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.

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.

Combinatorial characterization of bacterial taxa-driven differences in the microbiome of oyster reefs.

Oyster reefs are invaluable ecosystems that provide a wide array of critical ecosystem services, including water filtration, coastal protection, and habitat provision for various marine species. However, these essential habitats face escalating threats from climate change and anthropogenic stressors. To combat these challenges, numerous oyster restoration initiatives have been undertaken, representing a global effort to preserve and restore these vital ecosystems. A significant, yet poorly understood, component of oyster reefs is the microbial communities. These communities account for a substantial proportion of marine reefs and are pivotal in driving key biogeochemical processes. Particularly, the environmental microbiome plays a crucial role in supporting the health and resilience of oyster populations. In our study, we sought to shed light on the microbiome within oyster reef ecosystems by characterizing the abundance, and diversity of microorganisms in the soil, biofilm, and oysters in 4 sites using a combinatorial approach to identify differentially abundant microbes by sample type and by sampling location. Our investigation revealed distinct microbial taxa in oysters, sediment and biofilm. The maximum Shannon Index indicated a slightly increased diversity in Heron's Head (5.47), followed by Brickyard park (5.35), Dunphy Park (5.17) and Point Pinole (4.85). This is likely to be driven by significantly higher oyster mortality observed at Point Pinole during routine monitoring and restoration efforts. Interestingly Ruminococcus, Streptococcus, Staphylococcus, Prevotella, Porphyromonas, Parvimonas, Neisseria, Lactococcus, Haemophilus, Fusobacterium, Dorea, Clostridium, Campylobacter, Bacteroides, and Akkermansia were positively associated with the biofilm. Yet we have limited understanding of their beneficial and/or detrimental implications to oyster growth and survival. By unraveling the intricate relationships in microbial composition across an oyster reef, our study contributes to advancing the knowledge needed to support effective oyster reef conservation and restoration efforts.

Functionalized 3D-printed silk-hydroxyapatite scaffolds for enhanced bone regeneration with innervation and vascularization.

Our goal was to generate functionalized 3D-printed scaffolds for bone regeneration using silk-hydroxyapatite bone cements and osteoinductive, proangiogenic and neurotrophic growth factors or morphogens for accelerated bone formation. 3D printing was utilized to generate macroporous scaffolds with controlled geometries and architectures that promote osseointegration. We build on the knowledge that the osteoinductive factor Bone Morphogenetic Protein-2 (BMP2) can also positively impact vascularization, Vascular Endothelial Growth Factor (VEGF) can impact osteoblastic differentiation, and that Neural Growth Factor (NGF)-mediated signaling can influence bone regeneration. We assessed functions on the 3D printed construct via the osteogenic differentiation of human mesenchymal stem cells; migration and proliferation of human umbilical vein endothelial cells; and proliferation of human induced neural stem cells. The scaffolds provided mechanical properties suitable for bone and the materials were cytocompatible, osteoconductive and maintained the activity of the morphogens and cytokines. Synergistic outcomes between BMP-2, VEGF and NGF in terms of osteoblastic differentiation in vitro were identified, based on the upregulation of genes associated with osteoblastic differentiation (Runt-related transcription factor-2, Osteopontin, Bone Sialoprotein). Additional studies will be required to assess these scaffold designs in vivo. These results are expected to have a strong impact in bone regeneration in dental, oral and maxillofacial surgery.

Pattern and scale: evaluating generalities in crab distributions and marsh dynamics from small plots to a national scale.

The generality of ecological patterns depends inextricably on the scale at which they are examined. We investigated patterns of crab distribution and the relationship between crabs and vegetation in salt marshes at multiple scales. By using consistent monitoring protocols across 15 U.S. National Estuarine Research Reserves, we were able to synthesize patterns from the scale of quadrats to the entire marsh landscape to regional and national scales. Some generalities emerged across marshes from our overall models, and these are useful for informing broad coastal management policy. We found that crab burrow distribution within a marsh could be predicted by marsh elevation, distance to creek and soil compressibility. While these physical factors also affected marsh vegetation cover, we did not find a strong or consistent overall effect of crabs at a broad scale in our multivariate model, though regressions conducted separately for each site revealed that crab burrows were negatively correlated with vegetation cover at 4 out of 15 sites. This contrasts with recent smaller-scale studies and meta-analyses synthesizing such studies that detected strong negative effects of crabs on marshes, likely because we sampled across the entire marsh landscape, while targeted studies are typically limited to low-lying areas near creeks, where crab burrow densities are highest. Our results suggest that sea-level rise generally poses a bigger threat to marshes than crabs, but there will likely be interactions between these physical and biological factors. Beyond these generalities across marshes, we detected some regional differences in crab community composition, richness, and abundance. However, we found striking differences among sites within regions, and within sites, in terms of crab abundance and relationships to marsh integrity. Although generalities are broadly useful, our findings indicate that local managers cannot rely on data from other nearby systems, but rather need local information for developing salt marsh management strategies.

Transgenerational soil-mediated differences between plants experienced or naïve to a grass invasion.

Invasive species may undergo rapid change as they invade. Native species persisting in invaded areas may also experience rapid change over this short timescale relative to native populations in uninvaded areas. We investigated the response of the native Achillea millefolium to soil from Holcus lanatus-invaded and uninvaded areas, and we sought to determine whether differential responses between A. millefolium from invaded (invader experienced) and uninvaded (invader naïve) areas were mediated by soil community changes. Plants grown from seed from experienced and naïve areas responded differently to invaded and uninvaded soil with respect to germination time, biomass, and height. Overall, experienced plants grew faster and taller than their naïve counterparts. Naïve native plants showed negative feedbacks with their home soil and positive feedbacks with invaded soil; experienced plants were less responsive to soil differences. Our results suggest that native plants naïve to invasion may be more sensitive to soil communities than experienced plants, consistent with recent studies. While differences between naïve and experienced plants are transgenerational, our design cannot differentiate between differences that are genetically based, plastic, or both. Regardless, our results highlight the importance of seed source and population history in restoration, emphasizing the restoration potential of experienced seed sources.