Assessing the effect of sequential insect and nematode herbivory on each other’s performance via responses of host plants under drought stress in multitrophic interactions

Nematode–plant–caterpillar interactions are among the most common in natural and agricultural systems. While most studies investigating such plant-mediated interactions focus on snapshots of how caterpillars are affected by the nematode-infested roots, it is important to note that these interactions can be complex and multifaceted. For example, the impacts of caterpillar’s frequent attacks on plants with nematode-infested roots (and vice-versa) are still poorly understood, despite being necessary to reveal how such interactions might change and affect the plant over longer time periods (e.g., a growing season). In addition, little is known about the role of environmental conditions (e.g., drought) in facilitating (or helping avoid) future biotic stressors. In order to understand how one herbivore affects the establishment and preference of the other we used a generalist nematode (Meloidogyne incognita), a common crop-pest caterpillar (Spodoptera exigua), and tomato plants in a sequential-herbivory experiment complemented by a preference essay. Overall, we found that the first herbivore (primer) affects the success and preference of a second herbivore, but the effect depends on which part of the plant was attacked first. We also found that environmental conditions can significantly impact the observed patterns, as plants under drought conditions were more infected by nematodes and also preferred by caterpillars. Ultimately, plants are able to host and mediate (with a great cost to their growth and fitness) multiple herbivores if enemies partition resources or utilize different parts of the plant.