1. Introduction
Pollination is crucial for sexual reproduction in flowering plants. Over
80% of Angiosperms (including 75% of crop species), rely on animal
vectors for pollen transport between or within flowers (Herrera and
Pellmyr 2002, Ollerton et al. 2011). When pollen deposition is
inadequate to fertilize all available ovules, plants face pollen
limitation (PL) (Ashman et al. 2004a). Such pollen inadequacy can
be driven by various mechanisms, such as the low frequency of effective
pollinator visits and/or low quantity or quality of conspecific pollen
deposited in the stigmas (Ashman et al. 2004; Knight et
al. 2005). Regardless of the mechanism, meta-analyses compiling the
effect sizes of PL on fruit and/or seed production have shown that
pollen-limited plants can produce, on average, 75% less fruits and/or
seeds than pollen-supplemented flowers (not pollen-limited) (Knightet al. 2005). This negative effect of PL is observed in most
Angiosperm species investigated so far (see García-Camacho & Totland
2009; Wolowski et al. 2014; Burns et al. 2019). In the
near future, the negative effects of human activities on pollinators
worldwide are expected to progressively increase PL (González-Varoet al. 2013; Neuschulz et al. 2016), raising concerns
about the impacts of PL on the reproductive success and population
dynamics of plant species in pristine and human-disturbed habitats (e.g.
Knight 2004; Ward & Johnson 2005; Freitas et al. 2020; Soltaniet al. 2021).
Despite PL being a pivotal subject in plant reproductive biology, one
important consequence of PL has received little to no attention: its
effect on seed dispersal effectiveness, especially for plant species
dispersed by animals. The seeds of many Angiosperms, including 25-80%
of temperate and 50-90% of tropical species flora, are animal-dispersed
(Jordano & Schupp 2000). For those plants, variation in seed
recruitment and the spatial distribution of plants is dictated by the
outcome of disperser-plant interactions (Jordano 1995; Galetti et
al. 2013; Snell et al. 2019). Because the magnitude of PL
experienced by a population directly impacts the quantity and quality of
dispersal units (i.e. unit of propagation of a plant species and, in our
case, the entity located and removed by the disperser animals) produced
by a plant, PL could have cascading effects on the dynamics of
plant-disperser interactions, patterns of post-dispersal seed success,
and ultimately, on the spatial distribution of plants.
A search on the Web of Science database reveals that this link between
PL and seed dispersal has been dismissed, at least in part, due to the
non-integrative nature of studies evaluating the outcomes of pollination
and seed dispersal to plants. In February 2023, we found 3,765 and
20,219 studies focusing on PL or plant seed dispersal,
respectively (Boolean operators: “pollen limitation” OR “plant seed
dispersal”). However, only 328 studies (8.7% of total PL studies and
1.1% of total dispersal studies) focused on any connection between
these two ecological processes (Boolean operators: “pollen limitation”
AND “plant seed dispersal”). This suggests that most studies
quantifying PL and/or evaluating its effects on plant reproductive
success neglect natural processes following seed formation. Similarly,
studies describing the dynamic of seed dispersal by animals have focused
on a spatial snapshot of a particular dispersal system, mostly
neglecting the pre-dispersal processes driving the availability of
dispersal units, such as PL. Considering that pollination and seed
dispersal are two of the most threatened processes regulating plant
demography and regeneration (Neuschulz et al. 2016), we propose
an integrative approach that allow us to evaluate the interplay between
these processes, improving our ability to predict and manage plant
populations in different ecological scenarios.
Here, we present a new conceptual framework about the mechanisms through
which PL can directly and/or indirectly affect the outcome of seed
dispersal by animals (Fig. 1). We incorporate the quantitative and
qualitative effects of PL on plant reproduction (pre-dispersal
processes) into the Seed Dispersal Effectiveness approach (SDE) – the
most common approach used to evaluate the outcome of seed dispersal for
plant species. According to the SDE, the outcome (or effectiveness) of
seed dispersal for a given plant is determined by the product of the
number of seeds dispersed by all dispersers in the community
(quantitative component) and the probability that dispersed seeds
survive to adulthood (qualitative component) (Schupp et al.2010). While providing a valuable guide for SDE quantification, this
approach still neglects the role of the pre-dispersal processes, such as
PL. To bridge this gap, we first describe the direct effects of PL on
quantitative and qualitative traits of dispersal units produced by
animal-dispersed plants. Several of these effects can interfere with the
value of a plant population as a foraging patch to dispersers, as well
as the value of dispersal units as a food resource to dispersers
(Donahue et al. 2003; Valenta & Nevo 2020). Then, we use Optimal
Foraging Theory (OFT) (MacArthur & Pianka 1966) to predict how the
effects of PL on dispersal units can affect disperser foraging behavior
and, consequently, quantitative and qualitative components of SDE.
Finally, we discuss the consequences of this indirect link between two
key ecological processes for the ecological and evolutionary dynamic of
animal-dispersed plants. To bolster our framework, we use two of the
most common types of seed dispersal observed in nature as models:
endozoochory (i.e. seed dispersal by frugivores that ingest the fruits
while visiting the mother plants - Soltani et al. 2018) and
myrmecochory (i.e. seed dispersal by ants that transport the diaspores
to their nest – observed in more than 23,000 Angiosperm species -
Lengyel et al. 2010). Using these dispersal strategies, we
propose scenarios in which PL should affect specific outcomes for
dispersal, hoping to spur novel research directions on the subject.