Direct and indirect non-consumptive predator effects in a tri-trophic system

Predators can affect prey populations not only through direct consumption but also via non-consumptive effects (NCEs), whereby the mere presence of a predator—perceived by the prey—alters its behavior and physiology. In herbivorous prey, such effects may extend beyond direct interactions, as plants can perceive predator-associated cues and respond defensively. These plant-mediated responses may, in turn, affect herbivore performance, constituting an indirect pathway of NCEs.
Here, we investigated both direct and indirect NCEs in multiple tri-trophic combinations involving two solanaceous host plants (Solanum lycopersicum and S. tuberosum), two herbivores (Leptinotarsa decemlineata and Trichoplusia ni), and a predatory hemipteran (Podisus maculiventris). We assessed herbivore performance on plants previously exposed to predator cues or untreated controls. Plant tissues were chemically analyzed to validate induction of defensive responses. A full-factorial experimental design was used to assess the interaction between direct and indirect NCEs.
We found clear evidence for plant-mediated (indirect) NCEs; however, herbivore responses were highly context-dependent: predator presence suppressed, enhanced, or had no effect on herbivore growth depending on the specific plant–herbivore combination. No interaction was found between direct and indirect NCEs.
These findings provide the first empirical demonstration of indirect NCEs mediated by plant responses to predator cues. The observed context dependence suggests that such effects may be common but previously overlooked, and in some cases misattributed to direct NCEs. These results highlight the need to broaden the scope of NCE research in multi-trophic systems.