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\begin{document}

\title{A conceptual framework linking pollen limitation and seed dispersal
effectiveness}



\author[1]{Laura Leal}%
\author[2]{Matthew Koski}%
\affil[1]{Universidade Federal de São Paulo}%
\affil[2]{Clemson University}%


\vspace{-1em}



  
  \date{May 21, 2024}


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\selectlanguage{english}
\begin{abstract}
Seed production and dispersal are crucial ecological processes impacting
plant demography, species distributions, and community assembly.
Plant-animal interactions commonly mediate both seed production and seed
dispersal, but current research often examines pollination and seed
dispersal separately, which hinders our understanding of how pollination
services affect downstream dispersal services. To fill this gap, we
propose a conceptual framework exploring how pollen limitation can
impact the effectiveness of seed dispersal for endozoochorous and
myrmecochorous plant species. We summarize the quantitative and
qualitative effects of pollen limitation on plant reproduction and use
Optimal Foraging Theory to predict its impact on the foraging behavior
of seed dispersers. In doing so, we offer a new framework that poses
numerous hypotheses and empirical tests to investigate downstream
effects of pollen limitation on seed dispersal effectiveness and,
consequently, post-dispersal ecological processes occurring at different
levels of biological organization. Finally, considering the importance
of pollination and seed dispersal outcomes to plant eco-evolutionary
dynamics, we discussed the implications of our framework for future
studies exploring the demographic and evolutionary impacts of pollen
limitation for animal-dispersed plants.%
\end{abstract}%



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\textbf{Hosted file}

\verb`Table 1_summary_v5.docx`  available at \url{https://authorea.com/users/598572/articles/631083-a-conceptual-framework-linking-pollen-limitation-and-seed-dispersal-effectiveness}

\textbf{A conceptual framework linking pollen limitation and seed
dispersal effectiveness}

Laura C. Leal\textsuperscript{1,2} \& Matthew Koski\textsuperscript{2}

\textsuperscript{1} Departamento de Ecologia e Biologia Evolutiva,
Universidade Federal de S\selectlanguage{ngerman}ão Paulo, Diadema, São Paulo, Brazil. E-mail:
laura.leal@unifesp.br

\textsuperscript{2} Department of Biological Sciences, Clemson
University, Clemson, SC, USA

Statement of authorship: LCL and MHK conceived the framework, LCL wrote
the first draft of the manuscript, and both contributed substantially to
revisions.

Data accessibility statement: No quantitative data was used in the
manuscript.

Type of article: Perspective Paper

Abstract: 177 words

Main text: 7492 words

Number of references: 159

Additional elements: 3 figures and 1 table.

Correspondence author: Laura Leal -- laura.leal@unifesp.br -- phone: +55
11 3385-4137



\textbf{Abstract}

Seed production and dispersal are crucial ecological processes impacting
plant demography, species distributions, and community assembly.
Plant-animal interactions commonly mediate both seed production and seed
dispersal, but current research often examines pollination and seed
dispersal separately, which hinders our understanding of how pollination
services affect downstream dispersal services. To fill this gap, we
propose a conceptual framework exploring how pollen limitation can
impact the effectiveness of seed dispersal for endozoochorous and
myrmecochorous plant species. We summarize the quantitative and
qualitative effects of pollen limitation on plant reproduction and use
Optimal Foraging Theory to predict its impact on the foraging behavior
of seed dispersers. In doing so, we offer a new framework that poses
numerous hypotheses and empirical tests to investigate downstream
effects of pollen limitation on seed dispersal effectiveness and,
consequently, post-dispersal ecological processes occurring at different
levels of biological organization. Finally, considering the importance
of pollination and seed dispersal outcomes to plant eco-evolutionary
dynamics, we discussed the implications of our framework for future
studies exploring the demographic and evolutionary impacts of pollen
limitation for animal-dispersed plants.

\textbf{Keywords:} elaiosome, frugivory, mutualistic interactions,
pollination biology, populational dynamic, optimal foraging theory, seed
disperser behavior



\textbf{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 \emph{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 \emph{et al.} 2004; Knight \emph{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)
(Knight\emph{et al.} 2005). This negative effect of PL is observed in
most Angiosperm species investigated so far (see García-Camacho \&
Totland 2009; Wolowski \emph{et al.} 2014; Burns \emph{et al.} 2019). In
the near future, the negative effects of human activities on pollinators
worldwide are expected to progressively increase PL
(González-Varo\emph{et al.} 2013; Neuschulz \emph{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 \emph{et al.}
2020; Soltani\emph{et 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 \emph{et
al.} 2013; Snell \emph{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 \emph{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 \emph{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 \emph{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 \emph{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 \emph{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 \emph{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.

\textbf{2. Effects of pollen limitation on dispersal unit and seed
traits}

PL can quantitatively and qualitatively affect the reproductive success
of plants dispersed by animals (Ashman \emph{et al.} 2004a;
Knight\emph{et al.} 2005). In fact, most of the physiological mechanisms
underlying these effects, especially the qualitative ones, are
relatively unknown, and little information that exists has not yet been
synthesized. For this reason, we summarize some of the main effects of
PL on dispersal unit traits, focusing on the traits that could be
related to seed dispersal.

\emph{2.1. Pollen limitation impacts on the dispersal unit traits}

Quantitative effects of PL on seed set are by far the most common
effects of PL reported in literature (Knight et al. 2005). Reviews on
the effect of PL on plant reproductive success are rife with examples in
which the number of fruits per plant and/or seeds per fruit were
negatively affected by the inadequacy of pollen receipt (See Burd 1994,
Ashman et al 2004, Knight et al 2005, Wolowski et al. 2014, Camacho \&
Totland 2018, Burns et al. 2019 and references therein). This negative
effect can be expected for both endozoocochorous and myrmecochorous
plant species since fruit and seed development depend on the success of
ovule fertilization regardless of the dispersal system.

In addition to its quantitative effects, PL can also strongly influence
traits of the dispersal units mediating attraction of dispersers. These
effects have been relatively neglected in pollination studies. However,
physiological studies, mainly focused on crop plant species, indicate
that such effects are likely driven by patterns of hormone secretion
during fruit development. Most hormones regulating the differentiation
of ovaries into fruits are secreted by seeds -especially auxin and
gibberellin (Osga \& Reineck 2003, Pattinson et al. 2014,
Balanguera-Lopez et al. 2020). Auxin secreted by seeds also boosts
ethylene production, another plant hormone directly driving fruit
ripening and, consequently, seed development (Balanguera-Lopez et al.
2020). By negatively affecting the number of seeds per fruit, PL can
directly interfere with the volume of hormones secreted and,
consequently, with patterns of fruit development.

For endozoocochoric plants producing fleshy fruits, the decline in the
number of seeds per fruit has been associated with changes in fruit
shape, a trait that can determine the chances of fruit removal by
dispersers (Valenta \& Nevo 2020 - but see section 3.1). Several studies
focusing on endozoochorous crop plant species such as apples
(Brookfield\emph{et al.} 1996; Buccheri \& Di Vaio 2005), kiwi (Lai
\emph{et al.}1990), cherimoya (Gonzalez et al. 2006), and grapes
(Boselli et al. 1995) have shown that the variability of fruit shapes is
higher when seed number per fruit is low. For apples and cherimoya,
specifically, the formation of misshapen fruits was associated with a
low frequency of pollinator visitation (Brookfield et al. 1996,
Matsumoto et al. 2012) and/or low pollen load (Gonzalez et al. 2006),
two of the main mechanisms leading to PL for plants (Ashman \emph{et
al.} 2004a). Therefore, dispersal units from pollen-limited flowers are
more likely to be more variable in shape than the ones from not
pollen-limited flowers.

Reduced seed number in fleshy endozoochorous fruits has also been
associated with changes in the chemical composition of the fleshy pulp,
fruit size, and the time of maturation (Pattison \emph{et al.} 2014).
Regarding pulp composition, the hormones secreted by the seeds increase
the activity and strength of fruits as a sink organ within the plant
(Balaguera-López \emph{et al.} 2020). The more seeds per fruit, the
greater the secretion of such hormones and likely the higher the
resource allocation from other plant parts to fruits (Olivieri \emph{et
al.} 1994; Knight \emph{et al.} 2006 and references therein). Therefore,
by receiving relatively fewer resources, fruits from pollen-limited
flowers should be smaller and/or less nutritionally valuable than those
from non-pollen-limited flowers (but see Petit 2011). Like the studies
investigating the relationship between seed number and fruit shape,
studies investigating the relationship between seed number, fruit size,
and pulp composition have mainly used crop plant species as models.
In\emph{Vitis vinifera} (Vitaceae), for instance, there is a strong
positive relationship among seed number, acidity, and solid soluble
content of the fruit's pulp (Boselli \emph{et al.} 1995). A similar
relationship was observed for apple lineages in which fruit size and
weight, calcium concentration, and pulp firmness was positively related
to seed number per fruit (Keulemans et al 1996, Bucheri \& Vaio 2005).
In addition to its effects on fruit composition, PL can interfere with
the timing of fruit maturation since fruits bearing more seeds tend to
mature faster (Gorchov 1985, Patterson 1990). Therefore, by reducing the
number of seeds per fruit, PL can indirectly affect not only the quality
of the pulp consumed by the frugivores but also the temporal patterns of
fruit availability to the endozoocochorous dispersers.

The effects of PL on myrmecochorous fruits should differ from those of
endozoochorous fruits because myrmecochorous fruits are not fleshy.
Myrmecochorous plants instead produce dehiscent dry fruits that shelter
a few to several diaspores comprised of a seed plus elaiosome, a lipidic
ant-attractive appendage attached to the seed that serves as a food
reward to ants (Beattie 1985). Worldwide, myrmecochorous fruits release
these diaspores in two ways (Lengyel \emph{et al.} 2010). The first and
most common is ballistic ejection of diaspores from explosively
dehiscing fruits (Rico-Gray \& Oliveira 2007). Alternatively, ripe
fruits can dehisce (sometimes while still connected to the parental
plant), dropping mature diaspores beneath the maternal plant (Gorb \&
Gorb 2003). Regardless of the strategy, disperser ants interact only
with diaspores scattered over the soil surface and are therefore, not
directly attracted to fruits. Thus, any potential PL effect on the
traits of myrmecochorous fruits should play a minor role in the
attraction of disperser ants. For this reason, we focus on the potential
effects of PL on myrmechocorous diaspore traits (seed + elaiosome).

Compared to endozoochorous fruits, there is limited data on the
physiological mechanism regulating myrmecocochorous diaspore development
and the influence of PL on it. This is especially true if we focus on
elaiosome development. Structures classified as elaiosomes can develop
from different tissues across taxa (i.e. parts of fruits, seeds, and
less frequently flowers) (Mayer et al. 2005), meaning that physiological
mechanisms governing their development should also be markedly variable
across species. Regardless of its structural origin, however, elaiosome
development still depends on ovule fertilization and patterns of plant
resource allocation to fruits (Ciccarelli \emph{et al.} 2005).
Therefore, the development of myrmechocorous diaspores should be driven
by the same general mechanisms regulating fruit and seed development in
other species. It is thus likely that pollen-limited myrmecochorous
fruits that produce fewer seeds should secrete less fruit-regulating
hormones and receive fewer resources from the maternal plant. In this
case, myrmechorous diaspores from pollen-limited flowers should be
smaller and bear a smaller and/or less nutritious elaiosome than the
ones produced by not pollen-limited flowers. These are important traits
determining diaspores attractiveness to ants---diaspores bearing larger
elaiosomes, with higher lipidic content are more likely to be removed by
ants (Mark \& Olesen 1996; Fischer \emph{et al.} 2008; Clark \& King
2012). These generalizations about the PL effect on myrmechocorous
diaspores traits, however, are still largely hypothetical due to the
lack of empirical data and remain to be evaluated.

\emph{Pollen limitation effects on seed traits}

Attributes of seed vigor, like the likelihood of seed germination and
establishment, are important for determining a seed's success
post-dispersal, regardless the dispersal mode (Baskin \& Baskin 2014).
Although not directly related to disperser's responses to dispersal
units, seed vigor may interact with disperser's responses to dispersal
unit traits (see 3.2) and consequently drive the qualitative SDE
component of animal-dispersed plant species. For this reason, the
effects of PL on this seed vigor will be included in our framework.

Theoretical models predict that PL should reduce the number of seeds
produced while increasing seed mass -- a parameter directly correlated
to seed vigor (Petit 2011; Huang \emph{et al.} 2017; Huang \& Burd
2019a, a; Lalonde \& Roitberg 2022). According to such models, by
reducing the number of fertilized ovules, PL modifies the trade-off
between seed number and seed size, increasing resources allocated to
each seed (Ida \emph{et al.} 2015). Considering that seed mass is one of
the main traits determining the chances of seed survival and
establishment (seed vigor, from now on) (Saatkamp \emph{et al.} 2014),
these models suggest that the negative quantitative effect of PL on
plant reproductive success may be compensated, at least partially, by
its positive effect on the chances of seed post-dispersal survival.
However, empirical studies evaluating the relationship between seed
number and size have reported positive (e.g. Johnston 1991), negative
(Navarro 1998; Hegland \& Totland 2007; Baskin \& Baskin 2018), or even
neutral effects (e.g. Niesenbaum 1993; Hegland \& Totland 2007, 2008;
Runquist \& Moeller 2013; Chen \& Zhao 2017). These studies have also
shown that PL can affect seed vigor even when it does not affect the
seed number/size trade-off (Winsor et al. 2000, Kalla \& Ashman 2002,
Colling 2004, Russo \emph{et al.} 2006). For instance,
in\emph{Ranunculus acris} (Ranunculaceae), a facultative bird-dispersed
species, PL did not affect the number of seeds produced per fruit but
reduced seed mass by 18\% (Hegland \& Totland 2007), a result likely
driven by a decline in the quality of pollen fertilizing the ovules.
Together, theoretical and empirical evidence indicate that PL effects on
seed vigor can vary from negative to positive, depending on the plant
species and/or conditions under which plants are grown (Baskin \& Baskin
2014, 2018).

\textbf{Indirect effects of pollen limitation on dispersers behavior and
seed dispersal effectiveness (SDE)}

Seed dispersal is a product of the foraging behavior and movement of
animals consuming fruits or diaspores (Russo \emph{et al.} 2006). For
this reason, its outcome can be directly or indirectly influenced by any
factor interfering with disperser foraging and movement decisions. Based
on the quantitative and qualitative effects of PL on plant reproduction
described above, PL has the strong potential to modify the relative
value of fruit resources to dispersers and the spatial and temporal
configuration of these fruit resources to dispersers (i.e. resource
landscape), consequently affecting the patterns of dispersers feeding,
movement, and seed transportation within the habitat (Abrahms \emph{et
al.} 2021). Therefore, the PL indirect effect on the dispersers foraging
behavior should be the main mechanism driving PL effects on SDE of
animal-dispersed plant species.

The Optimal Foraging Theory (OFT - MacArthur \& Pianka 1966) is a
valuable theoretical framework that allow us to predict the fine-scale
behavioral decisions of disperser species in response to the
quantitative and qualitative effect of PL on plant reproductive success.
According to OFT, seed dispersers make foraging decisions to maximize
their energy intake and fitness, moving between food sources accordingly
(Schoener 1971; Abrahms \emph{et al.} 2021). Dispersers are thus
expected to strategically maximize acquired energy relative to the
energetic costs of searching, handling, and consuming food resources,
consuming non-optimal food items with decreasing probability (MacArthur
\& Pianka 1966, Sobral et al. 2010, Sebastian-Gonzalez et al. 2016).
Therefore, whenever modifying the relative value of plants and/or
dispersal units to dispersers, PL can predictably modify the dispersers
foraging decisions (Westcott \emph{et al.} 2005; Russo \emph{et
al.}2006), and consequently the SDE of animal-dispersed plants. Some of
these PL-SDE effects are predictable and supported by empirical
evidence, allowing us to propose directional hypotheses about the
influences of PL on different components of SDE. However, in some cases,
the direction and strength of PL's effects on disperser's behavior still
rely on empirical evidence of PL's effects on the qualitative traits of
plant dispersal units. In these cases, we proposed non-directional
hypotheses and explored alternative scenarios as a way of fueling new
research on the underlying mechanisms driving the effects of PL on SDE.
Both directional and non-directional hypotheses are summarized in Table
01.

\emph{Indirect effects of pollen limitation on the quantitative
component of Seed Dispersal Effectiveness (SDE)}

The number of dispersal units (i.e. fruits for endozoochory; diaspores
for myrmechocory), dispersal unit size, and dispersal unit shape are the
more intuitive plant attributes that can indirectly affect the SDE
quantitative component of pollen-limited plants (Fig.1, Table 1). These
attributes are not only the main ones affected by PL but also the
primary traits influencing the disperser's foraging decisions within and
between habitats (Jordano 1987; Westcott \emph{et al.} 2005; Côrtes \&
Uriarte 2013). As such, they are the best traits to set the initial
pathways for future studies investigating indirect links between PL and
seed dispersal.

Within a given habitat, fruiting plants represent favorable foraging
patches to the dispersers, with dispersers moving non-randomly among
these plants (Westcott \emph{et al.} 2005; Côrtes \& Uriarte 2013).
Plants producing more dispersal units can be considered high-quality
foraging patches since the relatively higher abundance of food resources
to dispersers might maximize their energy intake while reducing search
costs (Russo \emph{et al.} 2006). Following OFT, it is expected then
that dispersers not only visit high-quality fruiting plants more
frequently but also leave these less frequently than the poor-quality
ones (Donahue \emph{et al.} 2003; Abrahms \emph{et al.} 2021; King \&
Marshall 2022). Therefore, by reducing the number of dispersal units
produced by the plants, PL can indirectly compromise the frequency of
disperser visits, the time of disperser residence at plants, and,
consequently, the number of seeds removed from the parental plant (Fig.1
and Table 1).

The positive relationship between the number of dispersal units produced
by plants and their attractiveness to dispersers is reported in several
empirical and theoretical studies evaluating the foraging decisions of
frugivores within and between populations of endozoocochorous plant
species. For instance, frugivorous birds (e.g. Jordano 1995, Russo 2003,
Christianini \& Oliveira 2009, Palacio et al. 2015, Guerra et al. 2017)
and mammals (e.g. Guitian \& Munilla 2010, Lambert et al. 2006, Nakagawa
et al. 2007) track fruit abundance on individual plants leading to a
positive relationship between fruit set, visitation frequency, and fruit
removal rates. Additionally, some studies have shown that frugivore's
visitation rate and duration are positively associated with the number
of seeds removed per frugivore's visit in most of the endozoocochorous
plants (e.g. Howe \& De Steven 1979; Jordano 1987; Jordano \& Schupp
2000). Thus, the negative PL effect on the plant fruit set can
indirectly compromise the seed dispersal rate, and consequently the
quantitative component of SDE of endozoochorous plants (Table 1).

Although ant dispersers do not directly interact with the myrmecochorous
fruits, variation in fruit set can also drive patterns of ant
interaction with the diaspores. Some studies have shown that ant
dispersers are more likely to interact with diaspores produced by
non-ballistic myrmecochorous plants with larger fruit sets, since the
diaspores tend to accumulate around these plants and become more
attractive to the disperser ants (Gorb \& Gorb 2000; Boulay \emph{et
al.} 2007). Even in myrmecochorous taxa with primary ballistic
dispersal, the diaspores are ejected over short distances from the
parent plant (commonly less than one meter) (Culver \& Beattie 1978;
Leal \emph{et al.} 2007; Beaumont \emph{et al.} 2009). Thus, diaspore
density should be higher near parent plants with higher reproductive
output, regardless of their primary dispersal mechanism. In this
scenario, PL can indirectly affect ant disperser decisions, which may
prefer to forage away from pollen limited myrmecochorous plants or
patches within their foraging area. If so, pollen-limited myrmecochorous
individuals should contribute disproportionally less to the seed
dispersal to other microsites than not pollen-limited ones (SDE
quantitative component) (Table 01).

In addition to the variation in the number of dispersal units, the
effects of PL on dispersal unit traits can modify their relative value
to dispersers and, consequently, the quantitative component of SDE for
the plants (Fig.01). For endozoochorous plants, as described above,
fruits bearing fewer seeds tend to be smaller, commonly offering less
nutritious rewards to dispersers (Johnson \emph{et al.} 1985; Herrera
1987). In this case, OFT predicts that the preferential consumption of
the larger fruits with higher nutritional content (i.e., those from not
pollen-limited plants) maximizes the frugivore's energetic gain per
fruit removed (May \emph{et al.} 2019; Ghosh \emph{et al.} 2020).
Indeed, there is a large body of empirical studies showing that fruit
size is one of the main traits driving the patterns of frugivores
interactions with endozoochoric fruits (Wheelwright 1993;
Woodward\emph{et al.} 2005; Martínez \emph{et al.} 2008). Additionally,
dispersers can differ in their nutritional requirements which can
mediate their preferences for fruits available in the community
(Albrecht \emph{et al.} 2018; Valenta \& Nevo 2020) Therefore, if PL
negatively affects fruit size and/or nutritional value to frugivores, it
may indirectly interfere with the frugivore visitation rate, and
consequently, the number of seeds removed from pollen-limited
endozoocochoric plants (Fig.1; Table 1).

For myrmecochorous plants, diaspore traits are the main factors
determining ant foraging preferences. In general, disperser ants
interact preferentially with larger diaspores, diaspores with a higher
elaiosome-to-seed ratio, and those bearing elaiosomes with higher
lipidic content (Gómez \emph{et al.} 2005; Boulay \emph{et al.} 2006;
Leal \emph{et al.} 2014b, a; Miller \emph{et al.} 2020). Like in
endozoochory, this preference is predicted by OFT because the higher the
elaiosome-to-seed ratio, and/or the elaiosome lipidic content, the
higher the net energetic intake for ants per diaspore removed (Bono \&
Heithaus 2002; Byk \& Del\selectlanguage{english}-Claro 2011). Therefore, PL can indirectly
modify the patterns of myrmecochorous diaspores removal whenever
negatively affecting elaiosome size and/or lipidic content. The
magnitude of the effect of PL on ant foraging preferences will depend
though on the quantification of the PL impacts on myrmecochorous
diaspores traits, which remains to be addressed in future studies (see
2.2; Table 1).

The links between dispersal unit size, nutrient content, and
attractiveness to dispersers are often linear and well explored in the
literature, allowing us to propose testable predictions about the
indirect effect of PL on the quantitative SDE component (Table 01).
However, the consequences of PL's impact on other dispersal units'
traits to the SDE quantitative component are more difficult to infer.
For instance, endozoochoric fruits from pollen-limited flowers should
differ in shape and color from non-limited ones. Both fruit color and
shape influence fruit attractiveness to frugivores (Valido \emph{et
al.}2011; Duan \emph{et al.} 2015). Therefore, PL's effect on these
traits should also affect the patterns of frugivore's interaction with
fruits. However, dispersers' responses to these traits are expected to
be more variable and context-dependent than their response to propagule
size and nutrient content. While net energy income is a universal
currency determining the success of foraging strategies across all
disperser clades, disperser's responses to fruit shape and color will
depend on the cognitive and learning ability of dispersers in
associating these traits with fruit quality (Nevo \emph{et al.} 2018).
Commonly, endozoochoric plants are visited by a diverse set of frugivore
species such as lizards (Valido \& Olesen 2019), birds (Howe 1987), bats
(Charles-Dominique \& Cockle 2001), rodents (Godo \emph{et al.} 2022),
and other mammals (Matias \emph{et al.} 2010), that largely vary in
their learning and cognitive abilities. Therefore, PL may affect the
quantitative SDE component if it results in the formation of misshapen
and/or miscolored fruits, but this effect should largely depend on the
type of seed dispersers available and their cognitive abilities (Healy
\& Jones 2002; Duan \emph{et al.} 2015) (Table 01).

Finally, PL's effects on color and shape are expected to have little or
no influence on the quantitative component of SDE for myrmecochorous
plant species. Ants use chemical cues to locate food resources within
their foraging area, including myrmecochorous diaspores and, so far, we
lack evidence that they can respond to the visual cues of the diaspores
(Sheridan \emph{et al.} 1996; Reifenrath \emph{et al.} 2012). For this
reason, PL is more likely to shape ant responses to myrmecochorous
diaspores if it affects diaspores chemical signals or concentrations,
which has never been evaluated.

\emph{Indirect effects of pollen limitation on the qualitative component
of Seed Dispersal Effectiveness (SDE)}

Pollen limitation can affect the qualitative component of SDE by
influencing: (i) the probability of pre-dispersal predation, (ii) the
frequency of long-distance dispersal events, and (iii) the probability
of seed survival and (iv) post-dispersal seed germination (Fig. 1; Table
1). PL can indirectly affect the probability of dispersal units' damage
by natural enemies in two opposing directions. For some plant species,
producing many fruits is a strategy that satiate seed predators,
ensuring that some seeds escape pre-dispersal predation and be dispersed
to potentially favorable microsites (Jordano 1987; Bonal \emph{et
al.}2007; Francisco \emph{et al.} 2008). For those plants, PL can
indirectly reduce predator's satiation when reducing fruit or seed
number and, consequently, reduce the number of seeds escaping predation.
For plants in which fruit or seed set is not associated with the
satiation of predators, PL may increase the chance of seeds escaping
predation by reducing plant attractiveness to predators. Like seed
dispersers, pre-dispersal seed predators should preferentially forage in
dense resource patches to maximize energy intake (Donahue \emph{et al.}
2003; King \& Marshall 2022). Accordingly, plants that do not experience
PL could become more attractive to pre-disperser seed predators (e.g.
Trivedi \emph{et al.} 2004; Borchert \& DeFalco 2016; Bruno \emph{et
al.} 2021). In this case, PL could indirectly benefit the plants by
reducing fruit density and, consequently, the chances of the dispersal
unit's predation before removal by an effective disperser. It is even
plausible that the negative effect of PL for dispersal due to a
reduction in plant attractiveness to dispersers may be offset by a
reduction in the chance of seed pre-dispersal predation. Such
compensation has been observed in species producing fruits rich in
secondary metabolites which simultaneously reduces attractiveness to
both dispersers and predators (see Nelson \& Whitehead 2021 and
references therein).

Future studies should consider that the effect of PL on pre-dispersal
predation will depend on 1) the magnitude of the pre-dispersal predation
effect on SDE of plants occurring in different habitats and 2) on the
relative effect of the number of dispersal units on the attractiveness
of plants to dispersers and predators. PL effects should be stronger in
plant taxa for which the impact of pre-dispersal predation on
reproductive success is strong. Similarly, PL may have a neutral or even
positive effect on pre-dispersal predation when its negative impact on
plant attraction to seed predators is equal or higher than its influence
on the attractiveness of effective dispersers. Therefore, the direction
and magnitude of PL's indirect effects on the patterns of pre-dispersal
predation are likely variable across plant species and habitats and
remain to be tested (Table 1).

By compromising seed production, PL can indirectly affect the frequency
of long-distance seed removal. Most seeds dispersed by animals are
transported over relatively short distances from the source, while only
a small subset are moved over long distances (Nathan \emph{et al.} 2008;
Schurr \emph{et al.} 2018; Rogers \emph{et al.} 2019). Long-distance
removals disproportionally influence the SDE qualitative component
(Schupp \emph{et al.} 2010) since the seeds dispersed farther from
parental plants escape the zone of density-dependent mortality near the
parental plant, increasing the chances of survival and establishment
(Howe \& Smallwood 1982; Howe \& Miriti 2000). Despite their
significance, long-distance dispersal events are rare, and their
probability is directly related to the number of seeds removed by
dispersers -- something easily observed in studies reporting dispersal
kernel plots. These plots depict a probability-density function
characterizing the dispersal distance of seeds from a common source,
assuming an equal probability of dispersal in all directions
(Nathan\emph{et al.} 2012; Rogers \emph{et al.} 2019). Studies
evaluating the relationship between seed production and the frequency of
long-distance dispersal events showed that increases in seed production
lift the entire dispersal kernel, resulting in more long-distance
dispersal events (Schurr \emph{et al.} 2018; Schupp \emph{et al.}
2019)\emph{.}These results suggests that PL can indirectly compromise
the frequency of long-distance removals whenever reducing seed
production.

To demonstrate how PL can influence the frequency of long-distance
removals, we built dispersal kernel plot predicting the
probability-density function of seed dispersal from pollen-limited and
non-pollen limited plants (Fig. 2). We simulated two datasets: one
representing the distribution of 1000 seeds, representing the seed set
of plants that do not experience PL (Fig. 2A), and another set
representing the distribution of 250 seeds (Fig. 2B), representing the
mean effect size of PL on the number of dispersal units produced by
plants estimated by Knight \emph{et al.} (2005) (75\% decline in seed
set). As expected, the dispersal kernel plot from an adequately
pollinated plant, exhibited a longer tail than the one from the
pollen-limited plant (Fig. 3), indicating that long-distance removal
events are indeed more likely for plant not experiencing PL. For the
pollen-limited plant, the maximum removal distance was 37.22\% lower
than the not pollen-limited ones. This indicates that PL's effect on
crop size can indirectly negatively affect not only the frequency of
long-distance dispersal events but also the maximum dispersal distance.
This effect of PL on the frequency of long-distance dispersal is
expected for both endozoochorous and myrmecochorous plants, because
long-distance removals are rare, regardless of dispersal mode.

In addition to its numeric effect, PL may also impact the frequency of
long-distance dispersal events through its effects on dispersal unit
traits mediating interactions with high-quality dispersers. Within a
community, seed transportation is performed by several disperser species
that disperse the seeds over different distances (Jordano \& Schupp
2000). For both endozoochorous and myrmecochorous systems, the range of
seed dispersal distance and the frequency of long-distance events
performed by a given disperser can be predicted by physiological,
behavioral, and morphological traits of the disperser species (Stanton
2003; Dehling \emph{et al.} 2014). Frugivores or ants species foraging
over larger areas, for instance, are more likely to transport seeds over
long distances and are therefore considered high-quality dispersers
(Giladi 2006; Jordano \emph{et al.} 2007; Schurr \emph{et al.} 2018;
Anjos \emph{et al.} 2020; Godinez-Alvarez \emph{et al.} 2020).
Additionally, variation in the disperser traits can also affect their
responses to dispersal units' traits, since low and high-quality
dispersers can differ in their foraging preferences (e.g. Russo 2003;
Leal \emph{et al.} 2014b; Palacio \emph{et al.} 2020). Therefore, by
influencing the dispersal units' traits, PL can indirectly affect the
assemblage of dispersers interacting with the dispersal units and,
consequently, the quality of seed dispersal received by pollen-limited
plants.

In the case of myrmecochory, omnivorous small-bodied ant species,
foraging in groups and exhibiting recruitment behavior tend to consume
the elaiosomes where the diaspores are found, rarely removing the seeds
over long distances (Gunther \& Lanza 1989; Ness \emph{et al.} 2004;
Gove \emph{et al.} 2007; Leal \emph{et al.} 2014a). Therefore, these
species are considered low-quality dispersers (Giladi 2006;
Ben-Zvi\emph{et al.} 2021). Conversely, large-bodied carnivorous ant
species are considered high-quality dispersers, responsible for most of
the long-distance removal events of myrmecochorous diaspores (Giladi
2006; Gove \emph{et al.} 2007). Interestingly, high, and low-quality ant
dispersers respond differently to diaspore traits. While high-quality
disperser ants interact preferentially with larger diaspores and
lipid-rich elaiosomes, low-quality ants exhibit weak or no response to
intra- and interspecific variation in elaiosome size and composition
(Skidmore \& Heithaus 1988; Boulay \emph{et al.} 2006, 2007;
Gammans\emph{et al.} 2006; Leal \emph{et al.} 2014b, a). Therefore, PL
can compromise the SDE qualitative component of myrmecochorous plant
species whenever influencing the diaspores traits mediating
attractiveness to high-quality dispersers (Fig. 01).

Similar to myrmecochory, frugivore body size tends to correlate
positively with home range area (Jetz \emph{et al.} 2004) and fruit
consumption per visit (Jordano \& Schupp 2000), Then, long-distance
dispersal events for endozoochorous plants rely on a small subset of
large-bodied dispersers (Howe \& Smallwood 1982; Jordano \emph{et
al.}2007; Spiegel \& Nathan 2007; Schurr \emph{et al.} 2018;
Naniwadekar\emph{et al.} 2019). Generally, high-quality large-bodied
dispersers prefer large fruits (Wheelwright 1985; Burns 2013;
Sebastian-Gonzalez\emph{et al.} 2017). Therefore, by interfering with
fruit and/or seed size, PL can reduce the chances of seed dispersal by
large-bodied high-quality dispersers, and consequently the quality of
seed dispersal service received by the pollen-limited plants (Table 1).

Following dispersal, seed germination and seedling establishment depend
on seed vigor -- a seed physiological property determining its potential
for germination, emergence, and development (sensu Rajjou \emph{et
al.}2012). Differently from the other mechanisms explored in this
section, PL's effect on seed vigor should play no role in disperser's
foraging decisions. However, this effect can directly influence the
chances of post-dispersal seed survival, germination, and establishment
and, consequently the qualitative SDE component of animal-dispersed
plants (Fig. 2). Seed vigor is ultimately determined by embryo traits
and the amount and quality of resources allocated to the seed's nutrient
reserves (e.g. endosperms). It is expected that larger seeds, with
larger embryos and/or more nutritional reserves, are more vigorous than
the smaller ones (TeKrony \& Egli 1991; Ambika \emph{et al.} 2014;
Saatkamp \emph{et al.} 2019; Reed \emph{et al.} 2022). For this reason,
any processes decreasing seed size, as in the case of PL (Ashman\emph{et
al.} 2004a; Huang \& Burd 2019), can directly compromise seed vigor and,
consequently, the outcome of all post-dispersal processes driving the
SDE qualitative component.

The PL effects on seed vigor are expected to happen on both
endozoocochorous and myrmecochorous plants since they should occur
upstream of dispersal activity. However, in endozoochorous plants, the
impact of PL on the probability of seed germination and establishment
after dispersal will be likely driving by an interaction between PL
effects on seed vigor and the efficiency of seed cleaning by dispersers.
For instance, the pulp of endozoochorous fruits, especially drupes and
berries, often contains germination inhibitors preventing seed
germination while the fruit is still connected to the maternal plant
(Robertson \emph{et al.} 2006). Pulp attached to seeds after dispersal
can also preclude germination by affecting the microenvironment for seed
germination (Meyer \& Witmer 1998; Samuels \& Levey 2005). Therefore,
post-dispersal germination of seeds from endozoochorous species will
also depend on the efficiency of dispersers in separating seeds from
pulp (see Traveset \& Verdu 2002 and references therein). This
efficiency is determined by interactions among fruit chemistry,
morphology, and disperser identity (Traveset et al. 2007 and references
therein). Because PL can directly influence fruit chemistry and
morphology and, PL could indirectly affect the patterns of fruit
handling and seed cleaning by dispersers. Thus, by affecting fruit
traits, PL can indirectly affect the efficiency of pulp removal which
can determine the capacity of post-dispersal seed germination (Table 1).

\textbf{Challenges and future directions}

4.1. \textbf{The context-dependent nature of PL and its effects on SDE}

The processes mediating direct and indirect effects included in our
framework - plant physiological responses to PL, the magnitude of PL
effects on plant reproduction, behavioral responses of dispersers to
plant and fruit traits, and SDE outcomes - are likely to be highly
variable across space and time (Ashman \emph{et al.} 2004b;
Knight\emph{et al.} 2006; Burns \emph{et al.} 2019; Schupp \emph{et al.}
2019; van Leeuwen \emph{et al.} 2022). Such variability results from
external factors that jointly impact the magnitude of PL effect on plant
reproductive success and the plant and seed disperser responses to these
effects. For the sake of brevity, we will not explore all the extrinsic
factors that can modulate PL-SDE effects. Instead, we described the main
ones in Fig. 3 to detail our rationale about the context-dependent
nature of our framework. For instance, the magnitude of PL can be
influenced by factors such as the density of plants within (e.g.
Fausto\emph{et al.} 2001), the composition and structure of pollination
assemblage (e.g. Gomez \emph{et al.} 2010), the environmental and biotic
conditions (e.g. plant and pollinator competition and predation pressure
-Benoit \& Kalisz 2020 and references therein), and the pollinator's
physiological condition (Woodard \& Jha 2017) (Fig. 3). All these
factors will likely modulate the magnitude of any PL indirect effect on
the SDE of animal-dispersal plants. In addition, the effects of PL on
plant reproduction and responses of seed dispersers to it will likely be
influenced by factors regulating patterns of plant resource allocation
and the strategies of disperser's foraging and movement, respectively.
Some of these potential factors are the plant's and dispersers'
physiological condition (e.g. Navarro 1998; Moore \emph{et al.} 2022),
competition and predation pressure of the plant and dispersers (e.g.
Houle \emph{et al.} 2010; Burgos \emph{et al.} 2022), the abundance of
alternative feeding resources to dispersers (e.g. Correa \& Winemiller
2014) (Fig. 3). Therefore, direct and indirect effects of PL on SDE
should vary predictably according to the factors regulating the
ecological processes presented in our framework.

Surely, this variability will provide challenges to future studies
evaluating part or the entire PL-SDE framework. For instance, because of
its context-dependent nature, individual study cases may not provide
robust evidence about the overall PL-SDE effects occurring in different
habitats and/or involving different species. This generalization will
only be possible in the long-term, after accumulating empirical evidence
about the mechanisms proposed here. To reach this goal, future studies
must acknowledge the context-dependent nature of their empirical
evidence, directly evaluating the mechanisms underlying PL-SDE effects
across different geographical and temporal scales whenever possible.
Because most of the mechanisms underlying our PL-SDE framework still
rely on future evidence, it would be speculative to propose directional
hypotheses about how these extrinsic factors can moderate the magnitude
of the PL-SDE effects. For instance, although the disperser's
physiological state can influence how dispersers will interact with the
fruiting plants (Warne \emph{et al.} 2019), the magnitude and direction
of such interference will depend on the magnitude and direction of PL on
fruit quantity and quality. For this reason, we understand that the set
of innovative hypotheses proposed here (Table 01) are the starting point
for investigation into PL-SDE connections. Among those, we strongly
suggest that researchers focus immediate effort on understanding PL's
direct effects on plant reproductive physiology and dispersal unit
traits - the most neglected PL effect explored in the literature. We
suggest that because all the effects described here will likely depend
on the magnitude of PL effects on plant reproductive success
(Ashman\emph{et al.} 2004b; Knight \emph{et al.} 2005; Huang \& Burd
2019). For instance, future studies should experimentally manipulate the
magnitude of PL in focal populations, measure quantitative and
qualitative effects of PL on fruits, and then ideally, relate these to
disperser feeding strategies, and ultimately dispersal within and/or
across different reproductive seasons. Alternatively, identifying
populations that experience a range of PL severity could be an
observational approach to examining our framework. Studies focused on
the downstream effects of PL on dispersal will also benefit from a
predictive approach based on OFT-- a theory that has largely benefited
our comprehension of the ecology and evolution of animal foraging
strategies, including seed dispersers (Pyke 2019).

4.2 \textbf{Population, community, and evolutionary consequences of the
PL-SDE link}

Pollination and seed dispersal outcomes have long been recognized as
ecological processes regulating plant demography, geographical
distribution, and population growth (see Baer \& Maron 2018;
Snell\emph{et al.} 2019; Dawson-Glass \& Hargreaves 2022). Our framework
adds a new layer of complexity to this scenario, showing that
pollination and seed dispersal outcomes are not independent processes in
animal-dispersed plants. This non-independence modifies our perspectives
about the pathways through which pollination can influence plant
population dynamics. It highlights the (i) pollination's role as a
moderator of population processes of animal-dispersed plants is not only
dependent on the pollination outcome itself, but also on its
consequences for ecological processes occurring after fruit maturation,
and (ii) the role of PL on population dynamics of animal-dispersed plant
species can be more pervasive than previously expected, influencing a
number of post-dispersal processes and their consequences to other
levels of biological organization (e.g. assemblage composition and
community structure).

In addition to influencing our perspectives about the role of
pollination on plant population dynamics, our framework also brings
novel and concerning implications for flowering plant populations in
human-disturbed habitats. In pristine communities, the long-term
consequences of PL-SDE effects on population dynamics will likely depend
on their consistency over time and space. In these non-disturbed
habitats, PL impacts on plant population dynamic via SDE can be
counterbalanced by the influx of transported seeds from other
populations that are not pollen-limited (Kendrick \emph{et al.} 2017),
or in the case of iteroparous plant species, by seeds produced in
subsequent reproductive seasons when PL is less severe (Schermer\emph{et
al.} 2019; but see Tye \emph{et al.} 2020). However, plant species in
human-modified landscapes experience a relatively constant or even
progressively higher PL over time (Eckert \emph{et al.} 2010;
Sapir\emph{et al.} 2015) often due to the negative effects of
anthropogenic disturbances on the richness and abundance of pollinator
assemblages (Keith \emph{et al.} 2023). In disturbed habitats, the
strong and relatively constant PL could reduce the relative abundance of
pollen-limited species, progressively shifting communities towards those
dominated by species less prone to PL (e.g. self-compatible species;
Knight (Knight \emph{et al.} 2005; Cisternas\selectlanguage{english}-Fuentes \emph{et al.}2023).
Anthropogenic disturbances also modify seed disperser assemblage,
eroding seed dispersal services provided to endozoochorous and
myrmecochorous plants in disturbed habitats (Leal \emph{et al.} 2014a;
Valiente\selectlanguage{english}-Banuet \emph{et al.} 2015). Therefore, the concomitant decline
in both pollinators and seed dispersers could synergistically compromise
plant population growth and regeneration of plants through the links
between PL and SDE in disturbed habitats, which represent about 97\% of
terrestrial ecosystems (Plumptre \emph{et al.} 2021).

Finally, demographic impacts of PL on plant populations that are
mediated through dispersal have the potential to drive eco-evolutionary
feedbacks impacting floral traits involved in pollinator attraction and
plant mating systems (Fig.3). For instance, strong PL in a given
generation could negatively impact plant densities in the following
generation due to an overall reduction in the height of the seed
dispersal kernel (Fig. 3). A low density of reproductive plants can
reduce pollinator attraction and further exacerbate PL in the following
generation (Kunin 1993; Waites \& Agren 2004; Weber \& Kolb 2013; Koski
2023). Increasingly PL should result in stronger pollinator-mediated
selection which frequently favors individuals with larger or showier
floral displays (Trunschke \emph{et al.} 2017), and/or those with a
higher capacity for self-fertilization in species with mixed mating
systems (Pannell \emph{et al.} 2015). Finally, if the seeds of plants
favored by fecundity selection are also more effectively dispersed,
their offspring have a higher chance of long-distance dispersal. Thus,
the spatial distribution of genotypes with favorable floral traits could
be wider than those with unfavorable traits following severe pollinator
limitation.

4.3. \textbf{PL-SDE framework and its caveats as an opportunity for
multidisciplinary collaboration}

Historically, different types of ecological interactions have been
studied in isolation from one another, mostly neglecting that individual
fitness emerges from the interplay of these interactions across the
individual's lifespan. To overcome this, it is fundamental to improve
the bonds among different research areas. Our framework (Fig.1) and the
testable hypotheses associated with it (Table 1) exemplify innovative
ideas arising from multidisciplinary collaborations. To propose our
framework connecting two processes for the fitness of animal-dispersed
plants, we incorporated evidence from different research areas such as
pollination and dispersal ecology, agronomy, plant physiology, and
behavioral ecology. During our literature search, the isolation between
disciplines was made clear (e.g. agronomy from pollination and dispersal
ecology). Although our framework provides a guideline for future studies
focusing on PL-SDE connections, future investigations will be challenged
by the need for new multi-disciplinary collaborations. For instance,
ecological studies on PL would benefit from collaboration with plant
physiologists and biochemists to move beyond the common quantification
of PL's effects on fruit and/or seed set. Similarly, studies focused on
SDE would benefit from inclusion of pollination biologists and
behavioral ecologist to unravel the mechanisms indirectly driving the PL
effect on different SDE components. Without incorporating theoretical
and empirical tools from different but related areas, the knowledge gaps
brought to the surface by our study will persist and prevent the
proposition of innovative questions that can change our perspectives on
the forces driving the outcome of plant-animal interactions. Therefore,
beyond connecting the knowledge from different disciplines, our PL-SDE
framework provides a valuable opportunity to reduce the isolation of
related disciplines and enhance our understanding of the role of
ecological interactions in regulating plant population and community
dynamics.

\textbf{Acknowledgments}

We would like to thank Amanda Vieira, Paulo Enrique Peixoto, and
Alexandre Palaoro for their valuable suggestions in the first draft of
this manuscript. L.C. Leal thanks Sao Paulo Research Foundation
(International Research scholarship -- 2022/02501-6), the Clemson
International Services and the Department of Ecology and Evolutionary
Ecology from the Federal University of Sao Paulo -- specially Cinthia A.
Brasileiro and Jose Eduardo de Carvalho -- for all the help along her
sabbatical at Clemson University.

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\textbf{Figure captions}

\textbf{Figure 1:} By affecting the number and the traits of dispersal
units produced by plant species dispersed by animals, pollen limitation
can indirectly interfere with the foraging decisions of disperser
animals and, consequently, with their behavior when exploring fruiting
plants (yellow boxes). These disperser behaviors are directly related to
the outcome of some of the main factors determining the quantitative
(orange boxes) and qualitative components (green boxes) of Seed
Dispersal effectiveness for animal-dispersed plants. In this scheme,
seed vigor is the only plant trait that can directly affect the
qualitative component of SDE, without interfering with the disperser
behavior. Despite it, this trait was included in the scheme for the sake
of clarity of our rationale.

\textbf{Figure 2:} Hypothetical dispersal kernel plots representing the
effect of pollen limitation on crop size and its consequences for the
distance of seeds dispersed by animals. Since it is a theoretical model,
it represents the expected seed dispersal pattern regardless the metric
unit used to measure seed dispersal distance in study cases. According
to Knight et al. (2005), pollen-limited plants produced 75\% fewer
fruits than not pollen-limited ones. For this reason, we created two
data sets simulating this mean effect on plant seed set -- 1000 seeds
for pollen-limited plants (A) and 250 for not pollen-limited ones (B).
Then, we modeled the expected distribution of these seeds over a
distance gradient following a probability-density function.

\textbf{Figure 3} : General flowchart representing a simplified version
of our PL-SDE framework, its context-dependent nature, and its
implications to populational eco-evolutionary processes. In the dashed
boxes, we pointed out the main extrinsic effects that can drive the
outcome of PL-SDE effects and its consequences to animal-dispersed
plants. We also highlight the existence of ecological and evolutionary
consequences of PL-SDE links to plant demography and plant floral
traits, respectively.\selectlanguage{english}
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\textbf{Hosted file}

\verb`Table 1_summary_v51.docx`  available at \url{https://authorea.com/users/598572/articles/631083-a-conceptual-framework-linking-pollen-limitation-and-seed-dispersal-effectiveness}

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