Extending the elemental defense hypothesis: Low levels of metals may defend serpentine plants from herbivory

Background/Question/Methods Metals that are accumulated by plants living on ultramafic or serpentine soils can defend some plants against insect herbivores. Until now, however, this “elemental defense” has been demonstrated almost entirely in hyperaccumulator species (plants that accumulate metals at extrememly high concentrations, e.g., >1000 µg/g of dry plant tissue for Ni). Our study tested the hypothesis that metal concentrations below hyperaccumulator levels can defend serpentine-tolerant plants, which can accumulate metals at low concentrations, against herbivores. Using greenhouse experiments, we tested the effect of varying levels of Ni in the soil on Mimulus guttatus (Phrymaceae) plant growth and damage inflicted by Junonia coenia (Nymphalidae) caterpillars. We then tested whether low levels of Ni were toxic to caterpillars using artificial diet experiments. Results/Conclusions Greenhouse soil Ni treatments resulted in elevated Ni levels in M. guttatus plants (40 – 200 µg/g), but these were well below the levels found in hyperaccumulator plant species (> 1,000 µg/g). Ni-treated plants were significantly more resistant to herbivory, as estimated by both plant damage and caterpillar weight gain. For example, Ni concentrations as low as 40 µg/g reduced caterpillar herbivory by as much as 50%. Ni treatment did not affect plant tolerance to herbivory. Ni in artificial diet was toxic to J. coenia caterpillars at the lowest concentrations that we tested (218 µg/g and 467 µg/g). This study demonstrates that metal concentrations well below hyperaccumulator levels can defend serpentine plants against herbivory. Given that thousands of plant species occur on serpentine soils, this study suggests that elemental defenses may be more common in nature than previously believed and that they may play an important role in the ecology of a large number of plant species.