Ant seed removal in a non‐myrmecochorous Neotropical shrub: Implications for seed dispersal

Abstract

This study investigated ant seed removal of Piper sancti‐felicis, an early successional Neotropical shrub. Neotropical Piper are a classic example of bat‐dispersed plants, but we suggest that ants are underappreciated dispersal agents. We identified eleven ant species from the genera Aphaenogaster, Ectatomma, Paratrechina, Pheidole, Trachymyrmex, and Wasmannia recruiting to and harvesting P. sancti‐felicis seeds in forest edge and secondary forest sites at La Selva, Costa Rica. We also tested for differences in ant recruitment to five states in which ants can commonly encounter seeds: unripe fruit, ripe fruit, overripe fruit, bat feces, and cleaned seeds. Overall, ants harvested more seeds from ripe and overripe fruits than other states, but this varied among species. To better understand the mechanisms behind ant preferences for ripe/overripe fruit, we also studied how alkenylphenols, secondary metabolites found in high concentrations in P. sancti‐felicis fruits, affected foraging behavior in one genus of potential ant dispersers, Ectatomma. We found no effects of alkenylphenols on recruitment of Ectatomma to fruits, and thus, these compounds are unlikely to explain differences in ant recruitment among fruits of different maturity. Considering that P. sancti‐felicis seeds have no apparent adaptations for ant dispersal, and few ants removed seeds that were cleaned of pulp, we hypothesize that most ants are harvesting its seeds for the nutritional rewards in the attached pulp. This study emphasizes the importance of ants as important additional dispersers of P. sancti‐felicis and suggests that other non‐myrmecochorous, vertebrate‐dispersed plants may similarly benefit from the recruitment to fruit by ants.

Secondary metabolites in a neotropical shrub: spatiotemporal allocation and role in fruit defense and dispersal

“…Furthermore, several species of bird consume the infructescences of Piper , including tanagers (Thraupidae), sparrows (Emberizidae), manakins (Pipridae), toucans (Ramphastidae), cuckoos (Cuculidae), and pigeons and doves (Columbidae; Palmeirim et al 1989, Thies and Kalko 2004). Occasionally, other small mammals (Leiser‐Miller et al 2019) or ants (Thies and Kalko 2004, Clemente and Whitehead 2020) consume the infructescences of Piper . After consumption, the seeds passed by bats and birds are viable (Palmeirim et al 1989, Baldwin and Whitehead 2015).…”

Fruits, frugivores, and the evolution of phytochemical diversity

“…), and there is likely high competition below bat feeding roosts, which could, in some contexts, mean these seeds have little chance of survival. However, ripe Piper fruits on the forest floor are often rapidly discovered by ants and carried away piecemeal (Clemente and Whitehead 2020). The fate of these secondarily-dispersed seeds is still being addressed in our ongoing work, and these results will help shape understanding of the ultimate fitness consequences of amide-mediated changes in bat behavior.…”

“…Amides have multiple functional roles in fruits, affecting defense against fungal pathogens and insect seed predators (Whitehead and Bowers 2014) and the behavior and physiology of seed‐dispersing bats (Baldwin and Whitehead 2015, Whitehead et al 2016). These effects can have cascading consequences in the seed dispersal process, affecting, for example, secondary seed dispersal and dispersal distance (Baldwin et al 2020, Clemente and Whitehead 2020). Together, these studies suggest that amides may have evolved largely for their ecological roles in protecting seeds and shaping the quality of seed dispersal.…”

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

“…For instance, ants can act as primary dispersers (removing fruits directly from parent plants) or secondary dispersers (moving fruits or seeds that have been previously handled by other animals or dispersed some distance abiotically). Ant‐dispersed plants include species with lipid‐rich appendages (“elaiosomes”) adapted to ant dispersal (Giladi, 2006; Lengyel et al, 2010) as well as species with fleshy fruits that are dispersed by both vertebrate frugivores (as primary dispersers) and ants (as primary or secondary dispersers; Byrne & Levey, 1993; Clemente & Whitehead, 2020; Levey & Byrne, 1993). Seeds are not typically dispersed far by ants (only several meters) before they are either dropped or brought into the nest, and those brought into nests are often “redispersed” by foragers that subsequently carry seeds back outside of the nest to deposit them in refuse piles (Figure 1; e.g., Canner et al, 2012).…”