Bottom-up effects of alder-associated Frankia bacteria on red alder flea beetle (Altica ambiens)

Red alder (Alnus rubra) is frequently colonized with belowground nitrogen-fixing Frankia bacteria. While these bacteria are commonly considered plant mutualists, we discovered significant costs associated with Frankia-colonization through enhanced susceptibility of red alder seedlings to a specialist insect herbivore, the red alder flea beetle (Chrysomelidae: Altica ambiens). In feeding trials using leaves of red alder seedlings inoculated with Frankia (F+) and leaves from Frankia-free (F-) controls, beetles showed a significant preference for F+ plants. Leaf chemical analyses revealed greater soluble protein levels (11.1%) and a decrease in phenolic compounds (49.3%) in F+ plants when compared to F- plants. In an accompanying field study, we found a strong positive correlation between the colonization of alder seedlings with Frankia bacteria and leaf damage by the chrysomelid beetles (r = 0.894; P < 0.001). Our study demonstrates that belowground microbial plant symbionts can incur costs through an enhancement of aboveground herbivory.