Introduction
Different aspects of the drivers of plant species distribution and
abundance have been studied. Three main drivers are usually suggested to
shape plant species distribution and abundance: abiotic factors,
dispersal and biotic interactions (Soberon, 2007; Boulangeat, Gravel, &
Thuiller, 2012). Abiotic factors, such as soil moisture, temperature,
and nutrient availability, influence species distribution and abundance
in relation to a species’ fundamental niche (Chase and Leibold 2003).
Limited dispersal ability can prevent a species from reaching suitable
habitats, even if these are available. Conversely, excellent dispersal
ability can enable a species to colonize unsuitable sites through
continuous immigration (Pulliam 2000). Biotic interactions, including
both competition and facilitation among plant species, as well as
interactions at other trophic levels such as predation, herbivory, and
pollination, can also influence species distribution and abundance
(Meier et al. 2010).
Pollinators can mediate indirect plant-plant interactions by acting as
vectors, even between non-neighboring individuals, due to their ability
to move freely and cover long distances. While pollinators provide the
essential function of pollination, they can also have negative effects.
Recent studies have shown that among other things, pollinators can
transfer viruses between different species (Fetters 2023). More
importantly, pollen mixes from different species can move between
different donor and recipient species, a mechanism known as
interspecific pollen transfer. Interspecific pollen transfer has two
components: conspecific pollen loss and heterospecific pollen
interference (HPI hereafter) (Morales and Traveset 2008; Ashman and
Arceo-Gómez 2013). Conspecific pollen loss refers to the reduction of
pollen transferred between conspecific flowers due to loss to a
heterospecific recipient. HPI refers to the reduction in reproductive
output in the presence of heterospecific pollen (HP hereafter), despite
the presence of conspecific pollen (CP hereafter) that could fertilize
the ovules. HPI thus can potentially impact the female fitness of the
recipient species through reduced seed set (Morales and Traveset 2008),
while conspecific pollen loss can impact the male fitness of the donor
species (Waser 1978) through reduced pollen transfer.
Previous studies have explored HPI between native and alien species
(e.g. Suárez-Mariño, Arceo-Gómez, Sosenski, & Parra-Tabla,
2019;Malecore, Berthelot, Kleunen, & Razanajatovo, 2021). However, to
the best of our knowledge, no study has specifically addressed the role
of interspecific pollen transfer and in particular of HPI between
co-occurring rare and common native species. Given that species
distribution and abundance are crucial factors in determining a species’
endangerment status, understanding the mechanisms of heterospecific
pollen interference for rare species could provide insights for both
in-sit and ex-situ conservation strategies aimed at preserving plant
populations.
To mitigate HPI, plant species can either avoid or reduce heterospecific
pollen deposition or evolve tolerance to it (Arceo-Gómez, Raguso, &
Geber, 2016;Streher, Bergamo, Ashman, Wolowski, & Sazima, 2020;Hao,
Fang, & Huang, 2023). Avoidance or reduction mechanisms can occur at
the pre-pollination stage through alterations in flower phenology,
development of flower restrictiveness, reliance on specialized
pollinators, or the use of different deposition sites on the
pollinator’s body (Montgomery and Rathcke 2012). Tolerance mechanisms
occur at the post-pollination stage through pollen-stigma or
pollen-pollen interactions. Tolerance is expected to evolve after
exposure to heterospecific pollen. Therefore, in a plant community, if
no avoidance or reduction mechanism prevents heterospecific pollen
deposition, we can expect co-flowering species sharing common
pollinators to evolve mechanisms to tolerate HPI.
In a co-flowering plant community, it is expected that overall common
and abundant species receive more frequent visits from pollinators,
while rare species receive fewer visits. Thus, according to the
tolerance hypothesis (Hao et al. 2023), both rare and common species
should be adapted to receive heterospecific pollen from other common
species. On the other hand, both common and rare species should receive
heterospecific pollen less frequently from other rare species. A reduced
exposure means a lower need and chance to adapt to potential negative
effects from heterospecific pollen. We predict that both common and rare
species will experience HPI from rare donors but not from common donors.
The breeding system or self-compatibility of donor and recipient species
could be another factor determining the strength of HPI for co-occurring
species. Self-incompatible species present either mechanical or chemical
mechanism to avoid self-pollination (de Jong & Waser 1993), and these
mechanisms might similarly help in avoiding HPI. Thus, self-incompatible
species could be better equipped against HPI. In a conservation context,
self-compatibility could represent in some cases the only way for small
populations to persist, thus a higher susceptibility to HPI for rare
self-compatible species could further endanger them.
Another factor that has received attention in relation to HPI is the
recipient-donor species relatedness. For example, due to similar
recognition mechanism, it could be that only pollen from closely related
species germinate on the stigma of the recipient species. Therefore, HPI
might be reduced among distantly related species. While in a previous
study we showed that the phylogenetic distance between recipient and
donor species did not affect the overall strength of HPI (Malecore,
Berthelot, Kleunen, & Razanajatovo, 2021), this pattern could change
depending on the commonness or rarity of recipient and donor species.
In this study, we conducted hand-pollination experiments on a total of
eight co-occurring and co-flowering species, collected from wild
populations in Switzerland. Five of these species are rare, and three
are common in Switzerland. We will refer to species rarity or commonness
as species status. We performed pairwise heterospecific pollen crosses
as well as conspecific control treatments and measured seed set and seed
number as our outcome variables. Seed set and seed number serve as
proxies for reproductive success. We asked following questions: 1) Does
heterospecific pollen reduce seed set and seed number for common and
rare recipient species and does this reduction depend on recipient and
donor status? 2) Does heterospecific pollen reduce seed set for
self-compatible and self-incompatible recipient species and does this
reduction depend on recipient and donor self-compatibility? 3) Does
heterospecific pollen interference depend on recipient and donor
relatedness? By addressing these questions, we aimed to shed new light
on the complex interplay of factors that determine the distribution and
abundance of plant species within co-flowering communities. Ultimately,
gaining a deeper understanding of the mechanisms underlying
heterospecific pollen interference could help inform conservation
efforts aimed at preserving endangered species.