ReviewSensitivity of bats to urbanization: a review
Introduction
Urbanization is a major process of land use change that has considerably transformed habitats and landscapes available to wildlife. The on-going massive growth of urban areas has resulted in the replacement of original habitats in most areas of the world (Baker and Harris, 2007). Many studies have found that urbanization may have detrimental effects on animal species and communities, including: habitat loss and fragmentation (Scolozzi and Geneletti, 2012); road mortality and barrier effects (Baker and Harris, 2007); high density of domestic medium-sized predators such as cats and dogs (Patroneck et al., 1997, Young et al., 2011); effects of chemical and physical pollutants (Perugini et al., 2011), comprising anthropogenic noise and artificial illumination (Francis and Barber, 2013, Stone et al., 2009); and direct human interference (Markovchick-Nicholls et al., 2008). However, it is also known that urbanization may favour some species which succeed in human-altered conditions because they perform well in heterogeneous landscapes (Magle et al., 2012), benefit from the increased temperatures typical of urban areas (Costanza et al., 2001) or use the latter to shelter from large predators (Baker and Harris, 2007). Out of the many species that survive in urbanized areas, some, so-called ‘synurbic’, are more frequent, or abundant, in urban areas than in other habitats (Francis and Chadwick, 2012). Such species often show behavioural or ecological traits appearing to be tailored to cope with the challenges and opportunities offered by urban environments as a result of phenotypic plasticity or evolutionary processes (Magle et al., 2012). The task of exploiting novel urbanized environments may either lead to species exclusion or adjustment of behaviour and ecology, from foraging patterns to breeding timing and response to stress (Lowry et al., 2013). Successful species often show more “boldness” than others, including a stronger tendency towards risk-taking.
Bats are major contributors to biological diversity (Hutson et al., 2001), with over 1300 species known to date, a number that will most likely increase further thanks to the advances in molecular studies leading to the description of new cryptic species (Mayer et al., 2007). They also form large aggregations and in terms of abundance are among the most numerous living mammals (Jones et al., 2009). Bats are well known to provide a range of key ecosystem services, especially related to their diet and foraging behaviour (Kunz et al., 2011). The large amount of insect prey consumed by insectivorous bats – between 25 and 50% of their body mass – makes them excellent pest controllers, whereas nectar-feeding and fruit-eating bats act, respectively, as pollinators and dispersers for economically and ecologically relevant plants (Fujita and Tuttle, 1991).
Bats are also very sensitive to environmental anthropogenic alteration–which threatens the survival of many species (Hutson et al., 2001, Park, 2015)—so they may successfully be employed as bioindicators (Jones et al., 2009). One of the main general properties of a bioindicator is the tendency to show marked and prompt reactions to environmental changes (e.g. McGeoch, 1998). There is growing evidence that bats are profoundly influenced by urbanization exhibiting responses in terms of altered diversity, population size and behaviour. In this article we review the current knowledge of the effects of urbanization on bats and assess the potential of these mammals as bioindicators of this major land use process. As we will see, the response of bats to urbanization is highly species-specific. While some species show a strong degree of adaptation to urban habitat or are even favoured by it, others will decline in response to habitat loss and disturbance. Therefore, a species perspective is essential when assessing the effects of urbanization on bats, although species’ differential response will translate into structurally altered bat communities (Threlfall et al., 2012).
We will (1) summarize the effects of urban habitats on roosting, foraging and commuting behaviour, (2) look at habitat or landscape effects on bat communities, (3) discuss whether urban habitat may be regarded as an ecological trap for at least some species, and (4) evaluate the potential importance of bats as bioindicators of urbanization.
Section snippets
Urban roosts
Roosts are resources playing a central role to the natural history of bats (e.g. Kunz, 1982). Their availability has implications for both bat geographical distribution and the diversity of bat communities (e.g. Findley, 1993). Roost structure, microclimate and degree of protection from predators critically influence bat survival and reproductive success (Kunz and Lumsden, 2003). Since the onset of urbanization, with the appearance of buildings and other human constructions such as bridges,
Water availability in urban habitat
Because of their distinct morphology and physiology, bats are often exposed to dehydration: they lose much water through their body surface, particularly via the respiratory system and the wing membranes (Chew and White, 1960, Thomas and Cloutier, 1992). Especially in arid, semiarid or Mediterranean areas, where water is permanently or seasonally limiting, human-made water bodies created within or near urban sites such as artificial ponds, water reservoirs, cattle troughs or swimming pools may
Urbanization and foraging behaviour
Urbanization has often been described as detrimental to bat foraging, yet the reaction of foraging bats to it varies according to species. Although some species may successfully exploit urban roosting sites, their flexibility may not extend to foraging behaviour too. Markedly generalist species (in Europe, for example P. kuhlii, Pipistrellus pipistrellus and H. savii) are often those most likely to roost and forage near urban settlements (Duchamp et al., 2004). However, bats roosting in cities
Crossing urbanized landscapes
By replacing natural habitat or interrupting connectivity, urbanized areas and roads may interfere considerably with bat movement (Kerth and Melber, 2009). Generally speaking, biological corridors of different size, from riparian vegetation (Russo et al., 2002, Serra-Cobo et al., 2002) to hedgerows (Verboom and Huitema, 1997, Park, 2015), have been found to be of utmost importance to bat movement. Therefore, a decrease in landscape connectivity caused by urban expansion is likely to affect many
Soundscapes
Urban landscapes are typically filled with human-produced sounds (Botteldooren et al., 2004, Raimbault and Dubois, 2005). Urbanization is a major cause of fragmentation of terrestrial acoustic landscapes (Lynch et al., 2011), a process known to affect animal behaviour and distribution (Barber and Crooks, 2010, Francis and Barber, 2013). Acoustics plays a major role in a bat's life so these mammals are potentially affected by human-generated noise (Barber and Crooks, 2010), yet this aspect has
Influence on patterns of richness and diversity
Bats make no exception to the general rule that by replacing or fragmenting natural habitats, urban expansion alters community structure and dynamics, with inevitable consequences for species richness and diversity. Generalist, flexible species will dominate at the expense of more sensitive or specialized ones. Changed roosting and foraging conditions will translate into altered richness or diversity as a result of strongly species-specific, or at least guild-specific mechanisms (Luck et al.,
Urban areas and fitness in bats
Based on what we have seen so far, a somewhat simplistic synthesis of the effects of urbanization on bats is represented by a winner-or-loser model: some more opportunistic species would become synurbic and exploit the novel ecological conditions found in urban sites whereas most others, being less flexible, would be affected by the loss of habitat and/or the altered environmental conditions.
We suggest that individual fitness follows different paths along an urbanization gradient according to
Why might urban sites act as ecological traps for bats?
The reasons to support the hypothesis that urban sites may act as ecological traps for apparently tolerant or synanthropic species are summarized as follows.
Bats as bioindicators of urbanization
Overall, bats prove very sensitive to urbanization, although the magnitude and direction of the effects depend on the scale of analysis and are species-specific. The general pattern is that as urbanization expands, a reduction in richness of bat communities is recorded, associated with the decline or disappearance of urban-sensitive species and the population increase in urban-tolerant, or synurbic, species. Bats are thus promising candidates to track the effects of urbanization on wildlife
Acknowledgements
We are indebted to two anonymous reviewers for their useful comments on a previous ms version. Rarefaction analysis applied to estimate bat diversity in Fig. 2 was kindly carried out by Ignasi Torre.
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