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.

The long-lived deep-sea bivalve Acesta excavata is sensitive to the dual stressors of sediment and warming.

Human influence in the deep-sea is increasing as mining and drilling operations expand, and waters warm because of climate change. Here, we investigate how the long-lived deep-sea bivalve, Acesta excavata responds to sediment pollution and/or acute elevated temperatures. A. excavata were exposed to suspended sediment, acute warming, and a combination of the two treatments for 40 days. We measured O2 consumption, NH4+ release, Total Organic Carbon (TOC), and lysosomal membrane stability (LMS). We found suspended sediment and warming interacted to decrease O:N ratios, while sediment as a single stressor increased the release of TOC and warming increased NH4+ release in A. excavata. Warming also increased levels of LMS. We found A. excavata used protein catabolism to meet elevated energetic demands indicating a low tolerance to stress. A. excavata has limited capacity for physiological responses to the stressors of warming and sediment which may lead to decreased fitness of A. excavata.

Resilience against the impacts of climate change in an ecologically and economically significant native oyster.

Climate change is acidifying and warming our oceans, at an unprecedented rate posing a challenge for marine invertebrates vital across the globe for ecological services and food security. Here we show it is possible for resilience to climate change in an ecologically and economically significant oyster without detrimental effects to the energy budget. We exposed 24 pair-mated genetically distinct families of the Sydney rock oyster, Saccostrea glomerata to ocean acidification and warming for 4w and measured their resilience. Resilience was identified as the capacity to defend their acid-base balance without a loss of energy available for Scope for Growth (SFG). Of the 24 families, 13 were better able to defend their acid-base balance while eight had no loss of energy availability with a positive SFG. This study has found oyster families with reslience against climate change without a loss of SFG, is an essential mitigation strategy, in a critical mollusc.

Acclimation in intertidal animals reduces potential pathogen load and increases survival following a heatwave.

Intertidal animals can experience intense heat during a heatwave, leading to mortality. The causes of death for intertidal animals following heatwaves have often been attributed to a breakdown in physiological processes. This, however, contrasts with research in other animals where heatwave mortality is attributed to existing or opportunistic diseases. We acclimated intertidal oysters to four treatment levels, including an antibiotic treatment, and then exposed all treatments to a 50°C heatwave for 2 h, replicating what can be experienced on Australian shorelines. We found that both acclimation and antibiotics increased survival and reduced the presence of potential pathogens. Non-acclimated oysters had a significant shift in their microbiome, with increasing abundances of bacteria from the Vibrio genera, including known potential pathogens. Our results demonstrate that bacterial infection plays a pivotal role in post-heatwave mortality. We anticipate these findings to inform the management of aquaculture and intertidal habitats as climate change intensifies.

Warming and hypoxia threaten a valuable scallop fishery: A warning for commercial bivalve ventures in climate change hotspots.

Marine molluscs constitute the second largest marine fishery and are often caught in coastal and estuarine habitats. Temperature is increasing in these habitats at a rate greater than predicted, especially in warming "hotspots". This warming is accompanied by hypoxia in a duo of stressors that threatens coastal mollusc fisheries and aquaculture. Collapses of the northern bay scallop (Argopecten irradians irradians) fisheries on the Atlantic coast of the USA are likely to be driven by rapid rates of coastal warming and may provide an ominous glimpse into the prospects of other coastal mollusc fisheries in climate warming hotspots.

Microbiomes of the Sydney Rock Oyster are acquired through both vertical and horizontal transmission.

BACKGROUND: The term holobiont is widely accepted to describe animal hosts and their associated microorganisms. The genomes of all that the holobiont encompasses, are termed the hologenome and it has been proposed as a unit of selection in evolution. To demonstrate that natural selection acts on the hologenome, a significant portion of the associated microbial genomes should be transferred between generations. Using the Sydney Rock Oyster (Saccostrea glomerata) as a model, we tested if the microbes of this broadcast spawning species could be passed down to the next generation by conducting single parent crosses and tracking the microbiome from parent to offspring and throughout early larval stages using 16S rRNA gene amplicon sequencing. From each cross, we sampled adult tissues (mantle, gill, stomach, gonad, eggs or sperm), larvae (D-veliger, umbo, eyed pediveliger, and spat), and the surrounding environment (water and algae feed) for microbial community analysis. RESULTS: We found that each larval stage has a distinct microbiome that is partially influenced by their parental microbiome, particularly the maternal egg microbiome. We also demonstrate the presence of core microbes that are consistent across all families, persist throughout early life stages (from eggs to spat), and are not detected in the microbiomes of the surrounding environment. In addition to the core microbiomes that span all life cycle stages, there is also evidence of environmentally acquired microbial communities, with earlier larval stages (D-veliger and umbo), more influenced by seawater microbiomes, and later larval stages (eyed pediveliger and spat) dominated by microbial members that are specific to oysters and not detected in the surrounding environment. CONCLUSION: Our study characterized the succession of oyster larvae microbiomes from gametes to spat and tracked selected members that persisted across multiple life stages. Overall our findings suggest that both horizontal and vertical transmission routes are possible for the complex microbial communities associated with a broadcast spawning marine invertebrate. We demonstrate that not all members of oyster-associated microbiomes are governed by the same ecological dynamics, which is critical for determining what constitutes a hologenome.

Can seagrass modify the effects of ocean acidification on oysters?

Solutions are being sought to ameliorate the impacts of anthropogenic climate change. Seagrass may be a solution to provide refugia from climate change for marine organisms. This study aimed to determine if the seagrass Zostera muelleri sub spp. capricorni benefits the Sydney rock oyster Saccostrea glomerata, and if these benefits can modify any anticipated negative impacts of ocean acidification. Future and ambient ocean acidification conditions were simulated in 52 L mesocosms at control (381 µatm) and elevated (848 µatm) CO2 with and without Z. muelleri. Oyster growth, physiology and microbiomes of oysters and seagrass were measured. Seagrass was beneficial to oyster growth at ambient pCO2, but did not positively modify the impacts of ocean acidification on oysters at elevated pCO2. Oyster microbiomes were altered by the presence of seagrass but not by elevated pCO2. Our results indicate seagrasses may not be a panacea for the impacts of climate change.

Climate change alters shellfish reef communities: A temperate mesocosm experiment.

Climate change is expected to cause significant changes to rocky shore diversity. This study used outdoor mesocosms to test the predictions that warming and ocean acidification will alter the responses of native Trichomya hirsuta and introduced Mytilus galloprovincialis mussels, and their associated communities of infauna. Experiments consisted of orthogonal combinations of temperature (ambient 22 °C or elevated 25 °C), pCO2 (ambient 400 µatm or elevated 1000 µatm), mussel species (T. hirsuta or M. galloprovincialis), and mussel configuration (native, introduced, or both), with n = 3 replicates. Elevated pCO2 reduced the growth of T. hirsuta but not that of M. galloprovincialis, and warming and pCO2 influenced the infauna that colonised both species of mussels. There was a reduction in infaunal molluscs and an increase in polychaetes; there was, however, no effect on crustaceans. Results from this study suggest that climate-driven changes from one mussel species to another can significantly influence infaunal communities.

Microbiomes of an oyster are shaped by metabolism and environment.

Microbiomes can both influence and be influenced by metabolism, but this relationship remains unexplored for invertebrates. We examined the relationship between microbiome and metabolism in response to climate change using oysters as a model marine invertebrate. Oysters form economies and ecosystems across the globe, yet are vulnerable to climate change. Nine genetic lineages of the oyster Saccostrea glomerata were exposed to ambient and elevated temperature and PCO2 treatments. The metabolic rate (MR) and metabolic by-products of extracellular pH and CO2 were measured. The oyster-associated bacterial community in haemolymph was characterised using 16 s rRNA gene sequencing. We found a significant negative relationship between MR and bacterial richness. Bacterial community composition was also significantly influenced by MR, extracellular CO2 and extracellular pH. The effects of extracellular CO2 depended on genotype, and the effects of extracellular pH depended on CO2 and temperature treatments. Changes in MR aligned with a shift in the relative abundance of 152 Amplicon Sequencing Variants (ASVs), with 113 negatively correlated with MR. Some spirochaete ASVs showed positive relationships with MR. We have identified a clear relationship between host metabolism and the microbiome in oysters. Altering this relationship will likely have consequences for the 12 billion USD oyster economy.

Biotic habitats as refugia under ocean acidification.

Habitat-forming organisms have an important role in ameliorating stressful conditions and may be of particular relevance under a changing climate. Increasing CO2 emissions are driving a range of environmental changes, and one of the key concerns is the rapid acceleration of ocean acidification and associated reduction in pH. Such changes in seawater chemistry are anticipated to have direct negative effects on calcifying organisms, which could, in turn, have negative ecological, economic and human health impacts. However, these calcifying organisms do not exist in isolation, but rather are part of complex ecosystems. Here, we use a qualitative narrative synthesis framework to explore (i) how habitat-forming organisms can act to restrict environmental stress, both now and in the future; (ii) the ways their capacity to do so is modified by local context; and (iii) their potential to buffer the effects of future change through physiological processes and how this can be influenced by management adopted. Specifically, we highlight examples that consider the ability of macroalgae and seagrasses to alter water carbonate chemistry, influence resident organisms under current conditions and their capacity to do so under future conditions, while also recognizing the potential role of other habitats such as adjacent mangroves and saltmarshes. Importantly, we note that the outcome of interactions between these functional groups will be context dependent, influenced by the local abiotic and biotic characteristics. This dependence provides local managers with opportunities to create conditions that enhance the likelihood of successful amelioration. Where individuals and populations are managed effectively, habitat formers could provide local refugia for resident organisms of ecological and economic importance under an acidifying ocean.

Microbiome response differs among selected lines of Sydney rock oysters to ocean warming and acidification.

Oyster microbiomes are integral to healthy function and can be altered by climate change conditions. Genetic variation among oysters is known to influence the response of oysters to climate change and may ameliorate any adverse effects on oyster microbiome; however, this remains unstudied. Nine full-sibling selected breeding lines of the Sydney rock oyster (Saccostrea glomerata) were exposed to predicted warming (ambient = 24°C, elevated = 28°C) and ocean acidification (ambient pCO2 = 400, elevated pCO2 = 1000 µatm) for 4 weeks. The haemolymph bacterial microbiome was characterized using 16S rRNA (V3-V4) gene sequencing and varied among oyster lines in the control (ambient pCO2, 24°C) treatment. Microbiomes were also altered by climate change dependent on oyster lines. Bacterial α-diversity increased in response to elevated pCO2 in two selected lines, while bacterial ß-diversity was significantly altered by combinations of elevated pCO2 and temperature in four selected lines. Climate change treatments caused shifts in the abundance of multiple amplicon sequence variants driving change in the microbiome of some selected lines. We show that oyster genetic background may influence the Sydney rock oyster haemolymph microbiome under climate change and that future assisted evolution breeding programs to enhance resilience should consider the oyster microbiome.

Energetic lipid responses of larval oysters to ocean acidification.

Climate change will increase energetic demands on marine invertebrate larvae and make planktonic food more unpredictable. This study determined the impact of ocean acidification on larval energetics of the oysters Saccostrea glomerata and Crassostrea gigas. Larvae of both oysters were reared until the 9-day-old, umbonate stage under orthogonal combinations of ambient and elevated p CO 2 (340 and 856 µatm) and food was limited. Elevated p CO 2 reduced the survival, size and larval energetics, larvae of C. gigas being more resilient than S. glomerata. When larvae were fed, elevated p CO 2 reduced lipid levels across all lipid classes. When larvae were unfed elevated p CO 2 resulted in increased lipid levels and mortality. Ocean acidification and food will interact to limit larval energetics. Larvae of S. glomerata will be more impacted than C. gigas and this is of concern given their aquacultural status and ecological function.

Transgenerational plasticity responses of oysters to ocean acidification differ with habitat.

Transgenerational plasticity (TGP) has been identified as a critical mechanism of acclimation that may buffer marine organisms against climate change, yet whether the TGP response of marine organisms is altered depending on their habitat is unknown. Many marine organisms are found in intertidal zones where they experience episodes of emersion (air exposure) daily as the tide rises and recedes. During episodes of emersion, the accumulation of metabolic carbon dioxide (CO2) leads to hypercapnia for many species. How this metabolic hypercapnia impacts the TGP response of marine organisms to climate change is unknown as all previous transgenerational studies have been done under subtidal conditions, where parents are constantly immersed. Here, we assess the capacity of the ecologically and economically important oyster, Saccostrea glomerata, to acclimate to elevated CO2 dependent on habitat, across its vertical distribution, from the subtidal to intertidal zone. Tidal habitat altered both the existing tolerance and transgenerational response of S. glomerata to elevated CO2. Overall, larvae from parents conditioned in an intertidal habitat had a greater existing tolerance to elevated CO2 than larvae from parents conditioned in a subtidal habitat, but had a lower capacity for beneficial TGP following parental exposure to elevated CO2. Our results suggest that the TGP responses of marine species will not be uniform across their distribution and highlights the need to consider the habitat of a species when assessing TGP responses to climate change stressors.

Climate change alters the haemolymph microbiome of oysters.

The wellbeing of marine organisms is connected to their microbiome. Oysters are a vital food source and provide ecological services, yet little is known about how climate change such as ocean acidification and warming will affect their microbiome. We exposed the Sydney rock oyster, Saccostrea glomerata, to orthogonal combinations of temperature (24, 28 °C) and pCO2 (400 and 1000 µatm) for eight weeks and used amplicon sequencing of the 16S rRNA (V3-V4) gene to characterise the bacterial community in haemolymph. Overall, elevated pCO2 and temperature interacted to alter the microbiome of oysters, with a clear partitioning of treatments in CAP ordinations. Elevated pCO2 was the strongest driver of species diversity and richness and elevated temperature also increased species richness. Climate change, both ocean acidification and warming, will alter the microbiome of S. glomerata which may increase the susceptibility of oysters to disease.

Heatwaves alter survival of the Sydney rock oyster, Saccostrea glomerata.

Heatwaves are an increasing threat to organisms across the globe. Marine and atmospheric heatwaves are predicted to impact sessile intertidal marine organisms, especially when exposed at low tide and unable to seek refuge. The study aimed to determine whether a simulated atmospheric heatwave will alter the survival of selectively bred families of Sydney rock oysters (Saccostrea glomerata), and whether survival is dependent on morphological and physiological traits. The survival of S. glomerata families to a simulated atmospheric heatwave varied from 25 to 60% and was not correlated with morphology or physiology. Survival may depend on the presence of genotypes that translate into molecular defenses such as heat-shock proteins and inhibitor of apoptosis proteins that provide oysters with resilience. Understanding the responses among families of oysters to heatwaves is critical if we are to restore the ecological services of oyster reefs and sustain oyster aquaculture.

Can prior exposure to stress enhance resilience to ocean warming in two oyster species?

Securing economically and ecologically significant molluscs, as our oceans warm due to climate change, is a global priority. South eastern Australia receives warm water in a strengthening East Australia Current and so resident species are vulnerable to elevated temperature and marine heat waves. This study tested whether prior exposure to elevated temperature can enhance resilience of oysters to ocean warming. Two Australian species, the flat oyster, Ostrea angasi, and the Sydney rock oyster, Saccostrea glomerata, were obtained as adults and "heat shocked" by exposure to a dose of warm water in the laboratory. Oysters were then transferred to elevated seawater temperature conditions where the thermal outfall from power generation was used as a proxy to investigate the impacts of ocean warming. Shell growth, condition index, lipid content and survival of flat oysters and condition of Sydney rock oysters were all significantly reduced by elevated seawater temperature in the field. Flat oysters grew faster than Sydney rock oysters at ambient temperature, but their growth and survival was more sensitive to elevated temperature. "Stress inoculation" by heat shock did little to ameliorate the negative effects of increased temperature, although the survival of heat-shocked flat oysters was greater than non-heat shocked oysters. Further investigations are required to determine if early exposure to heat stress can enhance resilience of oysters to ocean warming.

Climate change rapidly warms and acidifies Australian estuaries.

Climate change is impacting ecosystems worldwide. Estuaries are diverse and important aquatic ecosystems; and yet until now we have lacked information on the response of estuaries to climate change. Here we present data from a twelve-year monitoring program, involving 6200 observations of 166 estuaries along >1100 kilometres of the Australian coastline encompassing all estuary morphologies. Estuary temperatures increased by 2.16 °C on average over 12 years, at a rate of 0.2 °C year-1, with waters acidifying at a rate of 0.09 pH units and freshening at 0.086 PSU year-1. The response of estuaries to climate change is dependent on their morphology. Lagoons and rivers are warming and acidifying at the fastest rate because of shallow average depths and limited oceanic exchange. The changes measured are an order of magnitude faster than predicted by global ocean and atmospheric models, indicating that existing global models may not be useful to predict change in estuaries.

Microplastics detected in haemolymph of the Sydney rock oyster Saccostrea glomerata.

Plastic waste is ubiquitous in marine environments. Despite the sheer volume of plastic waste, it remains relatively unknown how marine invertebrates will interact with microplastics (plastic <1 mm). Microplastics (<2 µm) were ingested by the economically and ecologically significant Sydney rock oyster Saccostrea glomerata and translocated to the haemolymph, perhaps via phagocytosis. The presence of microplastics in the haemolymph indicates that filter feeding S. glomerata can ingest and accumulate microplastics which are prevalent in the environment. This research shows microplastics can enter marine molluscs and highlights the need to monitor microplastics in the marine environment and aquaculture to safeguard the seafood industry.

Copper and ocean acidification interact to lower maternal investment, but have little effect on adult physiology of the Sydney rock oyster Saccostrea glomerata.

It remains unknown how molluscs will respond to oceans which are increasingly predicted to be warmer, more acidic, and heavily polluted. Ocean acidification and trace metals will likely interact to increase the energy demands of marine organisms, especially oysters. This study tested the interactive effect of exposure to elevated pCO2 and copper on the energetic demands of the Sydney rock oyster (Saccostrea glomerata) during reproductive conditioning and determined whether there were any positive or negative effects on their offspring. Oysters were exposed to elevated pCO2 (1000 µatm) and elevated copper (Cu 50 µg L-1 [0.787 µM]) in an orthogonal design for eight weeks during reproductive conditioning. After eight weeks, energetic demands on oysters were measured including standard metabolic rate (SMR), nitrogen excretion, molar oxygen to nitrogen (O:N) ratio, and pHe of adult oysters as well as the size and total lipid content of their eggs. To determine egg viability, the gametes were collected and fertilised from adult oysters, the percentage of embryos that had reached the trochophore stage after 24 h was recorded. Elevated pCO2 caused a lower extracellular pH and there was a greater O:N ratio in adult oysters exposed to copper. While the two stressors did not interact to cause significant effects on adult physiology, they did interact to reduce the size and lipid content of eggs indicating that energy demand on adult oysters was greater when both elevated pCO2 and copper were combined. Despite the lower energy, there were no negative effects on early embryonic development. In conclusion, elevated pCO2 can interact with metals and cause greater energetic demands on oysters; in response oysters may lower maternal investment to offspring.