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.