Cascading trait‐mediated interactions induced by ant pheromones

Abstract

Trait‐mediated indirect interactions ( TMII ) can be as important as density‐mediated indirect interactions. Here, we provide evidence for a novel trait‐mediated cascade (where one TMII affects another TMII ) and demonstrate that the mechanism consists of a predator eavesdropping on chemical signaling. Ants protect scale insects from predation by adult coccinellid beetles – the first TMII . However, parasitic phorid flies reduce ant foraging activity by 50% – the second TMII , providing a window of opportunity for female beetles to oviposit in high‐quality microsites. Beetle larvae are protected from ant predation and benefit from living in patches with high scale densities. We demonstrate that female beetles can detect pheromones released by the ant when attacked by phorids, and that only females, and especially gravid females, are attracted to the ant pheromone. As ants reduce their movement when under attack by phorids, we conclude that phorids facilitate beetle oviposition, thus producing the TMII cascade. We experimentally demonstrate a cascade of trait‐mediated indirect interactions involving two TMII units: (1) an ant–hemipteran mutualism unit, where the ants interfere with the ability of coccinellid predators to attack scale insects, and (2) a phorid fly‐ant‐hemipteran unit where the phorid flies reduce the foraging activity of the ants thus reducing their ability to interfere with the coccinellid predator. Through a series of experiments, we demonstrate that the gravid female coccinellid beetles indeed eavesdrop on the ant pheromone to find a window of opportunity to oviposit and hide their eggs in high‐quality microsites with high densities of their prey. This level of tight connection between a beetle predator and an ant that tends a hemipteran prey is unique in the scientific literature.