PREDATION RISK AFFECTS RELATIVE STRENGTH OF TOP-DOWN AND BOTTOM-UP IMPACTS ON INSECT HERBIVORES

Abstract

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 planthoppers, 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. Corresponding Editor: D. A. Spiller