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 (Brookfieldet al. 1996; Buccheri & Di Vaio 2005), kiwi (Lai 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 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 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 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 et
al. 1994; Knight 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. InVitis vinifera (Vitaceae), for instance, there is a strong
positive relationship among seed number, acidity, and solid soluble
content of the fruit’s pulp (Boselli 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 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 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 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.
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 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 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 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 et al. 2006). For instance, inRanunculus 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).
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 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 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 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 et al. 2005; Russo 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.
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 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 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 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 et al. 2003; Abrahms 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 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 et al. 2007; Beaumont 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 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 et al. 2019; Ghosh 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; Woodwardet al. 2005; Martínez et al. 2008). Additionally,
dispersers can differ in their nutritional requirements which can
mediate their preferences for fruits available in the community
(Albrecht 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 et al. 2005; Boulay et al. 2006;
Leal et al. 2014b, a; Miller 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‐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 et al.2011; Duan 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 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 (Godó et al. 2022),
and other mammals (Matías 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 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 et al. 1996; Reifenrath 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.
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 et al.2007; Francisco 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 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 et al. 2004; Borchert & DeFalco 2016; Bruno 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 et al. 2008;
Schurr et al. 2018; Rogers et al. 2019). Long-distance
removals disproportionally influence the SDE qualitative component
(Schupp 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 (Nathanet al. 2012; Rogers 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 et al. 2018; Schupp et al. 2019).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 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 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 et al. 2007; Schurr et al. 2018;
Anjos et al. 2020; Godínez-Alvarez 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 et al. 2014b; Palacio 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 et al. 2004;
Gove et al. 2007; Leal et al. 2014a). Therefore, these
species are considered low-quality dispersers (Giladi 2006; Ben-Zviet 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 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 et al. 2006, 2007; Gammanset al. 2006; Leal 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 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 et al.2007; Spiegel & Nathan 2007; Schurr et al. 2018; Naniwadekaret al. 2019). Generally, high-quality large-bodied dispersers
prefer large fruits (Wheelwright 1985; Burns 2013; Sebastián-Gonzálezet 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 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 et al. 2014;
Saatkamp et al. 2019; Reed et al. 2022). For this reason,
any processes decreasing seed size, as in the case of PL (Ashmanet 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 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 & Verdú 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).
Challenges and future directions
4.1. 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 et al. 2004b; Knightet al. 2006; Burns et al. 2019; Schupp et al. 2019;
van Leeuwen 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. Faustoet al. 2001), the composition and structure of pollination
assemblage (e.g. Gómez 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 et al. 2022),
competition and predation pressure of the plant and dispersers (e.g.
Houle et al. 2010; Burgos 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 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 (Ashmanet al. 2004b; Knight 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 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; Snellet 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 et al. 2017),
or in the case of iteroparous plant species, by seeds produced in
subsequent reproductive seasons when PL is less severe (Schermeret al. 2019; but see Tye et al. 2020). However, plant
species in human-modified landscapes experience a relatively constant or
even progressively higher PL over time (Eckert et al. 2010; Sapiret al. 2015) often due to the negative effects of anthropogenic
disturbances on the richness and abundance of pollinator assemblages
(Keith 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 et al. 2005; Cisternas‐Fuentes et al.2023). Anthropogenic disturbances also modify seed disperser assemblage,
eroding seed dispersal services provided to endozoochorous and
myrmecochorous plants in disturbed habitats (Leal et al. 2014a;
Valiente‐Banuet 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 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 & Ågren 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 et al. 2017), and/or those with a
higher capacity for self-fertilization in species with mixed mating
systems (Pannell 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. 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.
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 São 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 São Paulo – specially Cinthia A.
Brasileiro and José Eduardo de Carvalho – for all the help along her
sabbatical at Clemson University.
References
Abrahms, B., Aikens, E.O., Armstrong, J.B., Deacy, W.W., Kauffman, M.J.
& Merkle, J.A. (2021). Emerging Perspectives on Resource Tracking and
Animal Movement Ecology. Trends in Ecology & Evolution , 36,
308–320.
Albrecht, J., Hagge, J., Schabo, D.G., Schaefer, H.M. & Farwig, N.
(2018). Reward regulation in plant–frugivore networks requires only
weak cues. Nat Commun , 9, 4838.
Ambika, S., Manonmani, V. & Somasundar, G. (2014). Review on Effect of
Seed Size on Seedling Vigour and Seed Yield. Research J. of Seed
Science , 7, 31–38.
Anjos, D.V., Leal, L.C., Jordano, P. & Del‐Claro, K. (2020). Ants as
diaspore removers of non‐myrmecochorous plants: a meta‐analysis.Oikos , 129, 775–786.
Ashman, T.-L., Knight, T.M., Steets, J.A., Amarasekare, P., Burd, M.,
Campbell, D.R., et al. (2004a). Pollen limitation of plant
reproduction: ecological and evolutionary consequences. Ecology ,
85, 2408–2421.
Ashman, T.-L., Knight, T.M., Steets, J.A., Amarasekare, P., Burd, M.,
Campbell, D.R., et al. (2004b). Pollen limitation of plant
reproduction: ecological and evolutionary consequences. Ecology ,
85, 2408–2421.
Baer, K.C. & Maron, J.L. (2018). Pre‐dispersal seed predation and
pollen limitation constrain population growth across the geographic
distribution of Astragalus utahensis . J Ecol , 106,
1646–1659.
Balaguera-López, H.E., Fischer, G. & Magnitskiy, S. (2020). Seed-fruit
relationships in fleshy fruits: Role of hormones. A review. Rev.
Colomb. Cienc. Hortic. , 14.
Baskin, C.C. & Baskin, J.M. (2014). Seeds: ecology, biogeography,
and evolution of dormancy and germination . Second edition. Elsevier/AP,
San Diego, CA.
Baskin, J.M. & Baskin, C.C. (2018). Pollen limitation and its effect on
seed germination. Seed Sci. Res. , 28, 253–260.
Beattie, A.J. (1985). The Evolutionary Ecology of Ant–Plant
Mutualisms . 1st edn. Cambridge University Press.
Beaumont, K.P., Mackay, D.A. & Whalen, M.A. (2009). Combining distances
of ballistic and myrmecochorous seed dispersal in Adriana quadripartita
(Euphorbiaceae). Acta Oecologica , 35, 429–436.
Ben-Zvi, G., Seifan, M. & Giladi, I. (2021). Ant Guild Identity
Determines Seed Fate at the Post-Removal Seed Dispersal Stages of a
Desert Perennial. Insects , 12, 147.
Bonal, R., Muñoz, A. & Díaz, M. (2007). Satiation of predispersal seed
predators: the importance of considering both plant and seed levels.Evol Ecol , 21, 367–380.
Bono, J.M. & Heithaus, E.R. (2002). Sex ratios and the distribution of
elaiosomes in colonies of the ant, Aphaenogaster rudis. Insectes
soc. , 49, 320–325.
Borchert, M.I. & DeFalco, L.A. (2016). Yucca brevifolia fruit
production, predispersal seed predation, and fruit removal by rodents
during two years of contrasting reproduction. American Journal of
Botany , 103, 830–836.
Boselli, M., Volpe, B. & Di Vaio, C. (1995). Effect of seed number per
berry on mineral composition of grapevine (Vitis vinifera L.)
berries. Journal of Horticultural Science , 70, 509–515.
Boulay, R., Coll-Toledano, J. & Cerdá, X. (2006). Geographic variations
in Helleborus foetidus elaiosome lipid composition: implications for
dispersal by ants. Chemoecology , 16, 1–7.
Boulay, R., Coll-Toledano, J., Manzaneda, A.J. & Cerdá, X. (2007).
Geographic variations in seed dispersal by ants: are plant and seed
traits decisive? Naturwissenschaften , 94, 242–246.
Brookfield, P.L., Ferguson, I.B., Watkins, C.B. & Bowen, J.H. (1996).
Seed number and calcium concentrations of ‘Braeburn’ apple fruit.Journal of Horticultural Science , 71, 265–271.
Bruno, M.M.A., Massi, K.G., Christianini, A.V. & Hay, J. du V. (2021).
Individual crop size increases predispersal predation by beetles in a
tropical palm. Seed Sci. Res. , 31, 43–46.
Buccheri, M. & Di Vaio, C. (2005). Relationship Among Seed Number,
Quality, and Calcium Content in Apple Fruits. Journal of Plant
Nutrition , 27, 1735–1746.
Burgos, T., Fedriani, J.M., Escribano‐Ávila, G., Seoane, J.,
Hernández‐Hernández, J. & Virgós, E. (2022). Predation risk can modify
the foraging behaviour of frugivorous carnivores: Implications of
rewilding apex predators for plant–animal mutualisms. Journal of
Animal Ecology , 91, 1024–1035.
Burns, J.H., Bennett, J.M., Li, J., Xia, J., Arceo‐Gómez, G., Burd, M.,et al. (2019). Plant traits moderate pollen limitation of
introduced and native plants: a phylogenetic meta‐analysis of global
scale. New Phytol , 223, 2063–2075.
Burns, K.C. (2013). What causes size coupling in fruit–frugivore
interaction webs? Ecology , 94, 295–300.
Byk, J. & Del‐Claro, K. (2011). Ant–plant interaction in the
Neotropical savanna: direct beneficial effects of extrafloral nectar on
ant colony fitness. Population Ecology , 53, 327–332.
Charles-Dominique, P. & Cockle, A. (2001). Frugivory and Seed Dispersal
by Bats. In: Nouragues: Dynamics and Plant-Animal Interactions in
a Neotropical Rainforest (eds. Bongers, F., Charles-Dominique, P.,
Forget, P.-M. & Théry, M.). Springer Netherlands, Dordrecht, pp.
207–216.
Chen, M. & Zhao, X.-Y. (2017). Effect of pollen and resource limitation
on reproduction of Zygophyllum xanthoxylum in fragmented
habitats. Ecol Evol , 7, 9076–9084.
Ciccarelli, D., Andreucci, A.C., Pagni, A.M. & Garbari, F. (2005).
Structure and development of the elaiosome in Myrtus communis L.
(Myrtaceae) seeds. Flora - Morphology, Distribution, Functional
Ecology of Plants , 200, 326–331.
Cisternas‐Fuentes, A., Dwyer, R., Johnson, N., Finnell, L., Gilman, J.
& Koski, M.H. (2023). Disentangling the components of pollen limitation
in a widespread herb with gametophytic self‐incompatibility.American J of Botany , 110, e16122.
Clark, R.E. & King, J.R. (2012). The Ant,
<I>Aphaenogaster
picea</I>, Benefits From Plant Elaiosomes When
Insect Prey is Scarce. env. entom. , 41, 1405–1408.
Correa, S.B. & Winemiller, K.O. (2014). Niche partitioning among
frugivorous fishes in response to fluctuating resources in the Amazonian
floodplain forest. Ecology , 95, 210–224.
Côrtes, M.C. & Uriarte, M. (2013). Integrating frugivory and animal
movement: a review of the evidence and implications for scaling seed
dispersal: Frugivory, animal movement, and seed dispersal. Biol
Rev , 88, 255–272.
Culver, D.C. & Beattie, A.J. (1978). Myrmecochory in Viola: Dynamics of
Seed-Ant Interactions in Some West Virginia Species. The Journal
of Ecology , 66, 53.
Dawson-Glass, E. & Hargreaves, A.L. (2022). Does pollen limitation
limit plant ranges? Evidence and implications. Phil Trans R Soc
B , 377, 20210014.
Dehling, D.M., Töpfer, T., Schaefer, H.M., Jordano, P., Böhning-Gaese,
K. & Schleuning, M. (2014). Functional relationships beyond species
richness patterns: trait matching in plant-bird mutualisms across
scales: Trait matching in plant-bird mutualisms across scales.Global Ecology and Biogeography , 23, 1085–1093.
Donahue, M.J., Holyoak, M. & Feng, C. (2003). Patterns of Dispersal and
Dynamics among Habitat Patches Varying in Quality. The American
Naturalist , 162, 302–317.
Duan, Q., Goodale, E. & Quan, R. (2015). Bird fruit preferences match
the frequency of fruit colours in tropical Asia. Sci Rep , 4,
5627.
Eckert, C.G., Kalisz, S., Geber, M.A., Sargent, R., Elle, E., Cheptou,
P.-O., et al. (2010). Plant mating systems in a changing world.Trends in Ecology & Evolution , 25, 35–43.
Fausto, J.A., Eckhart, V.M. & Geber, M.A. (2001). Reproductive
assurance and the evolutionary ecology of self‐pollination inClarkia xantiana (Onagraceae). Am. J. Bot. , 88,
1794–1800.
Fischer, R.C., Richter, A., Hadacek, F. & Mayer, V. (2008). Chemical
differences between seeds and elaiosomes indicate an adaptation to
nutritional needs of ants. Oecologia , 155, 539–547.
Francisco, M.R., Lunardi, V.O., Guimarães, P.R. & Galetti, M. (2008).
Factors affecting seed predation of Eriotheca gracilipes (Bombacaceae)
by parakeets in a cerrado fragment. Acta Oecologica , 33,
240–245.
Freitas, L., Ribeiro, P.C.C., Cancio, A.S., Machado, M.A., Sampaio,
M.C., Forzza, R.C., et al. (2020). Population demography, genetic
variation and reproductive biology of two rare and endangered Neoregelia
species (Bromeliaceae). Botanical Journal of the Linnean Society ,
192, 787–802.
Galetti, M., Guevara, R., Côrtes, M.C., Fadini, R., Von Matter, S.,
Leite, A.B., et al. (2013). Functional Extinction of Birds Drives
Rapid Evolutionary Changes in Seed Size. Science , 340,
1086–1090.
Gammans, N., Bullock, J.M., Gibbons, H. & Schönrogge, K. (2006).
Reaction of Mutualistic and Granivorous Ants to Ulex Elaiosome
Chemicals. J Chem Ecol , 32, 1935–1947.
García-Camacho, R. & Totland, Ø. (2009). Pollen Limitation in the
Alpine: A Meta-Analysis. Arctic, Antarctic, and Alpine Research ,
41, 103–111.
Ghosh, S., Jeon, H. & Jung, C. (2020). Foraging behaviour and
preference of pollen sources by honey bee (Apis mellifera) relative to
protein contents. J Ecology Environ , 44, 4.
Giladi, I. (2006). Choosing benefits or partners: a review of the
evidence for the evolution of myrmecochory. Oikos , 112, 481–492.
Godínez-Alvarez, H., Ríos-Casanova, L. & Peco, B. (2020). Are large
frugivorous birds better seed dispersers than medium- and small-sized
ones? Effect of body mass on seed dispersal effectiveness. Ecology
and Evolution , 10, 6136–6143.
Godó, L., Valkó, O., Borza, S. & Deák, B. (2022). A global review on
the role of small rodents and lagomorphs (clade Glires) in seed
dispersal and plant establishment. Global Ecology and
Conservation , 33, e01982.
Gómez, C., Espadaler, X. & Bas, J.M. (2005). Ant behaviour and seed
morphology: a missing link of myrmecochory. Oecologia , 146,
244–246.
Gómez, J.M., Abdelaziz, M., Lorite, J., Jesús Muñoz-Pajares, A. &
Perfectti, F. (2010). Changes in pollinator fauna cause spatial
variation in pollen limitation: Pollinator assemblage and pollen
limitation. Journal of Ecology , 98, 1243–1252.
González-Varo, J.P., Biesmeijer, J.C., Bommarco, R., Potts, S.G.,
Schweiger, O., Smith, H.G., et al. (2013). Combined effects of
global change pressures on animal-mediated pollination. Trends in
Ecology & Evolution , 28, 524–530.
Gorb, E. & Gorb, S. (2000). Effects of seed aggregation on the removal
rates of elaiosome-bearing Chelidonium majus and Viola
odourata seeds carried by Formica polyctena ants: Seed
aggregation and removal by ants. Ecological Research , 15,
187–192.
Gove, A.D., Majer, J.D. & Dunn, R.R. (2007). A keystone ant species
promotes seed dispersal in a “diffuse” mutualism. Oecologia ,
153, 687–697.
Gunther, R.W. & Lanza, J. (1989). Variation in Attractiveness of
Trillium Diaspores to a Seed-dispersing Ant. American Midland
Naturalist , 122, 321.
Healy, S.D. & Jones, C.M. (2002). Animal learning and memory: an
integration of cognition and ecology. Zoology , 105, 321–327.
Hegland, J.S. & Totland, Ø. (2008). Is the magnitude of pollen
limitation in a plant community affected by pollinator visitation and
plant species specialisation levels? Oikos , 117, 883–891.
Hegland, S.J. & Totland, Ø. (2007). Pollen Limitation Affects Progeny
Vigour and Subsequent Recruitment in the Insect-Pollinated Herb
Ranunculus Acris. Oikos , 116, 1204–1210.
Herrera, C.M. (1987). Vertebrate‐Dispersed Plants of the Iberian
Peninsula: A Study of Fruit Characteristics. Ecological
Monographs , 57, 305–331.
Houle, A., Chapman, C.A. & Vickery, W.L. (2010). Intratree vertical
variation of fruit density and the nature of contest competition in
frugivores. Behavioral Ecology and Sociobiology , 64, 429–441.
Howe, H. (1987). Seed dispersal by fruit-eating birds and mammals. In:Seed dispersal . Murray, Daniel R.
Howe, H.F. & De Steven, D. (1979). Fruit production, migrant bird
visitation, and seed dispersal of Guarea glabra in Panama.Oecologia , 39, 185–196.
Howe, H.F. & Miriti, M.N. (2000). No question: seed dispersal matters.Trends in Ecology & Evolution , 15, 434–436.
Howe, H.F. & Smallwood, J. (1982). Ecology of Seed Dispersal.Annual Review of Ecology and Systematics , 1, 201–228.
Huang, Q. & Burd, M. (2019a). The Effect of Pollen Limitation on the
Evolution of Mating System and Seed Size in Hermaphroditic Plants.The American Naturalist , 193, 447–457.
Huang, Q. & Burd, M. (2019b). The Effect of Pollen Limitation on the
Evolution of Mating System and Seed Size in Hermaphroditic Plants.The American Naturalist , 193, 447–457.
Huang, Q., Burd, M. & Fan, Z. (2017). Resource Allocation and Seed Size
Selection in Perennial Plants under Pollen Limitation. The
American Naturalist , 190, 430–441.
Ida, T.Y., Harder, L.D. & Kudo, G. (2015). The consequences of
demand-driven seed provisioning for sexual differences in reproductive
investment in Thalictrum occidentale (Ranunculaceae). Journal of
Ecology , 103, 269–280.
Jetz, W., Carbone, C., Fulford, J. & Brown, J.H. (2004). The Scaling of
Animal Space Use. Science , 306, 266–268.
Johnson, R.A., Willson, M.F., Thompson, J.N. & Bertin, R.I. (1985).
Nutritional Values of Wild Fruits and Consumption by Migrant Frugivorous
Birds. Ecology , 66, 819–827.
Johnston, M.O. (1991). Pollen Limitation of Female Reproduction in
Lobelia Cardinalis and L. Siphilitica. Ecology , 72, 1500–1503.
Jordano, P. (1987). Avian Fruit Removal: Effects of Fruit Variation,
Crop Size, and Insect Damage. Ecology , 68, 1711–1723.
Jordano, P. (1995). Angiosperm Fleshy Fruits and Seed Dispersers: A
Comparative Analysis of Adaptation and Constraints in Plant-Animal
Interactions. The American Naturalist , 145, 163–191.
Jordano, P., García, C., Godoy, J.A. & García-Castaño, J.L. (2007).
Differential contribution of frugivores to complex seed dispersal
patterns. Proc. Natl. Acad. Sci. U.S.A. , 104, 3278–3282.
Jordano, P. & Schupp, E.W. (2000). Seed Disperser Effectiveness: The
Quantity Component and Patterns of Seed Rain for Prunus mahaleb.Ecological Monographs , 70, 591.
Keith, D.A., Benson, D.H., Baird, I.R.C., Watts, L., Simpson, C.C.,
Krogh, M., et al. (2023). Effects of interactions between
anthropogenic stressors and recurring perturbations on ecosystem
resilience and collapse. Conservation Biology , 37.
Kendrick, G.A., Orth, R.J., Statton, J., Hovey, R., Ruiz Montoya, L.,
Lowe, R.J., et al. (2017). Demographic and genetic connectivity:
the role and consequences of reproduction, dispersal and recruitment in
seagrasses. Biological Reviews , 92, 921–938.
King, A.J. & Marshall, H.H. (2022). Optimal foraging. Current
Biology , 32, R680–R683.
Knight, T.M. (2004). The effects of herbivory and pollen limitation on a
declining population of <i> Trillium grandiflorum
<i>. Ecol Appl , 14, 915–928.
Knight, T.M., Steets, J.A. & Ashman, T. (2006). A quantitative
synthesis of pollen supplementation experiments highlights the
contribution of resource reallocation to estimates of pollen limitation.Am. J. Bot. , 93, 271–277.
Knight, T.M., Steets, J.A., Vamosi, J.C., Mazer, S.J., Burd, M.,
Campbell, D.R., et al. (2005). Pollen Limitation of Plant
Reproduction: Pattern and Process. Annu. Rev. Ecol. Evol. Syst. ,
36, 467–497.
Koski, M.H. (2023). Pollinators exert selection on floral traits in a
pollen‐limited, narrowly endemic spring ephemeral. American J of
Botany , 110.
Kunin, W.E. (1993). Sex and the Single Mustard: Population Density and
Pollinator Behavior Effects on Seed-Set. Ecology , 74, 2145–2160.
Lai, R., Woolley, D.J. & Lawes, G.S. (1990). The effect of inter-fruit
competition, type of fruiting lateral and time of anthesis on the fruit
growth of kiwifruit (Actinidia deliciosa). Journal of
Horticultural Science , 65, 87–96.
Lalonde, R.G. & Roitberg, B.D. (2022). Mating System, Life-History, and
Reproduction in Canada Thistle (Cirsium arvense; Asteraceae), 9.
Leal, I.R., Wirth, R. & Tabarelli, M. (2007). Seed Dispersal by Ants in
the Semi-arid Caatinga of North-east Brazil. Annals of Botany ,
99, 885–894.
Leal, L.C., Andersen, A.N. & Leal, I.R. (2014a). Anthropogenic
disturbance reduces seed-dispersal services for myrmecochorous plants in
the Brazilian Caatinga. Oecologia , 174, 173–181.
Leal, L.C., Neto, M.C.L., de Oliveira, A.F.M., Andersen, A.N. & Leal,
I.R. (2014b). Myrmecochores can target high-quality disperser ants:
variation in elaiosome traits and ant preferences for myrmecochorous
Euphorbiaceae in Brazilian Caatinga. Oecologia , 174, 493–500.
van Leeuwen, C.H.A., Villar, N., Mendoza Sagrera, I., Green, A.J.,
Bakker, E.S., Soons, M.B., et al. (2022). A seed dispersal
effectiveness framework across the mutualism–antagonism continuum.Oikos , 2022, e09254.
Lengyel, S., Gove, A.D., Latimer, A.M., Majer, J.D. & Dunn, R.R.
(2010). Convergent evolution of seed dispersal by ants, and phylogeny
and biogeography in flowering plants: A global survey.Perspectives in Plant Ecology, Evolution and Systematics , 12,
43–55.
MacArthur, R.H. & Pianka, E.R. (1966). On Optimal Use of a Patchy
Environment. The American Naturalist , 100, 603–609.
Mark, S. & Olesen, J.M. (1996). Importance of Elaiosome Size to Removal
of Ant-Dispersed Seeds. Oecologia , 107, 95–101.
Martínez, I., García, D. & Obeso, J.R. (2008). Differential seed
dispersal patterns generated by a common assemblage of vertebrate
frugivores in three fleshy-fruited trees. Écoscience , 15,
189–199.
Matías, L., Zamora, R., Mendoza, I. & Hódar, J.A. (2010). Seed
Dispersal Patterns by Large Frugivorous Mammals in a Degraded Mosaic
Landscape. Restoration Ecology , 18, 619–627.
May, C.E., Vaziri, A., Lin, Y.Q., Grushko, O., Khabiri, M., Wang, Q.-P.,et al. (2019). High Dietary Sugar Reshapes Sweet Taste to Promote
Feeding Behavior in Drosophila melanogaster. Cell Reports , 27,
1675-1685.e7.
Meyer, G.A. & Witmer, M.C. (1998). Influence of Seed Processing by
Frugivorous Birds on Germination Success of Three North American Shrubs.The American Midland Naturalist , 140, 129–139.
Miller, C.N., Whitehead, S.R. & Kwit, C. (2020). Effects of seed
morphology and elaiosome chemical composition on attractiveness of fiveTrillium species to seed‐dispersing ants. Ecol Evol , 10,
2860–2873.
Moore, N.B., Stephens, R.B. & Rowe, R.J. (2022). Nutritional and
environmental factors influence small mammal seed selection in a
northern temperate forest. Ecosphere , 13, e4036.
Naniwadekar, R., Chaplod, S., Datta, A., Rathore, A. & Sridhar, H.
(2019). Large frugivores matter: Insights from network and seed
dispersal effectiveness approaches. J Anim Ecol , 88, 1250–1262.
Nathan, R., Klein, E., Robledo-Arnuncio, J.J. & Revilla, E. (2012).Dispersal kernels . Oxford University Press Oxford, UK.
Nathan, R., Schurr, F.M., Spiegel, O., Steinitz, O., Trakhtenbrot, A. &
Tsoar, A. (2008). Mechanisms of long-distance seed dispersal.Trends in Ecology & Evolution , 23, 638–647.
Navarro, L. (1998). Effect of pollen limitation, additional nutrients,
flower position and flowering phenology on fruit and seed production in
Salvia verbenaca (Lamiaceae). Nordic Journal of Botany , 18,
441–446.
Nelson, A.S. & Whitehead, S.R. (2021). Fruit secondary metabolites
shape seed dispersal effectiveness. Trends in Ecology &
Evolution , 36, 1113–1123.
Ness, J.H., Bronstein, J.L., Andersen, A.N. & Holland, J.N. (2004). Ant
body size predicts dispersal distance of ant-adapted seeds: implications
of small ant invasions. Ecology , 85, 1244–1250.
Neuschulz, E.L., Mueller, T., Schleuning, M. & Böhning-Gaese, K.
(2016). Pollination and seed dispersal are the most threatened processes
of plant regeneration. Sci Rep , 6, 29839.
Nevo, O., Valenta, K., Razafimandimby, D., Melin, A.D., Ayasse, M. &
Chapman, C.A. (2018). Frugivores and the evolution of fruit colour.Biol. Lett. , 14, 20180377.
Niesenbaum, R.A. (1993). Light or Pollen–Seasonal Limitations on
Female Reproductive Success in the Understory Shrub Lindera Benzoin.The Journal of Ecology , 81, 315.
Olivieri, I., Couvet, D. & Slatkin, M. (1994). Allocation of
Reproductive Effort in Perennial Plants Under Pollen Limitation.The American Naturalist , 144, 373–394.
Palacio, F.X., Siepielski, A.M., Lacoretz, M.V. & Ordano, M. (2020).
Selection on fruit traits is mediated by the interplay between
frugivorous birds, fruit flies, parasitoid wasps and seed‐dispersing
ants. J Evol Biol , 33, 874–886.
Pannell, J.R., Auld, J.R., Brandvain, Y., Burd, M., Busch, J.W.,
Cheptou, P., et al. (2015). The scope of Baker’s law. New
Phytol , 208, 656–667.
Patterson, K.J. (1990). Effects of pollination on fruit set, size, and
quality in feijoa ( Acca sellowiana (Berg) Burret). New
Zealand Journal of Crop and Horticultural Science , 18, 127–131.
Pattison, R.J., Csukasi, F. & Catalá, C. (2014). Mechanisms regulating
auxin action during fruit development. Physiol Plantarum , 151,
62–72.
Petit, S. (2011). Effects of mixed-species pollen load on fruits, seeds,
and seedlings of two sympatric columnar cactus species. Ecological
Research , 26, 461–469.
Plumptre, A.J., Baisero, D., Belote, R.T., Vázquez-Domínguez, E.,
Faurby, S., Jȩdrzejewski, W., et al. (2021). Where Might We Find
Ecologically Intact Communities? Front. For. Glob. Change , 4,
626635.
Pyke, G.H. (2019). Optimal Foraging Theory: An Introduction☆. In:Encyclopedia of Animal Behavior (Second Edition) (ed. Choe,
J.C.). Academic Press, Oxford, pp. 111–117.
Rajjou, L., Duval, M., Gallardo, K., Catusse, J., Bally, J., Job, C.,et al. (2012). Seed Germination and Vigor. Annu. Rev. Plant
Biol. , 63, 507–533.
Reed, R.C., Bradford, K.J. & Khanday, I. (2022). Seed germination and
vigor: ensuring crop sustainability in a changing climate.Heredity , 128, 450–459.
Reifenrath, K., Becker, C. & Poethke, H.J. (2012). Diaspore Trait
Preferences of Dispersing Ants. J Chem Ecol , 38, 1093–1104.
Robertson, A.W., Trass, A., Ladley, J.J. & Kelly, D. (2006). Assessing
the benefits of frugivory for seed germination: the importance of the
deinhibition effect. Funct Ecology , 20, 58–66.
Rogers, H.S., Beckman, N.G., Hartig, F., Johnson, J.S., Pufal, G., Shea,
K., et al. (2019). The total dispersal kernel: a review and
future directions. AoB PLANTS , 11, plz042.
Runquist, R.D.B. & Moeller, D.A. (2013). Resource reallocation does not
influence estimates of pollen limitation or reproductive assurance inClarkia xantiana subsp. parviflora (Onagraceae).American Journal of Botany , 100, 1916–1921.
Russo, S.E. (2003). Responses of dispersal agents to tree and fruit
traits in Virola calophylla (Myristicaceae): implications for selection.Oecologia , 136, 80–87.
Russo, S.E., Portnoy, S. & Augspurger, C.K. (2006). Incorporating
animal behavior into seed dispersal models: implications for seed
shadows. Ecology , 87, 3160–3174.
Saatkamp, A., Cochrane, A., Commander, L., Guja, L.K., Jimenez-Alfaro,
B., Larson, J., et al. (2019). A research agenda for seed-trait
functional ecology. New Phytologist , 221, 1764–1775.
Saatkamp, A., Poschlod, P. & Venable, D.L. (2014). The functional role
of soil seed banks in natural communities. In: Seeds: the ecology
of regeneration in plant communities (ed. Gallagher, R.S.). CABI, UK,
pp. 263–295.
Samuels, I.A. & Levey, D.J. (2005). Effects of gut passage on seed
germination: do experiments answer the questions they ask? Funct
Ecology , 19, 365–368.
Sapir, Y., Dorchin, A. & Mandelik, Y. (2015). Indicators of Pollinator
Decline and Pollen Limitation. In: Environmental Indicators (eds.
Armon, R.H. & Hänninen, O.). Springer Netherlands, Dordrecht, pp.
103–115.
Schermer, É., Bel‐Venner, M., Fouchet, D., Siberchicot, A., Boulanger,
V., Caignard, T., et al. (2019). Pollen limitation as a main
driver of fruiting dynamics in oak populations. Ecol Lett , 22,
98–107.
Schoener, T.W. (1971). Theory of Feeding Strategies. Annual Review
of Ecology and Systematics , 2, 369–404.
Schupp, E.W., Jordano, P. & Gómez, J.M. (2010). Seed dispersal
effectiveness revisited: a conceptual review. New Phytologist ,
188, 333–353.
Schupp, E.W., Zwolak, R., Jones, L.R., Snell, R.S., Beckman, N.G.,
Aslan, C., et al. (2019). Intrinsic and extrinsic drivers of
intraspecific variation in seed dispersal are diverse and pervasive.AoB PLANTS , 11, plz067.
Schurr, F.M., Spiegel, O., Steinitz, O., Trakhtenbrot, A., Tsoar, A. &
Nathan, R. (2018). Long-Distance Seed Dispersal. In: Annual Plant
Reviews online . John Wiley & Sons, Ltd, pp. 204–237.
Sebastián-González, E., Pires, M.M., Donatti, C.I., Guimarães Jr., P.R.
& Dirzo, R. (2017). Species traits and interaction rules shape a
species-rich seed-dispersal interaction network. Ecology and
Evolution , 7, 4496–4506.
Sheridan, S.L., Iversen, K.A. & Itagaki, H. (1996). The role of
chemical senses in seed-carrying behavior by ants: A behavioral,
physiological, and morphological study. Journal of Insect
Physiology , 42, 149–159.
Skidmore, B.A. & Heithaus, E.R. (1988). Lipid cues for seed-carrying by
ants inHepatica americana. J Chem Ecol , 14, 2185–2196.
Snell, R.S., Beckman, N.G., Fricke, E., Loiselle, B.A., Carvalho, C.S.,
Jones, L.R., et al. (2019). Consequences of intraspecific
variation in seed dispersal for plant demography, communities, evolution
and global change. AoB PLANTS , 11, plz016.
Soltani, E., Baskin, C.C., Baskin, J.M., Heshmati, S. & Mirfazeli, M.S.
(2018). A meta-analysis of the effects of frugivory (endozoochory) on
seed germination: role of seed size and kind of dormancy. Plant
Ecol , 219, 1283–1294.
Soltani, E., Benakashani, F., Baskin, J.M. & Baskin, C.C. (2021).
Reproductive biology, ecological life history/demography and genetic
diversity of the megagenus Astragalus (Fabaceae, Papilionoideae).Bot. Rev. , 87, 55–106.
Spiegel, O. & Nathan, R. (2007). Incorporating dispersal distance into
the disperser effectiveness framework: frugivorous birds provide
complementary dispersal to plants in a patchy environment. Ecol
Letters , 10, 718–728.
Stanton, M.L. (2003). Interacting Guilds: Moving beyond the Pairwise
Perspective on Mutualisms. The American Naturalist , 162,
S10–S23.
TeKrony, D.M. & Egli, D.B. (1991). Relationship of Seed Vigor to Crop
Yield: A Review. Crop Sci. , 31, 816–822.
Traveset, A. & Verdú, M. (2002). A meta-analysis of the effect of gut
treatment on seed germination. In: Seed Dispersal and Frugivory:
Ecology, Evolution and Conservation . CAB International.
Trivedi, M.R., Cornejo, F.H. & Watkinson, A.R. (2004). Seed Predation
on Brazil Nuts (Bertholletia excelsa) by Macaws (Psittacidae) in Madre
de Dios, Peru. Biotropica , 36, 118–122.
Trunschke, J., Sletvold, N. & Ågren, J. (2017). Interaction intensity
and pollinator‐mediated selection. New Phytol , 214, 1381–1389.
Tye, M., Dahlgren, J.P. & Sletvold, N. (2020). Pollen limitation in a
single year is not compensated by future reproduction. Oecologia ,
192, 989–997.
Valenta, K. & Nevo, O. (2020). The dispersal syndrome hypothesis: How
animals shaped fruit traits, and how they did not. Functional
Ecology , 34, 1158–1169.
Valido, A. & Olesen, J.M. (2019). Frugivory and Seed Dispersal by
Lizards: A Global Review. Front. Ecol. Evol. , 7, 49.
Valido, A., Schaefer, H.M. & Jordano, P. (2011). Colour, design and
reward: phenotypic integration of fleshy fruit displays: Phenotypic
integration of fleshy fruits. Journal of Evolutionary Biology ,
24, 751–760.
Valiente‐Banuet, A., Aizen, M.A., Alcántara, J.M., Arroyo, J., Cocucci,
A., Galetti, M., et al. (2015). Beyond species loss: the
extinction of ecological interactions in a changing world. Funct
Ecol , 29, 299–307.
Waites, A.R. & Ågren, J. (2004). Pollinator visitation, stigmatic
pollen loads and among-population variation in seed set in Lythrum
salicaria : Population size and pollination . Journal of
Ecology , 92, 512–526.
Ward, M. & Johnson, S.D. (2005). Pollen limitation and demographic
structure in small fragmented populations of Brunsvigia radulosa(Amaryllidaceae). Oikos , 108, 253–262.
Warne, R.W., Baer, S.G. & Boyles, J.G. (2019). Community Physiological
Ecology. Trends in Ecology & Evolution , 34, 510–518.
Weber, A. & Kolb, A. (2013). Local plant density, pollination and
trait–fitness relationships in a perennial herb. Plant Biology ,
15, 335–343.
Westcott, D.A., Bentrupperbäumer, J., Bradford, M.G. & McKeown, A.
(2005). Incorporating patterns of disperser behaviour into models of
seed dispersal and its effects on estimated dispersal curves.Oecologia , 146, 57–67.
Wheelwright, N.T. (1985). Fruit-Size, Gape Width, and the Diets of
Fruit-Eating Birds. Ecology , 66, 808–818.
Wheelwright, N.T. (1993). Fruit size in a tropical tree species:
variation, preference .by birds, and heritability. Vegetatio ,
107, 163–174.
Wolowski, M., Ashman, T.-L. & Freitas, L. (2014). Meta-Analysis of
Pollen Limitation Reveals the Relevance of Pollination Generalization in
the Atlantic Forest of Brazil. PLoS ONE , 9, e89498.
Woodard, S.H. & Jha, S. (2017). Wild bee nutritional ecology:
predicting pollinator population dynamics, movement, and services from
floral resources. Current Opinion in Insect Science , 21, 83–90.
Woodward, G., Ebenman, B., Emmerson, M., Montoya, J.M., Olesen, J.M.,
Valido, A., et al. (2005). Body size in ecological networks.Trends Ecol Evol , 20, 402–409.