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\begin{document}

\title{The dominant role of animal social status in vertebrate seed dispersal}



\author[1]{Savannah Bartel}%
\author[2]{John Orrock}%
\affil[1]{University of Wisconsin Madison}%
\affil[2]{University of Wisconsin}%


\vspace{-1em}



  
  \date{May 23, 2024}


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\selectlanguage{english}
\begin{abstract}
Seed dispersal directly affects plant establishment, gene flow, and
fitness. As a result, understanding patterns in seed dispersal is
fundamental to understanding plant ecology and evolution, as well as
addressing challenges of extinction and global change. Our ability to
understand dispersal is limited because few frameworks have emerged that
provide a means for predicting dispersal across time and space. We
provide a novel framework that links seed dispersal to animal social
status, a key component of behavior. Because social status affects
individual resource access and movement, it provides a critical link to
two factors that determine seed dispersal: the quantity of seeds
dispersed and the spatial patterns of dispersal. Moreover, individual
social status may have unappreciated effects on post-dispersal seed
survival and recruitment when social status affects individual habitat
use. Hence, environmental changes, such as selective harvesting and
urbanization, that affect animal social structure may have unappreciated
consequences for seed dispersal. The framework we present highlights
these exciting new hypotheses linking environmental change, social
structure, and seed dispersal. By outlining experimental approaches to
test these hypotheses, we hope to facilitate studies across a wide
diversity of plant-frugivore networks, which may uncover emerging
hotspots or catastrophic losses of seed dispersal.%
\end{abstract}%



\sloppy


\textbf{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 \emph{et
al.} 2010; Hirsch \emph{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 \emph{et al.} 2000; Kremer \emph{et al.} 2012; Corlett \&
Westcott 2013), and the outcomes of exotic plant invasions (Traveset \&
Richardson 2014; Baltzinger \emph{et al.} 2019). However, zoochory is
notoriously variable in both the quantity of seeds dispersed and
distance of seed movement (Schupp \emph{et al.} 2010; C\selectlanguage{ngerman}ôrtes \& Uriarte
2013; Rogers \emph{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 \emph{et al.} 2010; Côrtes \& Uriarte 2013; Zwolak 2018;
Rogers\emph{et 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 \emph{et al.} 2005; Russo \emph{et al.} 2006; Kremer\emph{et
al.} 2012; Beckman \& Rogers 2013; Sasal \& Morales 2013; Herrmann
\emph{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 \emph{et al.} 2017; Zwolak 2018; Brehm \emph{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 \emph{et al.} 2010; Brehm \emph{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.

\textbf{Social status affects the quantity of seeds dispersed}

Social status is often predictably related to an individual's ability to
monopolize preferred food items (Ward \& Webster 2016a), which likely
generates intraspecific variation among dispersal agents in the quantity
of seeds they disperse. This variation in seed dispersal may be most
evident in systems where fruit is a supplementary food item that is less
preferred to a food item that can be monopolized by dominant
individuals, leading to greater quantity of seeds dispersed by
subordinate individuals supplementing their diets with fruit. For
example, coyotes (\emph{Canis latrans} ) are social carnivores with
highly variable diets that often include fruit (Parker 1995; Mastro
2011), and fruit consumption by coyotes can provide seed-dispersal
services for a wide range of plant species across North America (Willson
1993; Cypher \& Cypher 1999; Roehm \& Moran 2013; Bartel \& Orrock 2021;
Draper \emph{et al.} 2021). Since coyote dominance hierarchies affect
individual access to carrion (i.e., dominant individuals have greater
access than subordinates; Gese et al. 1996; Atwood and Gese 2008), it is
likely that subordinate individuals consume greater amounts of fruit (a
secondary food item), transporting substantially greater quantities of
seeds than dominant individuals (Fig. 1). Since transient
(less-dominant) coyotes also have reduced access to ungulate carcasses
than territorial (more-dominant) individuals (Gese 2001), it is likely
that resident status is an important predictor of individual fruit
consumption, and subsequent seed dispersal, in coyote populations.
Moreover, social status related to space use is also likely to affect
dispersal distance (see below).

It may be quite common that subordinate individuals disperse
substantially more seeds than dominant individuals within carnivore
populations (Box 1) as well as many primate populations where social
status is known to dictate individual diet breadth. For example, in
Kenya, higher-ranking female vervets (\emph{Cercopithecus aethiops} )
consumed significantly less fruit than lower-ranking females
(Isbell\emph{et al.} 1999). This difference in diet is thought to be a
result of higher-ranking females monopolizing fungi, a larger component
of higher-ranking female diets, due to its abundance in restricted areas
(Isbell \emph{et al.} 1999). Rank differences in seed-dispersal efficacy
may also be the opposite in primate populations where fruit is both
preferred and can be monopolized by high-ranking individuals. In both
blue monkeys (\selectlanguage{english}\emph{Cercopithecus mitis stuhlmanni} ) and chimpanzees
(\selectlanguage{english}\emph{Pan troglodytes} ), high-ranking individuals consume
significantly more fruit than low-ranking individuals, which consume
significantly more foliage (Pazol \& Cords 2005; Murray \emph{et
al.}2006). Predicting how dominant and subordinate individuals vary in
effectiveness as seed-dispersal agents therefore requires an
understanding of which food item (fruit or an alternative resource) is
both preferred and monopolizable by dominant individuals (Fig. 1).

\textbf{The distance and quality of seed dispersal may vary with social
status}

Social status predictably impacts individual space use such that social
status may be used to predict the distance and quality of seed
dispersal, specifically characteristics of deposition sites which affect
the probability of post-dispersal predation and seedling establishment
(e.g., suitable microsite availability and abundance of natural enemies:
Schupp 1993; Schupp et al. 2010). In systems where a resource can be
monopolized (e.g., fruiting trees), the defense of resources by dominant
individuals can create situations where subordinates steal defended
resources and then move far away to avoid antagonistic encounters,
thereby elongating seed-dispersal kernels (Box 2, Fig. 2A). The contrast
in space use between resource-defending dominant individuals and
resource-stealing subordinates has been explicitly linked to patterns in
seed dispersal in a study of flying foxes (McConkey \& Drake 2006).
However, thieving behaviors by subordinates have been documented in a
variety of taxa, including birds, primates, and bats (Sallabanks 1993;
McConkey \& Drake 2006; Ward \& Webster 2016b; Tsuji \emph{et al.}2020),
indicating that this is a potentially profitable, yet largely untapped
area of research that may elucidate patterns in seed-dispersal kernels.

For group-living large mammals, an individual's rank within a dominance
hierarchy has well-documented effects on its movement across landscapes.
Dominant individuals often have more restricted home ranges, spending
more time in predictable, preferred habitat types (Aycrigg \& Porter
1997; Henry \emph{et al.} 2005; Wittemyer \emph{et al.} 2007; Dorning \&
Harris 2017; Kamler \emph{et al.} 2019). Subordinate individuals often
forego foraging efficiency to mitigate competition with dominants
(Henry\emph{et al.} 2005; Gilbert-Norton \emph{et al.} 2013; Dorning \&
Harris 2017), and this increased movement likely leads to an increase in
the diversity of habitats in which seeds may be deposited as well as
increased dispersal distance (Fig. 1). Broader distinctions between
territorial and transient individuals may also be used to predict
spatial patterns in seed dispersal and recruitment. For example,
territorial males in lekking blackbuck antelope (\emph{Antilope
cervicapra} ) populations defecate in dung piles, leading to spatially
concentrated patterns of seed arrival within male territories and
substantially higher rates of seedling recruitment on territories than
on random sites (Jadeja \emph{et al.} 2013). Since non-territorial males
in mixed-sex herds range over large areas and do not predictably deposit
seeds in dung piles, seed dispersal by non-territorial individuals is
likely lower in quality. This example highlights that commonly used
methods for estimating seed dispersal that rely upon individual movement
patterns and gut-retention time may not accurately capture intraspecific
variation in dispersal efficacy if the quality of deposition site for
plant recruitment is not also evaluated. Since individual movement and
habitat use is affected by social status, the quality of seed-deposition
sites may vary among individuals of different social statuses (Fig. 1).
Studies that not only estimate seed dispersal but also measure
post-dispersal seed fate (i.e., seed predation and recruitment) at
deposition sites will provide greater clarity on how the quality of seed
dispersal varies between individuals of different social statuses. For
example, past work shows that seed deposition in coyote scat increases
seed survival for rodent-preferred seeds but decreases seed survival for
arthropod-preferred seeds due to the contrasting effects of mesopredator
scat on rodents (aversion) and arthropods (attraction; Bartel and Orrock
2021). Hence, if dominant individuals deposit seeds in microhabitats
with different granivore communities than the microhabitats in which
subordinates deposit seeds, then the probability of post-dispersal seed
survival may drastically differ. This contrast may be most evident in
group-living canids, like coyotes, where dominant individuals spend more
time maintaining territory boundaries, often through scent-marking and
scat deposition, than subordinate individuals (Gese 2001). Since
territory boundaries often fall along habitat edges, including roads and
trails, seed fate may differ among dominant- and subordinate-dispersed
seeds if granivores either avoid or prefer edges.

An individual's efficacy as a seed-dispersal agent may change over its
lifetime if social status changes over a lifetime. For example, social
dominance in grizzly bear (\emph{Ursus arctos horribilis} ) populations
is typically a result of individual size (larger bears are dominant over
smaller bears) and reproductive status (females with cubs are
subordinate to single males; Ben-David et al. 2004; Gende and Quinn
2004). Since individual social status affects bear diet and space use
(Box 1), juvenile males are likely to become less effective
seed-dispersal agents over their lifetime, and females are likely to be
most effective seed-dispersal agents during their lifetime when they are
rearing cubs. The capacity for an individual's efficacy as a
seed-dispersal agent to rapidly change raises a clear distinction
between the effects of social status and personality on seed dispersal.
While definitions of animal personalities are often context- or
system-specific, personality is most broadly defined as individual
differences in behavior that are consistent across time and/or contexts
(Dall \emph{et al.} 2004; Stamps \& Groothuis 2010). In contrast, an
individual's social status has the capacity to change across time or
context, particularly as a result of changes in the individual's social
environment. While individual personality traits can sometimes be
correlated with social dominance (Briffa \emph{et al.} 2015),
personality and social dominance are not related in many animal
societies (Favati \emph{et al.} 2013; Funghi \emph{et al.} 2015;
Devost\emph{et al.} 2016). Dominance is the product of myriad
environmental factors (e.g., relative size, relative age, reproductive
status, maternal rank, social alliances; Favati et al. 2013; Funghi et
al. 2015; Devost et al. 2016; Strauss and Holekamp 2019; Ilany et al.
2021), but personality is by definition consistent across time and
context, though it may develop in response to individual experience
(Stamps \& Groothuis 2010). Hence, individual behaviors that are a
result of personality should remain consistent over short timespans, but
any changes to an individual's social environment that lead to a rapid
change in social status are expected to rapidly change individual
behavior and efficacy as a seed-dispersal agent.

\textbf{Consequences of global change for socially-mediated seed
dispersal}

Our framework illustrates that in many systems where fruit is a
supplemental resource for animals (e.g., carnivores and folivores),
subordinate individuals are likely to be the most effective
seed-dispersal agents, and thus may be critical for understanding
patterns in plant populations in the Anthropocene. First, since
subordinate individuals have less restricted home ranges and are more
likely to disperse beyond current conspecific territories (Aycrigg \&
Porter 1997; Henry \emph{et al.} 2005; Dorning \& Harris 2017;
Kamler\emph{et al.} 2019), subordinate individuals may be more likely to
provide long-distance seed-dispersal events. Long-distance seed
dispersal is critical for plant species range expansion to track
changing climates (Dyer 1995; Cain \emph{et al.} 2000; Corlett \&
Westcott 2013). Hence, subordinate individuals may facilitate range
expansions that allow plant species track changing climates (Fig. 3A).
Second, since subordinate individuals are more likely to utilize
less-preferred habitats (Aycrigg \& Porter 1997; Wittemyer \emph{et
al.}2007; Ward \emph{et al.} 2018), and urban habitats are often
demographic sinks (Vierling 2000; Lamb \emph{et al.} 2017, 2020),
subordinate individuals may be more likely to transport seeds into urban
habitats, playing a potentially unappreciated role in promoting the
spread and persistence of some plant populations in urban landscapes
(Fig. 3B). Differences in movement across fragmented landscapes due to
social status may also have important, yet unappreciated implications
for the efficacy of conservation corridors (i.e., thin strips of habitat
connecting otherwise isolated patches). While corridors have been shown
to increase plant species diversity, including animal-dispersed plants
(Damschen \emph{et al.} 2006, 2019), there is limited knowledge of how
an animal's social status affects its propensity to move through
corridors (but see Box 1 for discussion of work by Ford et al. (2017)).
Since subordinate individuals typically forage in a larger number of
patches in a landscape and are more likely to disperse from natal
habitats, we predict that subordinate individuals may disproportionately
contribute to seed movement through corridors and the consequent
benefits of corridors to plant diversity (Fig. 3C). Initiatives to
restore plant communities through corridor implementation may therefore
require wildlife management that maintains or restores social structure
in animal populations. Finally, if subordinate individuals have
significant contributions to the quantity and spatial spread of seed
dispersal, then subordinate individuals may facilitate the spread of
invasive plants.

Our framework also highlights how environmental changes that modify
animal social structure and behavior may have indirect consequences for
plant populations through changes in seed dispersal effectiveness. For
example, rank-dependent differences in diet and space use often only
occur during seasons when the preferred resource is limited and can be
monopolized (Pazol \& Cords 2005; Wittemyer \emph{et al.} 2007;
Tsuji\emph{et al.} 2020). Events that cause an overabundance of a
preferred resource (e.g., masting or human subsidies) could therefore
lead to a cryptic function loss of seed dispersal by subordinates
(McConkey and O'Farrill 2015; Box 2). It has been shown that animal
social network structure is relaxed near anthropogenic habitats (Belton
\emph{et al.}2018; Morrow \emph{et al.} 2019), indicating that areas of
high human activity may be hotspots of cryptic function loss of seed
dispersal if high-quality foods are no longer monopolized by dominant
individuals. While it is appreciated that animal species extinction can
lead to catastrophic loss in plant biomass due to seed-dispersal
limitation (Peres \emph{et al.} 2016), we posit that shifts in animal
social behavior may have similar deleterious effects on plant biomass. A
study by McConkey and Drake (2006) on seed dispersal by flying foxes
illustrated that seed dispersal services may be lost when animal
population densities fall below a threshold for density-dependent
behaviors that lead to seed dispersal (Box 2). Consequently, the
functional role of animals as seed-dispersal agents can be lost in the
early stages of species decline when social behaviors diminish, long
before species become rare (McConkey \& Drake 2006; McConkey \&
O'Farrill 2015, 2016). Finally, while it is known that harvesting
frugivorous animals causes seed-dispersal limitation (Peres \emph{et
al.} 2016), we posit that selective harvesting of dominant individuals
may also lead to seed-dispersal limitation (Box 1). By removing dominant
males or matriarchs from populations, selective harvesting can disrupt
social systems (Milner \emph{et al.} 2007), which may lead to reductions
in seed-dispersal efficacy by subordinate individuals if dominant
individuals are no longer able to establish territories or defend
preferred resources.

It is unclear if changes in the plant communities and the distribution
of resources may indirectly affect seed dispersal by changing the
identity and monopolizability of resources for social animals. For
example, human disturbances may modify the types of resources available,
which may alter consumer resource preferences (e.g., dominant
individuals that used to monopolize fungus patches switch to consuming
agricultural crops) and the quantity of seeds dispersed by individuals.
Encounter rates with resources should also change the nature of resource
preferences as well as the economics of resource defense. Global-change
forces, such as introduced plant invasions, that reduce encounter rates
with preferred resources may change the realization of preference as
well as the opportunities to monopolize preferred resources. Moreover,
it is possible that in cases where consumer preference does not change,
the monopolizability of preferred resources is diminished, which may
change the quantity of seeds dispersed by subordinate individuals. For
example, recent work suggests that carnivores may abandon carcasses more
quickly in the presence of human activity (Suraci \emph{et al.} 2019),
indicating that spatially clumped resources may be less defended by
dominant individuals when located near human activity, possibly leading
to greater access to preferred resources for subordinate individuals.

\textbf{Future Directions}

While centuries of research have been devoted to characterizing and
understanding animal social behavior, there is a surprisingly limited
amount of knowledge of how social behaviors affect trophic interactions
to generate patterns in communities. Since animal social status has
predictable, well-documented effects on individual diet and movement,
investigating how animal social behaviors contribute to intraspecific
variation in seed dispersal effectiveness may explain much of the
unresolved variation in seed dispersal and plant recruitment. There is
an important lacuna in non-primate systems for understanding how social
status may explain intraspecific variation in diet and space use, and
consequently seed dispersal effectiveness. While a few studies show that
social status explains individual diet composition in some potential
seed-dispersing vertebrates (e.g., pampas foxes and pronghorn; Dennehy
2001; Castillo et al. 2011), there is limited knowledge of how it may
explain the well-documented dietary variation in omnivorous species
where social status is known to determine resource access, such as many
carnivore species (Box 1). Since this current lacuna is likely due to
the difficulty of tracking both seed fate and the behaviors of cryptic
animals, we suggest methods for systems where animal behavior and seed
fate cannot be measured by direct human observation of wild animals
(Table 1).

Our framework also highlights that individual social status may play an
unappreciated role in determining post-dispersal seed survival and
recruitment when individuals of different social statuses utilize
different habitat types. We therefore strongly suggest that future
research measuring individual behavior, social status, and seed movement
also evaluate the quality of seed-deposition sites by measuring rates of
post-dispersal seed predation and seedling establishment (Table 1). We
predict that this framework will be most important in systems where
plant species are dispersal limited, animal social status affects
individual diet and movement, and fleshy fruit is an essential dietary
supplement for subordinate individuals (e.g., carnivore and folivore
populations). Understanding how social status affects seed dispersal may
be most critical in systems where animal social structure is modified or
destabilized, illuminating cryptic hotspots of seed dispersal loss.

\textbf{Acknowledgements}

We thank K.B. Strier, J. Kraus, C. Zirbel, C. Keller, M. Fuka, and A.
Weidemann for thoughtful discussion and helpful comments on the
manuscript. This work was supported by NSF DEB 2042211.

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\textbf{Tables and Figures}

\textbf{Table 1.} Example experimental designs to test our hypothesis
using non-invasive methods that could be adopted for a wide variety of
wildlife species, particularly for populations unhabituated to human
observers.\selectlanguage{english}
\begin{longtable}[]{@{}lll@{}}
\toprule
\begin{minipage}[b]{0.30\columnwidth}\raggedright\strut
\textbf{Approach}\strut
\end{minipage} & \begin{minipage}[b]{0.30\columnwidth}\raggedright\strut
\textbf{Social status estimation}\strut
\end{minipage} & \begin{minipage}[b]{0.30\columnwidth}\raggedright\strut
\textbf{Seed dispersal measurements}\strut
\end{minipage}\tabularnewline
\midrule
\endhead
\begin{minipage}[t]{0.32\columnwidth}\raggedright\strut
Experimental: Wild populations\strut
\end{minipage} & \begin{minipage}[t]{0.32\columnwidth}\raggedright\strut
Social interactions: Remote cameras to video-record behavior of
individuals in social context at foraging stations Each station has 2
food items: primary resource (e.g., carrion) and secondary resource
(fruit) Direction of aggressive/submissive behaviors indicates relative
dominance among individuals in a dyad or group Food item selection by
solitary individuals confirms a preference for primary resource and role
of social interactions in frugivory Link individual behavior to scat
collection: Food items are tagged with fine glitter or fluorescent dye
(unique color for each station) Hair snags near each food item to
capture DNA samples to ID individual genotypes\strut
\end{minipage} & \begin{minipage}[t]{0.32\columnwidth}\raggedright\strut
Dispersal distance: Presence/color of glitter or dye in scat indicates
distance and direction of movement from station Quantity of seeds
dispersed: Count number of seeds per scat deposit Germination trials to
estimate \# viable seeds per scat Sequence DNA from scat to link
individual genotypes from scat and feeding station assay Quality of seed
dispersal: Estimate rates of seed removal (see Bartel \& Orrock 2021 for
seed removal tray design) in microhabitats where scat is found\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.32\columnwidth}\raggedright\strut
Experimental: Captive populations\strut
\end{minipage} & \begin{minipage}[t]{0.32\columnwidth}\raggedright\strut
Human observers record direction of aggressive/submissive behaviors to
estimate each captive group's dominance hierarchy Each group is given 2
food items: primary resource (e.g., carrion) and secondary resource
(fruiting shrubs)\strut
\end{minipage} & \begin{minipage}[t]{0.32\columnwidth}\raggedright\strut
Dispersal distance: Observations of individual gut retention times can
be used with published estimates of movement distances in wild
populations to estimate potential dispersal distance Quantity of seeds
dispersed: Count number of seeds per scat deposit per individual
Germination trials to estimate seed viability\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.30\columnwidth}\raggedright\strut
Observational: Remote sensing\strut
\end{minipage} & \begin{minipage}[t]{0.30\columnwidth}\raggedright\strut
Remote cameras to video-record behavior of individuals in social context
at primary resources (e.g., carrion or fruiting trees) and secondary
resources (e.g., fruiting shrubs) Direction of aggressive/submissive
behaviors indicates relative dominance among individuals in a dyad or
group Individuals may be distinguished either visually in photos or with
radio-collars\strut
\end{minipage} & \begin{minipage}[t]{0.30\columnwidth}\raggedright\strut
Dispersal distance: Published estimates of gut retention times and
movement distances can be used to estimate potential dispersal distance
Quantity of seeds dispersed: Visually estimated through video recordings
at fruit sources (\# of visits and \# of seeds consumed per visit)\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.30\columnwidth}\raggedright\strut
Observational: Molecular analyses\strut
\end{minipage} & \begin{minipage}[t]{0.30\columnwidth}\raggedright\strut
Extensive scat collection may be done in systems where social status
carries a molecular signature. Identify individuals through genetic
analysis of scat. The following molecular approaches may be used
estimate individual social status: Fecal glucocorticoid concentration is
related to dominance in some cooperative breeding species (Creel 2001)
Reproductive hormone concentrations may be used in systems where
reproductive status affects dominance Genetic analyses to identify sex
may be used when sex affects dominance Average mass of scat per
individual may provide estimation of individual size when size affects
dominance\strut
\end{minipage} & \begin{minipage}[t]{0.30\columnwidth}\raggedright\strut
Quantity of seeds dispersed: Count number of seeds per scat deposit
Germination trials to estimate \# viable seeds per scat Quality of seed
dispersal: Estimate rates of seed removal in microhabitats where scat is
found\strut
\end{minipage}\tabularnewline
\bottomrule
\end{longtable}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

\textbf{Figure 1. A)} Social status has predictable effects on
individual resource access and space use that may explain
individual-level variation in seed dispersal effectiveness. Dominant
individuals monopolize preferred resources, forcing subordinate
individuals to supplement their diets to a greater extent with secondary
resources. Subordinate individuals may then disperse disproportionately
more or less seeds than dominant individuals, depending on whether fruit
is the primary or secondary resource. While this hypothesis has been
supported in recent work on Japanese macaques (Tsuji \emph{et al.}2020),
our framework demonstrates that this hypothesis could be applied to a
broad range of taxa. Our framework is also novel in its demonstration of
how social status may affect spatial patterns of seed dispersal, with
clear consequences for seedling establishment. Dominant individuals
typically defend territories with preferred habitat types, and
subordinate individuals generally have less restricted home ranges,
sample more habitat patches during a foray, and are more likely to go on
extraterritorial forays. Subordinate individuals are consequently more
likely to move seeds greater distances and deposit seeds in a broader
diversity of habitat types. Since post-dispersal seed survival and plant
recruitment are likely to vary across different habitats in a landscape
(e.g., differences in granivore abundance or resource availability), the
quality of seed dispersal services provided by subordinate individuals
may differ substantially from dominant individuals. \textbf{B)} We
provide predictions for the different types of seed dispersal kernels
that may arise due to animal social behavior, highlighting that the
outcome depends on food and habitat preferences of the animal dispersal
agent.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image2/image2}

\end{center}
\end{figure}

\textbf{Fig 2.} We provide predicted seed dispersal kernels and patterns
of seedling establishment for the two case studies described in Box
2.\textbf{A)} Japanese macaques of different social statuses differ in
seed-dispersal efficacy during non-masting years. Since subordinate
macaques provide higher-quality dispersal (i.e., lower rates of seed
mastication), we predict that the probability of seedling establishment
will be greater for seeds dispersed by subordinates than those dispersed
by dominant individuals, regardless of dispersal distance.
\textbf{B)}Flying foxes of different social statuses differ in
seed-dispersal efficacy. We expect that the probability of seedling
establishment remains low when seeds are dispersed by dominant
individuals because those seeds are dispersed directly below the mother
tree. The probability of seedling establishment should increase when
seeds are dispersed away from the mother tree by subordinate
individuals, escaping intraspecific competition and natural enemies.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image3/image3}

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\end{figure}

\textbf{Figure 3.} The effects of social status on seed dispersal may
have important implications for the movement and recruitment of plants
in the Anthropocene. \textbf{A)} Since subordinate individuals typically
have larger home ranges and disperse beyond the territories of
conspecifics, subordinate individuals are more likely to provide
long-distance seed dispersal services. Since long-distance seed
dispersal is critical for many plants to expand range boundaries,
subordinate individuals may facilitate plant movement to track changing
climate. \textbf{B)} Subordinate individuals are more likely to disperse
into urban habitats. Subordinates may therefore facilitate plant species
dispersal and persistence urban habitats. \textbf{C)} Since subordinate
individuals have larger home ranges and are more likely to disperse
beyond current conspecific territories, they may be more likely to use
corridors. The movement of subordinate individuals through corridors
likely facilitates plant movement through corridors, promoting plant
establishment in otherwise isolated habitat patches.

\textbf{Boxes}

\textbf{Box 1. Carnivores as variable seed dispersal agents}

Carnivores can be important agents of directed, long-distance dispersal
(Herrera 1989; Willson 1993; Rost \emph{et al.} 2012; L\selectlanguage{ngerman}ópez-Bao \emph{et
al.} 2015; Hämäläinen \emph{et al.} 2017; Shakeri \emph{et al.} 2018),
and rodent aversion to carnivore scat promotes the survival of
scat-dispersed seeds (Bartel \& Orrock 2021). Individual niche
specialization (i.e., where intraspecific variation in seed dispersal
effectiveness should be most pervasive) is most common in upper trophic
levels (Araújo \emph{et al.} 2011), and many carnivore species exhibit
high intraspecific variability in diet composition (Dumond \emph{et
al.}2001; Darimont \emph{et al.} 2009; López-Bao \& González-Varo 2011;
Cypher \emph{et al.} 2014; Davis \emph{et al.} 2015; Newsome \emph{et
al.} 2015; Manlick \emph{et al.} 2019). For carnivore populations with
dominance hierarchies, rank can constrain individual resource access
(Zimen 1976, 1981; Tilson \& Hamilton 1984; Gese \emph{et al.} 1996) and
space use (Gese 2001; Henry \emph{et al.} 2005; Dorning \& Harris 2017;
Kamler \emph{et al.} 2019), which likely produces predictable
intraspecific variation in the quantity and distance of seeds dispersed.
Below, we describe two carnivore species where recent work on social
behavior indicates that social structure may predict individual seed
dispersal effectiveness.

\textbf{Black-backed jackal (\emph{Canis mesomelas})}

Black-backed jackals have the potential to be effective seed-dispersal
agents when soft mast, a supplementary resource, is included in
individual diets (Do \emph{et al.} 2009; Kamler \emph{et al.} 2020).
While it has not yet been evaluated whether individual rank within the
dominance hierarchy affects soft mast consumption in this species, it
has been shown that rank affects individual space use such that
subordinate individuals move farther distances and are more likely to go
on extraterritorial forays (Kamler \emph{et al.} 2019), likely
increasing the distance that seeds are moved and the diversity of
habitats where seeds arrive.

\textbf{Brown bear (\emph{Ursus arctos})}

Brown bears consume the soft mast of at least 101 plant species spanning
24 families and 42 genera (García-Rodríguez \emph{et al.} 2021). A
single fecal deposit from a brown bear can contain thousands of seeds
(Willson 1993), creating a massive seed dispersal event. While brown
bears do not form cooperative packs, social dominance and subordination
within populations has predictable effects on individual resource access
and space use. In salmon-supported populations, dominant individuals
(typically large males) displace subordinate individuals (particularly
females with cubs) at salmon streams (Ben-David \emph{et al.} 2004;
Gende \& Quinn 2004). Since time spent at a salmon stream is positively
correlated with salmon assimilation in brown bear diets and negatively
correlated with plant matter assimilation (Deacy \emph{et al.} 2018), it
is likely that the monopolization of salmon streams by dominant
individuals leads to consistently greater quantities of seed-dispersal
services by subordinate individuals. Moreover, since the vast majority
of long-distance movement by bears is done by dispersing subadults
(Barto\selectlanguage{polish}ń \selectlanguage{english}\emph{et al.} 2019), these subordinate individuals are most
likely to disperse plant species beyond current range boundaries (Fig.
3A). Lamb and colleagues (2020) also show that urban habitats serve as
demographic sinks for brown bear populations, and urban populations are
supported by immigration by dispersing subadults. These subordinate,
subadult bears may therefore contribute substantially to the dispersal
and persistence of some plant populations in urban areas (Fig. 3B).
Since hunters typically target resident male bears (Gosselin \emph{et
al.} 2017; Leclerc \emph{et al.} 2019), this form of selective harvest
disrupts brown bear social structure, leading to increased infanticide
when immigrant males disperse into newly opened territories
(Gosselin\emph{et al.} 2017). Whether or not the persistent disruption
of brown bear social structure by selective harvesting generates
cascading effects on seed dispersal remains an open question. Moreover,
it is widely appreciated that brown bears use corridors to access
otherwise isolated habitat patches, and corridors are particularly
important for the dispersal of subadults into urban habitats (Clevenger
\& Waltho 2005; Ford \emph{et al.} 2017; Lamb \emph{et al.} 2020).
Corridors designed to facilitate brown bear movement through fragmented
landscapes may therefore have unappreciated benefits for the dispersal
of many bear-dispersed plant species.

\textbf{Box 2. Case studies where social status affects seed dispersal
effectiveness}

Despite the pervasive effects of social status on individual resource
access and space use, only a few case studies have demonstrated that the
effects of social status on individual behavior lead to predictable
patterns in intraspecific variation in seed dispersal effectiveness.
Importantly, these case studies also illustrate that increases in
availability of resources for subordinate individuals (e.g., masting
events or population decline) can lead to seed dispersal limitation when
subordinates no longer require fruit as a secondary resource or rely on
thieving tactics. We provide predicted seed dispersal kernels and
patterns of seedling establishment for both case studies (Fig. 2).

\textbf{Japanese macaques (\emph{Macaca fuscata})}

Japanese macaques are omnivorous primates that prefer nuts over soft
mast. Tsuji et al. (2020) found that in a year when the preferred nut
resource was low in abundance, high-ranking individuals monopolized this
resource, forcing low-ranking individuals to consume and disperse soft
mast. Low-ranking individuals also provided higher-quality seed
dispersal as subordinates had lower rates of seed mastication (Fig. 2A).
In contrast, during the masting year for nuts, there were no differences
between social ranks in seed dispersal effectiveness. Since subordinate
individuals had greater access to nuts, they consumed and dispersed less
soft mast. Dominant individuals continued to be low-quantity seed
dispersers, but the quality of seed dispersal increased during the mast
year due to lower rates of seed mastication.

\textbf{Flying fox (\emph{Pteropus tonganus})}

Dominant flying foxes defend fruiting trees as territories, repelling
subordinate intruders that seize fruit to consume in a distant location.
Since dominant, territorial individuals rarely move away from the trees
they defend, most seeds dispersed by these individuals fall below the
mother tree. Since subordinate individuals move seeds further distances
from the mother tree, these individuals provide higher-quality and
long-distance seed dispersal (Fig. 2B). However, in order for
subordinate individuals to exhibit this fruit-thieving strategy, all
fruiting trees need to be saturated with dominant, fruit-defending
individuals. McConkey et al. (2006) show that once flying fox densities
fell below a certain threshold, trees were no longer saturated by
dominant individuals, allowing most individuals to remain in their
trees, reducing the frequency of fruit-thieving behaviors and rates of
seed dispersal away from defended trees.

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