Recruitment of a threatened foundation oyster species varies with large and small spatial scales.

Understanding how habitat attributes (e.g., patch area and sizes, connectivity) control recruitment and how this is modified by processes operating at larger spatial scales is fundamental to understanding population sustainability and developing successful long-term restoration strategies for marine foundation species-including for globally threatened reef-forming oysters. In two experiments, we assessed the recruitment and energy reserves of oyster recruits onto remnant reefs of the oyster Saccostrea glomerata in estuaries spanning 550 km of coastline in southeastern Australia. In the first experiment, we determined whether recruitment of oysters to settlement plates in three estuaries was correlated with reef attributes within patches (distances to patch edges and surface elevation), whole-patch attributes (shape and size of patches), and landscape attributes (connectivity). We also determined whether environmental factors (e.g., sedimentation and water temperature) explained the differences among recruitment plates. We also tested whether differences in energy reserves of recruits could explain the differences between two of the estuaries (one high- and one low-sedimentation estuary). In the second experiment, across six estuaries (three with nominally high and three with nominally low sedimentation rates), we tested the hypothesis that, at the estuary scale, recruitment and survival were negatively correlated to sedimentation. Overall, total oyster recruitment varied mostly at the scale of estuaries rather than with reef attributes and was negatively correlated with sedimentation. Percentage recruit survival was, however, similar among estuaries, although energy reserves and condition of recruits were lower at a high- compared to a low-sediment estuary. Within each estuary, total oyster recruitment increased with patch area and decreased with increasing tidal height. Our results showed that differences among estuaries have the largest influence on oyster recruitment and recruit health and this may be explained by environmental processes operating at the same scale. While survival was high across all estuaries, growth and reproduction of oysters on remnant reefs may be affected by sublethal effects on the health of recruits in high-sediment estuaries. Thus, restoration programs should consider lethal and sublethal effects of whole-estuary environmental processes when selecting sites and include environmental mitigation actions to maximize recruitment success.

Meta-analysis of ecosystem services associated with oyster restoration.

Restoration of foundation species promises to reverse environmental degradation and return lost ecosystem services, but a lack of standardized evaluation across projects limits understanding of recovery, especially in marine systems. Oyster reefs are restored to reverse massive global declines and reclaim valuable ecosystem services, but the success of these projects has not been systematically and comprehensively quantified. We synthesized data on ecosystem services associated with oyster restoration from 245 pairs of restored and degraded reefs and 136 pairs of restored and reference reefs across 3500 km of U.S. Gulf of Mexico and Atlantic coastlines. On average, restoration was associated with a 21-fold increase in oyster production (mean log response ratio = 3.08 [95% confidence interval: 2.58-3.58]), 34-97% enhancement of habitat provisioning (mean community abundance = 0.51 [0.41-0.61], mean richness = 0.29 [0.19-0.39], and mean biomass = 0.69 [0.39-0.99]), 54% more nitrogen removal (mean = 0.43 [0.13-0.73]), and 89-95% greater sediment nutrients (mean = 0.67 [0.27-1.07]) and organic matter (mean = 0.64 [0.44-0.84]) relative to degraded habitats. Moreover, restored reefs matched reference reefs for these ecosystem services. Our results support the continued and expanded use of oyster restoration to enhance ecosystem services of degraded coastal systems and match many functions provided by reference reefs.

La restauración de especies fundadoras promete revertir la degradación ambiental y restituir servicios ambientales perdidos, pero la falta de evaluación estandarizada de proyectos limita la comprensión de la recuperación, especialmente en sistemas marinos. Los bancos de ostión son restaurados para revertir declinaciones globales masivas y recuperar servicios ecosistémicos valiosos, pero el éxito de estos proyectos no ha sido cuantificado sistemática ni integralmente. Sintetizamos datos sobre los servicios ecosistémicos asociados con la restauración de ostiones de 245 pares de bancos restaurados y degradados y 136 pares de bancos restaurados y de referencia a lo largo de 3500 km de costa del Golfo de México y Atlántico norteamericanos. En promedio, la restauración se asoció con un incremento de 21 veces en la producción de ostión (media de proporción de respuesta log = 3.08 [95% IC 2.58-3.58]), mejoras entre 34 y 97% en el aprovisionamiento de hábitat (abundancia media = 0.51 [0.41-0.61], riqueza media = 0.29 [0.19-0.39], y biomasa media = 0.69 [0.39-0.99]), 54% más remoción de nitrógeno (media = 0.43 [0.13-0.73]), y 89-95% más nutrientes en sedimento (media = 0.67 [0.27-1.07]) y materia orgánica (media = 0.64 [0.44-0.84]) en relación con hábitats degradados. Más aun, estos servicios ecosistémicos de los bancos restaurados fueron muy similares en los bancos de referencia. Nuestros resultados sustentan el uso continuo y expandido de la restauración de ostiones para mejorar los servicios ecosistémicos de sistemas costeros degradados y que sean parecidos a las numerosas funciones proporcionadas por los bancos de referencia.

The shell matrix of the european thorny oyster, Spondylus gaederopus: microstructural and molecular characterization.

Molluscs, the largest marine phylum, display extraordinary shell diversity and sophisticated biomineral architectures. However, mineral-associated biomolecules involved in biomineralization are still poorly characterised. We report the first comprehensive structural and biomolecular study of Spondylus gaederopus, a pectinoid bivalve with a peculiar shell texture. Used since prehistoric times, this is the best-known shell of Europe's cultural heritage. We find that Spondylus microstructure is very poor in mineral-bound organics, which are mostly intercrystalline and concentrated at the interface between structural layers. Using high-resolution liquid chromatography tandem mass spectrometry (LC-MS/MS) we characterized several shell protein fractions, isolated following different bleaching treatments. Several peptides were identified as well as six shell proteins, which display features and domains typically found in biomineralized tissues, including the prevalence of intrinsically disordered regions. It is very likely that these sequences only partially represent the full proteome of Spondylus, considering the lack of genomics data for this genus and the fact that most of the reconstructed peptides do not match with any known shell proteins, representing consequently lineage-specific sequences. This work sheds light onto the shell matrix involved in the biomineralization in spondylids. Our proteomics data suggest that Spondylus has evolved a shell-forming toolkit, distinct from that of other better studied pectinoids - fine-tuned to produce shell structures with high mechanical properties, while limited in organic content. This study therefore represents an important milestone for future studies on biomineralized skeletons and provides the first reference dataset for forthcoming molecular studies of Spondylus archaeological artifacts.

Timing Metabolic Depression: Predicting Thermal Stress in Extreme Intertidal Environments.

AbstractAnticipatory changes in organismal responses, triggered by reliable environmental cues for future conditions, are key to species' persistence in temporally variable environments. Such responses were tested by measuring the physiological performance of a tropical high-shore oyster in tandem with the temporal predictability of environmental temperature. Heart rate of the oyster increased with environmental temperatures until body temperature reached ∼37°C, when a substantial depression occurred (∼60%) before recovery between ∼42° and 47°C, after which cardiac function collapsed. The sequential increase, depression, and recovery in cardiac performance aligned with temporal patterns in rock surface temperatures, where the risk of reaching temperatures close to the oysters' lethal limit accelerates if the rock heats up beyond ∼37°C, coinciding closely with the body temperature at which the oysters initiate metabolic depression. The increase in body temperature over a critical threshold serves as an early-warning cue to initiate anticipatory shifts in physiology and energy conservation before severe thermal stress occurs on the shore. Cross-correlating the onset of physiological mechanisms and temporal structures in environmental temperatures, therefore, reveals the potential role of reliable real-time environmental cues for future conditions in driving the evolution of anticipatory responses.

Differences in induced thermotolerance among populations of Olympia oysters.

An organism's ability to cope with thermal stress is an important predictor of survival in a changing climate. One way in which organisms may acclimatize to thermal stress in the short-term is through induced thermotolerance, whereby exposure to a sublethal heat shock enables the organism to subsequently survive what might otherwise be a lethal event. Whether induced thermotolerance is related to basal thermotolerance is not well understood for marine organisms. Furthermore, whether populations often differ in their capacity for induced thermotolerance is also unclear. Here, we tested for differences in basal thermotolerance and induced thermotolerance among six populations of Olympia oysters (Ostrea lurida) from three California estuaries. Oysters were raised under common-garden laboratory conditions for a generation and then exposed to two treatments (control or sublethal heat shock) followed by a spectrum of temperatures that bound the upper critical temperature in order to determine LT50 (temperature at which 50% of the population dies). All populations exhibited induced thermotolerance by increasing their LT50 to a similar maximum temperature when extreme thermal stress was preceded by a sublethal heat shock. However, populations differed in their basal thermotolerance and their plasticity in thermotolerance. Populations with the highest basal thermotolerance were least able to modify upper critical temperature, while the population with the lowest basal thermotolerance exhibited the greatest plasticity in the upper critical temperature. Our results highlight that populations with high basal thermotolerance may be most vulnerable to climate warming because they lack the plasticity required to adjust their upper thermal limits.

Bending and branching of calcite laths in the foliated microstructure of pectinoidean bivalves occurs at coherent crystal lattice orientation.

Foliated calcite is widely employed by some important pteriomorph bivalve groups as a construction material. It is made from calcite laths, which are inclined at a low angle to the internal shell surface, although their arrangement is different among the different groups. They are strictly ordered into folia in the anomiids, fully independent in scallops, and display an intermediate arrangement in oysters. Pectinids have particularly narrow laths characterized by their ability to change their growth direction by bending or winding, as well as to bifurcate and polyfurcate. Electron backscatter analysis indicates that the c-axes of laths are at a high, though variable, angle to the growth direction, and that the laths grow preferentially along the projection of an intermediate axis between two a-axes, although they can grow in any intermediate direction. Their main surfaces are not particular crystallographic faces. Analyses done directly on the lath surfaces demonstrate that, during the bending/branching events, all crystallographic axes remain invariant. The growth flexibility of pectinid laths makes them an excellent space-filling material, well suited to level off small irregularities of the shell growth surface. We hypothesize that the exceptional ability of laths to change their direction may be promoted by the mode of growth of biogenic calcite, from a precursor liquid phase induced by organic molecules.

Mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (Saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development.

BACKGROUND: The black-lip rock oyster (Saccostrea echinata) has considerable potential for aquaculture throughout the tropics. Previous attempts to farm S. echinata failed due to an insufficient supply of wild spat; however, the prospect of hatchery-based aquaculture has stimulated renewed interest, and small-scale farming is underway across northern Australia and in New Caledonia. The absence of knowledge surrounding the population genetic structure of this species has raised concerns about the genetic impacts of this emerging aquaculture industry. This study is the first to examine population genetics of S. echinata and employs both mitochondrial cytochrome c oxidase subunit I gene (COI) and single nucleotide polymorphism (SNP) markers. RESULTS: The mitochondrial COI data set included 273 sequences of 594 base pair length, which comprised 74 haplotypes. The SNP data set included 27,887 filtered SNPs for 272 oysters and of these 31 SNPs were identified as candidate adaptive loci. Data from the mitochondrial COI analyses, supports a broad tropical Indo-Pacific distribution of S. echinata, and showed high haplotype and nucleotide diversities (0.887-1.000 and 0.005-0.008, respectively). Mitochondrial COI analyses also revealed a 'star-like' haplotype network, and significant and negative neutrality tests (Tajima's D = - 2.030, Fu's Fs = - 25.638, P < 0.001) support a recent population expansion after a bottleneck. The SNP analyses showed significant levels of population subdivision and four genetic clusters were identified: (1) the Noumea (New Caledonia) sample location; (2) the Bowen (north Queensland, Australia) sample location, and remaining sample locations in the Northern Territory, Australia (n = 8) were differentiated into two genetic clusters. These occurred at either side of the Wessel Islands and were termed (3) 'west' and (4) 'east' clusters, and two migrant individuals were detected between them. The SNP data showed a significant positive correlation between genetic and geographic distance (Mantel test, P < 0.001, R2 = 0.798) and supported isolation by distance. Three candidate adaptive SNPs were identified as occurring within known genes and gene ontology was well described for the sex peptide receptor gene. CONCLUSIONS: Data supports the existence of genetically distinct populations of S. echinata, suggesting that management of wild and farmed stocks should be based upon multiple management units. This research has made information on population genetic structure and connectivity available for a new aquaculture species.

Oyster reproduction is affected by exposure to polystyrene microplastics.

Plastics are persistent synthetic polymers that accumulate as waste in the marine environment. Microplastic (MP) particles are derived from the breakdown of larger debris or can enter the environment as microscopic fragments. Because filter-feeder organisms ingest MP while feeding, they are likely to be impacted by MP pollution. To assess the impact of polystyrene microspheres (micro-PS) on the physiology of the Pacific oyster, adult oysters were experimentally exposed to virgin micro-PS (2 and 6 µm in diameter; 0.023 mg·L(-1)) for 2 mo during a reproductive cycle. Effects were investigated on ecophysiological parameters; cellular, transcriptomic, and proteomic responses; fecundity; and offspring development. Oysters preferentially ingested the 6-µm micro-PS over the 2-µm-diameter particles. Consumption of microalgae and absorption efficiency were significantly higher in exposed oysters, suggesting compensatory and physical effects on both digestive parameters. After 2 mo, exposed oysters had significant decreases in oocyte number (-38%), diameter (-5%), and sperm velocity (-23%). The D-larval yield and larval development of offspring derived from exposed parents decreased by 41% and 18%, respectively, compared with control offspring. Dynamic energy budget modeling, supported by transcriptomic profiles, suggested a significant shift of energy allocation from reproduction to structural growth, and elevated maintenance costs in exposed oysters, which is thought to be caused by interference with energy uptake. Molecular signatures of endocrine disruption were also revealed, but no endocrine disruptors were found in the biological samples. This study provides evidence that micro-PS cause feeding modifications and reproductive disruption in oysters, with significant impacts on offspring.

Ocean acidification but not warming alters sex determination in the Sydney rock oyster, Saccostrea glomerata.

Whether sex determination of marine organisms can be altered by ocean acidification and warming during this century remains a significant, unanswered question. Here, we show that exposure of the protandric hermaphrodite oyster, Saccostrea glomerata to ocean acidification, but not warming, alters sex determination resulting in changes in sex ratios. After just one reproductive cycle there were 16% more females than males. The rate of gametogenesis, gonad area, fecundity, shell length, extracellular pH and survival decreased in response to ocean acidification. Warming as a sole stressor slightly increased the rate of gametogenesis, gonad area and fecundity, but this increase was masked by the impact of ocean acidification at a level predicted for this century. Alterations to sex determination, sex ratios and reproductive capacity will have flow on effects to reduce larval supply and population size of oysters and potentially other marine organisms.

Examination of the potential relationship between boring sponges and pea crabs and their effects on eastern oyster condition.

The eastern oyster Crassostrea virginica provides a number of ecosystem services and is an important commercial fishery species along the US East and Gulf Coasts. Oyster populations have declined dramatically due to overharvesting, habitat loss, and disease. As restoration efforts and aquaculture of oysters continue to increase throughout their range, it is important to consider the impacts of a number of potential oyster pests, including the boring sponge Cliona spp. and the pea crab Zaops (Pinnotheres) ostreum, on oyster populations. Both of these have been demonstrated to reduce oyster growth, condition, and in some instances, reproductive output. Boring sponges in particular are a major concern for oyster growers and managers. Our monitoring efforts have suggested that pea crabs might be more prevalent in sponge-infested oysters; we therefore conducted an observational study to determine if there was any relationship between pea crab prevalence and sponge presence, and to examine whether the presence of both pests had synergistic effects on oyster condition. At 2 very different sample sites, North Carolina and New Jersey, oysters with 1 pest (i.e. boring sponge) were significantly more likely to have the second pest (i.e. pea crab) than the background population. Furthermore, sponge presence negatively affected oyster condition in North Carolina only, while pea crabs significantly reduced condition at both locations. When sponges and pea crabs were present together, the effects on oyster condition were additive. This study provides further evidence that interactions between an individual and a fouling/pest organism can alter oyster susceptibility to other parasites.

Contrasting impacts of ocean acidification and warming on the molecular responses of CO2-resilient oysters.

BACKGROUND: This study characterises the molecular processes altered by both elevated CO2 and increasing temperature in oysters. Differences in resilience of marine organisms against the environmental stressors associated with climate change will have significant implications for the sustainability of coastal ecosystems worldwide. Some evidence suggests that climate change resilience can differ between populations within a species. B2 oysters represent a unique genetic resource because of their capacity to better withstand the impacts of elevated CO2 at the physiological level, compared to non-selected oysters from the same species (Saccostrea glomerata). Here, we used proteomic and transcriptomic analysis of gill tissue to evaluate whether the differential response of B2 oysters to elevated CO2 also extends to increased temperature. RESULTS: Substantial and distinctive effects on protein concentrations and gene expression were evident among B2 oysters responding to elevated CO2 or elevated temperature. The combination of both stressors also altered oyster gill proteomes and gene expression. However, the impacts of elevated CO2 and temperature were not additive or synergistic, and may be antagonistic. CONCLUSIONS: The data suggest that the simultaneous exposure of CO2-resilient oysters to near-future projected ocean pH and temperature results in complex changes in molecular processes in order to prevent stress-induced cellular damage. The differential response of B2 oysters to the combined stressors also indicates that the addition of thermal stress may impair the resilience of these oysters to decreased pH. Overall, this study reveals the intracellular mechanisms that might enable marine calcifiers to endure the emergent, adverse seawater conditions resulting from climate change.

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.

Intertidal oysters reach their physiological limit in a future high-CO2 world.

Sessile marine molluscs living in the intertidal zone experience periods of internal acidosis when exposed to air (emersion) during low tide. Relative to other marine organisms, molluscs have been identified as vulnerable to future ocean acidification; however, paradoxically it has also been shown that molluscs exposed to high CO2 environments are more resilient compared with those molluscs naive to CO2 exposure. Two competing hypotheses were tested using a novel experimental design incorporating tidal simulations to predict the future intertidal limit of oysters in a high-CO2 world; either high-shore oysters will be more tolerant of elevated PCO2 because of their regular acidosis, or elevated PCO2  will cause high-shore oysters to reach their limit. Sydney rock oysters, Saccostrea glomerata, were collected from the high-intertidal and subtidal areas of the shore and exposed in an orthogonal design to either an intertidal or a subtidal treatment at ambient or elevated PCO2 , and physiological variables were measured. The combined treatment of tidal emersion and elevated PCO2  interacted synergistically to reduce the haemolymph pH (pHe) of oysters, and increase the PCO2  in the haemolymph (Pe,CO2 ) and standard metabolic rate. Oysters in the intertidal treatment also had lower condition and growth. Oysters showed a high degree of plasticity, and little evidence was found that intertidal oysters were more resilient than subtidal oysters. It is concluded that in a high-CO2 world the upper vertical limit of oyster distribution on the shore may be reduced. These results suggest that previous studies on intertidal organisms that lacked tidal simulations may have underestimated the effects of elevated PCO2.

Fast-growing oysters show reduced capacity to provide a thermal refuge to intertidal biodiversity at high temperatures.

Ecosystem engineers that modify the thermal environment experienced by associated organisms might assist in the climate change adaptation of species. This depends on the ability of ecosystem engineers to persist and continue to ameliorate thermal stress under changing climatic conditions-traits that may display significant intraspecific variation. In the physically stressful intertidal, the complex three-dimensional structure of oysters provides shading and traps moisture during aerial exposure at low tide. We assessed variation in the capacity of a faster- and slower-growing population of the Sydney Rock Oyster, Saccostrea glomerata, to persist, form three-dimensional structure and provide a cool microhabitat to invertebrates under warmer conditions. The two populations of oysters were exposed to a temperature gradient in the field by attaching them to passively warmed white, grey and black stone pavers and their growth, survivorship and colonisation by invertebrates was monitored over a 12-month period. Oysters displayed a trade-off between fast growth and thermal tolerance. The growth advantage of the fast-growing population diminished with increasing substrate temperature, and at higher temperatures, the faster-growing oysters suffered greater mortality, formed less habitat, and were consequently less effective at ameliorating low-tide air temperature extremes than slower-growing oysters. The greater survivorship of slower-growing oysters, in turn, produced a cooler microclimate which fed back to further bolster oyster survivorship. Invertebrate recruitment increased with habitat cover and was greater among the slower than the faster-growing population. Our results show that the capacity of ecosystem engineers to serve as microhabitat refugia to associated organisms in a warming climate displays marked intraspecific variation. Our study also adds to growing evidence that fast growth may come at the expense of thermal tolerance.

Evaluation of the impact of bioaccumulation of PAH from the marine environment on DNA integrity and oxidative stress in marine rock oyster (Saccostrea cucullata) along the Arabian sea coast.

Marine pollution due to oil spills is of great concern globally for their impact on the health of marine ecosystems. We assessed the genotoxic effects and oxidative stress due to genotoxic pollutants accumulated from the ambient marine environment in the tissues of marine rock oyster, Saccostrea cucullata along the Arabian Sea coast around Goa, India. The extent of DNA damage in S. cucullata was determined by comet assay as variation of comet parameter: mean % tail DNA along the coast with respect to that at the reference site (Tiracol, Goa, India). In addition, the oxidative stress responses of rock oysters exposed to marine pollutants such as polycyclic aromatic hydrocarbons (PAHs) were assessed as a function of variation in antioxidant enzyme activities such as glutathione-s-transferase (GST), catalase (CAT) and superoxide dismutase (SOD) along the coast. Spearman correlation analysis showed significant correlation between different components of PAHs (viz., 2-3-PAH, 4-6-PAH and oxy-PAH) in the tissues of the rock oysters and the antioxidant enzyme activities. The antioxidant enzyme activities in S. cucullata increased with increasing concentrations of PAHs in tissues in the following order of sampling sites: Tiracol < Arambol < Betul < Velsao. Among the PAHs, oxy-PAH was found to be most predominant in causing DNA damage in S. cucullata. These results provide an insight into environmental genotoxicity and oxidative stress induced by PAHs along the Arabian Sea coast, India.

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.

Effects of intraspecific diversity on survivorship, growth, and recruitment of the eastern oyster across sites.

Intraspecific diversity, particularly of foundation species, can significantly affect population, community, and ecosystem processes. Examining how genetic diversity relates to demographic traits provides a key mechanistic link from genotypic and phenotypic variation of taxa with complex life histories to their population dynamics. We conducted a field experiment to assess how two metrics of intraspecific diversity (cohort diversity, the number of independent juvenile cohorts created from different adult source populations, and genetic relatedness, genetic similarity among individuals within and across cohorts) affect the survivorship, growth, and recruitment of the foundation species Crassostrea virginica. To assess the effects of both cohort diversity and genetic relatedness on oyster demographic traits under different environmental conditions, we manipulated juvenile oyster diversity and predator exposure (presence/absence of a cage) at two sites differing in resource availability and predation intensity. Differences in predation pressure between sites overwhelmingly determined post-settlement survivorship of oysters. However, in the absence of predation (i.e., cage treatment), one or both metrics of intraspecific diversity, in addition to site, influenced long-term survivorship, growth, and recruitment. While both cohort diversity and genetic relatedness were negatively associated with long-term survivorship, genetic relatedness alone showed a positive association with growth and cohort diversity alone showed a positive association with recruitment. Thus, our results demonstrate that in the absence of predation, intraspecific diversity can affect multiple demographic traits of a foundation species, but the relative importance of these effects depends on the environmental context. Moreover, the magnitude and direction of these effects vary depending on the diversity metric, cohort diversity or genetic relatedness, suggesting that although they are inversely related in this system, each captures sufficiently different components of intraspecific diversity. Given the global loss of oyster reef habitat and rapid decline in oyster population size, our results are particularly relevant to management and restoration. In addition, aquaculture, which commonly excludes predators during early life history stages, may benefit from incorporation of oyster cohort diversity into standard practice.

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.

Latitudinal gradients in ecosystem engineering by oysters vary across habitats.

Ecological theory predicts that positive interactions among organisms will increase across gradients of increasing abiotic stress or consumer pressure. This theory has been supported by empirical studies examining the magnitude of ecosystem engineering across environmental gradients and between habitat settings at local scale. Predictions that habitat setting, by modifying both biotic and abiotic factors, will determine large-scale gradients in ecosystem engineering have not been tested, however. A combination of manipulative experiments and field surveys assessed whether along the east Australian coastline: (1) facilitation of invertebrates by the oyster Saccostrea glomerata increased across a latitudinal gradient in temperature; and (2) the magnitude of this effect varied between intertidal rocky shores and mangrove forests. It was expected that on rocky shores, where oysters are the primary ecosystem engineer, they would play a greater role in ameliorating latitudinal gradients in temperature than in mangroves, where they are a secondary ecosystem engineer living under the mangrove canopy. On rocky shores, the enhancement of invertebrate abundance in oysters as compared to bare microhabitat decreased with latitude, as the maximum temperatures experienced by intertidal organisms diminished. By contrast, in mangrove forests, where the mangrove canopy resulted in maximum temperatures that were cooler and of greater humidity than on rocky shores, we found no evidence of latitudinal gradients of oyster effects on invertebrate abundance. Contrary to predictions, the magnitude by which oysters enhanced biodiversity was in many instances similar between mangroves and rocky shores. Whether habitat-context modifies patterns of spatial variation in the effects of ecosystem engineers on community structure will depend, in part, on the extent to which the environmental amelioration provided by an ecosystem engineer replicates that of other co-occurring ecosystem engineers.