Intraspecific variability in herbivore response to elemental defences is caused by the metal itself

Some plants are able to accumulate on their leaves metals taken from the soil, using this as a defence against herbivorous arthropods. However, herbivore response to metal accumulation in plants is known to be variable. While some species and taxonomic groups are less affected than others, hormetic effects have also been observed in spider mites, herbivorous crop pests. Still, knowledge on the range and causes of intraspecific variation in the response of herbivores to metal accumulation is lacking. Here, using two species of spider mites, Tetranychus urticae and Tetranychus evansi, we tested the variation in 17 populations in response to cadmium-accumulating tomato plants and the drivers of such variation. We observed a nonlinear, hormetic response of mites to plants with cadmium in some, but not all, populations. The same pattern was recaptured in artificial diets with different concentrations of cadmium but not in artificial diets with sugars, which change in the plant in response to cadmium. This indicates that herbivores on metal-accumulating plants respond to metals, not to the variations in leaf carbohydrates. Therefore, metals exert different effects on herbivores according to the amount accumulated, but independently of other studied plant traits. This knowledge is key to the understanding of the mechanisms underlying herbivore responses to metal-based plant defences and to pesticides containing heavy metals. Additionally, our findings draw attention to the need of considering intraspecific variation and nonlinearities when studying the effects of metals and other contaminants on herbivorous arthropods.

Automated summary

Some plants accumulate metals on their leaves as a defense against herbivorous arthropods, but the response of herbivores to metal accumulation is variable. In this study, we tested the variation in response to cadmium-accumulating tomato plants in two species of spider mites. We found a nonlinear, hormetic response in some populations, indicating that herbivores respond to metals and not to changes in leaf carbohydrates. This knowledge is important for understanding herbivore responses to metal-based plant defenses and pesticides.