Globally, biodiversity faces unprecedented pressures from human actions (Newbold et al., 2015; Joppa et al., 2016), including climatic changes, intensification and industrialization of land use practices in agricultural areas (Sala et al., 2000; Foley et al., 2005) and forests, as well as increased urbanization (Liu et al., 2020). Especially the past 30 years revealed an unprecedented rate of global urbanization and gain in the spatial extend of urban land cover (Liu et al., 2020), with high human population density in cities (Antrop, 2004; Lambin and Geist, 2008). However, in Europe, urbanization is rather characterized by urban sprawl than by large metropolitan areas, and smaller towns and villages within agricultural areas shape large parts of the landscape. This is also true for Germany, where differences in demographic population trends, especially between the north-east and the south of the country, determine the extent of urban sprawl into rural areas and the heterogeneity in land cover. Especially southern regions of the country are currently experiencing an increased population growth (Hollbach-Grömig et al., 2012) and urban development in rural areas, resulting in more urbanized and fragmented rural landscapes.

Regions that have undergone the process of urbanization are characterized by an increased amount of impervious surfaces as the dominating landcover (McKinney, 2006) due to buildings, industrial areas and increased need for infrastructure. In turn, vegetation is mostly limited to smaller parks, gardens and roadside vegetation (McKinney, 2008). These structural changes result in increased air and noise pollution and habitat loss for wildlife, compared to non-urban habitats (Grimm et al., 2008; McDonnell et al., 2009; Niemelä et al., 2011). Increasingly urbanized rural regions however may remain rather heterogenous landscapes, as impervious surfaces within urban settlements directly neighbors agricultural and semi-natural environments. In addition, villages and smaller towns are a mosaic of old and newly constructed housing areas and homesteads with different modernization standards. They provide a multitude of structures (e.g., old tiled rooves and building crevices) that offer potential habitat for wildlife including many bird (Rosin et al., 2016) and bat species. However, the increasing re-migration trend towards rural areas in the highly populated South of Germany results in increased renovation of older buildings, and growing villages and towns. While modernizations mostly include the renewal of roofs and improved insulation to meet climate-friendly standards, newly developed housing areas are characterized by very similar and well-insulated buildings (Antrop, 2004) with smaller properties, gardens and immature woody vegetation, and thus provide less architectural and structural heterogeneity within entire neighborhoods.

Urbanization has complex effects not only on the structural composition of the environment, but also on the occurrence and behavior of wildlife (e.g., McKinney, 2006; Rivkin et al., 2019), which may inhabit or visits urban areas for different reasons, including additional roosting opportunities and food sources (e.g., Blair, 2001; Kühn et al., 2004; Clergeau et al., 2006; Strohbach et al., 2009). Several wildlife species are known to strive urban areas. In particular, in moderate developed urban areas, suburbs, smaller towns, and villages seem to provide new roosting and foraging grounds. While several studies investigated the effect of increased urban density in larger, often metropolitan areas (e.g., Lumsden and Bennett, 2005; Threlfall et al., 2011; Hale et al., 2012; Straka et al., 2019), very few studies so far focused on the dispersed urbanization process in rural areas (but see Gili et al., 2020). However, it is here, where urbanization processes are changing landscapes most drastically and where humans and wildlife of nearby agricultural and forested areas can more likely come in closer contact.

One of the most species richest group of mammals that occur in urban areas are bats (Jung and Threlfall, 2018). By eating up to 80–100% of their own body mass in insects per night (Puig-Montserrat et al., 2015), they provide an essential ecosystem function as insect and pest control. Among a broad variety of prey insects, they also consume mosquitos, an important vector of infectious diseases (Gonsalves et al., 2013). Maintaining diverse bat populations in urbanized areas of rural regions, is thus not only in the interest of wildlife conservation, but also to sustainable management of nearby agricultural areas and production forests, but it is also important for human health.

Previous studies on bats along gradients of urbanization generally revealed a decline in species richness and bat activity with increasing urbanization (e.g., Duchamp et al., 2004; Jung and Kalko, 2011; Threlfall et al., 2011; Luck et al., 2013; Jung and Threlfall, 2016, 2018). In particular, urban density and continuous impervious surfaces have been generally linked to lower bat species richness and activity (Threlfall et al., 2011; Dixon, 2012; Caryl et al., 2016). Positive effects on bats have been attributed to vegetation and forest cover in the urban area (Kalda et al., 2015; Moretto et al., 2019; Gili et al., 2020; Straka et al., 2021) and the surrounding landscapes (Duchamp and Swihart, 2008; Treitler et al., 2016). This suggests that vegetation within urban areas is a crucial prerequisite to increase habitat suitability for bats (Lumsden and Bennett, 2005; Caryl et al., 2016) also when foraging on insect accumulations around street lights (Avila-Flores and Fenton, 2005; Kerbiriou et al., 2020; Straka et al., 2021). Tolerance to urbanization is further known to differ between bat species and has been linked to species traits (Jung and Threlfall, 2018), namely lower echolocation call frequency, higher mobility, and flexible roosting strategies. Thus, especially fast flying and rather flexible and opportunistic species are likely to dominate urban assemblages (Luck et al., 2013; Jung and Threlfall, 2018). However, the effect of urbanization differs due to the extent of urban development (Jung and Threlfall, 2016; Gili et al., 2020). Therefore, rural villages likely provide suitable habitat also for less urban tolerant bat species. Especially in the light of the ongoing biodiversity crisis, climatic changes, and the emergence of zoonotic diseases, it is crucial to understand how the alteration of rural regions due to increased urbanization, affects occurrence, behavior and species composition of bats, and how can rural regions uphold biodiverse landscapes and safeguard regional bat diversity to assure vital ecosystem services within urbanized rural regions.

Here, we investigated whether and how urban development in rural landscapes affects bats. We specifically ask how spatial, structural, and architectonic environmental features of rural urban areas, locally and at the neighborhood scale, affect bat species occurrence and behavior to derive environmental parameters of the urban environments that may support bat species diversity and vital bat activity. Such knowledge is of high relevance for urban planners and conservation ecologists to target strategies for biodiversity inclusion within increasingly urbanized rural landscapes.

Our standardized acoustic monitoring resulted in a total of 53,208 recordings of bats in villages and towns of the Schwäbische Alb. Of those, 2.1% (N = 1,097) contained feeding buzzes and 13% (N = 6,952) included social calls. In total, we identified 13 species or sonotypes, with P. pipistrellus as the most frequent recorded species (Supplementary Table S2).

Urbanization is a strong environmental driver (Piano et al., 2019). It can be seen as the most drastic form of land use change (McKinney, 2006; Shochat et al., 2006) and is no longer limited to the expansion and densification of metropolitan areas but rather extends far beyond city boundaries into rural areas (McDonald, 2008). We investigated whether and how urban heterogeneity of villages in rural landscapes affects activity of bats. Such knowledge is crucial for a guided management and conservation of bats in rural areas (Racey and Entwistle, 2003), where land use intensification in the surrounding agricultural landscapes causes habitat loss (Rosin et al., 2016) and dramatic declines in insect prey (Hallmann et al., 2017; Seibold et al., 2019) while climatic changes favor the spread of insect pests such as the Tiger mosquitoes, a vector for various disease.

Our results revealed that the combination of local and neighborhood conditions in rural urban areas affects the occurrence of different bat species. Species occurrence significantly decreased with increasing urban extent, confirming that even very restricted urban development in rural areas restructures biotic communities of bats (see, e.g., Jung and Threlfall, 2016). However, bat occurrence and activity increased with local greenspace, in particular openly structured woody vegetation as it is typical for parklands, orchards and older village gardens. This also highlighted the potential of local conditions to support diverse bat assemblages and vital bat activity in rural urban areas. Our results are in agreement with previous studies in urban (Moretto et al., 2019; Gili et al., 2020) and in agricultural landscapes (Lumsden and Bennett, 2005; Heim et al., 2015; Kalda et al., 2015; Treitler et al., 2016), where woody vegetation and tree cover are considered key components for higher diversity and abundance of bats. Moretto et al. (2019), even showed that the positive effect of single trees in urban areas extends into the neighborhood. Hereby in particular, the retention of large and old trees has previously been shown to be critical for urban biodiversity conservation (Threlfall et al., 2012) and even buffers negative effects of light pollution (Straka et al., 2019). Nevertheless, our results also indicated the importance of non-woody vegetated areas, such as traditionally managed meadows or orchards, which are important habitat especially for gleaning Myotis and Plecotus species. Overall, this emphasizes the positive effects of even small, differently structures vegetated areas, such as for example residential gardens, single trees, and orchards even within structurally rather poor urban areas and supports the idea that very local decisions on management can help to support the occurrence of different bat species in urbanized rural landscapes.

Bat activity and feeding activity were mainly affected by local environmental parameters, including architectonic features as a key parameter explaining varying bat activity between different urban sites. We found highest bat activity in residential areas with 1–2 story houses. This is consistent with Pearce and Walters (2012), who reported a negative association between roof height and bat activity. Buildings with 1–2 stories are most often family residentials, surrounded by gardens, resulting in a mosaic of impervious surfaces and vegetation patches locally. In addition, many householders are implementing practices to enhance wildlife, such as limiting the use of pesticides and planting a variety of different plants (Good, 2000), potentially resulting in a higher insect diversity compared to nearby agricultural areas (Seibold et al., 2019). We however found notable differences between residential areas of different construction ages. Our results indicated higher bat activity in residential areas built between 1950–2000, suggesting that those are currently better habitats for bats. Such residential areas are often characterized by less well-insulated and not yet renovated houses, large and well-grown gardens, small ponds or rain barrels and are thus structurally more diverse. Housing areas with historic buildings constructed prior to 1900 showed less bat activity. This is likely due to renovation and modernization of these historic buildings. Especially newly constructed neighborhoods and buildings (constructed after 2000) however revealed lowest bat activity. New buildings are well insulated to meet climate-friendly standards, but no longer provide crevices under roofs or facades. Additionally, new developed building areas generally lack old growth trees, and are often surrounded by rather young vegetation and smaller premises, and thus provide only limited foraging or roosting grounds for bats.

Several bat species, in particular flexible and opportunistic species are known to persist in and might even benefit from additional resources in urban areas (Russo and Ancillotto, 2015; Jung and Threlfall, 2016). However, several studies have cautioned that the response towards urbanization is species-specific and trait-dependent (e.g., Jung and Threlfall, 2016), and urbanization likely functions as a strong trait-based environmental filter (Jung and Threlfall, 2018), resulting in altered species assemblages (e.g., Grimm et al., 2008). Our results showed that bat assemblages in villages were dominated by P. pipistrellus, which together with the group Nyctaloid and P. nathusii comprised the vast majority of our recordings. P. pipistrellus is an edge foraging bat, with a very broad distribution range, tolerating also rough climate conditions typical for lower mountain areas as the Schwäbische Alb plateau where our study took place. All other species were much less recorded in villages, although long term data obtained in this area from 2008–2012 (Jung and Tschapka, 2022) shows, that those are present in surrounding forest and grassland areas. This is in accordance with prior studies, that indicated that species richness may be generally low in urban areas, but total abundance of bats increases due to the occurrence of a few dominating urban-tolerant species (Avila-Flores and Fenton, 2005; Francis and Chadwick, 2012; Krauel and LeBuhn, 2016). Pipistrelle bats can be frequently observed within urban areas (Gaisler et al., 1998), are known to roost in buildings (Dietz et al., 2009), and show opportunistic foraging behavior by hunting regularly around street-lights (Rydell and Racey, 1995). Thus, pipistrelle bats seem to be rather resource generalists that benefit from additional roosting and foraging sites provided by urban structures. In contrast, Myotis species showed lower activity rates as the total impervious surface increased. This is consistent with a prior study (Jung and Threlfall, 2018), and particularly gleaning bats, such as Myotis or Plecotus, are less likely to forage in urban areas. Myotis and Plecotus species, specialized to listen for prey generated noises, and known to collect ground-dwelling arthropods (e.g., carabids) from the ground, were also almost exclusively detected in villages with high amount of non-woody vegetation, e.g., grassland or orchards. Similar results have been reported by Uhrin et al. (2017), who showed a positive association of grassland landcover with the occurrence of P. auritus. It is however important to note, that Myotis and Plecotus may very well roost in village barns or church attics but rather leave the urban setting for foraging in nearby grassland or forest habitats, if the urban neighborhood provides enough green and connective elements for a safe commute.

Our study provides important insight on how the process of increased urbanization in rural areas affects bat species occurrence and behavior. Our results indicate that a lack of connectivity in the neighborhood due to limited greenness and vegetation likely restricts the accessibility of different urban sites while local conditions may rather determine the quality of urban habitats for roosting, and foraging. Thus, the retention of green areas, such as village meadows, old and large trees in village centers and farmer’s gardens, which have been an essential part of the local culture, are key to maintain biodiversity in rural areas. Altogether, these green elements can serve as a green infrastructure, connecting villages with habitats in the surrounding landscape matrix and assuring movement of wildlife. This includes bats as well as the provision of valuable ecosystem services (e.g., the consumption of mosquitos) within rural urbanized landscapes. In addition, within increasingly urbanized rural landscapes, strategies are needed to decrease negative impacts on biodiversity by urban expansion and modernizations. Particularly, new constructed housing areas and modernized historic buildings revealed lower bat diversity and activity, which is likely due to the lack of potential roosting sites in well-insulated buildings and roof structures and gardens with predominantly young vegetation. It may be a matter of natural development that those areas can support biodiversity in the future, but it is also and foremost a matter of integrating the space for natural development in urban planning and the consciousness for biodiversity inclusion in the cause of modernizations by local residents.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: This work is based on data (ID: 31295) elaborated by the project “birds&bats” of the Biodiversity Exploratories program (DFG Priority Program 1374). The dataset will be available publicly in the Biodiversity Exploratories Information System (http://doi.org/10.17616/R32P9Q). However, as this data is part of further analysis at the national level it underlies an embargo period of three years from the end of data collection/data assembly. After this period this dataset will be made publicly available via the same data repository: KJ and LP (2021): Bat activity urban sites Exploratory ALB summer 2021. Biodiversity Exploratories Information System. Dataset https://www.bexis.uni-jena.de/. Dataset id: 31295.

Ethical review and approval was not required for the animal study because we used passive acoustic monitoring as a method, which in a non-invasive technique to gather information about bat activity and behavior. We did not disturb animals in any way.

This study has been conceived and designed by KJ. Data collection and analysis were performed by LP. The first draft of the manuscript was written by LP jointly edited by LP and KJ. All authors contributed to the article and approved the submitted version.

This work has been funded by the DFG Priority Program 1374 "Biodiversity-Exploratories" (JU 2752/2-1 granted to KJ).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.