Parasitoids of leaf herbivores enhance plant fitness and do not alter caterpillar‐induced resistance against seed beetles

Abstract

Abstract Organisms of the third trophic level can indirectly interact with plants. However, whether parasitoids of herbivores have a positive effect on plant fitness has been controversial. In addition to possible effects on plant fitness, parasitoid‐mitigated herbivory can modify plant physiological responses and thereby alter the plant‐mediated indirect interactions between different herbivore species. These types of indirect multitrophic interactions remain largely unexplored. Thus, to understand the full effect of the third trophic level on plants, it is necessary to consider the context of the community of interacting species, both herbivores and their enemies. Here, we investigated whether parasitoids of leaf‐feeding caterpillars affect plant fitness (seed quantity and quality) and the consequences for seed‐dwelling insects at the second and third trophic levels through plant‐mediated effects. To test this, we exposed lima bean plants (Phaseolus lunatus), under controlled field conditions, to caterpillars (Spodoptera latifascia) that were unparasitized or parasitized by the parasitoid species Cotesia marginiventris. Later in the season, we measured seed production and infestation by seed beetles and their parasitoids. We found that parasitoids significantly reduced the leaf damage inflicted by the caterpillars, such that the plants suffered no loss in seed production. Yet, parasitoids had no effect on the emergence of seed beetles (Zabrotes subfasciatus and Acanthoscelides obtectus), which was equally reduced in plants attacked by unparasitized and by parasitized caterpillars. Seeds from undamaged plants were significantly more attacked by Z. subfasciatus beetles. Parasitism rates of seed beetle larvae were similar for all treatments. Although parasitized caterpillars did not damage the plants enough to reduce seed production (unlike unparasitized caterpillars), the damage they inflicted induced resistance against other herbivores. Taken together, these results show how parasitoids can indirectly enhance plant fitness in the context of the local multitrophic ecological networks. These findings have significant implications for natural and agricultural systems since they reveal that the indirect interaction between plants and parasitoids can be beneficial in communities with multiple herbivore species.