Abstract Silicon (Si) supplementation can enhance symbiotic functions in some legumes (Fabaceae) with their nitrogen‐fixing rhizobia, such as root nodulation and nitrogen fixation. However, it is still poorly understood how Si influences legume–insect interactions. Here, we investigated how a symbiotic legume responds not only to Si supplementation but also to herbivory treatment with varying infestation levels in two events. We conducted a controlled climate chamber experiment by growing Medicago truncatula plants inoculated with rhizobia. For half of the plants, the soil was kept without Si (−Si), whereas the other half was regularly supplemented with Si (+Si). We then infested the plants with caterpillars of Spodoptera littoralis with 0, 1 or 3 larvae and 0, 1 or 1 larva in single herbivory attack and in double herbivory attack, respectively. To understand plant responses to such treatment combinations, we examined 16 functional traits. Nodule number, nodule fresh mass and nodule leghaemoglobin concentrations were not affected in single attack plants. However, increasing levels of herbivory led to decreases in such measured traits in double attack plants. Foliar C to N ratio increased in single attack plants but decreased in double attack plants with increasing levels of herbivory, indicating contrasting resource allocation. Herbivory did not affect the content of foliar Si, which was higher in +Si than −Si plants. Si and herbivory led to reduced foliar phenolics in double attack plants, suggesting a potential trade‐off between silicification and phenolic production. Si and herbivory led to increased trichome densities in single attack plants, but patterns were less clear in double attack plants. Herbivory but not Si reduced plant biomass with increasing levels of herbivory in double attack plants. Relative growth rates of the caterpillars, as proxy for plant resistance, decreased mainly due to herbivory treatment, when fed on single attack plants. Using a trait‐based approach, we provide novel insights to better understand the response of a legume to Si supplementation and different herbivory levels and events. We conclude that herbivory predominantly exerts much stronger effects than Si on various plant traits, pointing to a necessity to respond to herbivory by induced defence strategies. Read the free Plain Language Summary for this article on the Journal blog.
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