Low-pH seawater alters indirect interactions in rocky-shore tidepools.

Ocean acidification is expected to degrade marine ecosystems, yet most studies focus on organismal-level impacts rather than ecological perturbations. Field studies are especially sparse, particularly ones examining shifts in direct and indirect consumer interactions. Here we address such connections within tidepool communities of rocky shores, focusing on a three-level food web involving the keystone sea star predator, Pisaster ochraceus, a common herbivorous snail, Tegula funebralis, and a macroalgal basal resource, Macrocystis pyrifera. We demonstrate that during nighttime low tides, experimentally manipulated declines in seawater pH suppress the anti-predator behavior of snails, bolstering their grazing, and diminishing the top-down influence of predators on basal resources. This attenuation of top-down control is absent in pools maintained experimentally at higher pH. These findings suggest that as ocean acidification proceeds, shifts of behaviorally mediated links in food webs could change how cascading effects of predators manifest within marine communities.

Ocean change within shoreline communities: from biomechanics to behaviour and beyond.

Humans are changing the physical properties of Earth. In marine systems, elevated carbon dioxide concentrations are driving notable shifts in temperature and seawater chemistry. Here, we consider consequences of such perturbations for organism biomechanics and linkages amongst species within communities. In particular, we examine case examples of altered morphologies and material properties, disrupted consumer-prey behaviours, and the potential for modulated positive (i.e. facilitative) interactions amongst taxa, as incurred through increasing ocean acidity and rising temperatures. We focus on intertidal rocky shores of temperate seas as model systems, acknowledging the longstanding role of these communities in deciphering ecological principles. Our survey illustrates the broad capacity for biomechanical and behavioural shifts in organisms to influence the ecology of a transforming world.

Shifts in seawater chemistry disrupt trophic links within a simple shoreline food web.

Marine intertidal systems have long served as focal environments for ecological research, yet these environments are changing due to the entry of human-produced carbon dioxide into seawater, which causes 'ocean acidification' (OA). One component of OA is a decline in seawater pH, an alteration known to disrupt organism behaviors underlying predator-prey interactions. To date, however, studies examining OA's effects on feeding relationships consider predominantly simple direct interactions between consumers and their food sources. Here, we extended these established approaches to test how decreased seawater pH might alter cascading effects that span tiered linkages in trophic networks. We employed a model shoreline food web incorporating a sea star predator (Leptasterias hexactis), an herbivorous snail prey (Tegula funebralis), and a common macroalgal resource for the prey (Mazzaella flaccida). Results demonstrate direct negative effects of low pH on anti-predator behavior of snails, but also weakened indirect interactions, driven by increased snail consumption of macroalgae even as sea stars ate more snails. This latter outcome arose because low pH induced 'foolhardy' behaviors in snails, whereby their flight responses were supplanted by other activities that allowed for foraging. These findings highlight the potential for human-induced changes in seawater chemistry to perturb prey behaviors and trophic dynamics with accompanying community-level consequences.

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

Organism-level effects of ocean acidification (OA) are well recognized. Less understood are OA's consequences for ecological species interactions. Here, we examine a behaviourally mediated predator-prey interaction within the rocky intertidal zone of the temperate eastern Pacific Ocean, using it as a model system to explore OA's capacity to impair invertebrate anti-predator behaviours more broadly. Our system involves the iconic sea star predator, Pisaster ochraceus, that elicits flee responses in numerous gastropod prey. We examine, in particular, the capacity for OA-associated reductions in pH to alter flight behaviours of the black turban snail, Tegula funebralis, an often-abundant and well-studied grazer in the system. We assess interactions between these species at 16 discrete levels of pH, quantifying the full functional response of Tegula under present and near-future OA conditions. Results demonstrate the disruption of snail anti-predator behaviours at low pH, with decreases in the time individuals spend in refuge locations. We also show that fluctuations in pH, including those typical of rock pools inhabited by snails, do not materially change outcomes, implying little capacity for episodically benign pH conditions to aid behavioural recovery. Together, these findings suggest a strong potential for OA to induce cascading community-level shifts within this long-studied ecosystem.

Predicting the effects of ocean acidification on predator-prey interactions: a conceptual framework based on coastal molluscs.

The influence of environmental change on species interactions will affect population dynamics and community structure in the future, but our current understanding of the outcomes of species interactions in a high-CO2 world is limited. Here, we draw upon emerging experimental research examining the effects of ocean acidification on coastal molluscs to provide hypotheses of the potential impacts of high-CO2 on predator-prey interactions. Coastal molluscs, such as oysters, mussels, and snails, allocate energy among defenses, growth, and reproduction. Ocean acidification increases the energetic costs of physiological processes such as acid-base regulation and calcification. Impacted molluscs can display complex and divergent patterns of energy allocation to defenses and growth that may influence predator-prey interactions; these include changes in shell properties, body size, tissue mass, immune function, or reproductive output. Ocean acidification has also been shown to induce complex changes in chemoreception, behavior, and inducible defenses, including altered cue detection and predator avoidance behaviors. Each of these responses may ultimately alter the susceptibility of coastal molluscs to predation through effects on predator handling time, satiation, and search time. While many of these effects may manifest as increases in per capita predation rates on coastal molluscs, the ultimate outcome of predator-prey interactions will also depend on how ocean acidification affects the specified predators, which also exhibit complex responses to ocean acidification. Changes in predator-prey interactions could have profound and unexplored consequences for the population dynamics of coastal molluscs in a high-CO2 ocean.