Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree

Unregulated hunting of large-bodied frugivores is ubiquitous in tropical forests. Due to their low fecundity and complex social organization, large primates are often the first tropical forest vertebrates to be extirpated by hunting. Large primates are important seed dispersers and the only dispersal vectors of many large-seeded plants, leading to concerns that primate-dispersed trees will succumb to large-scale recruitment failure wherever they co-occur with overhunting. We used a field experiment in a remote, nonhunted region of the western Brazilian Amazon to test how the seedling recruitment success of a primate-dispersed Sapotaceae tree (Manilkara bidentata) is affected by distance from parent trees, protection from vertebrate seed predators, and gastro-intestinal seed cleaning associated with passage through frugivorous vertebrates. Only seed cleaning significantly increased the rate of seedling recruitment. Janzen–Connell effects have been widely purported as the central mechanism for recruitment failure, but our results suggest that for many tropical forest plant species Janzen–Connell effects are a second-order effect that acts once seeds have been successfully cleaned of fruit pulp by gut treatment. As an illustration of the relative importance of the sheer quantity of seeds ingested by woolly monkeys (Lagothrix cana), we further estimate the density and dispersal services provided by a complete primate assemblage to show that L. cana cleans and disperses nearly one million seeds per km2 per 24-day Manilkara fruiting season, amounting to over 71% of the seed dispersal services provided by the entire primate assemblage. The disperser vacuum in the absence of L. cana greatly reduces the quantity of cleaned seeds deposited on the forest floor. For similar fleshy-fruited species where gut passage greatly increases survival, a simple lack of redundancy in seed consumption may be the primary driver of recruitment failure resulting from large-primate extirpation due to overhunting, with Janzen–Connell effects secondarily influencing recruitment success as a function of either dispersal distance or seed density.