Trade-offs in defense allocation: How soil legacy modulates plant-herbivore-predator dynamics

Cover crops, non-cash crops grown between cash crop cycles, are increasingly recognized for their ability to improve soil quality and regulate pest populations. Yet the ecological mechanisms by which cover crop legacies influence plant defenses and multitrophic interactions remain poorly understood. We hypothesized that distinct cover crops establish unique soil legacies that shape the defensive responses of subsequent plants to herbivory, leading to trade-offs between direct and indirect defense strategies. Using soils conditioned by three cover crops (Pea (Pisum sativum), Radish (Raphanus sativus), and Triticale (× Triticosecale) and a fallow control, we examined how these soil legacies affected maize defense chemistry and interactions with both herbivores and their natural enemies. We measured herbivory-induced volatile emissions, benzoxazinoid (BX) toxins in plants and herbivores, and protease inhibitor activity, and conducted predator choice assays to assess changes in trophic interactions. Distinct cover crop legacies resulted in defense trade-offs in maize. Plants grown in pea conditioned soils emitted higher proportions of indole in their volatile blends, enhancing indirect defenses, but exhibited lower BX levels, reducing direct chemical protection. Conversely, maize from fallow-conditioned soils invested more in direct chemical defenses but had weaker volatile-mediated attraction of predators. Notably, predators preferred herbivores fed on pea-conditioned maize, which accumulated more BXs despite lower plant BX content. Our findings show that cover crop legacies can act as an ecological levers, influencing how plants allocate defenses shape aboveground food web dynamics. By aligning cover crop selection with desired defense outcomes, farmers could leverage soil legacies as a natural means of pest suppression, linking fundamental ecological processes with sustainable agricultural management.