Prey state shapes the effects of temporal variation in predation risk

Abstract

The ecological impacts of predation risk are influenced by how prey allocate foraging effort across periods of safety and danger. Foraging decisions depend on current danger, but also on the larger temporal, spatial or energetic context in which prey manage their risks of predation and starvation. Using a rocky intertidal food chain, we examined the responses of starved and fed prey (Nucella lapillus dogwhelks) to different temporal patterns of risk from predatory crabs (Carcinus maenas). Prey foraging activity declined during periods of danger, but as dangerous periods became longer, prey state altered the magnitude of risk effects on prey foraging and growth, with likely consequences for community structure (trait-mediated indirect effects on basal resources, Mytilus edulis mussels), prey fitness and trophic energy transfer. Because risk is inherently variable over time and space, our results suggest that non-consumptive predator effects may be most pronounced in productive systems where prey can build energy reserves during periods of safety and then burn these reserves as 'trophic heat' during extended periods of danger. Understanding the interaction between behavioural (energy gain) and physiological (energy use) responses to risk may illuminate the context dependency of trait-mediated trophic cascades and help explain variation in food chain length.

Trait-mediated indirect interactions among residents of rocky shore tidepools

“…than fed snails, and TMII strength was not significantly weaker when snails were hungry. This was surprising because lower energetic reserves consistently increase risky foraging behavior and weaken TMIIs in many organisms (Werner & Anholt 1993, Clark 1994, Lima 1998b, Heithaus et al 2007, Matassa & Trussell 2014). Though we did not detect a strong effect of size and hunger of T. funebralis on fleeing and TMII in response to Leptasterias spp.…”

“…There is mounting evidence that these statedependent decisions by prey can alter the strength of TMII (Sih 1992, Freeman 2006. 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.…”

“…The fewer marine examples of TMII (Dill et al 2003, Long & Hay 2012 are generally from the laboratory (Appleton & Palmer 1988, Behrens Yamada et al 1998, Aschaffenburg 2008, Quinn et al 2012 or from wave-protected marine environments such as estuaries (but see Raimondi et al 2000, Trussell et al 2004, Heithaus et al 2007, Wada et al 2013, Matassa & Trussell 2014. The underrepresentation of examples from opencoast marine envi ronments might be because strong turbulence and advection dilute cues, render chemical cues less detectable and diminish the importance of TMII (Weissburg & Zimmer-Faust 1993, Weissburg et al 2002, Large et al 2011.…”

“…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.…”

“…Trussell et al 2004, Gravem & Morgan 2016 before conducting experiments during high tides when waves and currents rapidly mix and advect cues (e.g. Matassa & Trussell 2014). Tidepools also offer an advantage over other marine systems because replicate communities can be manipulated, and habitat shifts out of tidepools can be clearly defined (Trussell et al 2002(Trussell et al , 2004.…”