Fruit secondary metabolites alter the quantity and quality of a seed dispersal mutualism

Plant secondary metabolites are key mechanistic drivers of species
interactions. These metabolites have primarily been studied for their role
in defense, but they can also have complex consequences for mutualisms,
including seed dispersal. Although the primary function of fleshy fruits
is to attract seed-dispersing animals, fruits often contain complex
mixtures of toxic or deterrent secondary metabolites that can reduce the
quantity or quality of seed dispersal mutualisms. Furthermore, because
seeds are often dispersed across multiple stages by several dispersers,
the net consequences of fruit secondary metabolites for the effectiveness
of seed dispersal and ultimately plant fitness are poorly understood.
Here, we tested the effects of amides, nitrogen-based defensive compounds
common in fruits of the neotropical plant genus Piper (Piperaceae), on
seed dispersal effectiveness (SDE) by ants, which are common secondary
seed dispersers. We experimentally added amide extracts to Piper fruits
both in the field and lab, finding that amides reduced the quantity of
secondary seed dispersal by reducing ant recruitment (87%) and fruit
removal rates (58% and 66% in the field and lab, respectively). Moreover,
amides not only reduced dispersal quantity but also altered seed dispersal
quality by shifting the community composition of recruiting ants (notably
by reducing the recruitment of the most effective disperser by 90% but
having no detectable effect on the recruitment of a cheater species that
removes fruit pulp without dispersing seeds). Although amides did not
affect the distance ants initially carried seeds, they altered the quality
of seed dispersal by reducing the likelihood of ants cleaning seeds (67%)
and increasing their likelihood of redispersing seeds outside of the nest
(200%). Overall, these results demonstrate that secondary metabolites can
alter the effectiveness of plant mutualisms, by both reducing mutualism
quantity and altering mutualism quality through multiple mechanisms. These
findings present a critical step in understanding the factors mediating
the outcomes of seed dispersal and, more broadly, demonstrate the
importance of considering how defensive secondary metabolites influence
the outcomes of mutualisms surrounding plants.