Predation risk affects relative strength of top-down and bottom-up impacts on insect herbivores

Elucidating the relative strength of top-down and bottom-up forces in communities of phytophagus insects has been a major historical focus. Current consensus is that both forces play a role, but it is poorly known if these forces act differently on herbivores in the same assemblage and what factors underlie this variation. Using manipulative experiments with an assemblage of sap-feeding phytophagous insects (six species of plant-hoppers, leafhoppers, and heteropteran bugs) inhabiting intertidal Spartina marshes, we examined the association between herbivore behavior, risk of predation, and ultimately the relative impact of top-down (wolf spider predation) and bottom-up (host-plant nutrition) factors on the population density of each sap-feeding herbivore. A factorial experiment on open Spartina islets in the field (two levels of plant nutrition crossed with two levels of spider predation) showed that bottom-up and top-down manipulations differentially affected the various sap-feeders. Overall, bottom-up effects dominated in this sap-feeder community, whereby the density of all six sap-feeders increased when the nitrogen content of Spartina was elevated. By contrast, wolf-spider addition significantly suppressed populations of only the Prokelisia species and had little impact on the other four sap-feeder species in the community. Functional-response experiments and behavioral studies revealed that certain species (Prokelisia planthoppers) were at much higher risk of attack by wolf spiders than other sap-feeders in the assemblage and that risk of predation was associated with a species' particular "escape/defensive behavior." Moreover, risk of spider predation was roughly linked to the strength of top-down impacts in the field, because species with ineffective escape behaviors and a high risk of spider attack (Prokelisia planthoppers) were the only sap-feeders whose populations were suppressed by spider predation in the field. Thus, specific behavioral characteristics of the sap-feeders on Spartina influenced risk of predation and the relative strength of top-down and bottom-up impacts on their population dynamics. Notably, all herbivores in this system were positively influenced by elevated plant nutrition, only the common sap-feeder species (Prokelisia planthoppers) were adversely affected by spider predation, and it was the rarer sap-feeders in the assemblage that were least impacted by predation. These results call into question the overall pervasiveness of top-down forces and underscore the primacy of basal resources in structuring this community of phytophagous insects.