Species-specific plant-mediated effects between herbivores converge at high damage intensity

Abstract

Plants are often exposed to multiple herbivores and densities of these attackers (or corresponding damage intensities) often fluctuate greatly in the field. Plant-mediated interactions vary among herbivore species and with changing feeding intensity, but little is known about how herbivore identity and density interact to determine plant responses and herbivore fitness. Here, we investigated this question using Triadica sebifera (tallow) and two common and abundant specialist insect herbivores, Bikasha collaris (flea beetle) and Heterapoderopsis bicallosicollis (weevil). By manipulating densities of leaf-feeding adults of these two herbivore species, we tested how variations in the intensity of leaf damage caused by flea beetle or weevil adults affected the performance of root-feeding flea beetle larvae and evaluated the potential of induced tallow root traits to predict flea beetle larval performance. We found that weevil adults consistently decreased the survival of flea beetle larvae with increasing leaf damage intensities. In contrast, conspecific flea beetle adults increased their larval survival at low damage then decreased larval survival at high damage, resulting in a unimodal pattern. Chemical analyses showed that increasing leaf damage from weevil adults linearly decreased root carbohydrates and increased root tannin, whereas flea beetle adults had opposite effects as weevil adults at low damage and similar effects as them at high damage. Furthermore, across all feeding treatments, flea beetle larval survival correlated positively with concentrations of carbohydrates and negatively with concentration of tannin, suggesting that root primary and secondary metabolism might underlie the observed effects on flea beetle larvae. Our study demonstrates that herbivore identity and density interact to determine systemic plant responses and plant-mediated effects on herbivores. In particular, effects are species-specific at low densities, but converge at high densities. These findings emphasize the importance of considering herbivore identity and density simultaneously when investigating factors driving plant-mediated interactions between herbivores, which advances our understanding of the structure and composition of herbivore communities and terrestrial food webs.

Keywords: above- and belowground herbivore interaction; conspecific and heterospecific herbivore interaction; density-dependent effect; herbivore-induced specific response; identity and density of herbivores; plant-herbivore interaction; plant-induced defense; resistance and susceptibility.