Wave damping by giant kelp, Macrocystis pyrifera.

BACKGROUND AND AIMS: The increased likelihood and severity of storm events has brought into focus the role of coastal ecosystems in provision of shoreline protection by attenuating wave energy. Canopy-forming kelps, including giant kelp (Macrocystis pyrifera), are thought to provide this ecosystem service, but supporting data are extremely limited. Previous in situ examinations relied mostly on comparisons between nominally similar sites with and without kelp. Given that other factors (especially seafloor bathymetry and topographic features) often differ across sites, efforts to isolate the effects of kelp on wave energy propagation confront challenges. In particular, it can be difficult to distinguish wave energy dissipation attributable to kelp from frictional processes at the seabed that often covary with the presence of kelp. Here, we use an ecological transition from no kelp to a full forest, at a single site with static bathymetry, to resolve unambiguously the capacity of giant kelp to damp waves. METHODS: We measured waves within and outside rocky reef habitat, in both the absence and the presence of giant kelp, at Marguerite Reef, Palos Verdes, CA, USA. Nested within a broader kelp restoration project, this site transitioned from a bare state to one supporting a fully formed forest (density of 8 stipes m-2). We quantified, as a function of incident wave conditions, the decline in wave energy flux attributable to the presence of kelp, as waves propagated from outside and into reef habitat. KEY RESULTS: The kelp forest damped wave energy detectably, but to a modest extent. Interactions with the seabed alone reduced wave energy flux, on average, by 12 ±â€…1.4 % over 180 m of travel. The kelp forest induced an additional 7 ±â€…1.2 % decrease. Kelp-associated declines in wave energy flux were slightly greater for waves of longer periods and smaller wave heights. CONCLUSIONS: Macrocystis pyrifera forests have a limited, albeit measurable, capacity to enhance shoreline protection from nearshore waves. Expectations that giant kelp forests, whether extant or enhanced through restoration, have substantial impacts on wave-induced coastal erosion might require re-evaluation.

Species' attributes predict the relative magnitude of ecological and genetic recovery following mass mortality.

Theoretically, species' characteristics should allow estimation of dispersal potential and, in turn, explain levels of population genetic differentiation. However, a mismatch between traits and genetic patterns is often reported for marine species, and interpreted as evidence that life-history traits do not influence dispersal. Here, we couple ecological and genomic methods to test the hypothesis that species with attributes favouring greater dispersal potential-e.g., longer pelagic duration, higher fecundity and larger population size-have greater realized dispersal overall. We used a natural experiment created by a large-scale and multispecies mortality event which created a "clean slate" on which to study recruitment dynamics, thus simplifying a usually complex problem. We surveyed four species of differing dispersal potential to quantify the abundance and distribution of recruits and to genetically assign these recruits to probable parental sources. Species with higher dispersal potential recolonized a broader extent of the impacted range, did so more quickly and recovered more genetic diversity than species with lower dispersal potential. Moreover, populations of taxa with higher dispersal potential exhibited more immigration (71%-92% of recruits) than taxa with lower dispersal potential (17%-44% of recruits). By linking ecological with genomic perspectives, we demonstrate that a suite of interacting life-history and demographic attributes do influence species' realized dispersal and genetic neighbourhoods. To better understand species' resilience and recovery in this time of global change, integrative eco-evolutionary approaches are needed to more rigorously evaluate the effect of dispersal-linked attributes on realized dispersal and population genetic differentiation.

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.

Facilitation alters climate change risk on rocky shores.

A huge fraction of global biodiversity resides within biogenic habitats that ameliorate physical stresses. In most cases, details of how physical conditions within facilitative habitats respond to external climate forcing remain unknown, hampering climate change predictions for many of the world's species. Using intertidal mussel beds as a model system, we characterize relationships among external climate conditions and within-microhabitat heat and desiccation conditions. We use these data, along with physiological tolerances of two common inhabitant taxa (the isopod Cirolana harfordi and the porcelain crab Petrolisthes cinctipes), to examine the magnitude of climate risk inside and outside biogenic habitat, applying an empirically derived model of evaporation to simulate mortality risk under a high-emissions climate-warming scenario. We found that biogenic microhabitat conditions responded so weakly to external climate parameters that mortality risk was largely unaffected by climate warming. In contrast, outside the biogenic habitat, desiccation drove substantial mortality in both species, even at temperatures 4.4-8.6°C below their hydrated thermal tolerances. These findings emphasize the importance of warming-exacerbated desiccation to climate-change risk and the role of biogenic habitats in buffering this less-appreciated stressor. Our results suggest that, when biogenic habitats remain intact, climate warming may have weak direct effects on organisms within them. Instead, risk to such taxa is likely to be indirect and tightly coupled with the fate of habitat-forming populations. Conserving and restoring biogenic habitats that offer climate refugia could therefore be crucial to supporting biodiversity in the face of climate warming.

Flow, form, and force: methods and frameworks for field studies of macroalgal biomechanics.

Macroalgae are ecologically important organisms that often inhabit locations with physically challenging water motion. The biomechanical traits that permit their survival in these conditions have been of interest to biologists and engineers alike, but logistical and technical challenges of conducting investigations in macroalgal habitats have often prevented optimal study of these traits. Here, we review field methods for quantifying three major components of macroalgal biomechanics in moving water: fluid flow, macroalgal form, and hydrodynamic force. The implementation of some methodologies is limited due to the current state and accessibility of technology, but many of these limitations can be remedied by custom-built devices, borrowing techniques from other systems, or shifting lab-based approaches to the field. We also describe several frameworks for integrating flow, form, and force data that can facilitate comparisons of macroalgal biomechanics in field settings with predictions from theory and lab-based experiments, or comparisons between flow conditions, habitats, and species. These methods and frameworks, when used on scales that are relevant to the examined processes, can reveal mechanistic information about the functional traits that permit macroalgae to withstand physically challenging water motion in their habitats, using the actual fluid flows, macroalgal forms, and physical forces that occur in nature.

Seagrass-driven changes in carbonate chemistry enhance oyster shell growth.

Quantifying the strength of non-trophic interactions exerted by foundation species is critical to understanding how natural communities respond to environmental stress. In the case of ocean acidification (OA), submerged marine macrophytes, such as seagrasses, may create local areas of elevated pH due to their capacity to sequester dissolved inorganic carbon through photosynthesis. However, although seagrasses may increase seawater pH during the day, they can also decrease pH at night due to respiration. Therefore, it remains unclear how consequences of such diel fluctuations may unfold for organisms vulnerable to OA. We established mesocosms containing different levels of seagrass biomass (Zostera marina) to create a gradient of carbonate chemistry conditions and explored consequences for growth of juvenile and adult oysters (Crassostrea gigas), a non-native species widely used in aquaculture that can co-occur, and is often grown, in proximity to seagrass beds. In particular, we investigated whether increased diel fluctuations in pH due to seagrass metabolism affected oyster growth. Seagrasses increased daytime pH up to 0.4 units but had little effect on nighttime pH (reductions less than 0.02 units). Thus, both the average pH and the amplitude of diel pH fluctuations increased with greater seagrass biomass. The highest seagrass biomass increased oyster shell growth rate (mm day-1) up to 40%. Oyster somatic tissue weight and oyster condition index exhibited a different pattern, peaking at intermediate levels of seagrass biomass. This work demonstrates the ability of seagrasses to facilitate oyster calcification and illustrates how non-trophic metabolic interactions can modulate effects of environmental change.

Coast-wide evidence of low pH amelioration by seagrass ecosystems.

Global-scale ocean acidification has spurred interest in the capacity of seagrass ecosystems to increase seawater pH within crucial shoreline habitats through photosynthetic activity. However, the dynamic variability of the coastal carbonate system has impeded generalization into whether seagrass aerobic metabolism ameliorates low pH on physiologically and ecologically relevant timescales. Here we present results of the most extensive study to date of pH modulation by seagrasses, spanning seven meadows (Zostera marina) and 1000 km of U.S. west coast over 6 years. Amelioration by seagrass ecosystems compared to non-vegetated areas occurred 65% of the time (mean increase 0.07 ± 0.008 SE). Events of continuous elevation in pH within seagrass ecosystems, indicating amelioration of low pH, were longer and of greater magnitude than opposing cases of reduced pH or exacerbation. Sustained elevations in pH of >0.1, comparable to a 30% decrease in [H+ ], were not restricted only to daylight hours but instead persisted for up to 21 days. Maximal pH elevations occurred in spring and summer during the seagrass growth season, with a tendency for stronger effects in higher latitude meadows. These results indicate that seagrass meadows can locally alleviate low pH conditions for extended periods of time with important implications for the conservation and management of coastal ecosystems.

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.

Brief exposure to intense turbulence induces a sustained life-history shift in echinoids.

In coastal ecosystems, attributes of fluid motion can prompt animal larvae to rise or sink in the water column and to select microhabitats within which they attach and commit to a benthic existence. In echinoid (sea urchin and sand dollar) larvae living along wave-exposed shorelines, intense turbulence characteristic of surf zones can cause individuals to undergo an abrupt life-history shift characterized by precocious entry into competence - the stage at which larvae will settle and complete metamorphosis in response to local cues. However, the mechanistic details of this turbulence-triggered onset of competence remain poorly defined. Here, we evaluate in a series of laboratory experiments the time course of this turbulence effect, both the rapidity with which it initiates and whether it perdures. We found that larvae become competent with turbulence exposures as brief as 30 s, with longer exposures inducing a greater proportion of larvae to become competent. Intriguingly, larvae can remember such exposures for a protracted period (at least 24 h), a pattern reminiscent of long-term potentiation. Turbulence also induces short-term behavioral responses that last less than 30 min, including cessation of swimming, that facilitate sinking and thus contact of echinoid larvae with the substratum. Together, these results yield a novel perspective on how larvae find their way to suitable adult habitat at the critical settlement transition, and also open new experimental opportunities to elucidate the mechanisms by which planktonic animals respond to fluid motion.

Expected limits on the ocean acidification buffering potential of a temperate seagrass meadow.

Ocean acidification threatens many marine organisms, especially marine calcifiers. The only global-scale solution to ocean acidification remains rapid reduction in CO2 emissions. Nevertheless, interest in localized mitigation strategies has grown rapidly because of the recognized threat ocean acidification imposes on natural communities, including ones important to humans. Protection of seagrass meadows has been considered as a possible approach for localized mitigation of ocean acidification due to their large standing stocks of organic carbon and high productivity. Yet much work remains to constrain the magnitudes and timescales of potential buffering effects from seagrasses. We developed a biogeochemical box model to better understand the potential for a temperate seagrass meadow to locally mitigate the effects of ocean acidification. Then we parameterized the model using data from Tomales Bay, an inlet on the coast of California, USA which supports a major oyster farming industry. We conducted a series of month-long model simulations to characterize processes that occur during summer and winter. We found that average pH in the seagrass meadows was typically within 0.04 units of the pH of the primary source waters into the meadow, although we did find occasional periods (hours) when seagrass metabolism may modify the pH by up to ±0.2 units. Tidal phasing relative to the diel cycle modulates localized pH buffering within the seagrass meadow such that maximum buffering occurs during periods of the year with midday low tides. Our model results suggest that seagrass metabolism in Tomales Bay would not provide long-term ocean acidification mitigation. However, we emphasize that our model results may not hold in meadows where assumptions about depth-averaged net production and seawater residence time within the seagrass meadow differ from our model assumptions. Our modeling approach provides a framework that is easily adaptable to other seagrass meadows in order to evaluate the extent of their individual buffering capacities. Regardless of their ability to buffer ocean acidification, seagrass meadows maintain many critically important ecosystem goods and services that will be increasingly important as humans increasingly affect coastal ecosystems.

Sand Dollar Larvae Show Within-Population Variation in Their Settlement Induction by Turbulence.

Settlement-the generally irreversible transition from a planktonic phase to a benthic phase-is a critical stage in the life history of many shoreline organisms. It is reasonable to expect that larvae are under intense selection pressure to identify appropriate settlement habitat. Several decades of studies have focused mainly on local indicators that larvae use to identify suitable habitat, such as olfactory cues that indicate the presence of conspecifics or a favored food source. Our recent work has shown that the larvae of seashore-dwelling echinoids (sea urchins, sand dollars, and kin) can be primed to settle following a brief exposure to a broader-scale indicator of their approach to shore: an increase in fluid turbulence. Here we demonstrate that this priming shows within-population variation: the offspring of certain Pacific sand dollar (Dendraster excentricus) parents-both specific fathers and specific mothers, regardless of the other parent-are more responsive to turbulence than others. In particular, the observation of the effect correlating, in some cases, with specific fathers leads us to conclude that these behavioral differences are likely genetic and thus heritable. We also report that turbulence exposure causes larvae to temporarily sink to the bottom of a container of seawater and that larvae that respond in this way are also more likely to subsequently settle. We hypothesize a two-step scenario for the evolution of turbulence responsiveness at settlement and suggest that the evolutionary origin of these behaviors could be a driving force for population differentiation and speciation.

Plastic responses of bryozoans to ocean acidification.

Phenotypic plasticity has the potential to allow organisms to respond rapidly to global environmental change, but the range and effectiveness of these responses are poorly understood across taxa and growth strategies. Colonial organisms might be particularly resilient to environmental stressors, as organizational modularity and successive asexual generations can allow for distinctively flexible responses in the aggregate form. We performed laboratory experiments to examine the effects of increasing dissolved carbon dioxide (CO2) (i.e. ocean acidification) on the colonial bryozoan Celleporella cornuta sampled from two source populations within a coastal upwelling region of the northern California coast. Bryozoan colonies were remarkably plastic under these CO2 treatments. Colonies raised under high CO2 grew more quickly, investing less in reproduction and producing lighter skeletons when compared with genetically identical clones raised under current surface atmosphere CO2 values. Bryozoans held under high CO2 conditions also changed the Mg/Ca ratio of skeletal calcite and increased the expression of organic coverings in new growth, which may serve as protection against acidified water. We also observed strong differences between source populations in reproductive investment and organic covering reaction norms, consistent with adaptive responses to persistent spatial variation in local oceanographic conditions. Our results demonstrate that phenotypic plasticity and energetic trade-offs can mediate biological responses to global environmental change, and highlight the broad range of strategies available to colonial organisms.

Ocean acidification compromises a planktic calcifier with implications for global carbon cycling.

Anthropogenically-forced changes in ocean chemistry at both the global and regional scale have the potential to negatively impact calcifying plankton, which play a key role in ecosystem functioning and marine carbon cycling. We cultured a globally important calcifying marine plankter (the foraminifer, Globigerina bulloides) under an ecologically relevant range of seawater pH (7.5 to 8.3 total scale). Multiple metrics of calcification and physiological performance varied with pH. At pH > 8.0, increased calcification occurred without a concomitant rise in respiration rates. However, as pH declined from 8.0 to 7.5, calcification and oxygen consumption both decreased, suggesting a reduced ability to precipitate shell material accompanied by metabolic depression. Repair of spines, important for both buoyancy and feeding, was also reduced at pH < 7.7. The dependence of calcification, respiration, and spine repair on seawater pH suggests that foraminifera will likely be challenged by future ocean conditions. Furthermore, the nature of these effects has the potential to actuate changes in vertical transport of organic and inorganic carbon, perturbing feedbacks to regional and global marine carbon cycling. The biological impacts of seawater pH have additional, important implications for the use of foraminifera as paleoceanographic indicators.

Interactive effects of temperature, food and skeletal mineralogy mediate biological responses to ocean acidification in a widely distributed bryozoan.

Marine invertebrates with skeletons made of high-magnesium calcite may be especially susceptible to ocean acidification (OA) due to the elevated solubility of this form of calcium carbonate. However, skeletal composition can vary plastically within some species, and it is largely unknown how concurrent changes in multiple oceanographic parameters will interact to affect skeletal mineralogy, growth and vulnerability to future OA. We explored these interactive effects by culturing genetic clones of the bryozoan Jellyella tuberculata (formerly Membranipora tuberculata) under factorial combinations of dissolved carbon dioxide (CO2), temperature and food concentrations. High CO2 and cold temperature induced degeneration of zooids in colonies. However, colonies still maintained high growth efficiencies under these adverse conditions, indicating a compensatory trade-off whereby colonies degenerate more zooids under stress, redirecting energy to the growth and maintenance of new zooids. Low-food concentration and elevated temperatures also had interactive effects on skeletal mineralogy, resulting in skeletal calcite with higher concentrations of magnesium, which readily dissolved under high CO2 For taxa that weakly regulate skeletal magnesium concentration, skeletal dissolution may be a more widespread phenomenon than is currently documented and is a growing concern as oceans continue to warm and acidify.

Edge effects reverse facilitation by a widespread foundation species.

Dense aggregations of foundation species often mitigate environmental stresses for organisms living among them. Considerable work documents such benefits by comparing conditions inside versus outside these biogenic habitats. However, environmental gradients commonly arise across the extent of even single patches of habitat-forming species, including cases where stresses diverge between habitat interiors and edges. We ask here whether such edge effects could alter how habitat-forming species influence residents, potentially changing the strength or direction of interactions (i.e., from stress amelioration to exacerbation). We take as a model system the classic marine foundation species, Mytilus californianus, the California mussel. Results demonstrate that mussel beds both increase and decrease thermal stresses. Over a distance of 6 to 10 cm from the bed interior to its upper surface, peak temperatures climb from as much as 20 °C below to 5 °C above those of adjacent bedrock. This directional shift in temperature modification affects interactions with juvenile mussels, such that thermal stresses and associated mortality risk are higher at the bed surface, but substantially reduced deeper within the adult matrix. These findings provide a case example of how stress gradients generated across biogenic habitats can markedly alter ecological interactions even within a single habitat patch.

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.

Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability.

Although theory suggests geographic variation in species' performance is determined by multiple niche parameters, little consideration has been given to the spatial structure of interacting stressors that may shape local and regional vulnerability to global change. Here, we use spatially explicit mosaics of carbonate chemistry, food availability and temperature spanning 1280 km of coastline to test whether persistent, overlapping environmental mosaics mediate the growth and predation vulnerability of a critical foundation species, the mussel Mytilus californianus. We find growth was highest and predation vulnerability was lowest in dynamic environments with frequent exposure to low pH seawater and consistent food. In contrast, growth was lowest and predation vulnerability highest when exposure to low pH seawater was decoupled from high food availability, or in exceptionally warm locations. These results illustrate how interactions among multiple drivers can cause unexpected, yet persistent geographic mosaics of species performance, interactions and vulnerability to environmental change.

Nighttime dissolution in a temperate coastal ocean ecosystem increases under acidification.

Anthropogenic emissions of carbon dioxide (CO2) are causing ocean acidification, lowering seawater aragonite (CaCO3) saturation state (Ω arag), with potentially substantial impacts on marine ecosystems over the 21(st) Century. Calcifying organisms have exhibited reduced calcification under lower saturation state conditions in aquaria. However, the in situ sensitivity of calcifying ecosystems to future ocean acidification remains unknown. Here we assess the community level sensitivity of calcification to local CO2-induced acidification caused by natural respiration in an unperturbed, biodiverse, temperate intertidal ecosystem. We find that on hourly timescales nighttime community calcification is strongly influenced by Ω arag, with greater net calcium carbonate dissolution under more acidic conditions. Daytime calcification however, is not detectably affected by Ω arag. If the short-term sensitivity of community calcification to Ω arag is representative of the long-term sensitivity to ocean acidification, nighttime dissolution in these intertidal ecosystems could more than double by 2050, with significant ecological and economic consequences.

Rethinking competence in marine life cycles: ontogenetic changes in the settlement response of sand dollar larvae exposed to turbulence.

Complex life cycles have evolved independently numerous times in marine animals as well as in disparate algae. Such life histories typically involve a dispersive immature stage followed by settlement and metamorphosis to an adult stage on the sea floor. One commonality among animals exhibiting transitions of this type is that their larvae pass through a 'precompetent' period in which they do not respond to localized settlement cues, before entering a 'competent' period, during which cues can induce settlement. Despite the widespread existence of these two phases, relatively little is known about how larvae transition between them. Moreover, recent studies have blurred the distinction between the phases by demonstrating that fluid turbulence can spark precocious activation of competence. Here, we further investigate this phenomenon by exploring how larval interactions with turbulence change across ontogeny, focusing on offspring of the sand dollar Dendraster excentricus (Eschscholtz). Our data indicate that larvae exhibit increased responsiveness to turbulence as they get older. We also demonstrate a likely cost to precocious competence: the resulting juveniles are smaller. Based upon these findings, we outline a new, testable conception of competence that has the potential to reshape our understanding of larval dispersal and connectivity among marine populations.