Lethal and nonlethal predator effects on an herbivore guild mediated by system productivity

Indirect effects propagated through intervening species in a food web have important effects on community properties. Traditionally, these indirect effects have been conceptualized as mediated through density changes of the intervening species, but it is becoming increasingly apparent that those mediated through trait (phenotypic) responses also can be very important. Because density- and trait-mediated indirect effects have different properties, it is critical that we understand the mechanisms of transmission in order to predict how they will interact, and when or where they will be important. In this study, we examined the mechanisms and consequences of the lethal (density-mediated) and nonlethal (trait-mediated) effects of a larval odonate predator on a guild of four herbivore species (a larval anuran and three species of snails) and their resources. We also manipulated system productivity in order to explore the effects of environmental context on the transmission of these two types of indirect effects. We show that trait-mediated effects arising from the predator can be very strong relative to density-mediated effects on both the competing herbivores and the species composition and production of their resources. A number of these indirect effects are shown to be contingent on productivity of the system. We further present evidence that trait- and density-mediated indirect effects originating from a predator may be transmitted independently through different routes in a food web, particularly when spatial responses of the transmitting prey are involved. Finally, effects on prey growth due to trait responses to the predator varied from negative to positive in predictable ways as a function of time and indirect effects on the larger food web. These results indicate the important role that trait-mediated indirect effects can play in trophic cascades and keystone predator interactions, and we discuss how the mechanisms involved can be incorporated in theory.