Introduction
Seed dispersal is a fundamental process for the survival, reproduction,
and spread of plants because it is the only stage in the plant life
cycle when many plants may use movement to colonize new habitats, escape
competition, or evade attack by pathogens and herbivores (Howe &
Smallwood 1982; Howe & Miriti 2000, 2004; Jordano 2000; Schupp et
al. 2010; Hirsch et al. 2012; Carlo & Tewksbury 2014).
Animal-mediated seed dispersal is among the most common modes of seed
dispersal (Howe & Smallwood 1982; Jordano 2000; Herrera & Pellmyr
2002); 64% of gymnosperm and 27% of angiosperm plant species rely on
vertebrates for dispersal (Herrera 1989). As a result, understanding
patterns in animal-mediated seed dispersal (zoochory) may provide a
means to predict spatial patterns in plant recruitment (Beckman &
Rogers 2013), how plant species may respond to climate change (Dyer
1995; Cain et al. 2000; Kremer et al. 2012; Corlett &
Westcott 2013), and the outcomes of exotic plant invasions (Traveset &
Richardson 2014; Baltzinger et al. 2019). However, zoochory is
notoriously variable in both the quantity of seeds dispersed and
distance of seed movement (Schupp et al. 2010; Côrtes & Uriarte
2013; Rogers et al. 2019). Consequently, developing predictive
frameworks that enable more effective classification and prediction of
zoochory has been an ongoing challenge to ecologists for several decades
(Schupp et al. 2010; Côrtes & Uriarte 2013; Zwolak 2018; Rogerset al. 2019; Zwolak & Sih 2020).
While studies have shown that animal behavior provides a useful means
for predicting spatial patterns in plant recruitment (Wang & Smith
2002; Levey et al. 2005; Russo et al. 2006; Kremeret al. 2012; Beckman & Rogers 2013; Sasal & Morales 2013;
Herrmann et al. 2016), relationships between specific dispersal
agents and spatial patterns of dispersal often remain notably weak
(Getzin et al. 2014; Schupp et al. 2017; but see Levey et al. 2005 for
an exception) due to high intraspecific variability in the behavior of
seed-dispersal agents (Zwolak 2018). Such high intraspecific variation
in disperser efficacy may have important pragmatic ramifications because
species-level averages of disperser efficacy (i.e., mean number of seeds
dispersed by individuals of one species) are often used to predict how
changes in animal populations and communities may lead to losses in seed
dispersal(e.g., Peres et al. 2016; Culot et al. 2017). For example,
realized seed dispersal in fragmented habitats will be much lower than
what is predicted by a species-average approach if individual animals
that provide disproportionately greater contributions to seed dispersal
are also the individuals most likely to be lost or exhibit changes in
behavior in fragmented habitats (McConkey & O’Farrill 2016; Zwolak
2018). As such, identifying traits of dispersal agents that explain
intraspecific variation in behavior may provide the key to successfully
predicting seed dispersal (Côrtes & Uriarte 2013; González-Varo &
Traveset 2016; Schupp et al. 2017; Zwolak 2018; Brehm et
al. 2019; Zwolak & Sih 2020). Specifically, identifying individual
traits that may affect the quantity of seeds handled, the distance that
seeds are carried, and the microhabitat in which seeds are dispersed is
critical to predicting variation in the effectiveness of individual
agents of seed dispersal (Schupp et al. 2010; Brehm et al.2019).
Social status, which may reflect an individual’s age, size, sex, or rank
in a dominance hierarchy, may have an important bearing on individual
behaviors that directly and indirectly affect seed dispersal by animals.
The effectiveness of seed dispersal agents is described as the ‘number
of new adults produced by the dispersal activities of a disperser’
(Schupp 1993). Seed dispersal effectiveness is the product of the
quantity of seeds dispersed (quantitative component) and the probability
of seedling establishment (quality component; Schupp et al. 2010). Since
social status can affect individual diet composition, social status may
predict intraspecific variation in the quantity of seeds dispersed (Fig.
1). Recent work by Tsuji et al. (2020) provides compelling evidence that
social rank in Japanese macaques determines the quantity of seeds
dispersed by an individual, and we suggest that this may be applicable
for a broad diversity of taxa, including carnivores. We also highlight
that social status affects individual space use, which may explain
intraspecific variation in both the distance and quality of seed
dispersal (Fig. 1). Much of the unresolved variation in seed dispersal
could therefore be understood by a novel focus on animal social status.
We present a framework that provides important clarity on the
relationships between individual social status, animal behavior, and
seed dispersal, allowing for predictions of seed-dispersal patterns
across a broad spectrum of systems. This framework may also be used to
understand how animal social behavior affects our ability to mitigate
several timely ecological challenges, such as biological invasions,
plant persistence in urban environments, and plant persistence amidst
climate change. We highlight that in many systems, subordinate
individuals may be key agents of seed dispersal, illustrating that
individuals with minimal demographic contributions may have substantial
ecological contributions, i.e., subordinate animals may play a dominant
role in seed dispersal. Hence, environmental changes that affect animal
social structure may have unappreciated consequences for seed dispersal.
This framework is informed by two perspectives, described below, and can
be implemented across the wide diversity of plant-frugivore networks
that include social frugivores, which may reveal emerging hotspots or
catastrophic losses of seed dispersal in contexts where global change
disrupts animal social structure. While our framework specifically
focuses on zoochory, the general concepts and hypotheses that we present
could be applied to other forms of animal-mediated dispersal (e.g.,
dispersal of fungi or parasites) that are mediated by individual diet
and space use.