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.