Rooted disruptions: Below‐ground herbivory drives contrasting natural enemy foraging for hosts and prey

Abstract Although research on below‐ground multitrophic interactions has increased, comparative studies examining how root herbivores influence the foraging behaviour of different natural enemies—especially generalist predators—remains limited. Parasitoids are thought to depend on more host‐specific cues that reveal not only location but also quality of hosts, while predators utilize more general signals and are less dependent on prey quality. Thus, we expected that parasitoids would prefer hosts on plants without below‐ground damage, and parasitization on those plants would be higher. In contrast, we expected that a generalist predator would not distinguish between hosts on either plant. We investigated these questions using a focal system of corn aphids ( Rhopalosiphum maidis ), the convergent lady beetle ( Hippodamia convergens ), and the parasitoid Aphidius colemani on maize ( Zea mays ). Specifically, we determined how root feeding by Western corn rootworm (WCR, Diabrotica virgifera virgifera ) larvae altered aphid population growth, consumption by predators, and parasitism rates. We also analysed how the presence of WCR and aphids altered above‐ground maize volatile blends and natural enemy preference 24 h and 1 week after aphid herbivory. Feeding by WCR larvae reduced aphid population size by 39% after 2 weeks. In contrast to our predictions, A. colemani produced an equal number of mummies per female between the two treatments, while lady beetles consumed more aphids on control plants. However, A. colemani preferred plants with aphids alone over control plants after 24 h of aphid feeding but did not distinguish between other pairwise comparisons, while H. convergens did not distinguish between different herbivory treatments at 24 h or 1 week in choice assays. Analysis of above‐ground volatiles demonstrated that at both time points, the combination of above‐ and below‐ground herbivory explained more of the variation in volatile blends than either above‐ or below‐ground herbivory alone. Furthermore, the interaction of above‐ and below‐ground herbivory reduced volatile richness compared to single herbivory at 24 h. Our results suggest that below‐ground feeding can inhibit parasitoid ability to identify plants with hosts in a critical early search window, potentially weakening trophic linkages. Additionally, over biologically relevant timescales of herbivore population growth, we see a shift in the identity of natural enemies displaying preferences for specific herbivory treatments: In contrast to parasitoids, the presence of below‐ground herbivores enhanced lady beetle host location, but only after a week of aphid feeding. Read the free Plain Language Summary for this article on the Journal blog.