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Enhanced urban roadside vegetation increases pollinator abundance whereas

landscape characteristics drive pollination

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DOI: 10.1016/j.ecolind.2023.109980

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 Ecological Indicators 147 (2023) 109980

Contents lists available at ScienceDirect

Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Enhanced urban roadside vegetation increases pollinator abundance

whereas landscape characteristics drive pollination
Simon Dietzel a, *, Sandra Rojas-Botero a, Johannes Kollmann a, Christina Fischer b
a
Chair of Restoration Ecology, TUM School of Life Sciences, Technical University of Munich, Emil-Ramann-Straße 6, 85354 Freising, Germany
b
Faunistics and Wildlife Conservation, Department of Agriculture, Ecotrophology, and Landscape Development, Anhalt University of Applied Sciences, Strenzfelder Allee
28, 06406 Bernburg, Germany

A R T I C L E I N F O A B S T R A C T

Keywords: Roads cause pollution, habitat degradation and fragmentation, while recent studies report that roadside vege­
Green infrastructure tation can benefit plant and insect diversity. However, the factors that drive effects of roadside vegetation on
Insect conservation pollinator abundance and pollination need further attention. Our main interest in this study was to evaluate
Pollinometer
urban roadside enhancement by identifying direct and indirect effects of local resource availability and land­
Urban landscape
Wild bees
scape characteristics on pollinator abundance and quality of pollination, by using functionally different phy­
Wildflower strip tometer plants. Thus, we established 34 species-rich wildflower patches along urban roads, and monitored
flowering species and floral density at the local scale. At the landscape scale we measured the amount of
impervious surface within a radius of 500 m around the wildflower patches, as well as edge density of all major
land-use types, and distance to the city center. As control, we used 34 patches with existing species-poor roadside
green. The abundance of pollinators, i.e., honeybees, wild bees, and hoverflies, was sampled with colored pan
traps. Pollination was monitored based on fruit number and weight of three phytometer species, i.e., Fragaria ×
ananassa, Ranunculus acris, and Trifolium pratense, that differ in flower morphology and color, and attract
different pollinators. Pollinator abundance was positively related to local richness of flowering plants and floral
density. At the landscape scale, pollinator abundance was positively related to the proportion of impervious
surface but negatively to edge density. Phytometer-specific effects on pollination were moderated by landscape
characteristics: Fruit mass of F. x. ananassa was highest in the inner city, fruit number of R. acris was lower in
areas with high edge density, whereas in T. pratense fruit number increased with edge density, and was nega­
tively related with the proportion of impervious surface. There were no indirect effects of local and landscape
factors via pollinator abundance on pollination. The study of the three phytometer species revealed that roadside
enhancement can directly support fruit production in wild plants and crops in cities. Thereby, different landscape
characteristics influenced the quality of fruit set, which also depended on individual plant reproductive adap­
tations. This stresses the importance of using a set of complementary phytometer species in pollination experi­
ments, especially to gain insights into ecosystem functioning at coarser spatial scales.

1. Introduction
During the past decades, natural and semi natural ecosystems suf­
fered from large-scale degradation, mainly caused by land-use change
and widespread intensification, with detrimental effects on biodiversity,
ecosystem functioning, and human wellbeing (Haines-Young and Pot­
schin, 2010). Since conservation of intact ecosystems is no longer suf­
ficient, new ways of restoring biodiversity and ecosystem functions are
necessary. Thus, the United Nations declared 2021–2030 as the Decade
on Ecosystem Restoration, which was critically discussed within the
scientific community regarding the most suitable concepts and restora­
tion objectives, evaluation instruments, and costs (Cooke et al., 2019;
Young and Schwartz, 2019). For example, significant efforts have been
recently made to conserve insect pollinators that are severely affected by
habitat degradation and loss, yet crucial for crop production and wild
plant populations (Potts et al., 2016). However, evaluating measures for
pollinator restoration is time consuming and expensive, and requires
expert knowledge of the target species. An alternative is the use of
phytometers, i.e., standardized plants that are exposed in an experi­
mental setting to monitor site conditions (Dietrich et al., 2013). Using

* Corresponding author.
E-mail address: simon.dietzel@tum.de (S. Dietzel).

https://doi.org/10.1016/j.ecolind.2023.109980
Received 1 August 2022; Received in revised form 17 January 2023; Accepted 3 February 2023
Available online 9 February 2023
1470-160X/© 2023 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
S. Dietzel et al.
such plants to observe plant performance while monitoring the success
of an ecological intervention is said to be an inexpensive alternative with
high effectiveness and reliability (Strobl et al., 2018).
The conflicts between intensive land use and biodiversity are
particularly pronounced in cities, though some cities harbor more
diverse insect communities than rural areas (Wenzel et al., 2020). Thus,
scientists and practitioners propose the ecological enhancement of
urban green infrastructure, and the resulting studies highlight the po­
tential of urban green space for pollinators and associated ecosystem
services (Hall et al., 2017; Baldock et al., 2019). Roadside vegetation is a
type of urban green space of high ecological potential. Even though
roads have a negative environmental impact due to pollution and
habitat fragmentation, they can also connect pollinator habitats within
the urban landscape (Phillips et al., 2020a). For example, Phillips et al.
(2020b) described roadside vegetation as “hotspots of flowers and pol­
linators” that can exceed possible barrier or ecological trap effects.
Nevertheless, there are considerable knowledge gaps on the optimal
design and enhancement of roadside vegetation and its impact on pol­
linators and pollination, particularly in urban environments.
Along most urban roads, frequently mown and species-poor road­
sides prevail (Phillips et al., 2021b), with some ornamental shrubs or
trees, albeit with little ecological benefit (Mody et al., 2020). This green
infrastructure has to endure extreme site conditions, including climatic
extremes, degraded soils and human disturbances (Bretzel et al., 2016;
Phillips et al., 2021a). Besides these local factors, pollinators face several
stressors at the urban landscape level, i.e., extensive sealed surface,
habitat isolation, and large distances to (near-)natural ecosystems
(Wenzel et al., 2020). While the conservation of individual (rare) pol­
linators can be difficult to realize in cities, the ecological functionality of
urban green space recently moved into an increased focus of attention
(Fischer et al., 2016; Dietzel et al., 2022). In order to be able to evaluate
the effectiveness of restoration measures for ecological functionality, it
is necessary to further develop field methods and also to consider indi­
rect measurement methods.
For the evaluation of an improved design and enhancement of urban
roadside vegetation, aiming at the promotion of pollinators and the
preservation of the ecosystem function of pollination, it is therefore
important to understand the relative impact of local resource avail­
ability, landscape features, and potential interactions on pollinators and
pollination. It is also necessary to differentiate between direct effects of
local and landscape scale parameters on pollinators and pollination. By
combining insect observations with phytometers that serve as pollin­
ometers, plant reproduction in terms of fruit number and weight as in­
dicator for pollination can be assessed (Bartholomée and Lavorel, 2019),
while accounting for local resource availability, landscape quality and
the location along urban roads, measured as distance to the city center
(Theodorou et al., 2017; Mody et al., 2020). Ideally, phytometers
encompass several plant species and traits (Strobl et al., 2018), and
outbreeding plant species are preferred when monitoring pollination
success (Woodcock et al., 2014). Importantly, flower color, morphology,
and phenology are considered to attract different groups of pollinators
(Rosas-Guerrero et al., 2014). In this study, we therefore combined
observations on pollinator abundance with evidence on pollination of
phytometers to understand the direct and indirect effects of enhanced
roadside vegetation and the influence of the surrounding urban land­
scape. We established experimental wildflower patches along urban
roads covering an urbanization gradient. As control, we used the exist­
ing roadside greening, i.e., grass-dominated lawns. We selected three
phytometer species to measure local and landscape scale effects on fruit
production over two months in 2020 and 2021, respectively. In parallel,
we recorded pollinator abundance with pan traps. We then created a
theoretical model based on published evidence on interactions between
local resource availability, urban landscape characteristics and their
effects on pollinator abundance and pollination (Fig. 3). In doing so, we
asked the questions whether i) enhanced roadside vegetation positively
affects pollinator abundance and accordingly increases plant
2
Ecological Indicators 147 (2023) 109980
pollination; ii) there are species-specific responses of phytometer polli­
nation to different local and landscape environmental variables; iii) the
use of phytometer plants can serve to efficiently evaluate ecological
enhancement of urban green space.
2. Methods
2.1. Study area
Field assessment was conducted within Munich, S Germany
(48.13761, 11.57991; 515 m a.s.l.) in the years 2020 and 2021. This city
has a temperate climate: the average annual precipitation is about 946
mm, and the annual average temperature 10.2 ◦ C (Bavarian State
Institute for Agriculture and German Weather Service, 2022). Munich is
characterized by a high proportion of impervious surfaces, especially in
the city center, while few large parks constitute most of the urban green
space (Fig. 1). Most agricultural land occurs at the city outskirts,
whereas some small agricultural pockets are scattered throughout the
city.
2.2. Study design
Experimental wildflower patches were set up within species-poor
lawns along four main roads from the city center to suburban areas of
Munich (Fig. 1). The wildflower patches had a size of 8 m2 (2 m × 4 m),
where grass cover and 5 cm of topsoil were removed, the subsoil slightly
harrowed, and covered with a sand-substrate mixture. Then, a specif­
ically designed seed mixture was sown, consisting of 26 regional wild­
flower species that were attractive to pollinators (Table A.1). Grasses
were not included in the seed mixture, as at least some grasses were
present in the soil seed bank. Species selection was based on phyloge­
netic diversity and functional traits to address the requirements of as
many pollinators as possible. We paid particular attention to diverse
plant growth habits, flower forms, sizes, colors, and types of reward
(pollen, nectar, Fornoff et al., 2017). Besides ecological criteria, we also
took practical considerations for adequate performance at roadsides,
traffic safety, establishment, and maintenance. Seeds were obtained
from a regional producer (J. Krimmer, Pulling), and the sowing rate was
4 g/m2 mixed with 31 g/m2 of coarsely ground corn to ensure even
distribution. After that, the substrate was rolled, while the experimental
wildflower patches were not watered at any point during the
experiment.
In spring 2019, 17 flowering patches were established, and in 2020 a
second set of 17 patches at 20 m distance (Fig. 2). In addition, we set up
nearby control plots at 55 m distance to the second experimental patch.
The minimum distance between the 17 replicates of these triplets was
1.3 km. We chose three other roads without wildflower mixtures to
establish seven distant control sites, i.e., existing roadside green with a
minimum distance of 1.3 km to flowering patches (Fig. 1). The two
control types did not differ in plant species number or floral density
(Fig. A.2).
2.3. Vegetation and pollinator sampling
Vegetation and pollinators were sampled in June, July, and August
2020 and 2021, respectively. For surveying the wildflower patches, we
documented the number of flowering plant species and the number of
floral units of every species within five 50 cm × 50 cm frames system­
atically placed in the flowering patches (Fig. 2; cf. Baldock et al., 2015).
We counted every flowering plant species within a 2 m × 4 m plot on the
species-poor control sites. To standardize flower unit data, we calculated
floral density per m2 using floral unit data from the five frame counts
(factor 0.8), averaged over the period of phytometer field exposition per
plot, and the 8 m2 control plots (factor 0.125), respectively.
Pollinator sampling was carried out with 400 ml plastic pans (15 cm
diameter), colored with luminescent paint (blue, white, yellow
S. Dietzel et al. Ecological Indicators 147 (2023) 109980

Fig. 1. Distribution of the study sites within the city of Munich, S Germany. Land-cover types of agricultural areas, impervious surfaces, traffic and vegetated areas,
and water bodies are shown. Wildflower patches were sown along four urban roads (solid lines), whereas three roads were used as distant controls without enhanced
roadsides (open lines). Around all experimental sites, proportions of land-cover types were measured within a radius of 500 m radius (circles). The location within the
urban environment was measured as distance to the city center.

Fig. 2. Experimental design for monitoring pollinators and pollination at urban roadsides depending on local and landscape factors. Only one triplet of plots is shown
(out of 17 established), containing one wildflower patch sown in 2019 (red) and one in 2020 (orange). The patches were at 20 m distance to each other, and a nearby
control plot with the standard roadside greening at 55 m distance. Within each plot, three phytometer plants per species were exposed during their respective
flowering phase, within a total duration of eight weeks. During the same time period, pollinator abundance was recorded at the study plots with blue, white, and
yellow pan traps. Plant species and floral units were counted within the wildflower patches using five 0.5 m × 0.5 m frames, whereas on species poor control plots the
entire 2 m × 4 m area was sampled. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

SPARVAR Leuchtfarbe, Spray-Color GmbH), and filled with water and a
drop of odorless detergent (Westphal et al., 2008). Pan traps were
exposed on a single pole at vegetation height (50–70 cm; 40 cm in
control plots) to avoid disturbance by dogs. Traps were exposed three
times in June, July, and August for 48 h on dry and windless days with at
least 20 ◦ C day temperature. The collected insect samples were sorted by
orders, and the number of individuals was recorded. For further anal­
ysis, we summed up the number of individuals of solitary and social wild
bees, honey bees, and hoverflies, which were considered as the most
important pollinators (Osterbye, 1975; Kipling and Warren, 2014). For
analysis, pollinator abundance and floral density were averaged for
every plot by calculating the mean values of two sampling runs,
reflecting the two terms of phytometer exposure to field conditions.
Both types of controls were integrated as single observations in the
analysis, which best reflected the actual situation in the field, where
floral density and floral species richness varied within and among study

3
S. Dietzel et al. Ecological Indicators 147 (2023) 109980

Fig. 3. Postulated direct and indirect effects of local vegetation, surrounding landscape characteristics on pollinator abundance and pollination of the three phy­
tometer species. The relationships are based on evidence in the scientific literature. An increased offer of floral resources (green arrows) was assumed as the most
important factor driving pollinator abundance (yellow arrows), followed by urban landscape characteristics (blue arrows). Since the effect of impervious surfaces is
inconclusive in the literature, its effect direction is presented likewise. Pollinator abundance was assumed to strongly affect the fruit set of the phytometers, whereas
local and landscape variables were predicted to indirectly control pollination success. (For interpretation of the references to color in this figure legend, the reader is
referred to the web version of this article.)

plots during mass flowering of just one plant species, which occasionally
occurred during sampling. Moreover, sown wildflower patches devel­
oped heterogeneously in species richness and flower numbers, depend­
ing on abiotic site conditions (shading, soils, etc.). Based on these
observations, we analyzed this gradual increase in local floral avail­
ability along roadsides rather than categorically compare treatment and
control sites.
2.4. Phytometer plants and fruit measurements
To monitor pollination, we employed three phytometer species with
complementary traits (cf. Strobl et al., 2018), i.e., the crop species Fra­
garia × ananassa (Rosaceae, garden strawberry), which is visited by a
wide range of insects. Although able to self-pollinate, it is a proven in­
dicator for pollination and frequently used to measure this ecosystem
function (Klatt, 2013; Wietzke et al., 2018). We also chose local wild
species, i.e., Ranunculus acris (Ranunculaceae, meadow buttercup) and
Trifolium pratense (Fabaceae, red clover). Ranunculus acris is more likely
to attract dipterans such as hoverflies (Kipling and Warren, 2014),
whereas T. pratense is commonly visited by long-tongued bees, but can
also be partly pollinated by non-bee nocturnal insects (Theodorou et al.,
2020a; Kanduth et al., 2021; Alison et al., 2022).
For F. × ananassa, frozen plantlets (organic frigo plants) were ob­
tained from a commercial provider. We chose the late blooming cultivar
Malwina to temporally fit the flowering phase of the wildflower patches.
Ranunculus acris and T. pratense seedlings were produced from regional
seed material (J. Krimmer, Pulling). In spring, all plants were pre-grown
in individual plastic pots in a greenhouse (TUM GHL Dürnast) under
standard conditions (substrate, water, light, temperature) until flower
buds were visible.
We marked closed inflorescences with colored strings before placing
them on the experimental plots to ensure that only data from flowers
exposed to the urban setting were included. Flower buds produced
during field exposition were marked likewise and integrated into the
data analysis. We established three plants per plot for each phytometer
species and watered them depending on weather conditions. We covered
one flower of every plant with a meshed nylon bag to test differences in
plant responses to pollinator exclusion. Fragaria × ananassa was exposed
at the plots from June to July (max. 22 d), while R. acris (max. 27 d) and
T. pratense (max. 27 d) were set out from July to August. Fragaria ×
ananassa and R. acris were exposed in 2020 and 2021, and T. pratense
only in 2021. When all marked flowers had completed flowering (i.e.,
petals withered), the phytometers were relocated to a semi-open
greenhouse (GHL Dürnast, TUM) until the fruits were fully ripe.
Especially for the strawberry plants, we experienced some losses of
phytometers due to theft and vandalism in both years, resulting in a
smaller sample size than the wild species. Ripe fruits were harvested
when indicated by their color (F. × ananassa, R. acris) or degree of
dryness (R. acris, T. pratense). After harvesting, strawberries were
weighed, and fruits of R. acris and T. pratense were counted (Theodorou
et al., 2020b).
2.5. Landscape analysis
To analyze the urban landscape around the study plots, we retrieved
land-use data from the Open Street Map Project (OSM, Open Street Map
Contributors, 2020) and processed them using ArcMap software,
Version 10.8.1 (Esri Inc., 2020). The obtained OSM land-use information

4
S. Dietzel et al.
was aggregated into superordinate categories following the Corine Land
Cover classification (EEA, 2018), representing impervious and vegetated
areas. We also considered agricultural areas and water bodies
(Table A.3). We calculated the proportion of each land-use type within a
radius of 500 m around every plot. This perimeter was suitable
considering the low- to mid-range flying distances for most pollinators
we detected in the pan traps, according to their body sizes (Zurbuchen
et al., 2010; Bennett and Lovell, 2019). Landscape heterogeneity has
been identified as an pollinator promoting factor, providing niche di­
versity in terms of potential nesting sites and food resources (Winfree
et al., 2011). To account for that, we calculated the overall edge density
by dividing the total edge length by the area of the 500-m-radius
(Godefroid and Koedam, 2007). We did not distinguish between the
edges of the different land-use types of vegetated or impervious areas, as
even edges of roads or buildings can provide suitable nesting sites (bare
soil, pitted walls) or floral resources for solitary and social wild bees
(Ballare et al., 2019). To understand spillover effects of pollinators in the
urban outskirts or filter effects in the highly urbanized inner city, we
integrated the distance of the plots to the city center into the analysis
(Mody et al., 2020).
2.6. Statistical analysis
For statistical analysis, R version 4.2.1 (R Core Team, 2021) was
used. Colinearity of independent variables was tested by calculating the
Spearman correlation coefficient, and only variables with values < |0.7|
were included in the models (Dormann et al., 2013). Since agricultural
areas were hardly present at the study sites, we excluded them from the
analysis. We also excluded urban green space area, as it was negatively
correlated with the proportion of impervious surfaces. We decided to
include impervious surfaces instead of green space area, as it best de­
scribes the anthropogenic impact on our measurements (Fortel et al.,
2014; LfU, 2017).
To test the effects of the number of pollinators on pollination failure,
we counted fruits of F. × ananassa as insufficiently pollinated when their
mass was equal to or lower than those produced by flowers with the
exclusion bags. For R. acris and T. pratense, flowers that did not produce
fruits were equally assigned. We then applied a generalized linear mixed
model with binomial distribution (glmmTMB, version 1.1.2.3; Brooks
et al., 2017), including local resource availability (plant species rich­
ness, floral density) and urban landscape characteristics (proportion of
impervious surfaces, edge density, and distance to city center) as fixed
factors, as well as their two-way interactions with pollinator abundance.
Sampling year and phytometer species were used as covariates. We used
the triplet-ID as random factor to account for spatial autocorrelation
(two wildflower plots plus local control, cf. Fig. 2). Model residuals were
checked with the DHARMa R package, version 0.4.4 (Hartig, 2022).
To test for underlying phytometer-independent effects on pollina­
tion, we performed a cross-species analysis by converting the phy­
tometer measurements to the ratio of maximum observed per species.
After square rooting, we ran a linear mixed effect models with maximum
likelihood (R package nlme, Pinheiro and Bates, 2022) with plot triplets
as random factor, and included the sampling year as well as local and
landscape variables.
To test for the effects of local and landscape parameters on pollinator
abundance and phytometer fruit production, we also calculated linear
mixed effect models with maximum likelihood (Pinheiro and Bates,
2022). To test for temporal variability, we included sampling year as
covariate. To account for spatial autocorrelation of study sites and
phytometers, we used the triplet-ID and plant-ID nested in the plots as
random effects. Dependent variables were square rooted (F. × ananassa
fruit mass, R. acris fruit number) or log transformed (T. pratense fruit
number, log(x + 1)) to meet assumptions on data distribution. Floral
density data was log transformed (log(x + 1)), as its range showed
considerable variation among control and wildflower plots (min: 0, max.
584 per m2). We followed an automatic stepwise model reduction
5
Ecological Indicators 147 (2023) 109980
approach, considering p > 0.05 and decreasing AIC.
We then conducted a path analysis to disentangle the causal re­
lationships between local flower availability, urban landscape patterns,
pollinator abundance, and pollination success, indicated by the fruit set
of each phytometer plant separately. For the path analysis, we built
structural equation models (SEM) for each phytometer species sepa­
rately (R package piecewiseSEM, Lefcheck, 2016). Based on the litera­
ture, theoretical considerations, and our hypotheses, a conceptual model
guided the expectations of the study (Fig. 3). We assumed local resource
availability and urban landscape variables to directly affect pollinator
abundance, but with varying directions and strengths. Whereas for the
phytometers, we suggested pollinator abundance strongly driving fruit
set, with indirect effects of local and landscape characteristics. The full
SEM models with all relevant factors were manually reduced, taking
account of variables with the highest p-values and decreasing AIC. From
the minimal adequate model, we extracted p-values, standard estimates,
marginal and conditional R2, and checked values of Fisher’s C exact test
(p > 0.05). Residuals of the SEMs were checked with the residuals
function of the piecewiseSEM package (Lefcheck, 2016).
3. Results
3.1. Pollinator abundance and pollination success
In total, we recorded 1114 insect pollinators, 1017 bees and 97
hoverflies, with a mean of 13.0 ± 11.8 individuals per plot (0–52) in all
six sampling rounds (June, July, August; 2020 and 2021). Mean polli­
nator abundance at the wildflower patches was 17.9 ± 12.5 individuals,
twice as high as in control plots with 8.2 ± 7.8 individuals. Domestic
honeybee (Apis mellifera) was not particularly abundant in our samples.
In 2020, mean abundance was 10.9 %, and 12.2 % in 2021. In all
models, the two sampling years significantly differed (p < 0.001), while
both years showed similar effect directions.
Fruits were produced by all marked flowers of F. × ananassa, on
average 2.0 ± 1.2 fruits per plant (1–7), with a mean fruit mass of 5.4 ±
2.8 g (0.05–13.4 g). The fruit mass of 36.9 % was equal to or lower than
the average mass of fruits from pollinator excluded flowers and there­
fore considered insufficiently pollinated. For R. acris, the average flower
number was 6.0 ± 4.7 per plant, which produced on average 13.6 ±
10.8 fruits per flower (0–59), and 10.9 % of all flowers did not produce
fruits at all. In T. pratense, there were 4.6 ± 0.8 flower heads per plant,
40.3 ± 24.4 fruits per flower head (0–111), and only 6.5 % of all flower
heads did not produce any fruits.
3.2. Factors controlling pollination
Pollinator abundance significantly affected the probability of polli­
nation (p = 0.02, Est. 0.17). We also found a significant interaction
between pollinator abundance and edge density (p = 0.03, Est. 0.02),
indicating an overall positive effect on pollination success at low and
mid values of edge density, which no longer appeared in areas with high
edge density (Fig. 4).
The results of the cross species analysis did not provide additional
insights compared to the presented SEMs as followed. We added them to
the appendix (Fig. A.5).
3.3. Local and landscape drivers of pollinators and pollination
The path analysis for each phytometer revealed differential re­
sponses of pollinator abundance to local and landscape characteristics,
and showed a lack of mediation of pollinator abundance on fruit set of
the assessed phytometers (Fig. 5). Local resource availability, i.e., plant
species richness and floral density, positively affected pollinator abun­
dance. Moreover, only in T. pratense fruit production increased with
higher floral density. Plant species richness in the wildflower plots was
also positively related. Pollinator counts increased with the proportion
S. Dietzel et al.
Fig. 4. Factors influencing pollination success of phytometer species monitored in urban roadsides. (a) positive effect of pollinator abundance on pollination success
(generalized linear mixed model, p = 0.02); and (b) edge density and pollinator abundance interactively affected pollination success (p = 0.03; R2m = 0.15, R2c
= 0.26).
of impervious surfaces in the urban landscape and fewer pollinators
were recorded in areas with high edge density. Moreover, an increase in
the proportion of impervious surfaces negatively affected seed produc­
tion only in T. pratense. In contrast, fruit production in F. × ananassa and
R. acris did not respond to the proportion of impervious surfaces. Edge
density showed an opposite effect direction on pollination depending on
the phytometer species; it negatively influenced R. acris and positively
T. pratense. The distance of the plots to the city center influenced fruit
production only in F. × ananassa, resulting in a decrease in fruit mass
with increasing distance to the city center. No direct effect of pollinator
abundance on phytometer fruit set was detected even when dividing
6
Ecological Indicators 147 (2023) 109980
Fig. 5. Results of the structural equation
models on effects controlling pollinator
abundance and pollination in the phy­
tometers Fragaria × ananassa (FA), Ranun­
culus acris (RA), and Trifolium pratense (TP).
Arrow width and bold numbers display
standardized estimates and effect directions,
and asterisks indicate level of significance
(*p < 0.05, **p < 0.01, ***p < 0.001).
Marginal and conditional R2 values from the
three models are shown. Floral density and
flowering plant species richness (green ar­
rows) increased pollinator abundance; only
floral density directly affected fruit produc­
tion of T. pratense. Urban landscape charac­
teristics shaped pollinator abundance as well
as phytometer measurements (blue arrows):
a higher proportion of impervious surfaces
caused an increase in pollinator abundance,
whereas edge density had the opposite effect.
Fragaria × ananassa fruit mass declined with
increasing distance to the city center. (For
interpretation of the references to color in
this figure legend, the reader is referred to
the web version of this article.)
pollinators in functional groups (social bees, other wild bees, hoverflies,
other dipterans).
4. Discussion
4.1. Pollinator abundance at urban roadsides
We observed a positive relationship between the number of plant
species or floral units, and pollinator abundance at the improved patches
of urban roadside vegetation. Thus, although roadsides are among the
most disturbed habitats in cities, pollinators can benefit from their
S. Dietzel et al.
transformation into more species rich vegetation (Mody et al., 2020).
Enhanced urban roadside vegetation with extensive management (i.e.,
mowing once or twice per growing season) can support pollinators
(Baldock et al., 2019; Phillips et al., 2020b), whereas landscape-scale
effects shape urban pollinator communities in abundance, diversity,
and functionality in a more differentiated way (Wenzel et al., 2020).
This confirms our hypothesis, that enhanced resource availability along
urban roadsides directly increases pollinator abundance. On the other
hand, this increase did not translate to higher fruit sets in the phy­
tometers, instead fruit production was indirectly affected by landscape
characteristics, while the drivers of this observation remain to be
elucidated. At landscape scale, the number of pollinators increased in
areas with high rates of imperviousness, which most likely occurred due
to a concentration effect of pollinators that accumulated at the most
attractive sites within highly urbanized areas (cf. Sivakoff et al., 2018).
This was accompanied by a decrease of pollinator numbers in more
heterogeneous landscapes, as we found less individuals in areas with
higher edge density. This can be explained by a dilution effect due to
improved habitat quality and resource availability, which also has been
reported in other studies (e.g. Veddeler et al., 2006; Hegland, 2014;
Kleijn et al., 2018). However, the small size of the wildflower patches,
the closeness to adjacent roads, and the traffic intensity increasing air
turbulences and pollutant inputs may have negatively affected polli­
nator abundance at the local scale (Phillips et al., 2020a; Phillips et al.,
2021a). Yet, observations in urban gardens support our findings of local
vegetation factors exceeding landscape-scale effects on pollinator
abundance in urban environments (Pardee and Philpott, 2014; Hüls­
mann et al., 2015; McDougall et al., 2022). A moderate intensity of
urbanization can be beneficial for plant and pollinator diversity, and
certain traits of plants and pollinators determine whether they are
winners or losers from urbanization processes (Banaszak-Cibicka and
Żmihorski, 2012; Cochard et al., 2017). In this field, there are still gaps
in our knowledge about which plant and pollinator traits benefit and
which are deprived by urbanization, and how urban novel communities
are composed eventually (Sattler et al., 2011; Wenzel et al., 2020).
4.2. Factors influencing fruit production
We observed failures in pollination of a significant number of flowers
in all three phytometer species. Our analysis showed that low numbers
in pollinator abundance induced a decreased probability of fruit pro­
duction of the phytometer plants. This effect interacted with edge den­
sity, stressing the significance of landscape quality for urban pollination
(Pellissier et al., 2013). Yet, pollinator abundance could be related to the
very basic level of fruit production vs. pollination failure. Thereby,
plants most likely received a higher frequency of flower visits in areas
with low resource alternatives, which lead to the observed increase in
pollination probability in homogeneous areas. A deductive interpreta­
tion of the results through phytometer measurements can therefore be
derived somewhat counterintuitively that higher fruit weights or fruit
numbers can be observed primarily in areas that offer rather poor con­
ditions for pollinators. Local enhancement in flower availability and
plant diversity, in contrast, did not foster probability of fruit production.
Phytometer plants, therefore, seem to be not a good indicator for
measuring local effects on pollination to evaluate ecological function­
ality of urban roadsides.
4.3. Variation in quality of pollination of the three phytometers
Although floral resource availability significantly drove pollinator
abundance, this effect did not translate into an increased phytometer
fruit set and therewith quality of pollination. At the landscape scale,
distance to the city center, the amount of impervious surface and edge
density directly influenced phytometer fruit production (Pellissier et al.,
2013). For F. × ananassa, we found that the location within the city
matrix significantly influenced fruit mass, with the heaviest fruits near
7
Ecological Indicators 147 (2023) 109980
the city center decreasing towards the outskirts. Related to our findings
from the pollination success analysis, a concentration of pollinators at
less abundant foraging resources in highly urbanized areas near the city
center was most likely responsible for this observation. Also, fruit
number of R. acris responded negatively to increased edge density,
whereas T. pratense fruit numbers, by contrast, increased. The quality of
pollination (i.e. fruit mass or numbers) of all used phytometer species
was therefore more likely controlled beyond the level of mere pollinator
numbers, possibly by pollinator functional or species diversity (Low­
enstein et al., 2015). Hence, more research is needed to explain these
relationships between the spatial arrangement of green spaces, their
areal dimensions and vegetation composition, and thereby identify
those landscape elements that are functionally important to form het­
erogeneous, pollinator-friendly urban environments. With this knowl­
edge, one can propose ways to improve the ecological function of
pollination, even within increasingly densified cities (Haaland and van
den Bosch, 2015).
4.4. Evaluation of roadside enhancement using phytometers
The main aim of this study was to investigate the use of low cost
experimental methods for the evaluation of ecological interventions in
cities. Our findings did not show positive interrelation between fruit
production of three functionally different phytometer species and local
vegetation enhancement; suggesting when aiming at the promotion of
pollination in cities, local increase of floral resources and plant diversity
is not sufficient. The species-specific responses in pollination, moreover,
indicate that at the local scale, relationships between plants, pollinators,
and their pollination performance combine to form interaction networks
that can change from facilitation to competition already along several
very small scales (Hegland, 2014). Therefore, when investigating the
functionality of urban green space, research should be carried out on the
scale of landscape assemblages, i.e., how associations of large and small
green space elements within urban landscape shape pollination (Lep­
czyk et al., 2017). From this point of view, our findings suggest that
employing phytometer plants with different adaptations in their polli­
nation traits can be a practical and easy-to-use tool to study landscape-
level patterns that drive pollination in cities; thus, providing conclusive
insights into the effects of urban landscape quality on ecosystem
functioning.
5. Conclusion
Enhanced urban roadsides hold great potential for species-rich urban
green space at different spatial scales. Pollinators benefit from improved
local floral resources along urban roads, while landscape characteristics
influence the pollination of plant species. Adaptations in pollination of
the used phytometers are important factors to consider when urban
green space is evaluated. Therefore, using phytometers can be a low cost
method to study urban landscape quality in terms of its ecological
functionality. Yet, simply increasing local floral resources is insufficient
to enhance pollination in urban areas. Our findings underline that it is
crucial to provide spatially well-designed urban pollinator habitats
throughout city landscapes to promote the ecosystem function of polli­
nation. For urban planning, a functional assessment of the landscape
components and their arrangement are pivotal to enhancing the func­
tionality of green infrastructure.
Funding
This study was funded by the Bavarian State Ministry of the Envi­
ronment and Consumer Protection (KP01KPB-73852) and the non-profit
Regina-Bauer-Foundation.
S. Dietzel et al.
CRediT authorship contribution statement
Simon Dietzel: Methodology, Validation, Formal analysis, Investi­
gation, Data curation, Writing – original draft, Writing – review &
editing, Visualization, Project administration. Sandra Rojas-Botero:
Formal analysis, Investigation, Data curation, Writing – review & edit­
ing. Johannes Kollmann: Conceptualization, Methodology, Formal
analysis, Resources, Writing – review & editing, Supervision, Project
administration, Funding acquisition. Christina Fischer: Conceptuali­
zation, Methodology, Formal analysis, Data curation, Writing – review &
editing, Supervision, Project administration, Funding acquisition.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgements
We thank the Master students Joana Czermin, Nadja Berger, and
Marco Giardano for their support during fieldwork, data collection, and
processing. The student assistants Anja Dichtl, Franz Haertel, Julia
Hiller, and Phoebe Koppendorfer supported insect collection and sorting
in the lab. We are also grateful to Gudrun Kloos (Department for Public
Green Space, Munich) who provided permission for our experiment.
Professional seed producer Johann Krimmer (Pulling, Germany) pro­
vided local seed material and seedlings. Master gardener Robert Hansel
(GHL Dürnast, TUM) kindly advised us on cultivation of the phy­
tometers. Earlier versions of the paper benefited from helpful comments
by the editor and two reviewers.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.ecolind.2023.109980.
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