The defensive function of Ni in plants: Response of the polyphagous herbivore Spodoptera exigua (Lepidoptera: Noctuidae) to hyperaccumulator and accumulator species of Streptanthus (Brassicaceae)

Abstract

Metals sequestered by plants may defend them against herbivores and/or pathogens. We explored the effect of plant metal content on a polyphagous herbivore, Spodoptera exigua. Plant experiments used a Ni hyperaccumulator (Streptanthus polygaloides) and two Ni accumulator species (S. breweri and S. tortuosus). High- and low-Ni plants of each species were produced by growing plants on either Ni-amended or unamended soil. Mean leaf Ni contents for plants grown on Ni-amended soil and control soil, respectively, were: 1500 and 20 mg Ni kg-1 for S. polygaloides, 40 and 9 mg kg-1 for S. breweri, and 93 and 0.5 mg kg-1 for S. tortuosus. Neonate or second-instar Sp. exigua larvae were fed high- or low-metal leaves of each plant species, and survival and other parameters were monitored. High-Ni leaves of S. polygaloides were acutely toxic, resulting in 96% mortality within 10 days, whereas only 48% of larvae fed low-Ni leaves died. Low, and high-Ni leaves of S. breweri did not differ in their effects on larval survival, larval weight, adult weight, and duration of pupation. Leaves of S. tortuosus from high-Ni soil did not significantly affect larval survival relative to low-Ni leaves. However, larvae eating high-Ni leaves weighed significantly less and pupation was significantly delayed. Larval feeding experiments using artificial diet amended with Ni demonstrated a toxic threshold at 963 mg Ni kg-1 and a sublethal threshold at 535 mg Ni kg-1. Because plant material containing less Ni had detectable sublethal effects, we suggest that Ni interacts with other plant qualities (including secondary defensive compounds) to produce those effects. We conclude that hyperaccumulated Ni is a potent defense against polyphagous folivorous insects, but suggest that the sublethal impacts of the lesser Ni levels found in accumulator plant species may play only a minor defensive role against herbivores.