From the ground up: Belowground herbivory and phytoplasma infection influence aboveground herbivore performance

In cranberry ( Vaccinium macrocarpon ), phytoplasma infection increases plant susceptibility to herbivores; however, its role in shaping interactions between belowground and aboveground herbivores remains unclear. Here, we examined how phytoplasma infection and belowground herbivory by Japanese beetle ( Popillia japonica ) grubs jointly influence plant traits and performance of aboveground herbivores. Greenhouse experiments were conducted using a wild and a modern cranberry variety in a factorial design with infection status (uninfected vs. infected) and belowground herbivory (absence vs. presence). We measured nutrient (carbon and nitrogen) content, defence compounds (total phenolics and proanthocyanidins), and phytohormones (jasmonic acid [JA] and salicylic acid [SA]), along with performance of two foliar-feeding caterpillars, Sparganothis sulfureana and Lymantria dispar . Phytoplasma infection enhanced aboveground herbivore performance and was associated with higher nitrogen content, reduced phenolic compounds, lower JA levels, and elevated SA levels. In contrast, belowground herbivory induced plant defences, as evidenced by increased phenolics and JA, and reduced aboveground herbivore performance. Although the strength of these effects varied between varieties, the two factors produced opposing effects consistent with contrasting defence-related responses. Our findings show that phytoplasma infection and root herbivory exert contrasting influences on plant-mediated herbivore resistance, highlighting the importance of considering multiple stressors in plant-herbivore interactions within agroecosystems.