Prey State and Experimental Design Affect Relative Size of Trait- And Density-Mediated Indirect Effects

Abstract

Indirect effects, in which one species affects another through an intermediate species, can occur by changes in either the density or the traits of the intermediate species.Ecologists have focused primarily on density-mediated indirect effects, but have become interested in quantifying the relative sizes of trait-and density-mediated indirect effects. We examined how state-dependent prey behavior and experimental protocols affect the sizes of measured trait-and density-mediated indirect effects in a three-species chain (predator, prey, and resource). We found that the size of trait-mediated indirect effects relative to the size of density-mediated indirect effects increases as the level of resources increases. We also found that the relative contributions of trait-and density-mediated indirect effects depend on the timing of manipulations in relation to the state of individuals and their vulnerability to predators. In addition, we found that trait-mediated indirect effects that have been measured during a portion of a season may diminish or disappear when measured across a whole season because of behavioral compensation. These results show that the relative contributions of trait-and density-mediated indirect effects in a system will be variable, and experiments need to be designed to account for dynamic systems.

Predation in bird populations

“…For example, Swifts Apus apus probably escape nocturnal predation entirely by roosting on the wing (Lack 1956;Backman and Alerstam 2001), and Dunlins Calidris alpina may spend several hours aloft to avoid predation by Peregrines Falco peregrinus at high tide (Dekker 1998). In general, if resources are abundant so that the costs of anti-predation behaviour can be met then predation risk is unlikely to manifest itself in terms of prey being directly killed by predators (Luttbeg et al 2003;Bolnick and Preisser 2005;Preisser et al 2009). …”

Context‐dependent planktivory: interacting effects of turbidity and predation risk on adaptive foraging

“…Although still rare relative to the hundreds of studies that have demonstrated the strong influence of adaptive phenotypic plasticity in ecosystems (reviewed by Werner and Peacor 2003, Miner et al 2005, Ohgushi 2005), a handful of studies have demonstrated how environmental factors such as resource availability (Luttbeg et al 2003, Hawlena et al 2011, ecosystem productivity (Turner 2004, Werner andPeacor 2006), and landscape features (e.g., water depth, tidal flows, habitat complexity, canopy cover; Rothley and Dutton 2006, Heithaus et al 2009) can strongly influence nonconsumptive effects and TMIEs by altering the trade-offs associated with adaptive phenotypic responses.…”

Trait-mediated indirect interactions among residents of rocky shore tidepools

“…Finally, by conducting many replicate feeding and behavioral trials in the laboratory, we gained interesting insights regarding individual variation in predator−prey responses that warrant further attention. Our study adds to the growing body of empirical evidence supporting model predictions that individual variation in prey state alters TMII strength (Ovadia & Schmitz 2002, Luttbeg et al 2003, Persson & De Roos 2003, Kotler et al 2004, Freeman 2006, Rudolf 2012, Matassa & Trussell 2014, Gravem & Morgan 2016. …”

“…More recently, investigators have begun focusing on the context-dependency of TMII and factors altering its strength, such as environmental variation, features of informational cues, timing of measurements and individual variation in the traits of mediating species (Luttbeg et al 2003, Luttbeg & Trussell 2013, Matassa & Trussell 2014, Weissburg et al 2014, Gravem & Morgan 2016. For example, the transmission of predator cues to prey is strongly influenced by the environment, and air and water flow are particularly important for chemosensory cues (Smee et al 2010, Weissburg et al 2014.…”

“…For example, hungry prey individuals are often less responsive to predators, and therefore mediate weaker TMIIs (Heithaus et al 2007, Matassa & Trussell 2014, Gravem & Morgan 2016. Large individuals also might have different antipredator behaviors, vulnerabilities, energetic demands and feeding rates than smaller prey individuals, which might subsequently affect the strength of TMII (Luttbeg et al 2003, Persson & De Roos 2003, Freeman 2006, Gravem & Morgan 2016. Thus, individual variation in prey state likely alters the strength of TMII, but empirical tests are necessary to identify when individual variation is important, and whether such individual variation has community-level consequences.…”