Arsenic Hyperaccumulation in Pteris vittata Functions as a Toxic Lure and an Induced Defense Against Herbivores.

Abstract

Pteris vittata, a model arsenic hyperaccumulator, thrives in arsenic-contaminated soils. While arsenic accumulation is hypothesized to deter herbivores, its broader ecological impacts remain poorly understood. This study presents the first investigation of bidirectional interactions between insect herbivory and arsenic hyperaccumulation in P. vittata. Contrary to expectations, herbivorous insects preferentially consumed arsenic-containing tissues, more attracted to high-arsenic versus low-arsenic pinnae. However, larvae feeding on high-arsenic pinnae exhibited significant growth inhibition and negative weight gain. Arsenic accumulated primarily in insect cuticles and midguts, with substantial enrichment in exuviae (transfer coefficient: 5) and frass (transfer coefficient: 1.9), confirming exuviation and excretion as key detoxification pathways. Remarkably, herbivory by Spodoptera litura triggered a ~25% increase in arsenic concentrations of P. vittata pinnae. This induced elemental defense response was supported by enhanced arsenic distribution at wound sites and corresponding transporter protein upregulation. We propose an induce-trap defense hypothesis. Herbivore damage stimulates localized arsenic redistribution and potential attractant release, leading to dose-dependent insect toxicity while simultaneously strengthening plant defense. This intricate plant-insect interaction may explain the evolutionary persistence of arsenic hyperaccumulation in P. vittata.