Plant-defense mimicry facilitates rapid dispersal of short-lived seeds by hornets

Rates of seed dispersal have rarely been considered important. Here, we demonstrate through field observations and experiments that rapid dispersal is essential for the unusually short-lived seeds of Aquilaria sinensis (agarwood; Thymelaeaceae), which desiccate and die within hours of exposure by fruit dehiscence in the hot, dry forest canopy in tropical southwest China. We show that three species of Vespa hornets remove most seeds within minutes of exposure. The hornets consume only the fleshy elaiosomes and deposit most seeds in damp shade, where they can germinate, a mean of 166 m from the parent tree. Electrophysiological assays and field experiments demonstrate that the hornets are attracted by highly volatile short-carbon-chain (C5–C9) compounds, including aldehydes, ketones, alcohols, and acids, emitted from the dehiscent fruit capsule. These attractive fruit volatiles share 14 of 17 major electrophysiologically active compounds with those emitted from herbivore-damaged leaves, which attract predators, including hornets. Rapid seed dispersal thus appears to have been achieved in this species by the re-purposing of a rapid indirect defense mechanism. We predict that rapid seed dispersal by various mechanisms will be more widespread than currently documented and suggest that volatile attractants are more effective in facilitating this than visual signals, which are blocked by vegetation. [Display omitted] •Rapid seed dispersal is essential for the short-lived seeds of Aquilaria sinensis•Hornets remove seeds within minutes of exposure and deposit most in damp shade•Hornets are attracted by highly volatile fruit chemicals•These volatiles mimic those that attract predators to herbivore-damaged leaves Qin et al. demonstrate that rapid seed dispersal by hornets is essential for short-lived seeds of an agarwood plant. Hornets are attracted rapidly by highly volatile fruit chemicals, which appear to have been achieved by re-purposing of volatiles utilized in plant defense. Rapid seed dispersal seems widespread, and volatiles are effective signals.