Drivers of spatial variation in patterns of HP receipt
While there is a growing body of literature describing among-species differences in the intensity and diversity of HP receipt (reviewed in Morales & Traveset 2008, Ashman & Arceo-Gómez 2013, Arceo-Gómez et al. 2019a), little has been done to understand the extent and potential drivers of within-species variation in HP receipt across spatial scales. Here I briefly outline and provide evidence for four non-mutually exclusive and likely interlinked sources of within-species variation in HP receipt (Fig. 1). The first two (Fig. 1a-b) are related to the abundance and spatial distribution of the HP recipient, whereas the remaining two (Fig. 1c-d) are related to changes in the surrounding plant and pollinator community.
I and II. Density and fine-scale spatial arrangement of conspecific flowers - I) It is well known that variation in conspecific flower density can influence pollinator attraction, flower visitation rate, conspecific pollen deposition and overall reproductive success (e.g. Rathcke 1983, Kunin 1997, Hegland & Boeke 2006, Spigler & Chang 2008). What has been less explored, however, is how variation in conspecific flower density influences pollen transfer dynamics with co-flowering species, i.e. HP donation and receipt (Waal et al. 2015, Thomson et al. 2019; Fig. 1a). For instance, as conspecifics decrease in density across the landscape HP receipt can be expected to increase as a result of increasing pollinator visits to heterospecific flowers (Thomson et al. 2019, Ashman et al. 2020). Waal et al. (2015) found support for this prediction in an experimental study with South African daisies. They found an increase in HP receipt with decreasing conspecific density leading to reduced fecundity in populations of low relative abundance (Waal et al. 2015). However, it has also been proposed, that HP receipt may increase with increasing conspecific flower density as plants become larger and/or more frequent targets for HP delivery, particularly from wind-pollinated HP donors (Parra-Tabla et al. 2020). The direction of the relationship between conspecific density and HP receipt may thus depend on the pollination system (wind vs animal-pollinated) of the main HP donor. These predictions however, require further testing.
II) It has also been shown that density-dependent effects on HP receipt can be influenced by plant species’ spatial distribution within a site, particularly when pollinators respond to fine-scale (within meters) spatial patterns of flowering species distribution (e.g. intermixed vs isolated; Fig. 1b Thomson et al. 1982, Hanoteaux et al. 2013, Thomson et al. 2019). For instance, experimental studies have shown that within-species patterns of HP transfer dynamics can vary significantly between isolated, patchy and intermixed arrays of plants within a site (Bruckman & Campbell 2016, Thomson et al. 2019), with HP receipt typically increasing in intermixed arrays. Waal et al. (2015) even show evidence suggesting that the spatial aggregation of plants can buffer against the increasing incidence of HP receipt that occurs with decreasing conspecific density. It has further been shown that within-species variation in the diversity and intensity of HP receipt can be more than two times higher than among-species variation within a single community (Arceo-Gómez et al. 2016b), thus supporting the idea that fine-scale spatial drivers of HP receipt are at play. Overall, the evidence so far suggests that within-species patterns of HP receipt can vary extensively within and across communities, generating complex geographic mosaics of HP transfer and receipt. Population-level differences in pollen transfer dynamics may in turn lead to a mosaic of adaptive landscapes (discussed below) if population differences in HP receipt persist over time (e.g. Arceo-Gómez et al. 2016a, Fang et al. 2019). However, to my knowledge, very few studies have evaluated the extent and drivers of spatial variation in HP receipt within a species, which has limited our understanding of its potential evolutionary consequences.
III and IV. Co-flowering and pollinator community composition - III) The intensity and diversity of HP receipt in individual species may also vary with varying pollinator species composition across the landscape (identity, abundance and diversity; Herrera 1988, 1995), as pollinators vary in the size and diversity of HP loads they transfer (Fig. 1c; e.g. King et al. 2013, Arceo-Gómez et al. 2016b, Minnaar et al. 2019b). For instance, Johnson and Ashman (2019) showed that 70% of variation in the composition of HP loads transferred among plants across 13 communities in Hawaii was the result of differences in pollen loads transported by Apis mellifera . As a result, most of the site‐to‐site variation in HP receipt within a species was attributed to differences in the abundance of this introduced pollinator species (Johnson & Ashman 2019). In another study Kay et al. (2019) showed that hawkmoths vary extensively in the amount of HP transferred amongClarkia species, suggesting that the presence/absence of this pollinator can have large effects on overall HP transfer dynamics. Changes not only in the identity, but in the overall diversity of the flower visiting insect community, have also been predicted to lead to extensive changes in patterns of HP receipt (e.g. Arceo-Gómez et al. 2016b, Ashman et al. 2020). With HP load size predicted to increase with increasing pollinator diversity (Arceo-Gómez et al. 2016b).
IV) Fluctuations in plant species composition have also been shown to have large impacts on patterns of HP receipt (Fig. 1d). These changes in HP receipt can be mediated by variation in plant species identity, diversity and even in the functional trait composition in a community (e.g. floral trait similarity; Eaton et al. 2012). For instance, the abundance of a single plant species in co-flowering communities in Hawaii significantly altered patterns of HP receipt, with plants receiving smaller HP loads and being less connected via HP transfer in sites where it was dominant (Johnson & Ashman 2019). In another study, Arceo-Gómez and Ashman (2014a) showed that Mimulus guttatusplants receive up to four times more HP depending on the overall diversity of the plant community where they occur. Changes in plant community composition may not only alter overall HP load size and diversity but also the identity of the interacting partners. For instance, a recent study showed that the presence of one (invasive) species (Cirsium arvense ) causes a rearrangement of HP transfer interactions in the community, such that some HP transfer interactions disappear while new ones emerge (Daniels & Arceo-Gómez 2020). This reorganization of HP transfer interactions may also have the potential to alter species’ evolutionary trajectories within a community (Ashman & Arceo-Gómez 2013). What is evident from these studies, is that the intensity, diversity and identity of HP loads on individual recipient species can vary extensively across the landscape as a result of changes in plant and pollinator community composition, including the addition of invasive and non-native plants and pollinators to native communities. Moreover, even in cases where plant and pollinator community composition remain relatively constant, the identity of pairwise plant-plant interactions via HP transfer could still vary across communities, as it has been shown in plant-pollinator interaction networks (Carstensen et al. 2014). It is evident that individual plant species can experience large variation in the surrounding plant (e.g. Arceo-Gómez & Ashman, 2014a, Albor et al. 2019) and pollinator community (Herrera 1988, Cosacov et al. 2008), and evidence suggesting this plays a key role in mediating within-species variation in HP transfer dynamics is rapidly accumulating (e.g. Arceo-Gómez & Ashman 2014a, Ashman & Johnson 2019, Kay et al. 2019). In spite of this, and although studies have evaluated spatial changes in overall pollen transfer network structure (e.g. Emer et al. 2015, Tur et al 2016), to my knowledge no study has documented the extent to which changes in community species composition mediate within-species variation in HP receipt across a wide geographical scale.