Parasitoid-plant mutualism: Parasitoid attack of herbivore increases plant reproduction

Abstract

We tested whether a plant's life time seed production is increased by parasitization of herbivores in a tritrophic system, Arabidopsis thaliana (Brassicaceae) plants, Pieris rapae (Lepidoptera: Pieridae) caterpillars and the solitary endoparasitoid Cotesia rubecula (Hymenoptera: Braconidae). We established seed production for intact A. thaliana plants, plants that were mechanically damaged, plants fed upon by parasitized caterpillars and plants fed upon by unparasitized caterpillars. In the first experiment, with ecotype Landsberg (erecta mutant), herbivory by unparasitized P. rapae caterpillars resulted in a strongly reduced seed production compared to undamaged plants. In contrast, damage by P. rapae caterpillars that had been parasitized by C. rubecula did not result in a significant reduction in seed production. For the second experiment with the ecotype Columbia, the results were identical. Plants damaged by unparasitized caterpillars only produced seeds on regrown shoots. Seed production of plants that had been mechanically damaged was statistically similar to that of undamaged plants. Production of the first ripe siliques by plants fed upon by unparasitized caterpillars was delayed by 18-22 days for Landsberg and 9-10 days for Columbia. We conclude that parasitization of P. rapae by C. rubecula potentially confers a considerable fitness benefit for A. thaliana plants when compared to plants exposed to feeding damage by unparasitized P. rapae larvae. Plants that attract parasitoids and parasitoids that respond to herbivore-induced plant volatiles will both experience selective advantage, justifying the use of the term mutualism for this parasitoid-plant interaction. This type of mutualism is undoubtedly very common in nature.