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\begin{document}

\title{The effects of urbanisation on pollinators and pollination: A
meta-analysis}



\author[1]{Huan Liang}%
\author[1]{Yong-Deng He}%
\author[2]{Panagiotis Theodorou}%
\author[3]{Chun-Feng Yang}%
\affil[1]{Chinese Academy of Sciences Wuhan Botanical Garden}%
\affil[2]{Martin Luther University Halle Wittenberg}%
\affil[3]{Wuhan Botanical Garden, Chinese Academy of Sciences}%


\vspace{-1em}



  
  \date{May 22, 2024}


\begingroup
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\selectlanguage{english}
\begin{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.%
\end{abstract}%



\sloppy


\textbf{Reviews and Syntheses}

\textbf{The effects ofurbanisation on pollinators and pollination:A
meta-analysis}

Huan Liang\textsuperscript{1,2}, Yong-Deng He\textsuperscript{1,2,3},
Panagiotis Theodorou\textsuperscript{4,5*}\& Chun-Feng
Yang\textsuperscript{1,2*}

\textsuperscript{1}Core Botanical Gardens/Wuhan Botanical Garden,
Chinese Academy of Sciences, 430074 Wuhan, China

\textsuperscript{2} CAS Key Laboratory of Aquatic Botany and Watershed
Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, 430074
Wuhan, China

\textsuperscript{3}University of Chinese Academy of Sciences, 100049
Beijing, China

\textsuperscript{4}General Zoology, Institute of Biology,
Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany

\textsuperscript{5} German Centre for Integrative Biodiversity Research
(iDiv) Halle-Jena-Leipzig, 04103 Leipzig, Germany

\textbf{Running title:} A meta-analysis of urban effects

\textbf{E-mail addresses of all authors:}

Huan Liang, lianghuan@wbgcas.cn; Yong-Deng He,
heyongdeng20@mails.ucas.ac.cn

Panagiotis Theodorou, panatheod@gmail.com; Chun-Feng Yang,
cfyang@wbgcas.cn

\textbf{*Correspondence:}

Chun-Feng Yang, Wuhan Botanical Garden, Chinese Academy of Sciences,
Jiufeng Road 201, 430074 Wuhan, China

Phone: +86-27-8770 0874, FAX: +86-27-8770 0877, Email: cfyang@wbgcas.cn

Panagiotis Theodorou, General Zoology, Institute for Biology, Martin
Luther University Halle-Wittenberg, Hoher Weg 8, 06120 Halle, Germany

Phone: +49 (0)345 55 26511, FAX: +49 (0)345 55 27428, Email:
panatheod@gmail.com

\textbf{Statement of authorship}

HL and CFY designed the study; HL and YDH collected and undertook data
analysis; HL, PT, and CFY drafted the manuscript and participated in
data interpretation. All authors gave final approval for publication.

\textbf{Data accessibility statement}

The datasets we used in our meta-analysis will be archived in Figshare.

\textbf{Number of words, figures, tables, and references}

The number of words in the abstract is 200, and in the main text is
4837.

There are five figures, two tables and 73 references.

\textbf{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.

\textbf{Keywords:} urban, pollinator diversity, floral resources,
functional traits, plant reproductive success

\textbf{INTRODUCTION}

Urbanisation is one of the most profound drivers of anthropogenic change
with major impacts on global biodiversity (Seto \emph{et al.} 2012; Van
Klink \emph{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 \emph{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; Huang\emph{et 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 \emph{et al.} 2011) and
crops (Klein \emph{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 \emph{et
al.} 2015; Baldock 2020; Theodorou \emph{et al.} 2020b; Wenzel \emph{et
al.} 2020).

In general, urban development has negative effects on pollinators
(Faeth\emph{et al.} 2011; Fenoglio \emph{et al.} 2020; Millard \emph{et
al.}2021). Surprisingly, however, recent studies have also shown that
urbanisation can have neutral or even positive effects on pollinator
biodiversity (Theodorou \emph{et al.} 2020b; Wenzel \emph{et al.} 2020;
Millard \emph{et al.} 2021). These varying effects are hypothesised to
be due to differences at multiple levels (McKinney 2008; Faeth \emph{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
(Baldock\emph{et al.} 2015; Fenoglio \emph{et al.} 2020) and
urbanisation seems to benefit large-bodied, social, cavity-nesting,
generalist, as well as non-native species (Fitch \emph{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 (Faeth\emph{et al.} 2011; Fenoglio \emph{et
al.} 2020). Due to the high levels of urbanisation in the developed
world (Elmqvist \emph{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 \emph{et
al.} 2011; Murray \emph{et al.}2012; Theodorou \emph{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 (Baldock\emph{et al.} 2015; Theodorou \emph{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 \emph{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 (Pellissier\emph{et 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 \emph{et al.}
2013) and plants with open radial flowers attract more flower visitors
and may be less sensitive to the effects of urbanisation (Ollerton
\emph{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 \emph{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 \emph{et al.}2020; Ayers \& Rehan 2021; Maruyama \emph{et al.}
2021; Silva \emph{et al.} 2021), only two meta-analyses investigated the
overall effects of urbanisation on pollinator diversity (Fenoglio
\emph{et al.} 2020; Millard \emph{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.

\textbf{METHODS}

\textbf{Literature search and inclusion criteria}

We conducted a literature search in the ISI Web of Science and Scopus
databases (until 28 December 2021), using a combination of different
keywords depending on our research questions. To find publications
investigating the effects of urbanisation on pollinator diversity, we
used the keywords {[}urban* OR city OR cities OR town{]} AND
{[}pollinat*{]} AND {[}``species richness'' OR ``species diversity'' OR
abundance OR density OR Assemblage{]}. We replaced the last combination
with {[}trait OR phenology OR ``body size'' OR nest* OR sociality OR
diet{]} to find publications on the effects of urbanisation on
pollinator functional traits. To search for studies that investigate the
effects of urbanisation on pollination, we changed the last combination
to {[}''pollinat* service'' OR ''plant reproduc*'' OR seed OR fruit{]}.
This search yielded 719, 708 and 504 publications in Web of Science, and
454, 366 and 348 in Scopus, respectively. In addition, we also surveyed
recent reviews (e.g., Fenoglio \emph{et al.} 2020; Wenzel\emph{et al.}
2020) for relevant publications.

After removing duplicates, non-English papers and review papers, our
survey resulted in a total of 1 205 publications. The publications were
filtered by reading the title, abstract and full text according to the
following two criteria: (1) studies that reported pollinator abundance
and/or richness, phenology, nesting behavior, diet specialization, body
size, sociality, fruit set, seed set and visitation rates along
urbanisation gradients, or comparisons of urbanisation intensity within
urban, urban-rural or urban-natural land use categories; and (2)
provided numerical data and reported means, measures of variance and
sample sizes for different categories of comparison, or regression or
correlation coefficients for urbanisation gradient studies. A total of
133 publications met our criteria (Appendix S2).

\textbf{Data extraction and effect size calculation}

When two different landscape categories were compared; natural or rural
versus urban sites, we selected the most extreme category comparison
(natural versus urban; Fenoglio \emph{et al.} 2020). We obtained mean
values, sample sizes, and standard deviation from texts or tables
(\emph{mean value} -type data), for each of the two contrasting
ecosystems: control (natural, forest, rural, or suburban sites) versus
urban (urban sites). A meta-analysis may produce spurious results and
further exacerbate publication bias when excluding studies with missing
information. Therefore, we converted or imputed data from relevant
studies that report incomplete information on means, correlations,
variances and sample sizes (Koricheva \emph{et al.} 2013).

When the effect of urbanisation was measured using a continuous variable
(i.e., impervious surfaces, distance to the city centre or green area),
we extracted Pearson's correlation coefficients (r) or the coefficients
of determination (R\textsuperscript{2}; \emph{r} -type data). When none
of these values was reported, we used statistical values of parametric
tests (e.g., ANOVAs, Chi-square, t-tests; \emph{statistic values} -type
data). If these parameter values were only presented in graphs, we
estimated the values from the figures using WebPlotDigitizer
(Burda\emph{et al.} 2017). If the standard deviation was not shown in
graphs; but instead using a boxplot of minimum, maximum, first quartile
or third quartile, we estimated it according to Wan \emph{et al.}
(2014). Moreover, when all the above information was not available in
the main text, we calculated means and standard deviation or correlation
coefficients from supporting material and/or original datasets.

If a publication reported the results of several taxonomic groups or
cities separately, each was considered to be a separate observation
(Aguilar\emph{et al.} 2006). When abundance, species richness, traits,
or plant reproductive success were reported at multiple time points
(months or years), we selected the time point with the higher sample
size; if multiple time points had equal sample sizes, we chose the most
recent period of sampling, or if possible, we chose the sampling period
of maximum pollinator activity (Fenoglio \emph{et al.} 2020). For
pollination services, in addition to the fruit and seed set, the number,
rate and duration of visits were also extracted and used as proxies of
plant reproductive success (Kleijn \emph{et al.} 2015).

\textbf{Moderator variables}

\emph{Pollinator taxonomic group}

The abundance of pollinators and the number of pollinator species (or
families when species richness was not available) were extracted and
used as response variables. To assess whether the effects of
urbanisation differ between pollinator groups, we classified them
according to taxonomic affiliation; Aves, mammals, honey bees, bumble
bees, other wild bees, Lepidoptera, Diptera, and Coleoptera.

\emph{Climatic region}

We classified each study as tropical or non-tropical according to its
latitude (tropical \textless{} 23\selectlanguage{ngerman}°26'13.4'', non-tropical \textgreater{}
23°26'13.4''). We used the coordinates of each sampled city (a study
could have multiple cities) to assess the geographical and climatic
distribution of the studies. When the data were sampled in different
cities (e.g., Baldock \emph{et al.} 2015; Harrison \emph{et al.} 2018),
we took only the centroid of the respective region for simplicity and to
avoid overplotting (Maruyama\emph{et al.} 2021).

\emph{Plant and pollinator origin}

We extracted information on the origin (native or non-native) of the
pollinator and plant `pollinometer' species studied. If a species name
is given, but its origin is not available in the publication, we filled
in this information using Google scholar and other databases (references
see Appendix S2).

\emph{Pollinator and plant traits}

For pollinators, we collected several functional trait data (Table 1).
Activity length and seasonality (i.e., abundance and richness at
different seasons) data were collected for all pollinator groups. For
body size, we used the inter-tegular distance (ITD) for bees and the
wingspan for Lepidoptera. Hymenoptera pollinators were further
categorized based on (1) their nesting behaviour: above ground (tree,
wood, stem, above ground cavity) or below ground (within existing
tunnels or excavators), (2) sociality: social, solitary or parasitic and
(3) diet specialization; polylectic or oligolectic depending on if they
feed on various or a particular plant taxon (Michener 2007). Due to data
limitations, functional traits were collected mainly for Hymenoptera and
Lepidoptera (for details, see Table 1).

We categorized each flower as non-radial (e.g., \emph{Lotus} spp.) or
radial (e.g., Asteraceae) to test if flower morphology mediates the
effects of urbanisation on plant reproductive success.

\textbf{Effect size calculation andhierarchical meta-analysis}

We used Hedges' \emph{d} , weighted by sample size, as our effect
size.\emph{r} -type and \emph{statistic values} -type data were
transformed into Cohen's\emph{d} and then into Hedges' \emph{d} using
standard mathematical formulas (Koricheva \emph{et al.} 2013; Borenstein
\emph{et al.} 2021; Table S1). Hedges' \emph{d} was calculated using the
R statistical software (R Core Team 2021). In all cases, a negative
value of Hedges'\emph{d} reflects negative effects of urbanisation on
pollinator communities. Effect sizes were considered statistically
significant if their 95\% bias-corrected bootstrap confidence intervals
(CI) did not overlap with zero (Koricheva \emph{et al.} 2013; Borenstein
\emph{et al.} 2021).

Some publications provided more than one effect size, which may result
in pseudoreplication, so we carried out a hierarchical meta-analysis
that allows nesting effects within papers/studies (Tuck \emph{et
al.}2014). We included a publication-level random effect as a nesting
factor to incorporate this non-independency. We first performed a random
effects meta-analysis to calculate the overall mean effect size of
urbanisation on pollinator abundance and richness, flower abundance and
richness, functional traits, and pollination separately. Second, we
incorporated moderators, including the climatic region of the study, the
origin of the species, the taxonomic group of pollinators, and the
symmetry of the flowers. To assess the levels of the heterogeneity of
effect sizes, we calculated the P-value of the
Q\textsubscript{t}statistics. When they were statistically significant
(P \textless{} 0.05), the influence of the moderators on the effects of
urbanisation was examined using Q\textsubscript{m.}

To test whether a change in floral diversity (Hedges'\emph{d} for flower
abundance and richness) could predict a change in pollinator diversity
(Hedges' \emph{d} for pollinator abundance and richness), we fitted
maximum likelihood meta-regression models (Filazzola\emph{et al.} 2020).
The adjustment of Knapp and Hartung was then used to account for
uncertainty in the variance between studies, with overall model
significance against an F-distribution (Knapp \& Hartung 2003). All
analyses were conducted in R statistical software using
the\emph{metafor} package (Viechtbauer 2010; R Core Team 2021).

\textbf{Publication bias}

Publication bias was evaluated graphically by inspecting the asymmetry
of the funnel plots and statistically using Egger's regression tests
(Sterne \& Egger 2005). Significantly asymmetric results were then
augmented using the Trim and Fill method (Duval \& Tweedie 2000). The
Trim and Fill method estimates the number of missing studies due to
publication biases, calculates their effect sizes and standard errors
and adds them to the meta-analysis dataset. In addition, the Rosenberg's
fail-safe number was calculated. Rosenberg's fail-safe number represents
the number of non-significant, unpublished studies that must be added to
a meta-analysis to change the result from significant to non-significant
(Rosenberg 2005). A fail-safe number that is larger than 5n + 10, where
n is the number of studies used in the meta-analysis, is considered
robust (Rosenthal 1986).

\textbf{RESULTS}

We identified 133 publications and 837 observations reporting the
effects of urbanisation on pollinator abundance (228), richness (147),
phenology and functional traits (381), floral resources (58) and plant
reproductive success (116; Appendix S2). The geographical distribution
of the studies was clearly uneven (Fig. 1). More than three-quarters of
the studies were carried out in two continents (Europe 39.8\% and North
America 36.8\%), and the remaining studies were carried out in Asia
(12\%), South America (6\%), Oceania (3\%) and Africa (2.4\%).
Furthermore, 85.7\% of the studies were conducted in non-tropical
regions and only 14.3\% were conducted in tropical regions. Most studies
focused on bees and butterflies and a small number of studies involved
moths, beetles, flies, and vertebrate pollinators such as mammals, bats,
and hummingbirds (Appendix S2).

\textbf{Pollinator abundance and richness}

Overall, urbanisation had a negative effect on pollinator abundance
(\emph{d}= -0.42; 95\% CI = {[}-0.7, -0.15{]}; P = 0.003) and richness
(\emph{d}= -0.66; 95\% CI = {[}-0.96, -0.36{]}; P \textless{} 0.001;
Fig. 2). The heterogeneity of the effect sizes was large and
statistically significant for both abundance (Q\textsubscript{t} =
1450.11, df = 227, P \textless{} 0.001) and richness (Q\textsubscript{t}
= 908.31, df = 146, P \textless{} 0.001). The taxonomic identity of the
pollinator was not an important moderator of the effects of urbanisation
on pollinator abundance (Table 2). Although this moderator was not
significant, urbanisation had a significant negative effect on the
abundance of Lepidoptera (Fig. 2a). The taxonomic identity of the
pollinator was an important moderator of the effects of urbanisation on
pollinator richness (Table 2). The richness of Diptera, Hymenoptera, and
Lepidoptera was negatively influenced by urbanisation (Fig. 2b). When
the Hymenoptera were divided into bumble bees, honey bees and other wild
bees, the results were qualitatively similar. We did not detect an
effect of urbanisation on bumble bee, honey bee or other wild bee
abundance (Fig. S1).

The climatic region (tropical vs. non-tropical) did not explain the
heterogeneity of the effects of urbanisation on pollinator diversity
(Table 2). However, pollinators studied in non-tropical regions were
more severely influenced by urbanisation than in the tropics (Fig. 2a).
The origin of the pollinator was not an important moderator of the
effects of urbanisation on pollinator abundance (Table 2), however, it
was an important moderator of the effects of urbanisation on pollinator
richness (Table 2). Urbanisation had a negative effect on native
pollinator species richness and a positive effect on non-native
pollinator species richness (Fig. 2b).

Flowering plant richness had a positive effect on pollinator richness (F
= 5.838, P = 0.019; Fig. 3a, Table S2) and a positive effect, although
not statistically significant, on pollinator abundance (F = 3.490, P =
0.065; Fig. 3b, Table S2). Flowering plant abundance did not affect
pollinator biodiversity (Fig. S2, Table S2). Furthermore, urbanisation
was not found to influence the richness and abundance of flowering plant
species (Fig. S3, Table S3).

\textbf{Functional traits}

Regarding functional traits, urbanisation had a negative, although not
statistically significant effect on body size (\emph{d} = -0.16; 95\% CI
= {[} -1.46, 1.13{]}; p = 0.81, Fig. S4) and a positive, although not
statistically significant effect on activity length (\emph{d} = 1.34;
95\% CI = {[} -0.6, 3.28{]}; p = 0.18, Fig. S5). Nonetheless,
urbanisation had a strong negative effect on the abundance and richness
of spring pollinator communities (Figs 4a \& 4b). Furthermore,
urbanisation had a negative effect on the abundance of solitary bees and
on the abundance and richness of below ground nesting bees (Figs 4a \&
4b).

\textbf{Pollination service provision}

Urbanisation had an overall positive effect, although not statistically
significant, on pollination service provision (\emph{d} = 0.20; 95\% CI
= {[}-0.10, 0.51{]}; p = 0.19). The heterogeneity of the effect sizes
was large and statistically significant (Q\textsubscript{t} = 1543.29,
df = 115, P \textless{} 0.001). The pollinator groups sampled in the
studies that estimated pollination service provision differed
significantly in their contribution to plant reproductive success (Fig.
5, Table 2). Honey bees significantly boosted plant reproductive success
(Fig. 5). Flowering plants with radial flowers had an increased
reproductive success with increasing urbanisation (Table 2, Fig. 5). The
origin of plant species (native vs. non-native) did not explain the
effects of urbanisation on pollination services (Table 2). Urbanisation
had a positive effect, although not statistically significant, on the
pollination of both native and non-native plants (Fig. 5). The five
reproductive success indexes significantly explain the effects of
urbanisation on pollination (Table 2), with positive responses in
studies that estimated seed set and visitation duration; positive but
not statistically significant responses for studies that measured fruit
set and visitation rate and negative responses, although not
statistically significant, for studies that evaluated the number of
flower visits (Fig. 5). In addition, the richness and abundance of
pollinators were not significantly related to pollination service
provision (Fig. S6, Table S4)

\textbf{Publication bias}

The funnel plots were symmetric for body size and pollination service
provision (Fig. S7, Table S5). Although the funnel plots of pollinator
abundance and activity length were asymmetric (Fig. S7), the regression
estimates using the Trim and Fill method did not change. Pollinator
richness changed from significant to not significant; however, the
fail-safe number (N = 12 053) is much higher than the one required (N =
745), indicating that publication bias can be safely ignored (Table S5).
We interpreted asymmetry in funnel plots carefully given the small
sample sizes e.g., for activity length, or the lack of bidirectional
outcomes for the effects of urbanisation on some variables, e.g.,
pollinator richness, which have been found to decrease across a lot of
study systems, and thus will inevitably lead to a biased plot.

\textbf{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 (Fenoglio\emph{et al.}
2020; Millard \emph{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 \emph{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 \emph{et al.} 2020; Callaghan \emph{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 \emph{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 \emph{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 \emph{et al.} 2011; Elmqvist \emph{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 (Neame\emph{et al.}
2013; Geslin \emph{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 \emph{et al.} 2005; Pereira\emph{et al.} 2021).
Sociality is also hypothesised to be an important trait related to urban
environmental filters (Wenzel \emph{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 \emph{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 \emph{et al.} 2017; Fitch \emph{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 \emph{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 \emph{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 \emph{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 \emph{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
(Garibaldi\emph{et al.} 2013; Kleijn \emph{et al.} 2015; Hung \emph{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 \emph{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-\emph{Apis} bees (Ropars \emph{et
al.} 2019; Proesmans\emph{et 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.

\textbf{ACKNOWLEDGEMENTS}

We are grateful to all authors of the studies included in this
meta-analysis; without their previous work, this research would not be
possible. We acknowledge the financial support by the National Natural
Science Foundation of China (32100188, 31970253 and 32270243).

\textbf{CONFLICT OF INTEREST}

The authors have no conflict of interest to declare.

\textbf{ORCID}

Huan Liang https://orcid.org/0000-0003-3782-3724

Yong Deng He https://orcid.org/0000-0003-0468-1440

Panagiotis Theodorou https://orcid.org/0000-0002-4056-5300

Chun-Feng Yang https://orcid.org/0000-0002-0523-5138

\textbf{Figures and tables}

Figure 1-5

Table 1-2\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

\textbf{Figure 1} . (a) Distribution of studies included in the
meta-analyses (N=133). Circle sizes are proportional to the number of
studies. (b) Green space in cities, such as parks and road verges can
support diverse pollinators. (c) Photos of representative pollinator
taxa included in our database, left to right: mammals (e.g.,
nectar-feeding bat), Aves (\emph{Calypte anna} ), Lepidoptera
(\emph{Chaospes hemixantha} ), Hymenoptera (\emph{Halictus varentzowi}
), Diptera (\emph{Allobaccha apicalis} ), and Coleoptera (Brentidae
sp.). The first two photos were adapted from Flickr under Creative
Commons license CC BY 2.0., taken by Doug Greenberg and Becky Matsubara,
respectively. The other four photos were by Dr. Xiao-Fang Jin.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image2/image2}

\end{center}
\end{figure}

\par\null

\textbf{Figure 2} . Effects of urbanisation on (a) pollinator abundance
and (b) richness. Estimated mean effect sizes, 95\% confidence intervals
and sample size numbers of three moderators (climate region, pollinator
origin, taxonomic group) for explaining diversity are shown. *p
\textless{} 0.05, **p \textless{} 0.01, ***p \textless{} 0.001.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image3/image3}

\end{center}
\end{figure}

\textbf{Figure 3} . Relationships between change in (a) flowering plant
richness and pollinator richness and (b) flowering plant richness and
pollinator abundance. The solid black line shows the predicted
relationship and shaded areas indicate the 95\% confidence intervals.
Circles represent cases that investigated flowering plant and
pollinator diversity simultaneously, circle sizes are weighted by their
variances (1/sqrt(vi)) and different colors represent different
pollinator taxa (``mixed'' means there was more than one pollinator
order in that case study).\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image4/image4}

\end{center}
\end{figure}

\textbf{Figure 4} . Effects of urbanisation on seasonality and
functional traits of pollinator (a) abundance and (b) richness.
Estimated mean effect sizes, 95\% confidence intervals and sample size
numbers are shown. *p \textless{} 0.05, **p \textless{} 0.01, ***p
\textless{} 0.001.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image5/image5}

\end{center}
\end{figure}

\textbf{Figure 5.} Effects of urbanisation on overall pollination
services (N=116) depending on four moderators; flower symmetry,
reproductive success index, plant species origin, and pollinator group.
Estimated mean effect sizes, 95\% confidence intervals and sample size
are shown. *p \textless{} 0.05, **p \textless{} 0.01, ***p \textless{}
0.001.

\textbf{Table 1.} Description of pollinator and plant traits used in our
meta-analysis.\selectlanguage{english}
\begin{longtable}[]{@{}lllll@{}}
\toprule
\begin{minipage}[b]{0.17\columnwidth}\raggedright\strut
\strut
\end{minipage} & \begin{minipage}[b]{0.17\columnwidth}\raggedright\strut
Traits\strut
\end{minipage} & \begin{minipage}[b]{0.17\columnwidth}\raggedright\strut
Data type\strut
\end{minipage} & \begin{minipage}[b]{0.17\columnwidth}\raggedright\strut
Classification\strut
\end{minipage} & \begin{minipage}[b]{0.17\columnwidth}\raggedright\strut
Groups\strut
\end{minipage}\tabularnewline
\midrule
\endhead
\begin{minipage}[t]{0.19\columnwidth}\raggedright\strut
Pollinator\strut
\end{minipage} & \begin{minipage}[t]{0.19\columnwidth}\raggedright\strut
Seasonality\strut
\end{minipage} & \begin{minipage}[t]{0.19\columnwidth}\raggedright\strut
Categorical\strut
\end{minipage} & \begin{minipage}[t]{0.19\columnwidth}\raggedright\strut
Early spring/spring summer/autumn\strut
\end{minipage} & \begin{minipage}[t]{0.19\columnwidth}\raggedright\strut
A, D, H, L\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Activity length\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Continuous\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
-\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
H, L\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Body size\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Continuous\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
-\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
H, L\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Sociality\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Categorical\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Social/ solitary/ parasitic\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
H\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Nesting\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Categorical\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Above ground/below ground\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
H\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Diet\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Categorical\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Polylectic/oligolectic\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
H\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Plant\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Flower symmetry\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Categorical\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
Radial/non-radical\strut
\end{minipage} & \begin{minipage}[t]{0.17\columnwidth}\raggedright\strut
-\strut
\end{minipage}\tabularnewline
\bottomrule
\end{longtable}

A-Aves; D-Diptera; H-Hymenoptera; L-Lepidoptera.

\textbf{Table 2.} Summary table of meta-analysis with tests of
moderators on pollinator abundance, richness and pollination service
provision.\selectlanguage{english}
\begin{longtable}[]{@{}llllll@{}}
\toprule
Response variables & Moderators & Effect size & df & Q\textsubscript{m}
& p-value\tabularnewline
\midrule
\endhead
Abundance & Climate region & 228 & 1 & 0.07 & 0.79\tabularnewline
& Pollinator origin & 106 & 1 & 1.42 & 0.23\tabularnewline
& Taxonomic group (Order) & 214 & 4 & 5.75 & 0.22\tabularnewline
& Taxonomic group & 214 & 6 & 6.55 & 0.36\tabularnewline
Richness & Climatic region & 147 & 1 & 0.23 & 0.63\tabularnewline
& \textbf{Pollinator origin} & \textbf{20} & \textbf{1} & \textbf{9.91}
& \textbf{\textless{}0.0016}\tabularnewline
& \textbf{Taxonomic group} & \textbf{128} & \textbf{4} & \textbf{13.14}
& \textbf{0.0106}\tabularnewline
Pollination & Flower symmetry & 92 & 1 & 2.05 & 0.15\tabularnewline
& \textbf{Reproductive success index} & \textbf{116} & \textbf{4} &
\textbf{14.90} & \textbf{0.0049}\tabularnewline
& Plant origin & 99 & 1 & 0.38 & 0.54\tabularnewline
& \textbf{Flower visitor group} & \textbf{85} & \textbf{7} &
\textbf{15.36} & \textbf{0.0371}\tabularnewline
\bottomrule
\end{longtable}

Note: Significant moderators are indicated in bold.

\textbf{SUPPORTING INFORMATION}

Figure S1-7

Table S1-5

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