Prey state alters trait‐mediated indirect interactions in rocky tide pools

Abstract

Summary1. Several studies on trait-mediated indirect interactions (TMIIs) have shown that predators can initiate trophic cascades by altering prey behaviour. Although it is well recognized that individual prey state alters antipredator and foraging behaviour, few studies explore whether this state-dependent prey behaviour can alter the strength of the ensuing tritrophic cascade. Here, we link state-dependent individual behaviour to community processes by experimentally testing whether hunger level and body size of prey altered antipredator behaviour and thus changed the strength of trophic cascades between predators and primary producers. 2. In rocky intertidal tide pools on the California Coast, waterborne cues from the predatory seastar Leptasterias spp. (Stimpson) can cause the herbivorous snail Tegula (Chlorostoma) funebralis (A. Adams) to reduce grazing and flee tide pools, resulting in positive indirect effects on tide pool microalgae. 3. However, we show that the strength of this behaviourally-mediated cascade may be contingent on prey hunger level and body size. During short field experiments at low tide, mediumsized snails that were either newly collected from the field or fed for 1 week in the laboratory mediated strong TMIIs because they grazed less when seastars were present. In contrast, no TMIIs occurred when medium-sized snails had been starved for 1 week because they continued grazing regardless of seastar presence. Newly collected small snails fled from seastars but did not mediate cascades because they ate little algae. Despite reaching an apparent size refuge from predation, many newly collected large snails fled from seastars, but those individuals that remained tended to graze the algae more quickly, resulting in unexpected negative indirect effects of seastars on algae cover. The implication of this pattern for the natural system is unclear. 4. Because average hunger level and size of snails vary over time and space in nature, a mosaic of TMII strength may exist. 5. Overall, the strength of tritrophic TMIIs in tide pools depended on individual prey state, supporting model predictions and adding to sparse empirical evidence. This outcome suggests that patterns occurring system-wide over the long term may be influenced by the state-dependent decisions made by the individuals present.

Ocean acidification alters the response of intertidal snails to a key sea star predator

“…Although not directly tested in this experiment, OA-induced attenuation of antipredator responses by snails could potentially lead them to forage under a greater range of conditions (e.g. even in the presence of sea stars), thereby shifting the consumer pressure of black turban snails on their algal food [24]. In particular, if snails increased their grazing rates but did not experience an accompanying elevation in mortality from sea stars, then algal densities might decline; on the other hand, if impaired flight responses incurred greater mortality of snails, then the net result for algae could be positive.…”

“…Changes in snail behaviour also have the potential to influence densities of algal species consumed by Tegula, both because such changes could influence snail foraging activities, and because altered flight responses could increase mortality of snails and thus how many might graze on algae (i.e. behavioural shifts could modify indirect effects of Pisaster on basal taxa through either 'non-consumptive' or 'consumptive' pathways [23,24]). …”

Trait-mediated indirect interactions among residents of rocky shore tidepools

“…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.…”

“…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.…”

“…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.…”