Early herbivory attracts and facilitates subsequent specialist herbivores with consequences for plant performance

Plants are often attacked by multiple insect herbivores throughout their lifetime. Early‐arriving herbivores play a critical role in shaping plant responses, which in turn affect subsequent interactions. Later‐arriving herbivores can exploit damaged plants, but their role in modifying interactions and plant performance remains unclear. Thus, it is important to examine host plant preferences in late‐arriving herbivores, the cues guiding their behaviour, and the consequences of multiple herbivores.

We examined interactions between two insect herbivore specialists, Acalymma vittatum (Coleoptera: Chrysomelidae) and Anasa tristis (Hemiptera: Coreidae), which often overlap in sequence on shared Cucurbitaceae host plants. We characterized natural succession patterns, identified the cues influencing early‐ and late‐arriving herbivores, and tested the preference–performance hypothesis by determining whether the field‐identified cues driving A. tristis attraction and oviposition predicted improved offspring performance on plants previously colonized by A. vittatum . Finally, we investigated how A. vittatum ‐mediated recruitment of A. tristis influenced plant growth and reproductive traits by manipulating herbivory from both species in field experiments.

Field patterns showed that the presence, abundance, and oviposition behaviour of the late‐arriving herbivore, A. tristis , were strongly influenced by the presence and feeding activity of the early‐arriving herbivore, A. vittatum , but only on plants in the genus Cucurbita . In both choice and no‐choice bioassays, A. tristis adult females preferentially selected seedlings with active A. vittatum herbivory, and first‐instar hatchlings exhibited 28% greater growth on seedlings previously damaged by A. vittatum . A. tristis adult females did not respond to A. vittatum aggregation pheromone (chemical cue indicative of herbivory) in short‐range choice tests, nor to non‐ Cucurbita seedlings, regardless of prior herbivory. Field experiments showed that successive herbivory by A. vittatum and A. tristis significantly altered plant reproductive traits, delaying anthesis and reducing male flower and fruit production compared to control plants and those exposed only to A. vittatum . However, crop variety influenced the magnitude of these effects.

Together, these findings demonstrate that early‐arriving herbivores induce plant responses that increase the abundance of subsequent herbivores, with cascading negative effects on plants, compounding the effects of these herbivores.