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

Cover cropping—the practice of cultivating non-cash crops between cash crop cycles—has been found to influence soil quality and suppress weed establishment. Recently, this practice was found to significantly impact pest performance via changes in phytochemistry. Although there is evidence that soil legacies affect plant chemistry, their specific influence on plant defenses and interactions with higher trophic levels remains poorly understood. We hypothesize that different cover crop plants produce distinct soil legacies that can significantly influence the defensive responses of successive plants to insect herbivory—at least in part through changes in plant chemistry—with some legacies promoting stronger direct defenses and others enhancing indirect defenses that rely on natural enemies of herbivores. We examined the effect of distinct cover crops ( Pisum sativum , Raphanus sativus , × Triticosecale , and fallow soils) on both direct and indirect defenses against chewing herbivores in maize. We measured levels of herbivory-induced plant volatile chemicals, the plant toxins benzoxazinoids (BX) in both plants and herbivores, and protease inhibitor levels in maize grown under these cover-crop conditioned soils. Additionally, we conducted choice assays with a putative predator to assess whether soil conditioning influenced predator feeding preferences. Our results revealed that cover crop conditioning altered soil nutrient levels and observed trade-offs in plant defenses. Maize grown in pea-conditioned soils exhibited higher proportions of indole in their volatile blends, enhancing indirect defenses. However, these plants produced lower BX levels, reducing direct defenses. Conversely, plants in fallow-conditioned soils favored direct defenses but had weaker indirect defenses. Predators preferred herbivores from pea-conditioned plants. Interestingly, herbivores on pea-conditioned plants accumulated more BXs despite lower BX levels in these plants. These findings demonstrate that cover crop legacies act as a “programming” tool for plant defense strategy, orchestrating a tradeoff between indirect and direct defenses. By matching cover crop selection to desired defense outcomes, growers can potentially leverage soil legacies to enhance biological control via toxin or natural enemy mediated defense, paving the way for more targeted and sustainable pest management.