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 et al. 2005; Dorning & Harris 2017; Kamleret 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 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 et al.2007; Ward et al. 2018), and urban habitats are often demographic
sinks (Vierling 2000; Lamb 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 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 et al. 2007; Tsujiet 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 et al.2018; Morrow 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 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 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 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 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.