Belowground herbivory impacts heritable biomass distribution and root morphology traits in Asclepias syriaca

Background/Question/Methods Optimal partitioning theory predicts that organisms allocate biomass among organs and functions to maximize the acquisition of limiting resources, thereby increasing fitness. In perennial plants, different genotypes are expected to differ in their patterns of resource partitioning. Abiotic factors are also known to shape optimal resource partitioning. For example, heterogeneity in soil nutrients and water influences belowground biomass as well as root architecture, morphology, and turnover rates. We know remarkably little, however, about the effects of biotic factors, particularly belowground herbivory, on these key plant traits. In a growth chamber experiment, we planted 20 genotypes of the common milkweed Asclepias syriaca and measured seven above and belowground traits to estimate heritable differences in biomass distribution and whole plant morphology, accounting for total plant size. In a two-year field experiment using the same 20 genotypes, we manipulated root-feeding larvae of the red milkweed beetle Tetraopes tetraophthalmus and tested for single and interactive effects of herbivory and plant genotype on patterns of biomass distribution.

Results/Conclusions Genotypes differed significantly in their constitutive pattern of biomass distribution after accounting for total plant size; this overall effect was mostly due to variation in stem and fine root dry mass. Root morphology, including the length and diameter of the rhizome, significantly differed among genotypes. A measure of clonal growth potential (number of vegetative buds on the rhizome) also varied significantly. In the field, root herbivores decreased mean total biomass by 16%, but increased mean root:shoot ratio by 46%, and we observed a significant genotype by herbivory effect for this ratio. Our results are consistent with optimal partitioning theory, which predicts shifts toward higher root biomass fraction under unfavorable soil environmental conditions (root herbivory). Considering the interactive effects of plant genotype and belowground herbivory on plant resource distribution will advance our understanding of plant responses to environmental heterogeneity and help to refine optimality theory.