DISCUSSION
Overhunting can alter many plant-animal interactions, with consequences
ranging from altered dynamics of tropical tree populations (Brodieet al. 2009; Culot et al. 2017) to potential declines in
forest carbon storage (Bello et al. 2015; Peres et al.2016; Chanthorn et al. 2019). But we still have a limited
understanding of how the multiple effects of defaunation combine to
affect tree populations. Our results suggest that how a tropical tree
species responds to defaunation is primarily based on whether and how
the predation of its seeds is altered by hunting. But unfortunately,
even knowledge about altered seed predation rates still confers only
limited ability to predict population-level responses. Moreover, our
knowledge about how defaunation affects seed predation remains limited.
Granivory could increase (Galetti et al. 2015; Rosin & Poulsen
2016; Culot et al. 2017) or decrease (Wright et al. 2000;
Roldán & Simonetti 2001; Beckman & Muller-Landau 2007) under
defaunation and, even in the same forest, species can differ wildly in
how seed predation rates change in response to defaunation (Guariguataet al. 2000; Rosin & Poulsen 2016). In our model, we applied
changes in seed predation equally to all of our species, but our results
might have changed if seed predation varied according to species traits.
For example, Mendoza and Dirzo (2007) hypothesized that smaller seeds,
whose small-bodied predators would likely remain extant even in highly
defaunated systems, would face higher predation pressure than larger
seeds, whose predators would be eliminated by overhunting. However, we
conducted a review of studies that measured seed predation in
defaunation versus non-defaunation conditions (Table S4) and found that
seed size did not predict changes in predation pressure (Figure S4).
Though seed size did not correlate with change in seed predation, our
results show that small-seeded angiosperms were more demographically
sensitive to changes in seed predation than gymnosperms or large-seeded
species. This result provides a potential focus for future research:
understanding exactly how defaunation affects seed predation may be
particularly important for assessing the vulnerability of small-seeded
angiosperms.
Defaunation can also affect later life-stages via changes in herbivory
or other physical damage (Gardner et al. 2019). We did not
include such effects in our model because of very scant data connecting
defaunation to changes in sapling or adult vital rates. Removing
large-bodied ecosystem engineers such as elephants may impact older
plant life stages (Poulsen et al. 2018), though the distribution
of such megafauna and their foraging behaviour are highly variable
across the world’s tropical forests. While changes in herbivores and
ecosystem engineer abundances may significantly impact local plant
communities (Luskin et al. 2017), it is difficult to consider
these factors in a global assessment of defaunation.
Surprisingly, factors such as dispersal mode and the strength of density
dependence were unrelated to demographic responses to defaunation in our
model. Previous studies have assumed that dispersal limitation was the
most important effect of defaunation (Terborgh 2013), leading to
predictions that defaunation-induced losses of seed dispersal will
reduce carbon storage (Brodie & Gibbs 2009; Bello et al. 2015;
Dantas de Paula et al. 2018; Chanthorn et al. 2019).
However, given that defaunation alters seed predation as well as seed
dispersal, and that altered seed dispersal was unrelated to
population-level defaunation impacts, overhunting may not necessarily
cause the widespread replacement of heavy-wooded, vertebrate-dispersed
species by lighter-wooded species (with other means of dispersal) that
have been predicted. Therefore, whether defaunation will result in major
losses of forest carbon remains unclear. Indeed, not all defaunated
forests show decreases in biomass (Harrison et al. 2013; Bagchiet al. 2018). Despite attempts to model the impacts of
defaunation on tropical tree communities and ecosystems via altered seed
dispersal alone, our study shows that there is too much uncertainty
surrounding other defaunation effects—notably seed predation—to
currently be able to make accurate predictions about cascading impacts
on populations and ecosystem processes.
Likewise, phenotypic traits conferred little ability to predict
defaunation responses across species. While many of the traits did
correlate with the vital rates that determine population dynamics, these
correlations were relatively weak (Table S6). Importantly, of the traits
that we assessed, only seed mass significantly correlated with adult
survival, which, in long-lived woody plants, influences population
dynamics more than any other vital rate (Silvertown et al. 1993;
Zuidema 2000). Because large seeds are unlikely to be dispersed by small
vertebrates, many studies have assumed that large-seeded species are the
most vulnerable to defaunation (e.g. Bello et al. 2015; Osuriet al. 2016). However, in our study, large-seeded species were
less responsive to defaunation because of their lower adult mortality.
Our smaller-seeded species had stronger responses to defaunation, but
the direction of the response was mediated by how defaunation affected
seed predation. As seed mass does not predict changes in seed predation
(Figure S4), we still cannot use this trait to assess a priorispecies’ responses to defaunation.
What, then, can we predict about the consequences of defaunation for
tropical trees? We know from studies of individual species that
defaunation can cause significant population declines (Wright & Duber
2001; Culot et al. 2017), but we still have limited ability to
scale up these observations to predict patterns at the community or
ecosystem level. Phenotypic traits and even demographic vital rates are
not sufficient to predict defaunation effects. However, our results
highlight a fruitful direction for future research; an improved
understanding of seed predation—how it affects tree populations and
how it is affected by defaunation—would greatly reduce uncertainty
around the cascading impacts of defaunation. This will improve the
accuracy of predictions of the global consequences of overhunting for
tropical forests.