Abstract
Urbanisation is increasing worldwide, with major impacts on biodiversity, species interactions and ecosystem functioning. Pollination is an ecosystem function vital for terrestrial ecosystems and food security, however, the processes underlying the patterns of pollinator diversity and the ecosystem services they provide in cities have seldom been quantified. Here, we present a comprehensive meta-analysis, using 133 studies, on the effects of urbanisation on pollinator diversity and pollination. Our results confirm the widespread negative effects of urbanisation on pollinator diversity, particularly of Lepidoptera. Additionally, pollinator responses were found to be trait-specific, with below ground nesting, solitary, and spring flyers more severely affected from urbanisation. Meanwhile, cities promote a greater diversity of non-native pollinators, which may exacerbate conservation risks to native ones. Surprisingly, despite the negative effects of urbanisation on pollinator diversity, pollination services in cities are enhanced and mediated by the high flower visitation rates of abundant generalists and managed pollinators. We highlight that the richness of local flowering plants could mitigate the negative effects of urbanisation on pollinator diversity. Overall, the results demonstrate the varying magnitudes of multiple moderators on urban pollinators and pollination service provision and could help guide conservation actions for biodiversity and ecosystem function for a sustainable future.
Keywords: urban, pollinator diversity, floral resources, functional traits, plant reproductive success
INTRODUCTION
Urbanisation is one of the most profound drivers of anthropogenic change with major impacts on global biodiversity (Seto et al. 2012; Van Klink et al. 2020). Urban development results in habitat loss and fragmentation, increase in impervious surfaces, introduction of non-native species, heat-island effects and environmental pollution with largely negative influences on wildlife (Grimm et al. 2008; McKinney 2008). Urbanisation can affect individual fitness, life-history traits, population dynamics, species interactions, community structure and ecosystem functioning (e.g., Gaston 2010; Buchholz & Egerer 2020; Theodorou 2022). As urban areas continue to expand worldwide (United Nations 2018; Huanget al. 2019), there has been an increase in scientific, public, and political interest in how cities should be managed to promote biodiversity conservation, food production, and ecological restorations for a sustainable future. Pollinators are an important component of biodiversity due to the vital pollination services they provide to wild flowers (Ollerton et al. 2011) and crops (Klein et al. 2007). Currently, the study of pollinators in urban areas is of great interest due to the potential role of cities as refugia for species affected by agricultural intensification and the great premise of urban agriculture for food security (Baldock et al. 2015; Baldock 2020; Theodorou et al. 2020b; Wenzel et al. 2020).
In general, urban development has negative effects on pollinators (Faethet al. 2011; Fenoglio et al. 2020; Millard et al.2021). Surprisingly, however, recent studies have also shown that urbanisation can have neutral or even positive effects on pollinator biodiversity (Theodorou et al. 2020b; Wenzel et al. 2020; Millard et al. 2021). These varying effects are hypothesised to be due to differences at multiple levels (McKinney 2008; Faeth et al. 2011). Firstly, taxonomic group, life-history and functional traits could influence how a pollinator species responds to urbanisation. Previous studies have shown that Hymenoptera insects seem to be more resilient to urbanisation compared to Diptera and Lepidoptera (Baldocket al. 2015; Fenoglio et al. 2020) and urbanisation seems to benefit large-bodied, social, cavity-nesting, generalist, as well as non-native species (Fitch et al. 2019; Buchholz & Egerer 2020). Secondly, the effects of urbanisation on pollinators could vary between climatic regions due to differences in land-use history and practices, socioeconomics and geographic variation in pollinator communities (Faethet al. 2011; Fenoglio et al. 2020). Due to the high levels of urbanisation in the developed world (Elmqvist et al. 2013), the effects of urbanisation on pollinators are expected to be more severe in temperate compared to tropical regions. Thirdly, pollinators respond to the availability of local resources often irrespective of land-use change (Winfree et al. 2011; Murray et al.2012; Theodorou et al. 2020a). In moderately disturbed urban areas with abundant floral resources and continuity of floral resources, it is not surprising to document high pollinator biodiversity (Baldocket al. 2015; Theodorou et al. 2020b). All the above factors suggest that summarising a global pattern of the effects of urbanisation on pollinators is challenging and multiple moderators should be considered when attempting to do so.
Although we have a growing understanding of how urbanisation impacts different taxonomic and functional groups of pollinators, it is unclear whether these changes translate into shifts in pollination service provision (Theodorou 2022). The effects of urbanisation on the community structure and functional diversity of pollinators could reduce the efficiency or frequency of pollen transfer and could lead to pollen limitation (Irwin et al. 2018). In addition, urbanisation can affect abiotic and landscape features, the abundance of conspecific flowers and the diversity of flowering plants in an area. These factors may have an impact on pollinators’ foraging patterns, visitation rates, conspecific pollen deposition, and consequently influence plant reproduction (Pellissieret al. 2012). Similarly, to pollinators, the origin of the plant species, its functional traits and pollinator specialisation may influence its reproductive success in cities. Native plants are generally preferred by pollinators (Chrobock et al. 2013) and plants with open radial flowers attract more flower visitors and may be less sensitive to the effects of urbanisation (Ollerton et al.2007; Willmer 2011). Recent studies have investigated the effects of urbanisation on plant reproductive success by estimating fruit set and/or seed set or by using visitation rates and visit duration as proxies, and many studies have shown an increase in pollination service provision in cities driven by the high abundance of managed and generalist pollinator species (Theodorou et al. 2021; Theodorou 2022).
While there are some qualitative reviews on the effects of urbanisation on pollinators and pollination (Baldock 2020; Buchholz & Egerer 2020; Wenzel et al.2020; Ayers & Rehan 2021; Maruyama et al. 2021; Silva et al. 2021), only two meta-analyses investigated the overall effects of urbanisation on pollinator diversity (Fenoglio et al. 2020; Millard et al. 2021). In our study, we extend the research in this field by performing a hierarchical meta-analysis to assess how dependent the effects of urbanisation are on taxonomic group and origin (native vs. non-native) of the pollinator species, climatic region of the study and local floral food resource availability. We furthermore assess how urbanisation influences the phenology and seasonality, sociality, nesting behaviour, diet, and body size of pollinator communities. Finally, we investigate the potential effects of urbanisation on pollination service provision.