Laura M. Parker

Predicting the Response of Molluscs to the Impact of Ocean Acidification

Elevations in atmospheric carbon dioxide (CO2) are anticipated to acidify oceans because of fundamental changes in ocean chemistry created by CO2 absorption from the atmosphere. Over the next century, these elevated concentrations of atmospheric CO2 are expected to result in a reduction of the surface ocean waters from 8.1 to 7.7 units as well as a reduction in carbonate ion (CO32−) concentration. The potential impact that this change in ocean chemistry will have on marine and estuarine organisms and ecosystems is a growing concern for scientists worldwide. While species-specific responses to ocean acidification are widespread across a number of marine taxa, molluscs are one animal phylum with many species which are particularly vulnerable across a number of life-history stages. Molluscs make up the second largest animal phylum on earth with 30,000 species and are a major producer of CaCO3. Molluscs also provide essential ecosystem services including habitat structure and food for benthic organisms (i.e., mussel and oyster beds), purification of water through filtration and are economically valuable. Even sub lethal impacts on molluscs due to climate changed oceans will have serious consequences for global protein sources and marine ecosystems.

Persistence of positive carryover effects in the oyster, Saccostrea glomerata, following transgenerational exposure to ocean acidification

Ocean acidification (OA) is predicted to have widespread implications for marine organisms, yet the capacity for species to acclimate or adapt over this century remains unknown. Recent transgenerational studies have shown that for some marine species, exposure of adults to OA can facilitate positive carryover effects to their larval and juvenile offspring that help them to survive in acidifying oceanic conditions. But whether these positive carryover effects can persist into adulthood or the next generation is unknown. Here we tested whether positive carryover effects found in larvae of the oyster, Saccostrea glomerata following transgenerational exposure to elevated CO2, could persist into adulthood and whether subsequent transgenerational exposure of adults to elevated CO2 would facilitate similar adaptive responses in the next generation of larvae and juveniles. Following our previous transgenerational exposure of parental adults and first generation (F1) larvae to ambient (385 μatm) and elevated (856 μatm) CO2, newly settled F1 juveniles were transferred to the field at ambient CO2 for 14 months, until they reached reproductive maturity. At this time, the F1 adults were returned to the laboratory and the previous transgenerational CO2 exposure was repeated to produce F2 offspring. We found that the capacity of adults to regulate extracellular pH at elevated CO2 was improved if they had a prior history of transgenerational exposure to elevated CO2. In addition, subsequent transgenerational exposure of these adults led to an increase in the resilience of their larval and juvenile offspring. Offspring with a history of transgenerational exposure to elevated CO2 had a lower percentage abnormality, faster development rate, faster shell growth and increased heart rate at elevated CO2 compared with F2 offspring with no prior history of exposure to elevated CO2. Our results suggest that positive carryover effects originating during parental and larval exposure will be important in mediating some of the impacts of OA for later life-history stages and generations.

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.

Mixed Effects of Elevated pCO2 on Fertilisation, Larval and Juvenile Development and Adult Responses in the Mobile Subtidal Scallop Mimachlamys asperrima (Lamarck, 1819)

Ocean acidification is predicted to have severe consequences for calcifying marine organisms especially molluscs. Recent studies, however, have found that molluscs in marine environments with naturally elevated or fluctuating CO2 or with an active, high metabolic rate lifestyle may have a capacity to acclimate and be resilient to exposures of elevated environmental pCO2. The aim of this study was to determine the effects of near future concentrations of elevated pCO2 on the larval and adult stages of the mobile doughboy scallop, Mimachlamys asperrima from a subtidal and stable physio-chemical environment. It was found that fertilisation and the shell length of early larval stages of M. asperrima decreased as pCO2 increased, however, there were less pronounced effects of elevated pCO2 on the shell length of later larval stages, with high pCO2 enhancing growth in some instances. Byssal attachment and condition index of adult M. asperrima decreased with elevated pCO2, while in contrast there was no effect on standard metabolic rate or pHe. The responses of larval and adult M. asperrima to elevated pCO2 measured in this study were more moderate than responses previously reported for intertidal oysters and mussels. Even this more moderate set of responses are still likely to reduce the abundance of M. asperrima and potentially other scallop species in the world’s oceans at predicted future pCO2 levels.

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

ABSTRACT 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. Highlighted Article: Intertidal oysters are more vulnerable to ocean acidification than subtidal oysters, and this may limit their vertical distribution.

Adult exposure to ocean acidification is maladaptive for larvae of the Sydney rock oyster Saccostrea glomerata in the presence of multiple stressors

Parental effects passed from adults to their offspring have been identified as a source of rapid acclimation that may allow marine populations to persist as our surface oceans continue to decrease in pH. Little is known, however, whether parental effects are beneficial for offspring in the presence of multiple stressors. We exposed adults of the oyster Saccostrea glomerata to elevated CO2 and examined the impacts of elevated CO2 (control = 392; 856 µatm) combined with elevated temperature (control = 24; 28°C), reduced salinity (control = 35; 25) and reduced food concentration (control = full; half diet) on their larvae. Adult exposure to elevated CO2 had a positive impact on larvae reared at elevated CO2 as a sole stressor, which were 8% larger and developed faster at elevated CO2 compared with larvae from adults exposed to ambient CO2. These larvae, however, had significantly reduced survival in all multistressor treatments. This was particularly evident for larvae reared at elevated CO2 combined with elevated temperature or reduced food concentration, with no larvae surviving in some treatment combinations. Larvae from CO2-exposed adults had a higher standard metabolic rate. Our results provide evidence that parental exposure to ocean acidification may be maladaptive when larvae experience multiple stressors.

Rapid transcriptional acclimation following transgenerational exposure of oysters to ocean acidification.

Marine organisms need to adapt in order to cope with the adverse effects of ocean acidification and warming. Transgenerational exposure to CO2 stress has been shown to enhance resilience to ocean acidification in offspring from a number of species. However, the molecular basis underlying such adaptive responses is currently unknown. Here, we compared the transcriptional profiles of two genetically distinct oyster breeding lines following transgenerational exposure to elevated CO2 in order to explore the molecular basis of acclimation or adaptation to ocean acidification in these organisms. The expression of key target genes associated with antioxidant defence, metabolism and the cytoskeleton was assessed in oysters exposed to elevated CO2 over three consecutive generations. This set of target genes was chosen specifically to test whether altered responsiveness of intracellular stress mechanisms contributes to the differential acclimation of oyster populations to climate stressors. Transgenerational exposure to elevated CO2 resulted in changes to both basal and inducible expression of those key target genes (e.g. ecSOD, catalase and peroxiredoxin 6), particularly in oysters derived from the disease‐resistant, fast‐growing B2 line. Exposure to CO2 stress over consecutive generations produced opposite and less evident effects on transcription in a second population that was derived from wild‐type (nonselected) oysters. The analysis of key target genes revealed that the acute responses of oysters to CO2 stress appear to be affected by population‐specific genetic and/or phenotypic traits and by the CO2 conditions to which their parents had been exposed. This supports the contention that the capacity for heritable change in response to ocean acidification varies between oyster breeding lines and is mediated by parental conditioning.

Populations of Pacific Oysters Crassostrea gigas Respond Variably to Elevated CO2 and Predation by Morula marginalba

Ocean acidification is anticipated to decrease calcification and increase dissolution of shelled molluscs. Molluscs with thinner and weaker shells may be more susceptible to predation, but not all studies have measured negative responses of molluscs to elevated pCO2. Recent studies measuring the response of molluscs have found greater variability at the population level than first expected. Here we investigate the impact of acidification on the predatory whelk Morula marginalba and genetically distinct subpopulations of the Pacific oyster Crassostrea gigas. Whelks and eight family lines of C. gigas were separately exposed to ambient (385 ppm) and elevated (1000 ppm) pCO2 for 6 weeks. Following this period, individuals of M. marginalba were transferred into tanks with oysters at ambient and elevated pCO2 for 17 days. The increase in shell height of the oysters was on average 63% less at elevated compared to ambient pCO2. There were differences in shell compression strength, thickness, and mass among family lines of C. gigas, with sometimes an interaction between pCO2 and family line. Against expectations, this study found increased shell strength in the prey and reduced shell strength in the predator at elevated compared to ambient pCO2. After 10 days, the whelks consumed significantly more oysters regardless of whether C. gigas had been exposed to ambient or elevated CO2, but this was not dependent on the family line and the effect was not significant after 17 days. Our study found an increase in predation after exposure of the predator to predicted near-future levels of estuarine pCO2.

Ocean acidification narrows the acute thermal and salinity tolerance of the Sydney rock oyster Saccostrea glomerata

Coastal and estuarine environments are characterised by acute changes in temperature and salinity. Organisms living within these environments are adapted to withstand such changes, yet near-future ocean acidification (OA) may challenge their physiological capacity to respond. We tested the impact of CO2-induced OA on the acute thermal and salinity tolerance, energy metabolism and acid-base regulation capacity of the oyster Saccostrea glomerata. Adult S. glomerata were acclimated to three CO2 levels (ambient 380μatm, moderate 856μatm, high 1500μatm) for 5weeks (24°C, salinity 34.6) before being exposed to a series of acute temperature (15-33°C) and salinity (34.2-20) treatments. Oysters acclimated to elevated CO2 showed a significant metabolic depression and extracellular acidosis with acute exposure to elevated temperature and reduced salinity, especially at the highest CO2 of 1500μatm. Our results suggest that the acute thermal and salinity tolerance of S. glomerata and thus its distribution will reduce as OA continues to worsen.

Transcriptomic profiling of adaptive responses to ocean acidification

Some populations of marine organisms appear to have inherent tolerance or the capacity for acclimation to stressful environmental conditions, including those associated with climate change. Sydney rock oysters from the B2 breeding line exhibit resilience to ocean acidification (OA) at the physiological level. To understand the molecular basis of this physiological resilience, we analysed the gill transcriptome of B2 oysters that had been exposed to near‐future projected ocean pH over two consecutive generations. Our results suggest that the distinctive performance of B2 oysters in the face of OA is mediated by the selective expression of genes involved in multiple cellular processes. Subsequent high‐throughput qPCR revealed that some of these transcriptional changes are exclusive to B2 oysters and so may be associated with their resilience to OA. The intracellular processes mediated by the differentially abundant genes primarily involve control of the cell cycle and maintenance of cellular homeostasis. These changes may enable B2 oysters to prevent apoptosis resulting from oxidative damage or to alleviate the effects of apoptosis through regulation of the cell cycle. Comparative analysis of the OA conditioning effects across sequential generations supported the contention that B2 and wild‐type oysters have different trajectories of changing gene expression and responding to OA. Our findings reveal the broad set of molecular processes underlying transgenerational conditioning and potential resilience to OA in a marine calcifier. Identifying the mechanisms of stress resilience can uncover the intracellular basis for these organisms to survive and thrive in a rapidly changing ocean.