Bottom-Up Forces Mediate Natural-Enemy Impact in a Phytophagous Insect Community

We employed a combination of factorial experiments in the field and laboratory to investigate the relative magnitude and degree of interaction of bottom-up factors (two levels each of host-plant nutrition and vegetation complexity) and top-down forces (two levels of wolf-spider predation) on the population growth of Prokelisia planthoppers (P. dolus and P. marginata), the dominant insect herbivores on Spartina cordgrass throughout the intertidal marshes of North America. Treatments were designed to mimic combinations of plant characteristics and predator densities that occur naturally across habitats in the field. There were complex interactive effects between plant resources and spider predation on the population growth of planthoppers. The degree that spiders suppressed planthoppers depended on both plant nutrition and vegetation complexity, an interaction that was demonstrated both in the field and laboratory. Laboratory results showed that spiders checked planthopper populations most effectively on poor-quality Spartina with an associated matrix of thatch, all characteristics of high-marsh meadow habitats. It was also this combination of plant resources in concert with spiders that promoted the smallest populations of planthoppers in our field experiment. Planthopper populations were most likely to escape the suppressing effects of predation on nutritious plants without thatch, a combination of factors associated with observed planthopper outbreaks in low-marsh habitats in the field. Thus, there is important spatial variation in the relative strength of forces with bottom-up factors dominating under low-marsh conditions and top-down forces increasing in strength at higher elevations on the marsh. Enhancing host-plant biomass and nutrition did not strengthen top-down effects on planthoppers, even though nitrogen-rich plants supported higher densities of wolf spiders and other invertebrate predators in the field. Rather, planthopper populations, particularly those of Prokelisia marginata, escaped predator restraint on high-quality plants, a result we attribute to its mobile life history, enhanced colonizing ability, and rapid growth rate. Thus, our results for Prokelisia planthoppers suggest that the life history strategy of a species is an important mediator of top-down and bottom-up impacts. In laboratory mesocosms, enhancing plant biomass and nutrition resulted in increased spider reproduction, a cascading effect associated with planthopper increases on high-quality plants. Although the adverse effects of spider predation on planthoppers cascaded down and fostered increased plant biomass in laboratory mesocosms, this result did not occur in the field where top-down effects attenuated. We attributed this outcome in part to the intraguild predation of other planthopper predators by wolf spiders. Overall, the general paradigm in this system is for bottom-up forces to dominate, and when predators do exert a significant suppressing effect on planthoppers, their impact is generally legislated by vegetation characteristics.