DISCUSSION
Pollination is an important ecosystem function for both natural and
anthropogenic habitats yet, the effects of urbanisation on pollinators
and pollination are poorly known. In this study, we reviewed the
literature and performed a meta-analysis on the effects of urbanisation
on pollinators and pollination. Our meta-analysis revealed an overall
negative effect of urbanisation on pollinator abundance and richness.
The magnitude of the effect was dependent on the taxonomic group of the
pollinator, its origin and functional traits. Furthermore, flowering
plant richness had a positive effect on pollinator richness revealing
the importance of local habitat resource availability for pollinators.
Our meta-analysis also revealed that pollination services are enhanced
in urban areas most likely due to the high abundance of generalist and
managed pollinator species. Below, we expand on these results and
discuss their implications for pollinator conservation in cities.
Urbanisation results in a drastic modification of habitats with negative
effects on biodiversity (McKinney 2008). The
negative
effects of urbanisation on both pollinator abundance and richness,
reported in our study, are in line with previous meta-analyses (Fenoglioet al. 2020; Millard et al. 2021). The increase in
impervious surfaces, habitat loss, fragmentation, and degradation as
well as environmental pollution are the primary hypothesised drivers for
the observed reduction of pollinator biodiversity in cities
(González-Varo et al. 2013; Vanbergen & Initiative 2013). In
addition to the overall negative effects on pollinator biodiversity, our
results revealed that pollinator taxonomic groups differ in their
sensitivity to urbanisation. Lepidoptera was the taxonomic group that
was found to be most affected by urban development. Many butterflies and
months require specific host plants for larval development and nectar
consumption as adults and they appear to be very sensitive to urban
environmental stressors such as heat island effects, air and light
pollution (Ramírez-Restrepo & MacGregor-Fors 2017; Fenoglio et
al. 2020; Callaghan et al. 2021). Due to their sensitivity to
human disturbances, our results further highlight the suitability of
Lepidoptera as a bioindicator taxon to quantify responses to
urbanisation. Our results further demonstrate that Lepidoptera is the
taxonomic group most at risk from urbanisation and should be prioritised
for conservation in cities.
The
climatic
region of the study was not an important moderator of the effects of
urbanisation on pollinators. As has been shown in a previous study
(Fenoglio et al. 2020), urbanisation had a negative effect on
pollinator richness in both tropical and non-tropical cities. Urban
development is a global phenomenon that leads to convergence of urban
environments (Santangelo et al. 2022). This global convergence of
city environments could be the main driver of the observed declines of
pollinator species richness irrespective of the climatic region of the
study. Nonetheless, urbanisation significantly affected the abundance of
pollinators only in non-tropical regions. This lack of an effect could
be due to the relatively small number of studies conducted in the
tropics. Alternatively, it might reflect the high levels of urbanisation
and thus higher impact on pollinators in non-tropical temperate regions
(Faeth et al. 2011; Elmqvist et al. 2013).
Species responses to urbanisation are trait-specific (Buchholz and
Egerer, 2020; Wenzel et al. 2020), and the implementation of ecological
trait approaches for urban biodiversity conservation provides a
mechanistic understanding of the relationship between biodiversity and
urban environmental constrains. Urban landscapes can act as
environmental filters for pollinator species depending on their
ecological traits, facilitating or hindering their colonisation and
survival in cities (Buchholz & Egerer 2020). In our meta-analysis, we
found that the pollinator traits mainly affected by urbanisation are
those related to nesting behaviour and sociality.
In
regard to nesting behaviour, our analysis confirmed the hypothesis that
below ground nesting bees are negatively affected by urbanisation (Neameet al. 2013; Geslin et al. 2016). The increase in
impervious surfaces with urban development and the intensive management
of urban green land-uses result in a reduction in the availability of
suitable habitat (i.e., bare soil) for ground nesting bees (e.g.,
Andrenidae, Halictidae, Colletidae; Potts et al. 2005; Pereiraet al. 2021). Sociality is also hypothesised to be an important
trait related to urban environmental filters (Wenzel et al.2020). In our meta-analysis, we found the abundance of solitary bees to
be negatively affected by urbanisation. The lack of ecological and
behavioural flexibility as well as their relatively small population
sizes compared to social bees might be the main drivers of solitary bee
abundance declines with urbanisation (Chapman & Bourke 2001;
Banaszak-Cibicka & Zmihorski 2012). Although the pollinator activity
length was not affected by urbanisation, we found seasonal variation in
the effects of urbanisation on pollinator communities. Urbanisation had
strong negative effects on the abundance and richness of spring
pollinator communities. As suggested by previous studies, this might be
driven by the scarcity of spring-blooming shrubs and trees and the
overall lack of spring-foraging resources for pollinators in cities
(Matteson et al. 2008; Banaszak-Cibicka & Zmihorski 2012).
Solitary bee species that are ground-nesters and spring flyers (e.g.,
Andrenidae) are at increased risk due to urbanisation, and conservation
efforts should be primarily directed towards increasing spring floral
resource availability as well as nesting opportunities for those
pollinators in cities.
Pollinators of native or non-native origin also responded differently to
urbanisation. Non-native pollinator species richness increased, and
native pollinator species richness decreased with urbanisation. Our
results suggest that cities might be hotspots of non-native pollinator
species (Normandin et al. 2017; Fitch et al. 2019). This
phenomenon could be driven by species that are introduced into cities
through human activities, for example, urban beekeeping (Egerer &
Kowarik 2020). Following an introduction, a species’ diet breadth,
nesting behaviour and thermal tolerance might further facilitate its
establishment in cities.
Generalist
species with strong preferences for exotic flowering plants, cavity
nesters as well as species with
thermal
tolerance that matches the urban conditions are usually good urban
invaders (Goulson 2003; Hamblin et al. 2017). However, it is
worth noticing that non-native pollinators may exacerbate conservation
risks to native wild species by competition for floral resources, nest
sites, or transmission of parasites and pathogens (Fitch et al.2019).
Pollinators differ in their life-history traits however they all depend
on floral food resources for their survival (Willmer 2011). Floral
resources are a limiting factor for the populations of all pollinators.
Furthermore, there is a strong relationship between flowering plant
species richness and pollinator richness in a community (Ollerton 2017).
Our meta-regression analyses revealed, this
trivial,
although rarely explored intrinsic link between flowering plant richness
and pollinator diversity. This relationship is of great conservation
importance as it reinforces current pollinator initiatives that argue
for flower plantings to promote pollinator diversity.
In our meta-analysis, pollination services, estimated either as seed set
or flower visit duration, increased with urbanisation.
Pollination
could be influenced by pollinator visit quantity and “quality” as well
as by the structure of the local flowering plant community that could
influence visitation rates (Bruckman & Campbell 2014). The increase in
flower visit duration as well as seed set in cities point to the
importance of the
“quality”
of the pollinator in terms of the number of compatible pollen grains
deposited on stigmas (Ne’eman et al. 2010). The increase in
flower visit duration in cities suggests a lack of a
dilution
effect and pollination efficiency due to the potentially high supply of
floral resources in urban green land uses. Plants with radial flower
morphology particularly benefited from urbanisation. Plants with radial
flowers and a central cluster of anthers typically have shallow, exposed
nectaries, making both nectar and pollen easily available to flower
visitors (Willmer 2011). Plants with these floral traits are typically
thought of as generalists (Ollerton et al. 2007) and are visited
by many wild pollinator taxa including generalist and managed bee
species that could be abundant in cities.
The positive effect of urbanisation on pollination was driven by
generalists (bumble bees) and managed bee species (honey bees). Honey
bees and bumble bees are generalist pollinators and the most important
pollinators in both natural and agricultural ecosystems (Garibaldiet al. 2013; Kleijn et al. 2015; Hung et al. 2018).
The increase in honey bee visitation rates in cities is probably due to
urban beekeeping. Urban beekeeping is currently booming with both
benefits and negative implications (Ropars et al. 2019;
Sponsler
& Bratman 2021). Urban beekeeping might help with the pollination of
urban agricultural crops and wild flowering plants and provide locally
produced honey, however, it might also lead to resource competition with
wild pollinators and to increased transmission of diseases between honey
bees and non-Apis bees (Ropars et al. 2019; Proesmanset al. 2021; Sponsler & Bratman 2021). We argue that city
authorities should regulate the intensity of urban beekeeping and future
studies should further investigate the benefits and negative aspects of
urban beekeeping for wild pollinators and pollination in cities.
Nonetheless, based on our results, it appears that urban generalists and
managed pollinators provide adequate pollination services to flowering
plants.
In conclusion, our results provide evidence that urbanisation has
negative effects on pollinator communities however these are not
necessarily translated into negative effects on pollination service
provision. While we
acknowledge
the small sample size for some of our moderators, our meta-analysis
further highlighted that Lepidoptera are the pollinator group most
affected by urbanisation, and that pollinator ecological traits as well
as local floral resource richness could mediate the responses of
pollinators to urbanisation. Regarding pollination services, our results
point towards the importance of generalist bees as well as the managed
honey bee for plant reproduction in cities. Overall, more research in
cities is needed to guide conservation actions and policies for
pollinators and pollination for food security and wild flower
reproduction.