Introduction
Urbanization is occurring at an unprecedented rate and scale, and global
urban expansion is predicted to increase almost three-fold from 2000 to
2030 (Seto et al. 2010, 2012). Urban areas are characterized by
impervious surface such as pavement, concrete, and other human-made
structures that dominate the landscape, as opposed to pervious surfaces
such as soil or vegetation. Broadly, urban environments appear to reduce
species abundance and richness and homogenize the physical landscape and
the biological communities that occupy them (McKinney 2006, 2008, Piano
et al. 2020). As a result, urbanization may pose a threat to pollinator
communities and therefore the critical ecosystem services they provide.
Pollinators are threatened by a number of factors that may relate to or
interact with urbanization, including habitat loss, climate change,
invasive species, and pesticide use (Winfree et al. 2009, Potts et al.
2010, Vanbergen and Initiative 2013). The increase in impervious
surface, spatially disjointed development, and exacerbation of other
threats associated with urbanization are hypothesized to have
considerable consequences for pollinators and pollination services via
destruction and fragmentation of suitable habitat, changes in plant
community composition, and loss of nesting resources. However, these
potential impacts of urbanization on pollination are understudied
relative to other threats, and this has been highlighted as a critical
research direction for pollination ecology (Knight et al. 2018).
Urbanization has been repeatedly linked to lower pollinator abundance
and less diverse pollinator communities (Ahrné et al. 2009, Geslin et
al. 2016, Burdine and McCluney 2019, Pereira et al. 2020), with one city
in Brazil experiencing a 45% decline in bee species richness over 34
years of urban development (Cardoso and Gonçalves 2018). These
relationships, however, are highly variable across species, functional
traits, and scales (Bates et al. 2011, Banaszak-Cibicka and Żmihorski
2012, Geslin et al. 2016, Cardoso and Gonçalves 2018).
The ways in which urbanization influences the pollination of urban
plants is even less understood (Knight et al. 2018, Wenzel et al. 2020).
Urbanization may impact plant-pollinator interactions by changing
pollinator abundance, diversity, and behavior (Harrison and Winfree
2015). Changes in the pollinator community may in turn reduce the
quantity or quality of pollination services to plants, potentially
jeopardizing plant reproduction. For example, pollen limitation occurs
when seed or fruit production is limited by inadequate pollen receipt.
While pollen limitation is commonly observed in natural populations
(Burd 1994, Knight et al. 2005), it appears to be a major driver of
reproductive impairment for plants in fragmented habitats, such as those
in urban environments (Aguilar et al. 2006). Loss of pollination may be
especially pronounced for plants with more specialized floral morphology
because their pollination is limited to a narrow subset of pollinators.
If those pollinator species decline or are lost, there will be fewer
alternative pollinators that can provide pollination services in their
absence. For example, across several small conservation areas within an
urban matrix in South Africa, the loss of a single bee species resulted
in pollen limitation and seed set failure in six orchid species with a
specialized pollination system, while a more generalist species was
unaffected (Pauw 2007).
Effects of urbanization on plant-pollinator interactions and pollen
limitation can have implications for both wild and managed plant
communities, such as in urban agriculture. Agriculture worldwide relies
heavily on pollinators (Klein et al. 2007), and urban agriculture in
particular is becoming increasingly important for urban growth, with
almost one fifth of global food production occurring in or near urban
areas (Armar-Klemesu 2000). Cities can support equal or even greater
pollinator abundance and diversity than intensively used agricultural
areas (Hall et al. 2017, Wenzel et al. 2020), making urban agriculture
an important prospect in the face of growing food demand and concern
over the preservation of plant and pollinator populations. Urban farms
therefore provide a relevant and unique framework to study the impacts
of urbanization on pollination services.
Here, we aim to assess the effects of urbanization on pollination
services across a series of urban farms within the City of Chicago, IL,
USA. Specifically, we test whether and how pollinator visitation and
pollen limitation differ across varying levels of urbanization, as
measured by impervious surface, in two different pollination systems. We
focus on two plant species: Solanum lycopersicum (tomatoes;
Solanaceae) and Cucurbita pepo (squash; Cucurbitaceae), two
agriculturally important crops that each represent a unique pollination
morphology and ecology. Our experiment takes place within a network of
urban farm sites across a gradient of urbanization, ranging from the
urban core of Chicago, Illinois, USA out into the suburbs, to
investigate the following questions: (1) Is plant reproduction
pollen-limited at urban farm sites? (2) How does urbanization affect the
magnitude of pollen limitation? (3) How does urbanization affect
pollinator visitation? We expected plants at more urban sites to exhibit
the most pollen limitation, and that this effect would be greatest inS. lycopersicum as the more specialized species. We also
hypothesized that pollinator visitation to these species would be
negatively related to the level of urbanization. Our work helps to fill
an important gap in our understanding of how urbanization can impact
pollination services to different plant species.