Plant herbivore defenses typically escalate over the course of succession, paralleling increasing pressure from herbivores. We have observed increases in the herbivore resistance of a native plant, tall goldenrod, Solidago altissima (Asteraceae), over the first 15 years of oldfield succession in a large-scale field experiment in upstate New York. While our previous work has suggested that this increase in resistance is at least partially due to rapid microevolutionary shifts in the plant populations, plastic phenotypic shifts in response to changing conditions in the soil environment also contribute. Our field surveys revealed significant shifts in both the biomass and composition of soil microbial communities (bacterial and fungal) in the S. altissima rhizosphere over succession. We hypothesized that these microbial shifts would functionally affect plant metabolism and thereby at least partially mediate this increase in herbivore resistance that we observed over succession. In order to assess the capacity of these microbial shifts to alter herbivore resistance, we performed a soil microbiome transplant experiment with S. altissima plants and microbiomes from early (2 years post-agriculture), mid (6 years), and late (15 years) succession, and then characterized their resistance phenotypes through feeding assays with herbivores and analysis of leaf secondary metabolites.
Results/Conclusions
We found that the specialist goldenrod leaf beetle, Trirhabda virgata (Chrysomelidae), strongly preferred to eat leaves from S. altissima plants grown in soil media inoculated with early succession soil microbiomes (2 years) over their later succession (15 years) counterparts in a feeding choice experiment. This indicates that successional shifts in the soil microbiome can increase resistance to aboveground herbivores, likely contributing to the pattern of decreased herbivory on S. altissima plants we observed at later successional stages in the field. Likewise, the concentrations of several diterpene compounds in the leaves differed with successional microbiome age, suggesting a potential mechanism of resistance. These results also indicate that manipulating the soil microbiome may be a worthwhile target for altering plant resistance to herbivores, e.g. for improving crop resistance to insect pests.