Drought disrupts volatile-mediated predator foraging and oviposition, weakening trait-mediated top-down control

Abstract

O_LIDrought is a major abiotic stressor that can restructure trophic interactions by limiting herbivore success and disrupting chemical signaling between plants and natural enemies. In tritrophic systems, plant volatiles guide natural enemy foraging and reproductive investment, often scaling with herbivore density; however, it is unclear whether drought alters this relationship and weakens top-down control. C_LIO_LIUsing a tomato-aphid-ladybeetle system, we tested how drought and herbivore density jointly affect plant VOC emissions, predator behavior, and aphid dynamics. We manipulated water availability (well-watered vs. drought) and aphid density (low vs. high), and measured plant physiology, volatile profiles, predator visitation and oviposition, and aphid responses. C_LIO_LIDrought reduced stomatal conductance, plant biomass, and both total and compositional output of VOCs. Emission of key predator-attracting compounds (e.g., methyl salicylate, {beta}-myrcene) peaked in well-watered, high-density plants but was suppressed under drought. C_LIO_LILadybeetle visitation increased with aphid density but declined under drought, reflecting conserved shifts in volatile cues. Oviposition was concentrated on well-watered, high-density plants and associated with specific compounds (e.g., methyl salicylate, carvacrol), while others (e.g., cymene-7-ol, para, 1-octanol) were negatively associated. C_LIO_LIAphid suppression by predators occurred only under well-watered, high-density conditions. Under drought, aphid growth was already constrained, and predators had little additional effect on their abundance. However, both drought and predator presence influenced aphid demography, increasing production of dispersive alates. C_LIO_LIThese findings underscore the sensitivity of chemically mediated trophic interactions to environmental stress. Increased drought disrupts plant signaling, reducing natural enemy effectiveness, weakening biocontrol, and shifting herbivore population structure. Understanding how stress alters cue reliability is key to predicting community dynamics and managing ecosystem functions under stress. C_LI