:51–64Google Scholar
  95. Slabbekoorn H, Peet M (2003) Birds sing at a higher pitch in urban noise. Nature 424(6946):267CrossRefPubMedGoogle Scholar
  96. Slabbekoorn H, Ripmeester EAP (2008) Birdsong and anthropogenic noise: implications and applications for conservation. Mol Ecol 17:72–83CrossRefPubMedGoogle Scholar
  97. Stone EL, Jones G, Harris S (2009) Street lighting disturbs commuting bats. Current Biology 19:1123–1127Google Scholar
  98. Thomas NM, Duckworth J, Douangboubpha B, Williams M, Francis CM (2013) A checklist of bats (Mammalia: Chiroptera) from Lao PDR. Acta Chiropterologica 15(1):193–260CrossRefGoogle Scholar
  99. Threlfall CG, Law B, Penman T, Banks PB (2011) Ecological processes in urban landscapes: mechanisms influencing the distribution and activity of insectivorous bats. Ecography 34(5):814–826CrossRefGoogle Scholar
  100. Threlfall CG, Law B, Banks PB (2012a) Influence of landscape structure and human modifications on insect biomass and bat foraging activity in an urban landscape. PLoS ONE 7(6):e38800PubMedCentralCrossRefPubMedGoogle Scholar
  101. Threlfall CG, Law B, Banks PB (2012b) Sensitivity of insectivorous bats to urbanization: Implications for suburban conservation planning. Biol Conserv 146:41–52CrossRefGoogle Scholar
  102. Threlfall CG, Law B, Banks PB (2013a) Roost selection in suburban bushland by the urban sensitive bat Nyctophilus gouldi. J Mammal 94(2):307–319CrossRefGoogle Scholar
  103. Threlfall CG, Law B, Banks PB (2013b) The urban matrix and artificial light restricts the nightly ranging behaviour of Gould’s long-eared bat (Nyctophilus gouldi). Austral Ecol 38(8):921–930CrossRefGoogle Scholar
  104. UN (2012) System Task Team on the post-2015 UN development agenda: sustainable urbanization. Thematic think pieceGoogle Scholar
  105. UNPD (2012) World urbanization prospects: the 2011 revision. Highlights. United Nations Population Division, New York, USAGoogle Scholar
  106. Utthammachai K, Bumrungsri S, Chimchome V, Russ J, Mackie I (2008) The Habitat Use and Feeding Activity of Tadarida plicata in Thailand. Thai J For 27(2):21–27Google Scholar
  107. van der Ree R, McCarthy MA (2005) Inferring persistence of indigenous mammals in response to urbanisation. Anim Conserv 8(3):309–319CrossRefGoogle Scholar
  108. Viechtbauer W (2010) Conducting meta-analysis in R with the metafor package. J Statistical Softw 36(3):1–48Google Scholar
  109. Viechtbauer W (2013) The metafor package: a meta-analysis package for R. http://www.metafor-project.org
  110. Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116(5):882–892CrossRefGoogle Scholar
  111. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of earth’s ecosystems. Science 277(5325):494–499CrossRefGoogle Scholar
  112. Walsh AL, Harris S (1996) Factors determining the abundance of Vespertilionid bats in Britain: geographical, land class and local habitat relationships. J Appl Ecol 33(3):519–529Google Scholar
  113. Williams NSG, Morgan JW, McDonnell MJ, McCarthy MA (2005) Plant traits and local extinctions in natural grasslands along an urban–rural gradient. J Ecol 93(6):1203–1213CrossRefGoogle Scholar
  114. Zhao S, Da L, Tang Z, Fang H, Song K, Fang J (2006) Ecological consequences of rapid urban expansion: Shanghai, China. Front Ecol Environ 4(7):341–346CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Institute of Evolutionary Ecology and Conservation GenomicsUniversity of UlmUlmGermany
  2. 2.School of Ecosystem and Forest SciencesUniversity of MelbourneMelbourneAustralia

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