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.

Timing of stressors alters interactive effects on a coastal foundation species.

The effects of climate-driven stressors on organismal performance and ecosystem functioning have been investigated across many systems; however, manipulative experiments generally apply stressors as constant and simultaneous treatments, rather than accurately reflecting temporal patterns in the natural environment. Here, we assessed the effects of temporal patterns of high aerial temperature and low salinity on survival of Olympia oysters (Ostrea lurida), a foundation species of conservation and restoration concern. As single stressors, low salinity (5 and 10 psu) and the highest air temperature (40°C) resulted in oyster mortality of 55.8, 11.3, and 23.5%, respectively. When applied on the same day, low salinity and high air temperature had synergistic negative effects that increased oyster mortality. This was true even for stressor levels that were relatively mild when applied alone (10 psu and 35°C). However, recovery times of two or four weeks between stressors eliminated the synergistic effects. Given that most natural systems threatened by climate change are subject to multiple stressors that vary in the timing of their occurrence, our results suggest that it is important to examine temporal variation of stressors in order to more accurately understand the possible biological responses to global change.

Atmospheric rivers and the mass mortality of wild oysters: insight into an extreme future?

Climate change is predicted to increase the frequency and severity of extreme events. However, the biological consequences of extremes remain poorly resolved owing to their unpredictable nature and difficulty in quantifying their mechanisms and impacts. One key feature delivering precipitation extremes is an atmospheric river (AR), a long and narrow filament of enhanced water vapour transport. Despite recent attention, the biological impacts of ARs remain undocumented. Here, we use biological data coupled with remotely sensed and in situ environmental data to describe the role of ARs in the near 100% mass mortality of wild oysters in northern San Francisco Bay. In March 2011, a series of ARs made landfall within California, contributing an estimated 69.3% of the precipitation within the watershed and driving an extreme freshwater discharge into San Francisco Bay. This discharge caused sustained low salinities (less than 6.3) that almost perfectly matched the known oyster critical salinity tolerance and was coincident with a mass mortality of one of the most abundant populations throughout this species' range. This is a concern, because wild oysters remain a fraction of their historical abundance and have yet to recover. This study highlights a novel mechanism by which precipitation extremes may affect natural systems and the persistence of sensitive species in the face of environmental change.

Coast-wide recruitment dynamics of Olympia oysters reveal limited synchrony and multiple predictors of failure.

Recruitment of new propagules into a population can be a critical determinant of adult density. We examined recruitment dynamics in the Olympia oyster (Ostrea lurida), a species occurring almost entirely in estuaries. We investigated spatial scales of interannual synchrony across 37 sites in eight estuaries along 2,500 km of Pacific North American coastline, predicting that high vs. low recruitment years would coincide among neighboring estuaries due to shared exposure to regional oceanographic factors. Such synchrony in recruitment has been found for many marine species and some migratory estuarine species, but has never been examined across estuaries in a species that can complete its entire life cycle within the same estuary. To inform ongoing restoration efforts for Olympia oysters, which have declined in abundance in many estuaries, we also investigated predictors of recruitment failure. We found striking contrasts in absolute recruitment rate and frequency of recruitment failure among sites, estuaries, and years. Although we found a positive relationship between upwelling and recruitment, there was little evidence of synchrony in recruitment among estuaries along the coast, and only limited synchrony of sites within estuaries, suggesting recruitment rates are affected more strongly by local dynamics within estuaries than by regional oceanographic factors operating at scales encompassing multiple estuaries. This highlights the importance of local wetland and watershed management for the demography of oysters, and perhaps other species that can complete their entire life cycle within estuaries. Estuaries with more homogeneous environmental conditions had greater synchrony among sites, and this led to the potential for estuary-wide failure when all sites had no recruitment in the same year. Environmental heterogeneity within estuaries may thus buffer against estuary-wide recruitment failure, analogous to the portfolio effect for diversity. Recruitment failure was correlated with lower summer water temperature, higher winter salinity, and shorter residence time: all indicators of stronger marine influence on estuaries. Recruitment failure was also more common in estuaries with limited networks of nearby adult oysters. Large existing oyster networks are thus of high conservation value, while estuaries that lack them would benefit from restoration efforts to increase the extent and connectivity of sites supporting oysters.

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.

Testing local and global stressor impacts on a coastal foundation species using an ecologically realistic framework.

Despite the abundance of literature on organismal responses to multiple environmental stressors, most studies have not matched the timing of experimental manipulations with the temporal pattern of stressors in nature. We test the interactive effects of diel-cycling hypoxia with both warming and decreased salinities using ecologically realistic exposures. Surprisingly, we found no evidence of negative synergistic effects on Olympia oyster growth; rather, we found only additive and opposing effects of hypoxia (detrimental) and warming (beneficial). We suspect that diel-cycling provided a temporal refuge that allowed physiological compensation. We also tested for latent effects of warming and hypoxia to low-salinity tolerance using a seasonal delay between stressor events. However, we did not find a latent effect, rather a threshold survival response to low salinity that was independent of early life-history exposure to warming or hypoxia. The absence of synergism is likely the result of stressor treatments that mirror the natural timing of environmental stressors. We provide environmental context for laboratory experimental data by examining field time series environmental data from four North American west coast estuaries and find heterogeneous environmental signals that characterize each estuary, suggesting that the potential stressor exposure to oysters will drastically differ over moderate spatial scales. This heterogeneity implies that efforts to conserve and restore oysters will require an adaptive approach that incorporates knowledge of local conditions. We conclude that studies of multiple environmental stressors can be greatly improved by integrating ecologically realistic exposure and timing of stressors found in nature with organismal life-history traits.

The sensory ecology of nonconsumptive predator effects.

Nonconsumptive effects (NCEs) have been shown to occur in numerous systems and are regarded as important mechanisms by which predation structures natural communities. Sensory ecology-that is, the processes governing the production, propagation, and masking of cues by ambient noise-provides insights into the strength of NCEs as functions of the environment and modes of information transfer. We discuss how properties of predators are used by prey to encode threat, how the environment affects cue propagation, and the role of single sensory processes versus multimodal sensory processes. We discuss why the present body of literature documents the potential for strong NCEs but does not allow us to easily determine how this potential is expressed in nature or what factors or environments produce strong versus weak NCEs. Many of these difficulties stem from a body of literature in which certain sensory environments and modalities may be disproportionately represented and in which experimental methodologies are designed to show the existence of NCEs. We present a general framework for examining NCEs to identify the factors controlling the number of prey that respond to predator cues and discuss how the properties of predators, prey, and the environment may determine prey perceptive range and the duration and frequency of cue production. We suggest how understanding these relationships provides a schema for determining where, when, why, and how NCEs are important in producing direct and cascading effects in natural communities.

Hydrodynamic sensory stressors produce nonlinear predation patterns.

Predators often have large effects on community structure, but these effects can be minimized in habitats subjected to intense physical stress. For example, predators exert large effects on rocky intertidal communities on wave-protected shores but are usually absent from wave-swept shores where hydrodynamic forces prevent them from foraging effectively. The physical environment also can affect predation levels when stressors are not severe enough to be physically risky. In these situations, environmental conditions may constrain a predator's ability to locate prey and alleviate predation pressure. Yet, stress models of community structure have rarely considered the implications of such sensory or behavioral stressors, particularly when the sensory abilities of both predators and prey are affected by the same types of environmental conditions. Ecologists may classify certain environmental conditions as refuges if they impede predator foraging, but these conditions may not actually decrease predation levels if they simultaneously increase prey vulnerability to consumers. Using blue crabs (Callinectes sapidus) and hard clams (Mercenaria mercenaria) as a model system, we investigated the relationship between predation intensity and environmental stress in the form of hydrodynamics (i.e., flow velocity and turbulence). Blue crabs and hard clams are less responsive to each other in faster, more turbulent flows, but studies exploring how flow modulates the outcomes of crab-clam interactions in the field are lacking. We manipulated turbulence within field sites and compared predation levels within and between sites that differed in flow velocity and turbulence. Our results suggest that blue crabs are most effective foragers in flows with intermediate velocities and turbulence levels. Although these conditions are not ideal for blue crabs, lab studies indicate that they also compromise the ability of clams to detect and react to approaching crabs and, thereby, increase clam vulnerability to predators. Our results suggest that environmental stresses on perception (sensory stressors) may not cause a steady decay in predation rates when they simultaneously affect the behaviors of both predators and prey. Moreover, the relative contribution of lethal vs. nonlethal predator effects in communities also may be influenced by environmental forces that enhance the predator-avoidance abilities of prey or the foraging efficiency of predators.

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.

Author Correction: Accuracy and Precision of Tidal Wetland Soil Carbon Mapping in the Conterminous United States.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.

Accuracy and Precision of Tidal Wetland Soil Carbon Mapping in the Conterminous United States.

Tidal wetlands produce long-term soil organic carbon (C) stocks. Thus for carbon accounting purposes, we need accurate and precise information on the magnitude and spatial distribution of those stocks. We assembled and analyzed an unprecedented soil core dataset, and tested three strategies for mapping carbon stocks: applying the average value from the synthesis to mapped tidal wetlands, applying models fit using empirical data and applied using soil, vegetation and salinity maps, and relying on independently generated soil carbon maps. Soil carbon stocks were far lower on average and varied less spatially and with depth than stocks calculated from available soils maps. Further, variation in carbon density was not well-predicted based on climate, salinity, vegetation, or soil classes. Instead, the assembled dataset showed that carbon density across the conterminous united states (CONUS) was normally distributed, with a predictable range of observations. We identified the simplest strategy, applying mean carbon density (27.0 kg C m-3), as the best performing strategy, and conservatively estimated that the top meter of CONUS tidal wetland soil contains 0.72 petagrams C. This strategy could provide standardization in CONUS tidal carbon accounting until such a time as modeling and mapping advancements can quantitatively improve accuracy and precision.

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.

Flexibility foils filter function: structural limitations on suspension feeding.

Suspension feeders rely on filter structures of a variety of forms to capture food particles. Much effort has been devoted to examining the operation of such filters, but mechanistic evaluations have generally represented filter elements with artificially stiff cylinders. We extended this previous work to investigate how bending affects the function of flexible cylindrical filter elements. Scaled models of filters were constructed from materials with elastic moduli comparable to material stiffnesses of invertebrate appendages (1-177 GPa). These models were mounted on a sled to mimic the protrusion of filters away from an animal's body or from the substratum, and were towed through a vat of syrup to generate relative fluid motion at low Reynolds numbers (Re <10(-3), based on cylinder diameter and tow speed). Flow between filter elements was quantified at multiple positions along their lengths, and a hydrodynamic index of filter performance ('leakiness') was calculated. Leakiness generally increased with cylinder Re and distance from the filter base. At higher flexibilities, however, streamwise bending and lateral narrowing of the filter reduced projected area and slowed flow between elements. This effect decreased leakiness and reversed the otherwise monotonic trend for increased leakiness at higher cylinder Re. Additional experiments showed that filters composed of stouter elements were less susceptible to bending but experienced lower leakiness because of their reduced ability to transcend boundary layers formed over surfaces to which they attached. These findings indicate that filter bending can strongly alter the performance of particle capture apparatus in suspension feeders.

Alteration of sensory abilities regulates the spatial scale of nonlethal predator effects.

Many studies have shown that nonlethal predator effects such as trait-mediated interactions (TMIs) can have significant impacts on the structure and function of communities, but the role that environmental conditions play in modulating the scale and magnitude of these effects has not been carefully investigated. TMIs occur when prey exhibit behavioral or physiological responses to predators and may be more prevalent when abiotic conditions increase prey reactions to consumers. The purpose of this study was to determine if turbulence would alter the distance over which prey in aquatic systems respond to chemical cues emitted by predators in nature, thus changing the scales over which nonlethal predator effects occur. Using hard clams and blue crabs as a model predator-prey system, we investigated the effects of turbulence on clam reactive distance to predatory blue crabs in the field. Results suggest that turbulence diminishes clam reactions to predators and that the environmental context must be considered when predicting the extent of indirect predator effects in natural systems.

Slow-moving predatory gastropods track prey odors in fast and turbulent flow.

Olfactory searching by aquatic predators is reliant upon the hydrodynamic processes that transport and modify chemical signals. Previous studies indicate that the search behavior of some benthic crustaceans is hindered by rapid water flow and turbulent mixing of prey chemicals, but different sensory strategies employed by other taxa might offset such detrimental effects. Using a laboratory flume, we investigated the odor-tracking behavior of a marine gastropod whelk (Busycon carica) to test the generalization that turbulence interferes with chemically mediated navigation. We exposed individual whelks to turbulent odor plumes in free-stream velocities of 1.5, 5, 10 or 15 cm s(-1), or with one of two obstructions placed upstream of the odor source in an intermediate flow of 5 cm s(-1). Measurements of velocity and stimulus properties confirmed that obstruction treatments increased turbulence intensity and altered the fine-scale structure of downstream odor plumes. In all conditions tested, between 36-63% of test animals successfully located the odor source from 1.5 m downstream with no significant effect of flow treatment. Search behaviors, such as cross-stream meander were reduced at higher flow velocities and in the presence of obstructions, allowing whelks to reach the odor source significantly more quickly than in slower, less turbulent conditions. Our results demonstrate that whelks can respond to chemical information in fast and turbulent flow, and we suggest that these slow-moving predators can forage in hydrodynamic environments where the olfactory abilities of other taxa are limited.

Ecological consequences of chemically mediated prey perception.

To locate food, mobile consumers in aquatic habitats perceive and move towards sources of attractive chemicals. There has been much progress in understanding how consumers use chemicals to identify and locate prey despite the elusive identity of odor signals and the complex effects of turbulence on chemical dispersion. This review highlights how integrative studies on behavior, fluid physics, and chemical isolation can be fundamental in elucidating mechanisms that regulate species composition and distribution. We suggest three areas where further research may yield important ecological insights. First, although basic aspects of stimulatory molecules are known, our understanding of how consumers identify prey from a distance remains poor, and the lack of studies examining the influence of distance perception on food preference may result in inaccurate estimation of foraging behavior in the field. Second, the ability of many animals to find prey is greatest in unidirectional, low turbulence flow environments, although recent evidence indicates a trade-off in movement speed versus tracking ability in turbulent conditions. This suggests that predator foraging mode may affect competitive interactions among consumers, and that turbulence provides a hydrodynamic refuge in space or time, leading to particular associations between predator success, prey distributions, and flow. Third, studies have been biased towards examining predator tracking. Current data suggest a variety of mechanisms prey may use to disguise their presence and avoid predation; these mechanisms also may produce associations between prey distributions and flow environments. These examples of how chemical attraction may mediate interactions between consumers and their resources suggest that the ecology of chemically mediated prey perception may be as fundamental to the organization of aquatic communities as the ecology of chemical deterrence.