The contribution of trait-mediated indirect effects to the net effects of a predator

Abstract

Many prey modify traits in response to predation risk and this modification of traits can influence the prey's resource acquisition rate. A predator thus can have a ''nonlethal'' impact on prey that can lead to indirect effects on other community members. Such indirect interactions are termed trait-mediated indirect interactions because they arise from a predator's influence on prey traits, rather than prey density. Because such nonlethal predator effects are immediate, can influence the entire prey population, and can occur over the entire prey lifetime, we argue that nonlethal predator effects are likely to contribute strongly to the net indirect effects of predators (i.e., nonlethal effects may be comparable in magnitude to those resulting from killing prey). This prediction was supported by an experiment in which the indirect effects of a larval dragonfly (Anax sp.) predator on large bullfrog tadpoles (Rana catesbeiana), through nonlethal effects on competing small bullfrog tadpoles, were large relative to indirect effects caused by density reduction of the small tadpoles (the lethal effect). Treatments in which lethal and nonlethal effects of Anax were manipulated independently indicated that this result was robust for a large range of different combinations of lethal and nonlethal effects. Because many, if not most, prey modify traits in response to predators, our results suggest that the magnitude of interaction coefficients between two species may often be dynamically related to changes in other community members, and that many indirect effects previously attributed to the lethal effects of predators may instead be due to shifts in traits of surviving prey. I t has long been recognized that the effects of a predator can extend further than the species they consume. For example, killing a prey can indirectly affect other predators of the prey (causing exploitative competition) and resources of the prey (causing trophic cascades and keystone predator effects). Such indirect effects can have a large influence on the structure and dynamics of ecological communities (refs. 1-5 and reviewed in refs. 6-9). Traditionally, ecologists have ascribed these indirect effects of predators almost solely to their effects on prey density.Predators, however, also interact with prey by inducing changes in prey phenotype. Prey often respond to changes in predator density by modifying traits as diverse as behavior (10-12), morphology (12), and life history (12). These traitchanges may, in turn, affect other species interacting with these prey (13-18). For example, a predator-induced reduction in prey activity (making it a less efficient forager) may indirectly affect prey resources and consequently prey competitors. To distinguish such ''nonlethal'' predator effects from density-mediated indirect interactions (DMIIs, ref. 17) caused by chains of effects on density (''lethal'' effects) alone, these types of indirect interactions have been termed trait-mediated indirect interactions (TMIIs, ref. 17).Evidence is accumulating t...

Ecological consequences of phenotypic plasticity

“…Consequently, the predator, by consuming prey, indirectly affects the third species, typically referred to as a densitymediated indirect interaction. For example, predatory dragonfly larvae, through their consumption of frog tadpoles, indirectly interact with periphyton communities [15]. When dragonfly larvae are present, they consume tadpoles, thereby reducing tadpole density, which decreases the grazing pressure of tadpoles on the algae.…”

“…For example, in addition to eating tadpoles, dragonfly larvae also induce tadpoles to forage less, which causes an increase in algal densities [15]. Thus, Box 1.…”

Scaling-up anti-predator phenotypic responses of prey: impacts over multiple generations in a complex aquatic community

“…Experiments suggest that these NCEs and associated trait-mediated indirect effects (i.e. indirect effects of the predator on other species through induced changes in traits of the intervening prey, sensu [4]) can be as or more important than the direct and indirect effects arising from CEs of predators (reviewed in [12][13][14][15][16]). …”

Ecological and socioeconomic implications of a northern range expansion of black sea bass, Centropristis striata

“…NCEs may have equal or larger impacts on community structure than CEs; however, the strength of NCEs is context dependent and is influenced by both biotic and abiotic processes (Peacor and Werner 2001, Preisser et al 2005). …”

“…Predators can impact prey populations by consuming individuals (Hairston et al 1960, Paine 1980 and/or by inducing behavioral, morphological or physiological responses (Lima 1998a, Werner and Peacor 2003, Schmitz et al 2004). These latter responses, termed nonconsumptive effects (NCEs), may have an equal or larger impact on community structure than consumptive effects (Peacor and Werner 2001, Preisser et al 2005). For instance, behavioral avoidance of predators can potentially impact prey habitat use, foraging rates, energy allocation and ultimately population dynamics (e.g., Schmitz et al 1997, Grabowski 2004, Schmitz et al 2004.…”