Brian Gaylord

AVOIDING CURRENT OVERSIGHTS IN MARINE RESERVE DESIGN

The pun in the above title reflects two points. First, marine life cycles com- monly include a dispersive juvenile stage that is moved about by ocean currents. This stage often is the predominant, or only, means of dispersal that connects spatially disjunct pop- ulations. As a consequence, details of dispersal likely play a critical role in determining the effectiveness of marine reserves as a management and conservation tool. Curiously, however (and this is the second point of the title), although dozens of models for marine reserves now exist, few actually account explicitly for larval dispersal. Moreover, those that do include dispersal, do so almost exclusively by considering it to be a nondirectional spreading process (diffusion), ignoring the effects of directional transport by currents (ad- vection). Here we develop a population dynamical model for marine organisms with rel- atively sedentary adults whose larvae are transported in a simple flow field with both diffusive spreading and directional characteristics. We find that advection can play a dom- inant role in determining the effectiveness of different reserve configurations. Two of the most important consequences are: (1) with strong currents, multiple reserves can be mark- edly more effective than single reserves of equivalent total size; and (2) in the presence of strong currents, reserves can significantly outperform traditional, effort-based manage- ment strategies in terms of fisheries yield, and do so with less risk. These results suggest that successful reserve design may require considerable new efforts to examine explicitly the role of dispersal of young.

Evolutionary change during experimental ocean acidification

Rising atmospheric carbon dioxide (CO2) conditions are driving unprecedented changes in seawater chemistry, resulting in reduced pH and carbonate ion concentrations in the Earth’s oceans. This ocean acidification has negative but variable impacts on individual performance in many marine species. However, little is known about the adaptive capacity of species to respond to an acidified ocean, and, as a result, predictions regarding future ecosystem responses remain incomplete. Here we demonstrate that ocean acidification generates striking patterns of genome-wide selection in purple sea urchins (Strongylocentrotus purpuratus) cultured under different CO2 levels. We examined genetic change at 19,493 loci in larvae from seven adult populations cultured under realistic future CO2 levels. Although larval development and morphology showed little response to elevated CO2, we found substantial allelic change in 40 functional classes of proteins involving hundreds of loci. Pronounced genetic changes, including excess amino acid replacements, were detected in all populations and occurred in genes for biomineralization, lipid metabolism, and ion homeostasis—gene classes that build skeletons and interact in pH regulation. Such genetic change represents a neglected and important impact of ocean acidification that may influence populations that show few outward signs of response to acidification. Our results demonstrate the capacity for rapid evolution in the face of ocean acidification and show that standing genetic variation could be a reservoir of resilience to climate change in this coastal upwelling ecosystem. However, effective response to strong natural selection demands large population sizes and may be limited in species impacted by other environmental stressors.

Functional impacts of ocean acidification in an ecologically critical foundation species

SUMMARY Anthropogenic CO2 is reducing the pH and altering the carbonate chemistry of seawater, with repercussions for marine organisms and ecosystems. Current research suggests that calcification will decrease in many species, but compelling evidence of impaired functional performance of calcium carbonate structures is sparse, particularly in key species. Here we demonstrate that ocean acidification markedly degrades the mechanical integrity of larval shells in the mussel Mytilus californianus, a critical community member on rocky shores throughout the northeastern Pacific. Larvae cultured in seawater containing CO2 concentrations expected by the year 2100 (540 or 970 ppm) precipitated weaker, thinner and smaller shells than individuals raised under present-day seawater conditions (380 ppm), and also exhibited lower tissue mass. Under a scenario where mussel larvae exposed to different CO2 levels develop at similar rates, these trends suggest a suite of potential consequences, including an exacerbated vulnerability of new settlers to crushing and drilling attacks by predators; poorer larval condition, causing increased energetic stress during metamorphosis; and greater risks from desiccation at low tide due to shifts in shell area to body mass ratios. Under an alternative scenario where responses derive exclusively from slowed development, with impacted individuals reaching identical milestones in shell strength and size by settlement, a lengthened larval phase could increase exposure to high planktonic mortality rates. In either case, because early life stages operate as population bottlenecks, driving general patterns of distribution and abundance, the ecological success of this vital species may be tied to how ocean acidification proceeds in coming decades.

A physically based model of macroalgal spore dispersal in the wave and current-dominated nearshore

Propagule dispersal in seaweeds is a process influenced by a variety of biological and physical factors, the complexity of which has hindered efforts to understand colonization, persistence, post-disturbance recovery, and dynamics of algal populations in general. In view of this limitation, we employ here modifications to an existing turbulent-transport model to explore the mechanics of nearshore macroalgal spore dispersal and its relationship to coastal hydrodynamic conditions. Our modeling efforts focus on four example species of seaweed whose reproductive propagules span a wide range in sinking speed and height of release above the sea floor: the giant kelp Macrocystis pyrifera, the erect fucoid Sargassum muticum, the small filamentous brown alga Ectocarpus siliculosus, and the flaccid red alga Sarcodiotheca gaudichaudii. Results indicate that both propagule sinking speed and release height can affect dispersal distance substantially, but that the influence of these biological parameters is modulated strongly by the intensity of turbulence as dictated by waves and currents. In rapid flows with larger waves, it is primarily fluid dynamic processes, in particular current velocities, that determine dispersal distance. Additional simulations suggest that patterns of spore dispersal are highly skewed, with most propagules encountering the sea floor within a few meters to hundreds of meters of their parents, but with a sizeable fraction of spores also dispersing as far as kilometers. Such model predictions imply a much greater potential for longer range dispersal than has typically been assumed, a finding with important implications for understanding the demographics of algal populations and for predicting levels of connectivity among them.

Detailing agents of physical disturbance: wave-induced velocities and accelerations on a rocky shore

Abstract Water motion produced by breaking waves plays a defining role in structuring intertidal communities. However, despite the clear ecological importance of wave action, fine-scale details of the flows generated by breaking waves on rocky shores have not been well-described. This lack of information has hindered the efficacy of mechanistic studies aimed at exploring quantitatively the processes leading to wave-induced damage or mortality of organisms in littoral habitats. In response to these limitations, high-frequency field measurements of intertidal water velocities and accelerations were conducted simultaneously with recordings of inshore wave height at four representative sites in the mid-intertidal zone of a rocky shore. Maximum velocities and accelerations recorded under waves of measured height are presented and placed in the context of simple wave theories. Rates of occurrence of simultaneous velocities and accelerations are computed as a function of wave height, providing a means of linking instantaneous values of drag and lift to concurrent hydrodynamic accelerational forces. These data together provide an improved, high-resolution picture of the nature of flows typical of littoral environments and their relationship to wave height, and as such serve to reemphasize both the severity as well as the stochastic nature of the fluid motions that characterize wave-swept coasts.

MACROALGAL SPORE DISPERSAL IN COASTAL ENVIRONMENTS: MECHANISTIC INSIGHTS REVEALED BY THEORY AND EXPERIMENT

Passively dispersing propagules are often transported across a range of scales, with impacts on local processes tied to the density of settlement, and on regional processes influencing population connectivity. This dual set of effects has spurred research targeting both short- and long-distance ends of the dispersal spectrum. To date, however, dispersal distributions have been rigorously quantified primarily in terrestrial plants with seeds. Dispersal distributions in the ocean are by comparison poorly defined. This limitation arises with particular force in the habitat-forming giant kelp, Macrocystis pyrifera, where complex coastal flows affect self-fertilization and inbreeding depression near to a source, as well as propagule delivery dictating recovery of locally extinct populations farther away. Here we use a combination of theoretical and experimental approaches to examine spore dispersal in Macrocystis. Results from a physically based model, parameterized via field-measured hydrodynamics, are compar...

Ocean acidification increases the vulnerability of native oysters to predation by invasive snails.

There is growing concern that global environmental change might exacerbate the ecological impacts of invasive species by increasing their per capita effects on native species. However, the mechanisms underlying such shifts in interaction strength are poorly understood. Here, we test whether ocean acidification, driven by elevated seawater pCO2, increases the susceptibility of native Olympia oysters to predation by invasive snails. Oysters raised under elevated pCO2 experienced a 20% increase in drilling predation. When presented alongside control oysters in a choice experiment, 48% more high-CO2 oysters were consumed. The invasive snails were tolerant of elevated CO2 with no change in feeding behaviour. Oysters raised under acidified conditions did not have thinner shells, but were 29–40% smaller than control oysters, and these smaller individuals were consumed at disproportionately greater rates. Reduction in prey size is a common response to environmental stress that may drive increasing per capita effects of stress-tolerant invasive predators.

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.

Turbulent shear spurs settlement in larval sea urchins

Marine invertebrates commonly produce larvae that disperse in ocean waters before settling into adult shoreline habitat. Chemical and other seafloor-associated cues often facilitate this latter transition. However, the range of effectiveness of such cues is limited to small spatial scales, creating challenges for larvae in finding suitable sites at which to settle, especially given that they may be carried many kilometers by currents during their planktonic phase. One possible solution is for larvae to use additional, broader-scale environmental signposts to first narrow their search to the general vicinity of a candidate settlement location. Here we demonstrate strong effects of just such a habitat-scale cue, one with the potential to signal larvae that they have arrived in appropriate coastal areas. Larvae of the purple sea urchin (Strongylocentrotus purpuratus) exhibit dramatic enhancement in settlement following stimulation by turbulent shear typical of wave-swept shores where adults of this species live. This response manifests in an unprecedented fashion relative to previously identified cues. Turbulent shear does not boost settlement by itself. Instead, it drives a marked developmental acceleration that causes “precompetent” larvae refractory to chemical settlement inducers to immediately become “competent” and thereby reactive to such inducers. These findings reveal an unrecognized ability of larval invertebrates to shift the trajectory of a major life history event in response to fluid-dynamic attributes of a target environment. Such an ability may improve performance and survival in marine organisms by encouraging completion of their life cycle in advantageous locations.

Flow Forces on Seaweeds: Field Evidence for Roles of Wave Impingement and Organism Inertia

Hydrodynamic forces dislodge and kill large numbers of organisms in intertidal and subtidal habitats along rocky shores. Although this feature of wave-driven water motion is well recognized, the mechanics of force imposition on compliant organisms is incompletely understood. Here we undertake a field examination of two processes that are thought to impose many of the more dangerous forces that act on flexible benthic seaweeds: impingement of breaking waves directly on emergent organisms, and inertial effects tied to the rapid deceleration of mass that occurs when a passively moving but attached organism abruptly reaches the extent of its range of motion. We focus on two common and important seaweed species: one intertidal kelp (Egregia menziesii) and one subtidal kelp (Macrocystis pyrifera). Results support the concept that wave impingement and inertial effects produce intermittent force transients whose magnitudes commonly exceed values readily attributable to drag. Peak force transients are elevated by as much as a factor of 3 relative to drag in both small and large individuals, consistent with smaller seaweeds being more susceptible to brief impingement forces, and larger seaweeds being more vulnerable to inertial forces. Because both wave impingement and inertial effects vary with the size of an organism, they may have the potential to influence the demographics of physical disturbance in an array of flexible species.