INTRODUCTION
Over fifty percent of the earth’s land surface has been converted for
human use (Ritchie & Roser, 2019). Given recently observed declines in
pollinator populations (Goulson et al., 2015), understanding links
between urbanization and plant-pollinator interactions is of increasing
importance. Almost 90% of flowering plants are animal-pollinated
(Ollerton et al., 2011), and one-third of crops require pollinators to
produce fruit (Kearns et al., 1998). Declines have been reported in all
major groups of pollinators (Regan et al., 2015), which are associated
with declines in plant populations (Biesmeijer et al., 2006). While land
conversion from natural to urban areas has been proposed as a major
driver of pollinator decline (Bates et al., 2011; Forister et al., 2019;
Hernandez et al., 2009), other work has challenged the assumption that
urbanization is universally detrimental to pollinators (Baldock et al.,
2015; Owen, 2010; Saure, 1996). Effects of urbanization tend to be
species-specific, with some species increasing and others decreasing in
abundance in urban areas (Cane et al., 2006; Matteson et al., 2008;
Carre et al., 2009). This may reflect differences in the ability of
individuals of certain species to exploit patchy urban floral resources,
or a lack of continuously blooming flowers that result in insufficient
food intake of pollinators with certain phenologies.
Given ongoing land conversion, remnant or restored natural habitat
within urban areas will be increasingly important refuges of pollinator
biodiversity (Goddard et al., 2010). The extent to which habitat
fragments can support pollinator biodiversity depends on whether there
are sufficient floral resources from which pollinators can obtain food,
and whether these resources persist over time. Pollinators are expected
to maximize their net energy intake while foraging (Stephens & Krebs,
1986), and their foraging choices depend on the distribution of floral
resources, the energetic value of those resources, and the local
ecological context (MacArthur & Pianka, 1966). Therefore, pollinator
foraging choices may promote the persistence of outcrossing plants if
ecological conditions facilitate pollinator transfer of conspecific
pollen among plant individuals (Aguilar & Galetto, 2004).
Plant receipt of conspecific pollen is facilitated by short-term
specialization of pollinators on particular plant species. Several
non-mutually exclusive mechanisms can drive short-term specialization,
including flower constancy and frequency dependence in plant choice.
Flower constancy occurs when pollinators forage primarily on the same
plant species within a single trip (Waser, 1986; Wissel, 1977), which
can be facilitated by interspecific competition (Brosi & Briggs, 2013;
Futuyma & Moreno, 1988). Decreases in flower constancy lead to greater
heterospecific pollen transfer among plants and reduced plant
reproductive success (Brosi & Briggs, 2013; Galen & Gregory, 1989).
Frequency dependence in plant choice occurs when there is a relationship
between plant relative abundance and pollinator preference for that
species (Krebs & others, 1989). Pollinators have been observed to
exhibit both positive and negative frequency dependence in plant choice
(Rushing et al., 2006), which are thought to occur due to difficulties
in efficiently foraging on multiple floral types consecutively (Chittka
& Thomson, 1997).
Optimal diet theory predicts positive frequency dependence in plant
choice (MacArthur & Pianka, 1966), but results of past examinations of
plant relative abundance as a driver of pollinator foraging choices have
been mixed (Eckhart et al., 2006; Schmid et al., 2016; Benadi & Pauw,
2018). Both positive and negative frequency dependence in plant choice
can drive short term specialization, but they have different effects on
plant species persistence in small habitat fragments. Negative frequency
dependence is predicted to lead to species coexistence, but positive
frequency dependence is predicted to lead to the decline of rare species
(Chesson, 2000, but see Molofsky & Bever 2002).
Here, we test five hypotheses regarding how short-term ecological
specialization of pollinators may change in urban environments. We first
characterize visitation of pollinators to plants and pollen loads on
pollinators’ bodies, and we quantify the amount of conspecific pollen
relative to heterospecific pollen carried by pollinators in natural and
urban sites across a major urban in California. We then test the
hypotheses that (1) the amount of conspecific pollen carried by
pollinators is higher in natural sites than in urban sites; (2)
pollinators exhibit positive frequency dependent foraging across site
types; (3) pollinators carry more conspecific pollen at sites with less
heterogeneous plant communities; (4) pollinators carry more conspecific
pollen at sites with more heterogeneous pollinator communities; (5) the
abundance of floral resources at a community level facilitates
short-term pollinator specialization.