Cadmium induced metabolic reprogramming of tomato drives bottom-up cascade in a tomato-thrips-predator system

Cadmium (Cd) pollution disrupts plant-insect tri-trophic interactions in agroecosystems, yet the mechanisms remain poorly understood. In this study, we systematically investigated the effects of Cd exposure (1.0 mg/L) on the tomato (Solanum lycopersicum)-western flower thrips (Frankliniella occidentalis)-minute pirate bugs (Orius sauteri) system by integrating analyses of tomato photosynthetic physiology, untargeted metabolomics, and the fitness, behavior and Cd accumulation of the two insect species. Cd accumulated abundantly in tomato leaves (115.67 mg kg⁻¹), inhibited photosynthetic efficiency, and significantly enriched flavone, flavonol and monoterpenoid biosynthesis. Cd-stressed tomato plants significantly decreased the survival rate of F. occidentalis nymphs and adults, with a 17.0%-31.0% reduction at 72 h post-exposure. For the natural enemy O. sauteri, Cd stress reduced its predation rate on F. occidentalis by 14.1% (24 h) and 24.3% (48 h), and decreased its oviposition by 46.4%, while no significant effects were observed on adult survival or egg hatching rate. The leaf-to-thrips bio-concentration factor was only 0.0074, while the thrips-to-predator transfer ratio reached 0.16 due to differential excretion and detoxification capacity across trophic levels. Orius sauteri exhibited no olfactory or spatial preference between Cd-treated and control leaves, but its predation rate decreased by 32.6% when feeding on Cd-exposed thrips. Trophic Cd accumulation induced sublethal physiological stress in predators, restraining their predatory activity independent of plant avoidance behavior. This study demonstrates that Cd-induced tomato metabolic reprogramming initiates multi-layer adverse effects across three trophic levels, providing quantitative evidence for evaluating ecological risks of Cd contamination in vegetable IPM systems.