Past studies have shown that the extremely high levels of metals found in several hyperaccumulator plant species are toxic to various herbivores, making the plants more resistant to herbivore damage. However, the number of hyperaccumulators found on serpentine or other ultramafic soil types is far lower than that of metal-tolerant plants, which can accumulate metals at much lower levels. We tested the hypothesis that metal concentrations below hyperaccumulator levels have anti-herbivore effects or otherwise confer herbivore resistance or tolerance to plants. In a set of greenhouse experiments we determined the effect of several levels of Ni in the soil on the growth of plants from a metal-tolerant population of Mimulus guttatus and measured damage to the plants caused by the caterpillar, Junonia coenia. Plants with higher accumulated Ni levels were damaged less by caterpillars and had greater biomass at the conclusion of the experiment. In separate experiments, caterpillars fed artificial diet amended with increasing concentrations of Ni experienced increased mortality and decreased weight gain even at Ni concentrations well below hyperaccumulator levels. In conclusion, we found evidence of ‘elemental defense' in M. guttatus with Ni concentrations far below those found in hyperaccumulators and documented significant negative effects of below-hyperaccumulator levels of Ni on J. coenia caterpillars. This suggests that elemental defenses could be much more widespread in nature than previously hypothesized and warrants continued investigation of this phenomenon in the field.