Nonlinear effects of plant root and shoot jasmonic acid application on the performance of Pieris brassicae and its parasitoid Cotesia glomerata

1. Plant species employ several direct and indirect defence strategies to protect themselves against insect herbivores. Most studies, however, have focused on shoot-induced responses. Much less is known about interactions between below- and above-ground herbivores and how these may affect their respective parasitoids. 2. Here, we quantify the impact of below-ground induced responses vs. that of above-ground induced responses in a feral Brassica on the performance of Pieris brassicae and its endoparasitoid Cotesia glomerata. Jasmonic acid (JA) was applied to induce the plants above- or below-ground. The glucosinolate, sugar and amino acid levels of the leaves were analysed. 3. Pieris brassicae larvae grew significantly slower on shoot JA-induced (SJA) plants than on root JA-induced (RJA) and control plants, which were treated with acidic water. On RJA and control plants they showed similar developmental trajectories. Pupal masses, survival till eclosion and egg load, however, were similar on all plants. 4. The development of C. glomerata larvae on SJA plants was significantly longer than that on RJA and control plants. In contrast, the parasitoid's pupal stage lasted longer in hosts feeding on control plants. The total developmental times eventually were similar in all groups. However, the masses of male and female C. glomerata adults that developed hosts on control and RJA plants were significantly larger than those from hosts on SJA plants. JA application increased total glucosinolate contents and decreased the sugars and total amino acids levels independent of whether JA was applied. However, the trajectories of herbivore-induced glucosinolate levels differed between RJA and SJA plants. 5. These results show that the differential effects of above- and below-ground-induced responses on herbivores also affect higher trophic levels in a nonlinear fashion via differential changes in host plant quality. In particular, the indirect effects that below-ground herbivores have on the performance of above-ground parasitoids may exceed the direct effects of plant chemistry on herbivore performance. Consequently, above-ground and below-ground interactions mediated by induced plant responses have the potential to mediate insect community structure and function in complex way