Selectively bred oysters can alter their biomineralization pathways,promoting resilience to environmental acidification

Commercial shellfish aquaculture is vulnerable to the impacts of ocean acidification driven by increasing carbon dioxide (CO₂) absorption by the ocean as well as to coastal acidification driven by land run off and rising sea level. These drivers of environmental acidification have deleterious effects on biomineralization. We investigated shell biomineralization of selectively bred and wild‐type families of the Sydney rock oyster Saccostrea glomerata in a study of oysters being farmed in estuaries at aquaculture leases differing in environmental acidification. The contrasting estuarine pH regimes enabled us to determine the mechanisms of shell growth and the vulnerability of this species to contemporary environmental acidification. Determination of the source of carbon, the mechanism of carbon uptake and use of carbon in biomineral formation are key to understanding the vulnerability of shellfish aquaculture to contemporary and future environmental acidification. We, therefore, characterized the crystallography and carbon uptake in the shells of S. glomerata, resident in habitats subjected to coastal acidification, using high‐resolution electron backscatter diffraction and carbon isotope analyses (as δ¹³C). We show that oyster families selectively bred for fast growth and families selected for disease resistance can alter their mechanisms of calcite crystal biomineralization, promoting resilience to acidification. The responses of S. glomerata to acidification in their estuarine habitat provide key insights into mechanisms of mollusc shell growth under future climate change conditions. Importantly, we show that selective breeding in oysters is likely to be an important global mitigation strategy for sustainable shellfish aquaculture to withstand future climate‐driven change to habitat acidification.     

The value and opportunity of restoring Australia's lost rock oyster reefs

Recognizing the historical loss of habitats and the value and opportunities for their recovery is essential for mobilizing habitat restoration as a solution for managing ecosystem function. Just 200 years ago, Sydney rock oysters (Saccostrea glomerata) formed extensive reef ecosystems along Australia's temperate east coast, but a century of intensive harvest and coastal change now confines S. glomerata to encrusting the hard‐intertidal surfaces of sheltered coastal waters. Despite the lack of natural reef recovery, there appears enormous potential for the restoration of intertidal S. glomerata ecosystems across Australia's east coast, with large anticipated benefits to water quality, shoreline protection, and coastal productivity. Yet, no subtidal reefs remain and the potential for subtidal restoration is a critical knowledge gap. Here, we synthesize historical, ecological, and aquaculture literature to describe a reference system for the traits of S. glomerata reefs to inform restoration targets, and outline the barriers to, and opportunities and methods for, their restoration. These reefs support extremely biodiverse and productive communities and can ameliorate the environmental stress experienced by associated communities. Rock oyster restoration, therefore, provides an ecosystem‐based strategy for assisting the adaptation of marine biodiversity to a changing climate and intensive human encroachment. Though an estimated 92% of S. glomerata ecosystems are lost, there remains great potential to restore these valuable and resilient ecosystems.     

Warm temperature acclimation impacts metabolism of paralytic shellfish toxins from Alexandrium minutum in commercial oysters

Species of Alexandrium produce potent neurotoxins termed paralytic shellfish toxins and are expanding their ranges worldwide, concurrent with increases in sea surface temperature. The metabolism of molluscs is temperature dependent, and increases in ocean temperature may influence both the abundance and distribution of Alexandrium and the dynamics of toxin uptake and depuration in shellfish. Here, we conducted a large‐scale study of the effect of temperature on the uptake and depuration of paralytic shellfish toxins in three commercial oysters (Saccostrea glomerata and diploid and triploid Crassostrea gigas, n = 252 per species/ploidy level). Oysters were acclimated to two constant temperatures, reflecting current and predicted climate scenarios (22 and 27 °C), and fed a diet including the paralytic shellfish toxin‐producing species Alexandrium minutum. While the oysters fed on A. minutum in similar quantities, concentrations of the toxin analogue GTX1,4 were significantly lower in warm‐acclimated S. glomerata and diploid C. gigas after 12 days. Following exposure to A. minutum, toxicity of triploid C. gigas was not affected by temperature. Generally, detoxification rates were reduced in warm‐acclimated oysters. The routine metabolism of the oysters was not affected by the toxins, but a significant effect was found at a cellular level in diploid C. gigas. The increasing incidences of Alexandrium blooms worldwide are a challenge for shellfish food safety regulation. Our findings indicate that rising ocean temperatures may reduce paralytic shellfish toxin accumulation in two of the three oyster types; however, they may persist for longer periods in oyster tissue.     

The density and spatial arrangement of the invasive oyster Crassostrea gigas determines its impact on settlement of native oyster larvae

Understanding how the density and spatial arrangement of invaders is critical to developing management strategies of pest species. The Pacific oyster, Crassostrea gigas, has been translocated around the world for aquaculture and in many instances has established wild populations. Relative to other species of bivalve, it displays rapid suspension feeding, which may cause mortality of pelagic invertebrate larvae. We compared the effect on settlement of Sydney rock oyster, Saccostrea glomerata, larvae of manipulating the spatial arrangement and density of native S. glomerata, and non‐native C. gigas. We hypothesized that while manipulations of dead oysters would reveal the same positive relationship between attachment surface area and S. glomerata settlement between the two species, manipulations of live oysters would reveal differing density‐dependent effects between the native and non‐native oyster. In the field, whether oysters were live or dead, more larvae settled on C. gigas than S. glomerata when substrate was arranged in monospecific clumps. When, however, the two species were interspersed, there were no differences in larval settlement between them. By contrast, in aquaria simulating a higher effective oyster density, more larvae settled on live S. glomerata than C. gigas. When C. gigas was prevented from suspension feeding, settlement of larvae on C. gigas was enhanced. By contrast, settlement was similar between the two species when dead. While the presently low densities of the invasive oyster C. gigas may enhance S. glomerata larval settlement in east Australian estuaries, future increases in densities could produce negative impacts on native oyster settlement. Synthesis and applications: Our study has shown that both the spatial arrangement and density of invaders can influence their impact. Hence, management strategies aimed at preventing invasive populations reaching damaging sizes should not only consider the threshold density at which impacts exceed some acceptable limit, but also how patch formation modifies this.     

The effects of elevated temperature and dissolved ρCO2 on a marine foundation species

Understanding how climate change and other environmental stressors will affect species is a fundamental concern of modern ecology. Indeed, numerous studies have documented how climate stressors affect species distributions and population persistence. However, relatively few studies have investigated how multiple climate stressors might affect species. In this study, we investigate the impacts of how two climate change factors affect an important foundation species. Specifically, we tested how ocean acidification from dissolution of CO₂ and increased sea surface temperatures affect multiple characteristics of juvenile eastern oysters (Crassostrea virginica). We found strong impacts of each stressor, but no interaction between the two. Simulated warming to mimic heat stressed summers reduced oyster growth, survival, and filtration rates. Additionally, we found that CO₂‐induced acidification reduced strength of oyster shells, which could potentially facilitate crab predation. As past studies have detected few impacts of these stressors on adult oysters, these results indicate that early life stages of calcareous marine organisms may be more susceptible to effects of ocean acidification and global warming. Overall, these data show that predicted changes in temperature and CO₂ can differentially influence direct effects on individual species, which could have important implications for the nature of their trophic interactions.     

Moderate acidification affects growth but not survival of 6-month-old oysters

Oyster populations periodically exposed to runoff from acid sulfate soils (ASS) are of depressed abundance and have fewer smaller individuals than unaffected populations, despite having similar recruitment levels to unaffected sites during dry periods. We examined how the timing and duration of exposure to ASS runoff influences the growth and survival of successfully settled oysters. We predicted that among 6-month-old oysters, growth and survival would be (1) lower among individuals continuously exposed to ASS-acidified waters than those that are episodically exposed, and (2) most negatively affected during rainfall events, which enhance transport of ASS runoff to estuaries. Six-month-old Sydney rock oysters, Saccostrea glomerata, were deployed at ASS-affected and unaffected sites within each of two south-east Australian estuaries. After 10 weeks, oysters were transplanted within and across sites in an estuary and maintained in situ for another 10 weeks. Oysters that remained for 20 weeks at ASS-affected sites grew at just over half the rate of oysters at reference sites. Oysters transplanted from acidified to reference sites grew more than oysters transplanted from reference to acidified sites or oysters that remained at reference sites. Unexpectedly, overall oyster mortality was low. Greater rainfall, and hence a lower pH, is likely to have accounted for the greater impact of acidification on growth during the second 10 weeks. Where oysters recruit to a 6-month age cohort, they may be able to tolerate subsequent, moderate, acidification events. Reduced growth during acidification periods may be offset by positive growth during intervening dry periods.     

Genetic structure and effective population size of Sydney rock oysters in eastern Australia

Oyster reef habitats are critical to coastal biodiversity and their decline has prompted restoration efforts in Australia. Knowledge gaps exist regarding the population structure and diversity of key species in these habitats. This may be critical information for the design of effective restoration programs. Sydney rock oysters (Saccostrea glomerata) are the dominant reef-forming bivalve in eastern Australia. Wild populations of S. glomerata have declined due to overharvesting, disease outbreaks, coastal development and reduced water quality. Here, we use genetic markers identified by genome-wide sequencing to investigate the genetic structure and diversity of wild Sydney rock oysters throughout their distribution in eastern Australia. We examine evidence for past population bottlenecks and spatial genetic structure associated with the East Australian Current. Analysis of 3, 400 neutral single-nucleotide polymorphisms (SNPs) revealed a single population, and an overlap with two other Saccostrea sp. at the northernmost boundary of the distribution. We detected signals of asymmetric gene flow consistent with the direction of the East Australian Current, and spatial structure patterns of limited genetic isolation by distance and spatial autocorrelation in the northern region (which experiences stronger effects of the East Australian Current) but not in the southern region of the distribution. We found no evidence of significant recent bottlenecks, with high effective population size throughout the species’ range. This information will provide a baseline against which to assess the impact of restoration projects, and guide strategies for sourcing stock for the enhancement of wild oyster populations. Our results provide a positive outlook for the resilience and adaptive capacity of Sydney rock oysters, and highlight wild populations as valuable resources for aquaculture and restoration initiatives.

     

Bacterial diversity of the digestive gland of Sydney rock oysters,Saccostrea glomerata infected with the paramyxean parasite,Marteilia sydneyi

Aims: To determine whether the infestation by the protozoan paramyxean parasite, Marteilia sydneyi, changes the bacterial community of the digestive gland of Sydney rock oysters, Saccostrea glomerata. Methods and Results: Six 16S rDNA clone libraries were established from three M. sydneyi‐infected and three un‐infected oysters. Restriction enzyme analysis followed by sequencing representative clones revealed a total of 23 different operational taxonomic units (OTUs) in un‐infected oysters, comprising the major phyla: Firmicutes, Proteobacteria, Cyanobacteria and Spirocheates, where the clone distribution was 44, 36, 7 and 5%, respectively. Close to half of the OTUs are not closely related to any other hitherto determined sequence. In contrast, S. glomerata infected by M. sydneyi had only one OTU present in the digestive gland. Phylogenetic analysis of the 16S rDNA sequence reveals that this dominant OTU, belonging to the α‐Proteobacteria, is closely related to a Rickettsiales‐like prokaryote (RLP). Conclusions: The microbiota of the digestive gland of Sydney rock oysters is changed by infection by M. sydneyi, becoming dominated by a RLP, and generally less diverse. The bacterial community of un‐infected S. glomerata differs from previous studies in that we identified the dominant taxa as Firmicutes and α‐Proteobacteria, rather than heterotrophic γ‐Proteobacteria. Significance and Impact of the Study: This is the first culture‐independent study of the microbiota of the digestive glands of edible oysters to the species level. The commercial viability of the Sydney rock oyster industry in Australia is currently threatened by Queensland Unknown disease and the changes in the bacterial community of S. glomerata corresponding with infection by M. sydneyi sheds further light on the link between parasite infection and mortality in this economically damaging disease.     

Proteomic clues to the identification of QX disease-resistance biomarkers in selectively bred Sydney rock oysters,Saccostrea glomerata

The Sydney rock oyster, Saccostrea glomerata, is susceptible to infection by the protozoan parasite, Marteilia sydneyi, the causative agent of QX disease. M. sydneyi infection peaks during summer when QX disease can cause up to 95% mortality. The current study takes a proteomic approach using 2-dimensional electrophoresis and mass spectrometry to identify markers of QX disease resistance among Sydney rock oysters. Proteome maps were developed for QX disease-resistant and -susceptible oysters. Six proteins in those maps were clearly associated with resistance and so were characterized by mass spectrometry. Two of the proteins (p9 and p11) were homologous to superoxide dismutase-like molecules from the Pacific oyster, Crassostrea gigas, and the Eastern oyster, Crassostrea virginica. The remaining S. glomerata proteins had no obvious similarities to known molecules in sequence databases. p9 and p11 are currently being investigated as potential markers for the selective breeding of QX disease-resistant oysters.     

Ecological interactions in the provision of habitat by urban development: whelks and engineering by oysters on artificial seawalls

Abstract Increases in human population cause increased urbanization of most habitats, including the shoreline. This has many consequences for coastal environments, in particular the trend for artificial structures, such as seawalls, to replace natural habitats. Seawalls and natural shores support many of the common intertidal species, but others important on rocky shores are absent from or rare on many seawalls. The whelk Morula marginalba Blainville is an abundant and important predator on rocky shores of south‐eastern Australia, but is infrequently recorded on artificial substrata. In Sydney Harbour, where the Sydney rock oyster (Saccostrea glomerata Gould) was locally abundant, densities of M. marginalba on some seawalls appeared to be similar to those on rocky shores and to be larger than where there were few oysters. We sampled densities and sizes of whelks in four habitats, predicting and corroborating that: (i) on seawalls with many oysters, there would be more whelks than on seawalls with few oysters; (ii) where there are many oysters, densities of whelks would be similar on seawalls and rocky shores; and (iii) whelks would be larger where oysters were abundant. Growth and survival of whelks were measured to test hypotheses from the observed differences in size and density. Survival was greater in habitats with many oysters, which could explain differences in density, but size‐specific differences in survival could not explain differences in size among habitats. On seawalls but not on rocky shores, slower growth could explain the smaller size of whelks where there were few oysters. Seawalls provide important habitat for M. marginalba, but only via their indirect effects, mediated by oysters. These interactions cannot be predicted from those on natural rocky shores. Predicting how developed areas provide suitable habitat, either in management of conservation or in assessments of potential impacts clearly depends on understanding the roles of biogenic habitats.     

Predation by the endemic whelk Tenguella marginalba (Blainville, 1832) on the invasive Pacific oyster Crassostrea gigas (Thunberg, 1793)

The endemic mulberry whelk (Tenguella marginalba) is a common predator on Australian intertidal rocky shores. The introduced Pacific oyster (Crassostrea gigas), found within the natural range of T. marginalba, is potential prey for the whelk. In experiments designed to increase our understanding of predatory behaviour by the whelk on oysters, we found that adult T. marginalba detected C. gigas and increased movement in the presence of oyster prey. Tenguella marginalba showed a preference for smaller C. gigas, but consumed oysters up to 60?mm in shell height. To access oyster flesh, whelks used their radula to drill holes in the oyster’s shell. These holes were on average 0.68?±?0.09?mm in diameter, most frequently located central to the pericardial cavity on the right (upper) valve. Predation was greatest when predator and prey were both submerged, but was unaffected by a diurnal light cycle. When offered a choice among the native Sydney rock oysters (Saccostrea glomerata), mussels (Trichomya hirsuta) or the invasive C. gigas, whelks displayed no preference among prey. We conclude that the invasive oyster C. gigas represents a viable food source for T. marginalba, which may help to slow the spread of this invasive oyster throughout eastern Australia.     

Microsatellite markers for the Sydney rock oyster,Saccostrea glomerata,a commercially important bivalve in southeastern Australia

The Sydney rock oyster (Saccostrea glomerata) is a commercially important bivalve in southeastern Australian. We describe the isolation and characterization of nine microsatellite markers for S. glomerata. The loci are highly polymorphic, with between five and 20 alleles identified among 30 individuals. Expected heterozygosity levels ranged from 0.608 to 0.936. The markers will be used to study natural dispersal, translocations and population structure. We will also use the microsatellites to test the genetic effects of QX disease on oyster populations. This infectious parasitic disease has decimated S. glomerata productivity in a number of areas over the past few decades.     

Differential proteomic responses of selectively bred and wild‐type Sydney rock oyster populations exposed to elevated CO2

Previous work suggests that larvae from Sydney rock oysters that have been selectively bred for fast growth and disease resistance are more resilient to the impacts of ocean acidification than nonselected, wild‐type oysters. In this study, we used proteomics to investigate the molecular differences between oyster populations in adult Sydney rock oysters and to identify whether these form the basis for observations seen in larvae. Adult oysters from a selective breeding line (B2) and nonselected wild types (WT) were exposed for 4 weeks to elevated pCO₂ (856 μatm) before their proteomes were compared to those of oysters held under ambient conditions (375 μatm pCO₂). Exposure to elevated pCO₂ resulted in substantial changes in the proteomes of oysters from both the selectively bred and wild‐type populations. When biological functions were assigned, these differential proteins fell into five broad, potentially interrelated categories of subcellular functions, in both oyster populations. These functional categories were energy production, cellular stress responses, the cytoskeleton, protein synthesis and cell signalling. In the wild‐type population, proteins were predominantly upregulated. However, unexpectedly, these cellular systems were downregulated in the selectively bred oyster population, indicating cellular dysfunction. We argue that this reflects a trade‐off, whereby an adaptive capacity for enhanced mitochondrial energy production in the selectively bred population may help to protect larvae from the effects of elevated CO₂, whilst being deleterious to adult oysters.     

The effect of ocean acidification and temperature on the fertilization and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850)

This study investigated the synergistic effects of ocean acidification (caused by elevations in the partial pressure of carbon dioxide pCO₂) and temperature on the fertilization and embryonic development of the economically and ecologically important Sydney rock oyster, Saccostrea glomerata (Gould 1850). As pCO₂ increased, fertilization significantly decreased. The temperature of 26 °C was the optimum temperature for fertilization, as temperature increased and decreased from this optimum, fertilization decreased. There was also an effect of pCO₂ and temperature on embryonic development. Generally as pCO₂ increased, the percentage and size of D‐veligers decreased and the percentage of D‐veligers that were abnormal increased. The optimum temperature was 26 °C and embryonic development decreased at temperatures that were above and below this temperature. Abnormality of D‐veligers was greatest at 1000 ppm and 18 and 30 °C (≥90%) and least at 375 ppm and 26 °C (≤4%). Finally prolonged exposure of elevated pCO₂ and temperature across early developmental stages led to fewer D‐veligers, more abnormality and smaller sizes in elevated CO₂ environments and may lead to lethal effects at suboptimal temperatures. Embryos that were exposed to the pCO₂ and temperature treatments for fertilization and embryonic development had fewer D‐veligers, greater percentage of abnormality and reduced size than embryos that were exposed to the treatments for embryonic development only. Further at the elevated temperature of 30 °C and 750–1000 ppm, there was no embryonic development. The results of this study suggest that predicted changes in ocean acidification and temperature over the next century may have severe implications for the distribution and abundance of S. glomerata as well as possible implications for the reproduction and development of other marine invertebrates.     

A new mode of ammonite preservation – implications for dating of condensed phosphorite deposits

Unusual phosphatic casts of the ammonites Mortoniceras (Subschloenbachia) sp. and Stoliczkaia sp. from the upper Albian condensed phosphorite bed at Annopol, Poland, are discussed in terms of their taphonomic history. These specimens are interpreted as ‘secondary’ external casts of ammonite replicas preserved originally as attachment scars on oyster shells. The following genetic history is suggested for this previously undocumented mode of ammonite preservation: (1) settling of shells of dead ammonites on the seafloor; (2) colonization of these shells by oysters and formation of ammonite replicas on left valves of oysters; (3) dissolution of ammonite shells; (4) reworking and fragmentation of oyster shells; (5) casting of ammonite replicas by phosphatic material; and (6) separation of ammonite casts from oyster shells, either through mechanical disintegration or dissolution of the latter. The specimens studied were formed after dissolution of the ammonite conchs, not prior to this event as in the case of typical ammonite steinkerns (internal moulds). Therefore, they are here referred to as ‘pseudo‐steinkerns’. The time interval between loss of the original ammonite shells and the formation of oyster‐mediated pseudo‐steinkerns may be very extensive. Therefore, the pseudo‐steinkerns may potentially mislead in biostratigraphic dating of condensed phosphorite deposits.     

Chemical stimuli in coral reefs: how butterflyfishes find their food

Animals use sensory stimuli either to assess and select habitats, mates or food, as well as for communication. The present study aimed to understand the behavioural processes enabling several Chaetodon species (butterflyfishes) to locate one of their food sources (epibionts present on pearl oyster shells) at Rangiroa atoll (French Polynesia). Among the five species tested, our 2-channel choice flume chamber experiments identified three species that were attracted to their food source by chemical stimuli. HPLC experiments showed that pearl oysters and epibionts have specific and unique chemical fingerprints, either one or nine specific peaks, respectively. Overall, chemical stimuli are emitted by both epibionts (used directly by Chaetodon auriga, C. lunula and C. citrinellus) and live pearl oysters (used indirectly by C. auriga and C. lunula) to locate their food source. Biosynthesis of these chemical stimuli could be used to artificially attract butterflyfishes to pearl oyster rearing stations in order to increase the natural cleaning of pearl oyster shells and thus reduce one large cost for this aquaculture.     

Defining CO2 and O2 syndromes of marine biomes in the Anthropocene

Research efforts have intensified to foresee the prospects for marine biomes under climate change and anthropogenic drivers over varying temporal and spatial scales. Parallel with these efforts is the utilization of terminology, such as ‘ocean acidification’ (OA) and ‘ocean deoxygenation’ (OD), that can foster rapid comprehension of complex processes driving carbon dioxide (CO₂) and oxygen (O₂) concentrations in the global ocean and thus, are now widely used in discussions within and beyond academia. However, common usage of the terms ‘acidification’ and ‘deoxygenation’ alone are subjective and, without adequate contextualization, have the potential to mislead inferences over drivers that may ultimately shape the future state of marine ecosystems. Here we clarify the usage of the terms OA and OD as global, climate change‐driven processes and discuss the various attributes of elevated CO₂ and reduced O₂ syndromes common to coastal ecosystems. We support the use of the existing terms ‘coastal acidification’ and ‘coastal deoxygenation’ because they help differentiate the sometimes rapid and extreme nature of CO₂ and O₂ syndromes in coastal ecosystems from the global, climate change‐driven processes of OA and OD. Given the complexity and breadth of the processes involved in altering CO₂ and O₂ concentrations across marine ecosystems, we provide a workflow to enable contextualization and clarification of the usage of existing terms and highlight the close link between these two gases across spatial and temporal scales in the ocean. These distinctions are crucial to guide effective communication of research within the scientific community and guide policymakers responsible for intervening on the drivers to secure desirable future ocean states.