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.