DISCUSSION
The greater amount of conspecific pollen on pollinators from urban areas
suggests those pollinators exhibit greater short-term foraging
specialization than pollinators in natural sites. This finding was
corroborated by the higher species richness and diversity of pollen on
pollinators from natural sites, suggesting that pollinators in natural
sites visit more plant species during foraging trips. Finding greater
specialization among urban pollinators was contrary to our hypothesis
based on ecological theory that greater interspecific competition leads
to greater species-level specialization in resource use (Lawlor &
Smith, 1976). As expected, urban sites had lower insect species
richness, but this did not translate into lower specialization. On the
contrary, we found no relationship between insect species richness and
specialization. A possible reason for the discrepancy with theory is
that the lower specialization we found in natural areas could result
from effects of species richness on interspecific competition being
mediated by pollinator abundance. Total abundance of pollinator species
in our study sites is unknown, but it is plausible that even in cases
where species richness is high, low species evenness could prevent
interspecific competition from driving short term specialization.
Among the possible drivers of short-term specialization examined in this
study, we found several that may have acted synergistically to cause
urban pollinators to carry higher amounts of conspecific pollen than
pollinators from natural sites. First, total floral abundance of the
plant community was positively associated with higher conspecific pollen
amount, and the number of flowers per plant species was greater in urban
areas. Since there was no difference in plant species richness between
site types, it follows that pollinators would carry more conspecific
pollen in urban areas. Why might total floral abundance at the site
level predict conspecific pollen amount on individual pollinators? Most
pollinators do not have fixed affinities for certain plants (Waser et
al., 1996) and will continue to forage on flowers of particular species
when those flowers are sufficiently rewarding that travel costs incurred
by passing up flowers of less abundant species are low (Heinrich, 1979;
Waser, 1986). In addition, pollinators spend longer on flowers if there
is more, or higher quality nectar present (Thomson, 1986), which might
facilitate the accumulation of more pollen. In contrast, pollinators are
more likely to switch plant species when they consistently encounter
flowers of a particular species that are rewardless (GrĂ¼ter et al.,
2011). It is possible that pollinators experience rewarding flowers more
often than pollinators at natural sites because of the higher number of
flowers in urban sites. It is also possible that floral reward is
greater in urban sites due to an overall lower abundance of pollinators,
or more favorable ecological conditions such as moisture levels that
promote production of more flowers or flowers with greater rewards.
Moisture levels are higher in the urban sites used in this study (Tables
S2-S4; Figure S4), so investigating whether the higher water
availability translates into higher floral reward in urban sites would
thus be worthwhile.
Second, common pollinators were more specialized at urban sites than at
natural sites. Relative to natural sites, average conspecific pollen
amounts increased by 54% and 23% for A. mellifera and B.
vosnesenskii in urban sites. The increase in specialization of these
common species coupled with their greater abundance at urban sites
likely contributed to the higher conspecific pollen amounts found on
pollinators at urban sites. Third, pollinators carried more conspecific
pollen when caught on invasive plants, and floral abundance of invasive
plants was higher than that of non-invasive plants in urban areas.
Therefore, the preferential foraging on flowers of invasive species
likely led to the greater conspecific pollen amounts on pollinators in
urban sites. The high amounts of conspecific pollen on pollinators
foraging on invasive plants suggests that pollinators exhibit high
fidelity to invasive plant species in our urban sites. As for all plant
species, pollinator preference for invasive plants is context specific,
and tends to depend on the size of floral display, quality of food
resources, or plant density (Brown et al., 2002; King & Sargent, 2012).
The most common invasive species across sites in our data set were Wild
Radish (Raphanus raphanistrum ), Wild Mustard (Sinapis
arvensis ), and Hairy Vetch (Vicia villosa ). Each of these tend
to be present at high densities and have high amounts of nectar or
pollen reward (Davis et al., 1998; Marchand et al., 2015; Sahli &
Conner, 2007). Our finding that pollinators have higher floral fidelity
to invasive species motivates future research into how floral reward or
plant density may differ between native and invasive plants and how
these differences may influence pollinator choices in urban
environments.
Another potential driver that may contribute to the higher
specialization we observed for urban pollinators is the amount of energy
pollinators may need to spend acquiring sufficient resources in
different environments. The importance of pollinator movement to the
acquisition of sufficient resources is largely unknown (Harrison &
Winfree, 2015), but pollinators have been observed to spend longer
amounts of time in urban flower patches than in large continuous
countryside populations (Andrieu et al., 2009). Urban landscapes are
characterized by large regions of inhospitable habitat over which
pollinators may need to travel to reach food resources. This longer time
spent in urban fragments presumably allows pollinators to recoup
energetic costs of travel among patches. After arriving in an urban
patch, pollinators may be likely to continue foraging on the same
species of plant and not expend energy learning to manipulate
alternative floral types. The extent to which pollinators move among
urban fragments in our study area would be a valuable future research
direction.
Our findings have implications for plant species coexistence both in
urban and natural areas. On the one hand, the negative frequency
dependence in pollinator preference suggests a mechanism by which plant
species may coexist with one another and persist in urban fragments. On
the other hand, pollinator preference for invasive species may
facilitate invasive plant spread and loss of rare native plant species.
Many studies have reported positive relationships between urbanization
and invasive plant abundance (Bradley & Mustard, 2006; George et al.,
2009; Seabloom et al., 2006). Our results highlight a mechanism that may
underlie this pattern, whereby pollinator fidelity to invasive plants
facilitates their persistence in urban environments. Our results also
suggest that pollinator foraging choices may facilitate invasive plant
spread in natural areas. Pollinators were even more specialized when
they were caught foraging on invasive plants in natural environments
than they were when caught foraging on invasive plants in urban
environments. The fidelity to invasive plants, in both urban and natural
areas, suggests that rare native plant species may receive many fewer
visits by pollinators than common, invasive species. This may be
particularly problematic for the persistence of rarer native plants in
urban areas that are present at low abundance. Urban pollinators caught
on native plants still carried on average 53% conspecific pollen, but
this percent dropped to 42% for native plants that were present at less
than 20% frequency, and it dropped to 29% for plants that were present
at a frequency of 10% at the study sites. These decreases the
proportion of conspecific pollen with increasing rarity of native plants
suggest that continued augmentation of urban flora, along with removal
of invasive species may therefore be necessary to maintain plant species
diversity at these sites.
To our knowledge this is the first study that quantifies conspecific and
heterospecific pollen carriage of pollinators in natural and urban
sites. The conspecific pollen proportions found on pollinators suggest
there is a greater potential for conspecific pollen transfer among
plants in urban areas than in natural areas. It is worth noting that we
did not explicitly measure flower constancy, so we cannot know if
pollinators moved among flowers of the same individual plant or among
flowers of different individuals. Self-incompatible plants cannot
produce seeds unless they receive pollen from a different conspecific
individual (Castric & Vekemans, 2004). Therefore, it will be worthwhile
to explore whether the greater conspecific pollen proportions found on
urban pollinators are reflective of visits to single plant individuals
or several different plants of the same species.