Discussion
Urbanization is a prominent form of land use change, but we do not have
a clear picture of how urban development influences interspecific
interactions, including those that occur among plants and pollinators.
This understanding is important not only for wild plant populations but
also for the pollination services that generate food production for
humans (Klein et al. 2007, Ollerton 2017). Across a network of urban
farms spanning a gradient of urbanization in the city of Chicago, we
found that pollen limitation increases with increasing urbanization for
one of our two study species. In S. lycoperscium , we found that
both ecologically and agriculturally important measures of pollination
success were consistently limited by pollination services. We observed
pollen limitation across all sites, but critically, the magnitude of
pollen limitation was greater at more urban sites with greater
surrounding impervious surface. In contrast, for C. pepo , we
found little evidence of pollen limitation, although seed set was
pollen-limited at our most urban site. Consistent with our hypothesis,
impervious surface increased the magnitude of pollen limitation of fruit
set, however, this was a marginal and weak effect that we did not find
for seed set. Our results suggest that the increase in impervious
surface associated with urbanization can have negative consequences for
the pollination and reproduction of plants, but the extent to which this
occurs should depend on the plant species and its pollination ecology.
We tested for pollen limitation in two species, providing insight to how
susceptible a specialized versus generalized plant species may be to
increased pollen limitation in response to urbanization. Solanum
lycopersicum , which relies on a subset of bees with specialized
foraging behavior (buzz pollination), exhibited nearly ubiquitous pollen
limitation that was greater in magnitude at sites in more heavily
urbanized areas. Cucurbita pepo , which can be pollinated by the
majority of bees as well as other insect pollinators, displayed much
more variable fruit and seed production and little evidence of pollen
limitation. Our findings are consistent with broad trends between pollen
limitation and land use change, where plants in urban habitats are
generally more pollen-limited than those in natural or managed
landscapes, and those that are specialized on a particular pollinator
group may be especially vulnerable (Bennett et al. 2020). However,
urbanization likely has varying effects between species and study
systems, and these patterns in pollen limitation have only been observed
when broadly comparing urban to non-urban plants between different sites
(Bennett et al. 2020), as opposed to the same species in urban vs.
non-urban sites or across an urbanization gradient. Studies that
investigated the effects of urbanization at the species level have
focused on reproduction in wild plant species and thus far reported
mixed results. Species have exhibited similar reproduction between urban
and rural sites (Verboven et al. 2012, Barker and Sargent 2020), greater
pollen limitation in urban sites (Hou et al. 2019, Carper et al. 2022),
or less pollen limitation in urban sites, although this was in an
invasive species (Parker 1997). While our results are consistent with
the idea that specialized plant species are more susceptible to pollen
limitation in urban habitats, we only investigated one species each for
generalized and specialized pollination systems. Research incorporating
multiple specialized and generalized species within the same system is
needed to understand whether and how this pattern persists more broadly.
Patterns in pollination services should also be assessed across a
gradient of urbanization rather than placing sites into discrete urban
or non-urban categories. Even within our heavily urbanized sites
(impervious surface > 60%), we observed substantial
variation in pollen limitation and visitation, suggesting that responses
to urbanization are complex and may depend not only on whether a habitat
is urban, but the degree of urbanization as well as other factors beyond
impervious surface. Local habitat characteristics such as the amount of
available green space, gardening practices used in surrounding areas,
and floral and nesting resources from home gardens and other plantings
are likely to vary considerably across the urban landscape and could
play an important role in shaping pollinator communities. Additionally,
environmental factors such as heat, light, and soil moisture can affect
tomato reproduction by limiting pollen production, pollen viability, and
fruit production (Dingley et al. 2022). Because we were working within a
set of established and functioning urban farms in different areas of
Chicago, we could not control for small-scale variation in conditions
such as heat and sunlight, or neighborhood influences like the
surrounding floral landscape and nearby pesticide use. Studies that have
examined pollinator communities across urbanization gradients have been
able to identify local habitat factors that may interact with or offset
effects of landscape-level urbanization alone, such as floral resources,
pollinator foraging regime, habitat patch size, and season (Williams and
Winfree 2013, Choate et al. 2018, Rivkin et al. 2020, Birdshire et al.
2020, Gruver and CaraDonna 2021). Indeed, in both species, reproductive
success was variable across sites in the supplemental pollination
treatment where plants should be receiving sufficient pollen, and was
particularly low at a site with an intermediate level of impervious
surface (66.7%), providing evidence that other factors we did not
examine are affecting reproduction. Our results highlight the need for
more studies addressing the impacts of urbanization along urbanization
gradients rather than landscape categories, and incorporating local
habitat characteristics, to tease apart the relationships among
urbanization, pollination services, and plant reproduction, and the
mechanisms driving them (Wenzel et al. 2020).
If crops are pollen-limited in response to urbanization as we have shown
for sun gold tomatoes, then urban farms, especially those in heavily
urbanized areas, are likely underproducing. Understanding the drivers of
pollination services and pollen limitation in urban areas is necessary
to improve crop production at urban farms and support the reproduction
of wild and managed plant populations in or near urban habitats.
Pollinator visitation rates to S. lycopersicum flowers decreased
with impervious surface, suggesting that reduced visitation rates are
part of the explanation for the increase in pollen limitation at more
urban sites. Pollen limitation is a consequence of insufficient pollen
receipt, which could be the result of a deficit in either the quantity
or quality of pollen received. Pollen limitation could increase with
urbanization as a result of low pollinator visitation, as decreases in
pollinator abundance and richness have been observed in response to
urbanization across a range of systems and taxa (Ahrné et al. 2009,
Geslin et al. 2013, Fortel et al. 2014, Choate et al. 2018, Cardoso and
Gonçalves 2018, Pereira et al. 2020). These declines are likely due to a
combination of factors such as habitat fragmentation and loss of floral
or nesting resources and could substantially reduce visitation to plants
in these areas. Declining pollinator populations in response to
urbanization might explain the contrasting patterns we found between our
focal species. The lower visitation rates and greater pollen limitation
seen in S. lycopersicum , which relies on bees capable of
sonication, may reflect a reduced abundance of these pollinators.Cucurbita pepo , which can be pollinated by many bees as well as
other insect pollinators, may have a greater buffer against declining
pollinator populations as it can utilize a much broader range of
visitors.
On the other hand, the pollen limitation and visitation patterns we
observed may be related to more nuanced changes in plant-pollinator
interactions rather than overall pollinator abundance. Specifically,
changes in pollinator community composition or foraging behavior could
also be limiting plant reproduction by decreasing the quality of
pollination services provided to plants. There is support for the idea
that urban and suburban areas can serve as refuges to pollinators, with
neutral or even positive impacts of urbanization on pollinator groups
like bees (Carper et al. 2014, Hall et al. 2017, Theodorou et al. 2017),
especially when compared to primarily agricultural landscapes (Wenzel et
al. 2020). In Chicago specifically, studies have found diverse wild bee
communities that support pollination services to plants, where bee
richness was most related to floral diversity rather than impervious
surface (Lowenstein et al. 2015, Gruver and CaraDonna 2021). However,
the pollinator community differed in that highly urban areas housed more
non-native bee species and fewer native species than less urban areas
(Gruver and CaraDonna 2020, 2021).
The increase in pollen limitation and lower visitation rates that we
observed in S. lycopersicum in response to urbanization may
therefore reflect shifts in pollinator community composition.
Pollination of S. lycopersicum was carried out primarily by
solitary bees we could not identify in the field, followed by bumblebees
(Bombus spp.). Bombus visitation was not related to
impervious surface, suggesting that their abundance or pollination
behavior is not strongly driving pollen limitation, despite being one of
the most studied and commonly used group of pollinators for supplemental
pollination in S. lycopersicum (Cooley and Vallejo-Marín 2021).
Visitation by other, smaller bees decreased marginally with
urbanization. The decreased pollinator visitation and greater pollen
limitation we found in S. lycopersicum at more urban sites are
therefore likely driven by these other bee species. Although their buzz
pollination behavior and efficiency is less studied, smaller and often
solitary bees such as Lasioglossum , Melissodes , andAugochlora spp., are capable of buzz pollination and were
frequently observed sonicating our plants and more broadly across
Chicago (Cardinal et al. 2018, Rosi-Denadai et al. 2020, Gruver and
CaraDonna 2021). In an area where bee abundance was greater in urban
than non-urban sites, pollen limitation was still greater in urban areas
for two of the three species studied, and this was linked to lower
receipt of conspecific pollen for plants in the urban sites (Carper et
al. 2014, 2022). These results coincide with patterns of bees in urban
landscapes visiting a greater number of plant species overall, but a
lower proportion of available plant species, likely due to greater plant
richness (Baldock et al. 2015, Theodorou et al. 2017). Pollinator visit
and search durations have also been shown to increase in urban areas,
which could decrease overall visitation rates (Andrieu et al. 2009).
Pollination services may also be changing in response to less studied
abiotic characteristics of urbanization such as pesticide use, the urban
heat island effect, or anthropogenic air pollution (Wenzel et al. 2020,
Bloom et al. 2021, Descamps et al. 2021), which has been found to reduce
floral visits by pollinators by as much as 83–90% (Ryalls et al.
2022).
Taken together, our results suggest that pollination deficits can
increase with urbanization, and there are likely multiple interacting
factors underlying this relationship. Understanding the drivers behind
decreased pollination services in urban areas can help us develop best
practices for improving pollination services in the future. We
demonstrate here that between two plant species, the more specialized
was more pollen-limited and received lower pollinator visitation in
response to increasing urbanization when compared to the generalized
species. Strategies for encouraging pollinator visitation to crops to
increase yield could focus on providing habitat and planting resources
that support a range of pollinators, particularly those that visit both
specialist and generalist plant species, although the utility of these
strategies needs to be empirically tested with data. Further research
that considers multiple species across urbanization gradients and longer
time scales, with additional local and landscape level factors, is
necessary to understand the mechanisms behind the observed pollination
deficits that increase with urbanization.