We demonstrate an apparent trait-mediated indirect interaction (TMII) of predators on primary producers in a natural community by altering prey behavior over short and long time scales. Small predatory sea stars (Leptasterias spp.) caused herbivorous snails (Tegula funebralis) added to rocky intertidal tidepools to quickly flee into refuge microhabitats outside tidepools within days, and this was associated with a 58% increase in microalgal growth after 2 weeks. Similarly, removing sea stars caused snails to increase use of tidepools for 1–10 months. After adding sea stars to tidepools, snails quickly fled and then consistently increased use of refuges outside tidepools for 10 months. This was associated with average increases of 59% for microalgal growth over 1 month and 254% for macroalgal growth over 8 months inside tidepools. In 63 unmanipulated tidepools, densities of sea stars and snails were negatively correlated. High densities of snails were associated with unpalatable algal species and bare rock, while high densities of sea stars were associated with palatable algal species, suggesting that this apparent TMII may have community-level impacts. Though multiple lines of evidence suggest TMIIs were likely operating in this system, it was not possible to experimentally partition the relative contributions of TMIIs and density-mediated indirect interactions (DMIIs), so further caging experiments are necessary to distinguish their relative strengths. Overall, we suggest that predators can benefit primary producers by changing prey behavior even when predators and prey are unrestrained by cages or mesocosms, embedded in complex communities, and observed over multiple time scales.

Recent mass mortalities of two predatory sea star species provided an unprecedented opportunity to test the effect of predators on rocky intertidal prey. Mass mortalities provide insight that manipulative experiments cannot because they alter ecosystems on a larger scale, for longer time periods, and remove both organisms and their cues from the environment. We examined shifts in population size structure, vertical zonation, and use of emersed refuge habitats outside tidepools by the abundant herbivorous black turban snail Tegula funebralis, both before and after the successive mortalities of two predatory sea stars. The small cryptic predator Leptasterias spp. suffered a localized but extreme mortality event in November 2010, followed by two mass mortalities of the keystone predator Pisaster ochraceus in August 2011 and autumn 2013. After the local extinction of Leptasterias, the population size of Tegula more than doubled. Also, since Leptasterias primarily inhabited only mid to low intertidal tidepools at this site, small and medium sized snails (which are preferred by Leptasterias) shifted lower in the intertidal and into tidepools after the mortality of Leptasterias. After the mortality of Pisaster in August 2011, large snails did not shift lower in the intertidal zone despite being preferred by Pisaster. Small and medium sized snails became denser in the higher zone and outside tidepools, which was not likely due to Pisaster mortality. Previous studies concluded that Pisaster maintained vertical size gradients of snails, but our data implicate the overlooked predator Leptasterias as the primary cause. This natural experiment indicated that (1) predators exert top-down control over prey population sizes and lower limits, (2) vertical zonation of prey are dynamic and controlled in part by prey behavior, and (3) predators exert the strongest effects on more vulnerable individuals, which typically inhabit stressful habitats higher on the shore or outside tidepools to avoid predation. Because the mass mortalities of two predators drastically reduced both the predation pressure and the chemical cues of predators in the environment, we were able to investigate both the effects of predators on prey populations and the effects on mobile prey behavior.

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. 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. 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, medium-sized 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. Because average hunger level and size of snails vary over time and space in nature, a mosaic of TMII strength may exist. 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.

Nearly all of our understanding of rocky inter-tidal ecology comes from studies conducted at low tide. To study inter-tidal organisms at high tide, we anchored waterproof digital GoPro® video cameras in wave-exposed tidepools and recorded the daytime movements of the black turban snail, Tegula funebralis, over the tidal cycle between May and August 2012 near Bodega Bay, California. Overall, snails moved more quickly and presumably foraged more during low tides and on days with warmer air and perhaps water temperatures. This is similar to other ectotherms that exhibit increased metabolic rates, movement and foraging in warmer conditions. Snails also moved less during flood and high tides, may have moved downward in tidepools at flood tides, and showed evidence of reduced activity on days with larger waves. This inactivity and refuge seeking may have been a strategy to avoid dislodgment by waves. Analysis of snail trajectories showed foraging bouts indicated by alternating zig-zagging and straight movement. There was no effect of temperature, wave height, or tidal phase on distribution of snail turning angles, suggesting that they may have foraged consistently but moved faster during warm conditions and low tides, thereby grazing a larger area. This is one of few direct recordings of inter-tidal organisms on wave-exposed rocky shores during high tide. The methods used here are easily transferable to other studies, which are needed to increase our understanding of behaviors that structure rocky shore communities during high tide.

Human-caused global change produces biotic and abiotic conditions that increase the uncertainty and risk of failure of restoration efforts. A focus of managing for resiliency, that is, the ability of the system to respond to disturbance, has the potential to reduce this uncertainty and risk. However, identifying what drives resiliency might depend on how one measures it. An example of a system where identifying how the drivers of different aspects of resiliency can inform restoration under climate change is the northern coast of California, where kelp experienced a decline in coverage of over 95% due to the combination of an intense marine heat wave and the functional extinction of the primary predator of the kelp-grazing purple sea urchin, the sunflower sea star. Although restoration efforts focused on urchin removal and kelp reintroduction in this system are ongoing, the question of how to increase the resiliency of this system to future marine heat waves remains open. In this paper, we introduce a dynamical model that describes a tritrophic food chain of kelp, purple urchins, and a purple urchin predator such as the sunflower sea star. We run a global sensitivity analysis of three different resiliency metrics (recovery likelihood, recovery rate, and resistance to disturbance) of the kelp forest to identify their ecological drivers. We find that each metric depends the most on a unique set of drivers: Recovery likelihood depends the most on live and drift kelp production, recovery rate depends the most on urchin production and feedbacks that determine urchin grazing on live kelp, and resistance depends the most on feedbacks that determine predator consumption of urchins. Therefore, an understanding of the potential role of predator reintroduction or recovery in kelp systems relies on a comprehensive approach to measuring resiliency.