Separate and synergistic anti-herbivore effects of non-glandular trichomes and leaf chemistry in a desert plant

Plant defense phenotypes commonly integrate physical and chemical traits that may act synergistically against herbivores, but empirical evidence for synergy as a defense strategy remains limited. We experimentally tested the separate and combined effects of two common plant defenses, non-glandular trichomes and leaf chemistry, on the feeding, behavior, and performance of a generalist herbivore. We conducted choice and no-choice assays that exposed beet armyworm caterpillars (Spodoptera exigua, Noctuidae) to desert stingbush (Eucnide urens, Loasaceae) leaves with manipulated trichome cover and raised caterpillars on a diet containing factorial combinations of E. urens trichomes and leaf extracts. We assessed differences in caterpillar behavior, performance, and survival across treatments. We found a significant interactive effect of trichomes and leaf chemistry that markedly decreased caterpillar growth, providing evidence for a defense synergism. Both defenses also reduced caterpillar performance individually. Leaf extracts contained a high proportion of putatively defensive compounds, including iridoid glycosides, which were associated with reduced caterpillar growth and high mortality before pupation. Barbed trichomes impeded caterpillar movement and, when consumed, caused mandible damage and reduced eclosion rates compared to controls. Our results indicate that two commonly co-expressed plant defenses can synergistically reduce herbivore performance. These findings provide a rare example of trait synergy as a defense strategy and represent a step forward in the effort to study plant defense holistically, as suites or syndromes of defenses, rather than isolated traits.