Posts Tagged 'mollusks'

Ocean acidification affects the bioenergetics of marine mussels as revealed by high-coverage quantitative metabolomics

Graphical abstract.


  • The metabolic response of mussels to acidification was evaluated.
  • Acidification decreased energy storage and increased energy demands.
  • Acidification affected amino acid metabolism and biosynthesis.
  • Carry-over effects of acidification on cellular energy allocation were observed.


Ocean acidification has become a major ecological and environmental problem in the world, whereas the impact mechanism of ocean acidification in marine bivalves is not fully understood. Cellular energy allocation (CEA) approach and high-coverage metabolomic techniques were used to investigate the acidification effects on the energy metabolism of mussels. The thick shell mussels Mytilus coruscus were exposed to seawater pH 8.1 (control) and pH 7.7 (acidification) for 14 days and allowed to recover at pH 8.1 for 7 days. The levels of carbohydrates, lipids and proteins significantly decreased in the digestive glands of the mussels exposed to acidification. The 14-day acidification exposure increased the energy demands of mussels, resulting in increased electron transport system (ETS) activity and decreased cellular energy allocation (CEA). Significant carry-over effects were observed on all cellular energy parameters except the concentration of carbohydrates and cellular energy demand (Ec) after 7 days of recovery. Metabolomic analysis showed that acidification affected the phenylalanine, tyrosine and tryptophan biosynthesis, taurine and hypotaurine metabolism, and glycine, serine and threonine metabolism. Correlation analysis showed that mussel cell energy parameters (carbohydrates, lipids, proteins, CEA) were negatively/positively correlated with certain differentially abundant metabolites. Overall, the integrated biochemical and metabolomics analyses demonstrated the negative effects of acidification on energy metabolism at the cellular level and implicated the alteration of biosynthesis and metabolism of amino acids as a mechanism of metabolic perturbation caused by acidification in mussels.

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Sex and gametogenesis stage are strong drivers of gene expression in Mytilus edulis exposed to environmentally relevant plasticiser levels and pH 7.7

Plastic pollution and changes in oceanic pH are both pressing environmental issues. Little emphasis, however, has been placed on the influence of sex and gametogenesis stage when investigating the effects of such stressors. Here, we examined histology and molecular biomarkers of blue mussels Mytilus edulis exposed for 7 days to a pH 7.7 scenario (− 0.4 units) in combination with environmentally relevant concentrations (0, 0.5 and 50 µg/L) of the endocrine disrupting plasticiser di-2-ethylhexyl phthalate (DEHP). Through a factorial design, we investigated the gametogenesis cycle and sex-related expression of genes involved in pH homeostasis, stress response and oestrogen receptor-like pathways after the exposure to the two environmental stressors. As expected, we found sex-related differences in the proportion of developing, mature and spawning gonads in histological sections. Male gonads also showed higher levels of the acid–base regulator CA2, but females had a higher expression of stress response-related genes (i.e. sodcathsp70). We found a significant effect of DEHP on stress response-related gene expression that was dependent on the gametogenesis stage, but there was only a trend towards downregulation of CA2 in response to pH 7.7. In addition, differences in gene expression between males and females were most pronounced in experimental conditions containing DEHP and/or acidified pH but never the control, indicating that it is important to consider sex and gametogenesis stage when studying the response of mussels to diverse stressors.

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Calmodulin regulates the calcium homeostasis in mantle of Crassostrea gigas under ocean acidification

The biosynthesis of shell is a complicated calcification process in the marine bivalve, which can be severely impacted by ocean acidification (OA). Calmodulin (CaM) is a pivotal calcium regulator and thought to be crucial for calcification. In the present study, a CaM (designated CgCaM) with calcium-binding activity was identified from the Pacific oyster Crassostrea gigas with the objective to understand its possible role in the regulation of calcium homeostasis under acidification treatment. The open reading frame (ORF) of CgCaM was of 474 bp encoding a 17.5 kDa protein with four continuous EF-hand domains. CgCaM shared high similarity with CaMs from other invertebrates and vertebrates. The mRNA transcript of CgCaM was constitutively expressed in all detected tissues with the higher expression level in mantle, especially highest in the middle fold of the three folds of mantle. CgCaM was found to be mainly distributed in the mantle epithelium. When the oysters were exposed to acidified seawater, the expression level of CgCaM in the middle fold of mantle and the content of Ca2+ in this fold both decreased significantly. These results collectively suggested that CgCaM was involved in the regulation of calcium homeostasis in the middle fold of mantle under acidification treatment.

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Intestinal microbiota perturbations in the gastropod Trochus niloticus concurrently exposed to ocean acidification and environmentally relevant concentrations of sulfamethoxazole

Graphical abstract.


  • Exposure to OA leads to the microbiota dysbiosis in the intestine of T. niloticus.
  • Exposure to SMX barely affected the intestinal microbiota of T. niloticus.
  • Exposure to SMX accelerated spread of sulfonamide ARGs.


Ocean acidification (OA) and antibiotic pollution pose severe threats to the fitness of keystone species in marine ecosystems. However, the combined effects of OA and antibiotic pollution on the intestinal microbiota of marine organisms are still not well known. In this study, we exposed the herbivorous gastropod Trochus niloticus, a keystone species to maintains the stability of coral reef ecosystems, to acidic seawater (pH 7.6) and/or sulfamethoxazole (SMX, 100 ng/L, 1000 ng/L) for 28 days and determined their impacts on (1) the accumulation of SMX in the intestine of T. niloticus; (2) the characteristics of the intestinal microbiota in T. niloticus; (3) the relative abundances of sulfonamide resistance genes (i.e., sul1 and sul2) and intI1 in the intestinal microbiota of T. niloticus. Our results show that OA exposure leads to dramatic microbiota dysbiosis in the intestine of T. niloticus, including changes in bacterial community diversity and structure, decreased abundances of dominant species, existences of characteristic taxa, and altered functional predictions. In addition, SMX exposure at environmentally relevant concentrations had little effect on the intestinal microbiota of T. niloticus, whether in isolation or in combination with OA. However, after exposure to the higher SMX concentration (1000 ng/L), the accumulation of SMX in the intestine of T. niloticus could induce an increase in the copies of sul2 in the intestinal microbiota. These results suggest that the intestinal health of T. niloticus might be affected by OA and SMX, which might lead to fitness loss of the keystone species in coral reef ecosystems.

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Impacts of seawater pH buffering on the larval microbiome and carry-over effects on later-life disease susceptibility in Pacific oysters

Ocean acidification upwelling events and the resulting lowered aragonite saturation state of seawater have been linked to high mortality of marine bivalve larvae in hatcheries. Major oyster seed producers along North America’s west coast have mitigated impacts via seawater pH buffering (e.g., addition of soda ash). However, little consideration has been given to whether such practice may impact the larval microbiome, with potential carry-over effects on immune competency and disease susceptibility in later-life stages. To investigate possible impacts, Pacific oysters (Crassostrea gigas) were reared under soda ash pH buffered or ambient pH seawater conditions for the first 24 h of development. Both treatment groups were then reared under ambient pH conditions for the remainder of the developmental period. Larval microbiome, immune status (via gene expression), growth, and survival were assessed throughout the developmental period. Juveniles and adults arising from the larval run were then subjected to laboratory-based disease challenges to investigate carry-over effects. Larvae reared under buffered conditions showed an altered microbiome, which was still evident in juvenile animals. Moreover, reduced survival was observed in both juveniles and adults of the buffered group under a simulated marine heatwave and Vibrio exposure compared with those reared under ambient conditions. Results suggest that soda ash pH buffering during early development may compromise later-life stages under stressor conditions, and illustrate the importance of a long-view approach with regard to hatchery husbandry practices and climate change mitigation.

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Could acidified environments intensify illicit drug effects on the reproduction of marine mussels?

The increasing oceanic uptake is a direct response to the increasing atmospheric burden of CO2. Oceans are experiencing both physical and biogeochemical changes. This increase in CO2 hosts in oceans promotes changes in pH and seawater chemistry that can modify the speciation of compounds, largely due to dependent element speciation on physicochemical parameters (salinity, pH, and redox potential). So, ocean acidification can trigger enhanced toxicity of illicit drugs to non-target marine organisms due to the combined effects of crack cocaine and low pH (from 8.3 to 7.0 pH values) on the reproduction of the marine mussel Perna perna. Fertilization rate and embryo–larval development were used as endpoints to assess the effects of crack-cocaine concentrations (6.25, 12.5, 25, 50, and 100 mg L−1) and its association with pH values variation (8.3, 8.0, 7.5, and 7.0). The IC50 was calculated from the results of an embryo–larval assay in different methods of acidification (CO2 and HCl), which evidenced that HCl treatment was more toxic than CO2 treatment for the same drug concentrations. Results showed that the gametes of P. perna react to acidification when exposed to crack-cocaine concentration and pH reductions.

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Life-history traits in the Pacific oyster Crassostrea gigas are robust to ocean acidification under two thermal regimes

Ocean acidification and warming (OAW) are pressing contemporary issues affecting marine life and specifically calcifying organisms. Here, we investigated the direct effects of OAW on life-history traits of the Pacific oyster Crassostrea gigas, the most cultivated bivalve species worldwide. We also tested whether parental conditioning history shaped the phenotypic characters of their progenies (intergenerational carryover effects). Adult oysters and their offspring were exposed to two temperatures (18°C, +3°C) under ambient pH conditions or under an end-of-century acidification scenario (−0.33 pH unit). In adults, we monitored standard biometric and reproductive parameters, stress response by quantifying neuroendocrine metabolites and gamete quality. In larvae, we measured hatching rate, size, biochemical quality, and behavior. We found that reducing pH reduced growth rate and activated the serotonin system, but increasing temperature attenuated these effects. There was no effect of pH on reproduction at either temperature, and no intergenerational carryover effects. Larval characteristics were similar between treatments, regardless of parental conditioning history. Thus, the Pacific oyster seems robust to changes in pH, and increasing temperature is not an aggravating factor. We emphasize that the use of neuroendocrine indicators holds promise for revealing sublethal impacts of environmental changes.

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High sclerobiont calcification in marginal reefs of the eastern tropical Pacific

Graphical abstract.

A sclerobiont is any organism capable of fouling hard substrates. Sclerobionts have recently received attention due to their notable calcium carbonate contributions to reef structures and potential to offset drops in carbonate budgets in degraded reefs. However, due to their encrusting nature, it is difficult to quantify net calcium carbonate production at the level of individual taxonomic groups, and knowledge regarding the main environmental factors that regulate their spatial distributions is limited. In addition, the material types used to create experimental substrates, their orientations, and their overall deployment times can influence settlement and the composition of the resulting communities. Thus, comparative evaluations of these variables are necessary to improve future research efforts. In this study, we used calcification accretion units (CAUs) to quantify the calcium carbonate contributions of sclerobionts at the taxonomic group level and evaluated the effects of two frequently used materials [i.e., polyvinyl chloride (PVC) and terracotta (TCT) tiles] on the recruitment and calcification of the sclerobiont community in the tropical Mexican Pacific and the Midriff Island Region of the Gulf of California over 6 and 15 months [n = 40; 5 CAUs x site (2) x deployment time (2) x material type (2)]. The net sclerobiont calcification rate (mean ± SD) reached maximum values at six months and was higher in the Mexican Pacific (2.15 ± 0.99 kg m−2 y−1) than in the Gulf of California (1.70 ± 0.67 kg m−2 y−1). Moreover, the calcification rate was slightly higher on the PVC-CAUs compared to that of the TCT-CAUs, although these differences were not consistent at the group level. In addition, cryptic microhabitats showed low calcification rates when compared to those of exposed microhabitatsCrustosecoralline algae and barnacles dominated the exposed experimental surfaces, while bryozoans, mollusks, and serpulid polychaetes dominated cryptic surfaces. Regardless of the site, deployment time, or material type, barnacles made the greatest contributions to calcimass production (between 41 and 88%). Our results demonstrate that the orientation of the experimental substrate, and the material to a lesser extent, influence the sclerobiont community and the associated calcification rate. Upwelling-induced surface nutrient levels, low pH levels, and the aragonite saturation state (ΩAr) limit the early cementation of reef-building organisms in the tropical Mexican Pacific and promote high bioerosion rates in corals of the Gulf of California. Our findings demonstrate that sclerobionts significantly contribute to calcium carbonate production even under conditions of high environmental variability.

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Epigenetic-associated phenotypic plasticity of the ocean acidification-acclimated edible oyster in the mariculture environment

For marine invertebrates with pelagic-benthic life cycle, larval exposure to ocean acidification (OA) can affect adult performance in response to another environmental stressor. This carry-over effect has the potential to alter phenotypic traits. However, molecular mechanisms that mediate “OA” triggered carry-over effects have not been explored despite such information being key to improve species fitness and management strategies for aquafarming. This study integrated genome-wide DNA methylome and transcriptome to examine epigenetic modification-mediated carry-over OA impacts on phenotypic traits of the ecologically and commercially important oyster species Crassostrea hongkongensis under field conditions. Larvae of C. hongkongensis were exposed to control pH8.0 and low pH7.4 conditions mimicking OA scenario before being outplanted as post-metamorphic juveniles at two mariculture field sites with contrasting environmental stressors for nine months. The larval carry-over OA effect was found to have persistent impacts on the growth and survival trade-off traits on the outplanted juveniles, although the beneficial or adverse effect depended on the environmental conditions at the outplanted sites. The site-specific plasticity was demonstrated with a diverse DNA methylation-associated gene expression profile, with signal transduction and endocrine system being the most common and highly enriched functions. The highly methylated exons prevailed in the key genes related to general metabolic and endocytic responses and these genes are evolutionarily conserved in various marine invertebrates in response to OA. These results suggest that oysters with prior larval exposure history to OA had the capability to trigger rapid local adaptive responses via epigenetic modification to cope with multiple stressors in field.

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Ocean acidification modifies behaviour of shelf seabed macrofauna: a laboratory study on two ecosystem engineers, Abra alba and Lanice conchilega

The feeding activity and burrow ventilation by benthic invertebrates importantly affect the biodiversity and functioning of seafloor sediments. Here we investigated how ocean acidification can modify these behavioural activities in two common and abundant macrofaunal ecosystem engineering species in temperate continental shelf communities: the white furrow shell Abra alba and the sand mason Lanice conchilega. Using time-lapse imagery and sediment porewater hydraulic signatures we show that both species adapt their behaviour in response to predicted future pH conditions (−0.3 units). During a three-week laboratory experiment, A. alba reduced the duration per feeding event when suspension and deposit feeding (by 86 and 53%, respectively), and almost completely ceased suspension feeding under reduced seawater pH in comparison to ambient seawater pH (pH ∼ 8.2). This behavioural change reduces the intake of low pH water during feeding and respiration. L. conchilega increased its piston-pumping frequency by 30 and 52%, respectively, after one and two weeks of exposure to future pH conditions (−0.3 units) relative to ambient conditions. This change in irrigation activity suggests higher metabolic demands under low seawater pH, and also extended low water column pH conditions deeper into the seafloor. Because the distribution of other populations depends on the physicochemical setting by our focal species, we argue that the demonstrated behavioural plasticity will likely have cascading effects on seafloor diversity and functioning, highlighting the complexity of how ocean acidification, and climate change in general, will affect seafloor ecology.

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Gastropods underwent a major taxonomic turnover during the end-Triassic marine mass extinction event

Based on an exhaustive database of gastropod genera and subgenera during the Triassic–Jurassic transition, origination and extinction percentages and resulting diversity changes are calculated, with a particular focus on the end-Triassic mass extinction event. We show that gastropods suffered a loss of 56% of genera and subgenera during this event, which was higher than the average of marine life (46.8%). Among molluscs, gastropods were more strongly affected than bivalves (43.4%) but less than ammonoids, which were nearly annihilated. However, there were also pronounced differences among gastropod subclasses. The most strongly affected subclass was the Neritimorphia, which lost 72.7% of their Rhaetian genera; on the other extreme, the Heterobranchia remained nearly unaffected (11% loss). We analysed this extinction pattern with respect to larval development, palaeobiogeography, shell size, and anatomy and found that putative feeding of the pelagic larval stage, adaptation to tropical-temperate water temperatures, and flexibility of the mantle attachment were among the factors that might explain extinction resilience of heterobranchs during the end-Triassic crisis. Among molluscs, extinction magnitude roughly correlates with locomotion activity and thus metabolic rates. We suggest three potential kill mechanisms that could account for these observations: global warming, ocean acidification, and extinction of marine plankton. The end-Triassic extinction of gastropods therefore fits to proposed extinction scenarios for this event, which invoke the magmatic activity of the Central Atlantic Magmatic Province as the ultimate cause of death. With respect to gastropods, the effect of the end-Triassic mass extinction was comparable to that of the end-Permian mass extinction. Notably, Heterobranchia was relatively little affected by both events; the extinction resilience of this subclass during times of global environmental changes was therefore possibly a key aspect of their subsequent evolutionary success.

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Gadolinium ecotoxicity is enhanced in a warmer and acidified changing ocean as shown by the surf clam Spisula solida through a multibiomarker approach


  • Spisula solida accumulated Gd after just one day.
  • Climate change did not impact Gd accumulation and elimination.
  • Gd was not proficiently eliminated in 7 days.
  • Lipid peroxidation was greater in clams exposed to warming and Gd.
  • Gd showed enhanced ecotoxicity in climate change conditions.


Humans have exhaustively combusted fossil fuels, and released pollutants into the environment, at continuously faster rates resulting in global average temperature increase and seawater pH decrease. Climate change is forecasted to exacerbate the effects of pollutants such as the emergent rare earth elements. Therefore, the objective of this study was to assess the combined effects of rising temperature (Δ = + 4 °C) and decreasing pH (Δ = − 0.4 pH units) on the bioaccumulation and elimination of gadolinium (Gd) in the bioindicator bivalve species Spisula solida (Surf clam). We exposed surf clams to 10 µg L−1 of GdCl3 for seven days, under warming, acidification, and their combination, followed by a depuration phase lasting for another 7 days and investigated the Gd bioaccumulation and oxidative stress-related responses after 1, 3 and 7 days of exposure and the elimination phase. Gadolinium accumulated after just one day with values reaching the highest after 7 days. Gadolinium was not eliminated after 7 days, and elimination is further hampered under climate change scenarios. Warming and acidification, and their interaction did not significantly impact Gd concentration. However, there was a significant interaction on clam’s biochemical response. The augmented total antioxidant capacity and lipid peroxidation values show that the significant impacts of Gd on the oxidative stress response are enhanced under warming while the increased superoxide dismutase and catalase values demonstrate the combined impact of Gd, warming & acidification. Ultimately, lipid damage was greater in clams exposed to warming & Gd, which emphasizes the enhanced toxic effects of Gd in a changing ocean.

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Ocean acidification does not overlook sex: review of understudied effects and implications of low pH on marine invertebrate sexual reproduction

Sexual reproduction is a fundamental process essential for species persistence, evolution, and diversity. However, unprecedented oceanographic shifts due to climate change can impact physiological processes, with important implications for sexual reproduction. Identifying bottlenecks and vulnerable stages in reproductive cycles will enable better prediction of the organism, population, community, and global-level consequences of ocean change. This article reviews how ocean acidification impacts sexual reproductive processes in marine invertebrates and highlights current research gaps. We focus on five economically and ecologically important taxonomic groups: cnidarians, crustaceans, echinoderms, molluscs and ascidians. We discuss the spatial and temporal variability of experimental designs, identify trends of performance in acidified conditions in the context of early reproductive traits (gametogenesis, fertilization, and reproductive resource allocation), and provide a quantitative meta-analysis of the published literature to assess the effects of low pH on fertilization rates across taxa. A total of 129 published studies investigated the effects of ocean acidification on 122 species in selected taxa. The impact of ocean acidification is dependent on taxa, the specific reproductive process examined, and study location. Our meta-analysis reveals that fertilization rate decreases as pH decreases, but effects are taxa-specific. Echinoderm fertilization appears more sensitive than molluscs to pH changes, and while data are limited, fertilization in cnidarians may be the most sensitive. Studies with echinoderms and bivalve molluscs are prevalent, while crustaceans and cephalopods are among the least studied species even though they constitute some of the largest fisheries worldwide. This lack of information has important implications for commercial aquaculture, wild fisheries, and conservation and restoration of wild populations. We recommend that studies expose organisms to different ocean acidification levels during the entire gametogenic cycle, and not only during the final stages before gametes or larvae are released. We argue for increased focus on fundamental reproductive processes and associated molecular mechanisms that may be vulnerable to shifts in ocean chemistry. Our recommendations for future research will allow for a better understanding of how reproduction in invertebrates will be affected in the context of a rapidly changing environment.

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Exposure of commercially exploited shellfish to changing pH levels: how to scale-up experimental evidence to regional impacts

Ocean acidification has become one of the most intensively studied climate change topics and it is expected to have both direct and indirect impacts on species, ecosystems, and economies. Experiments have been performed on different taxa, life stages, and at different pH levels. Despite this wealth of information, several key challenges remain, including (1) uncertainty about how to incorporate current pH ranges and variability experienced by organisms into experiments, and (2) how to bring this information together to support analysis and assessments at the broader ecosystem level. Sophisticated modelling tools are needed to ‘scale-up’ from experimental results to regional-scale insights. This paper highlights the challenges of combining information to determine how commercially exploited species may be affected under future pH levels, and how modelling and experimental results might be better aligned, using northwest Europe and the waters around the British Isles as an example. We argue that in most cases the current evidence does not offer sufficient information into impacts at projected pH levels, and that future experiments should be designed to consider the pH levels actually experienced by organisms, as well as variability in pH. These types of study are key in safeguarding commercially exploited shellfish stocks.

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Effects of ocean acidification and tralopyril on bivalve biomineralization and carbon cycling: a study of the Pacific Oyster (Crassostrea gigas)

Graphical abstract.


  • The toxicity of combined exposure fell in between tralopyril and OA alone.
  • Tralopyril and/or OA activates stress defense and interferes with energy metabolism.
  • Tralopyril and/or OA affects bivalve biomineralization and marine carbon cycling.


The combined effects of emerging pollutants and ocean acidification (OA) on marine organisms and marine ecosystems have attracted increasing attention. However, the combined effects of tralopyril and OA on marine organisms and marine ecosystems remain unclear. In this study, Crassostrea gigas (C. gigas) were exposed to tralopyril (1 μg/L) and/or OA (PH = 7.7) for 21 days and a 14-day recovery acclimation. To investigate the stress response and potential molecular mechanisms of C. gigas to OA and tralopyril exposure alone or in combination, as well as the effects of OA and/or tralopyril on bivalve biomineralization and marine carbon cycling. The results showed that the combined toxicity was between that of acidification and tralopyril alone. Single or combined exposure activated the general stress defense responses of C. gigas mantle, affected energy metabolism and biomineralization of the organism and the carbon cycle of the marine ecosystem. Moreover, acidification-induced and tralopyril-induced toxicity showed potential recoverability at molecular and biochemical levels. This study provides a new perspective on the molecular mechanisms of tralopyril toxicity to bivalve shellfish and reveals the potential role of tralopyril and OA on marine carbon cycling.

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Environmental change impacts on shell formation in the muricid Nucella lapillus

Environmental change is a significant threat to marine ecosystems worldwide. Ocean acidification, global warming and long-term emissions of anthropogenic effluents are all negatively impacting aquatic life. Marine calcifying organisms, in particular, are expected to be severely affected by decreasing seawater pH, resulting in shell dissolution and retardations during the formation and repair of shells. Understanding the underlying biological and environmental factors driving species vulnerabilities to habitat alterations is thus crucial to our ability to faithfully predict impacts on marine ecosystems under an array of environmental change scenarios. So far, existing knowledge about organism responses mainly stems from short to medium term laboratory experiments of single species or over- simplified communities. Although these studies have provided important insights, results may not translate to organism responses in a complex natural system requiring a more holistic experimental approach. In this thesis, I investigated shell formation mechanisms and shape and elemental composition responses in the shell of the important intertidal predatory muricid Nucella lapillus both in situ and across heterogeneous environmental gradients. The aim was to identify potential coping mechanisms of N. lapillus to environmental change and provide a more coherent picture of shell formation responses along large ecological gradients in the spatial and temporal domain. To investigate shell formation mechanisms, I tested for the possibility of shell recycling as a function to reduce calcification costs during times of exceptional demand using a multi-treatment shell labelling experiment. Reports on calcification costs vary largely in the literature. Still, recent discoveries showed that costs might increase as a function of decreasing calcification substrate abundance, suggesting that shell formation becomes increasingly more costly under future environmental change scenarios. However, despite the anticipated costs, no evidence was found that would indicate the use of functional dissolution as a means to recycle shell material for a more cost-efficient shell formation in N. lapillus. To investigate shell formation responses, I combined morphometric and shell thickness analyses with novel statistical methods to identify natural shape and thickness response of N. lapillus to large scale variability in temperature, salinity, wind speed and the carbonate system across a wide geographic range (from Portugal to Iceland) and through time (over 130 years). I found that along geographical gradients, the state of the carbonate system and, more specifically, the substrate inhibitor ratio ([HCO3−][H+]−1) (SIR) was the main predictor for shape variations in N. lapillus. Populations in regions with a lower SIR tend to form narrower shells with a higher spire to body whorl ratio. In contrast, populations in regions with a higher SIR form wider shells with a much lower spire to body whorl ratio. The results suggest a widespread phenotypic response of N. lapillus to continuing ocean acidification could be expected, affecting its phenotypic response patterns to predator or wave exposure regimes with profound implications for North Atlantic rocky shore communities. On the contrary, investigations of shell shape and thickness changes over the last 130 years from adjacent sampling regions on the Southern North Sea coast revealed that contrary to global predictions, N. lapillus built continuously thicker shells while maintaining a consistent shell shape throughout the last century. Systematic modelling efforts suggested that the observed shell thickening resulted from higher annual temperatures, longer yearly calcification windows, nearshore eutrophication, and enhanced prey abundance, which mitigated the impact of other climate change factors. An investigation into the trace elemental composition of common pollutant metals in the same archival N. lapillus specimens revealed that shell Cu/Ca and Zn/Ca concentration ratios remained remarkably constant throughout the last 130 years despite substantial shifts in the environmental concentration. However, Pb/Ca concentration ratios showed a definite trend closely aligned with leaded petrol emissions in Europe over the same period. Discussing physiological and environmental drivers for the observed shell bound heavy metal patterns, I argue that, unlike for Pb, constraints on environmental dissolved Cu species abundance and biologically mediated control on internal Zn levels were likely responsible for a decoupling of shell-bound to total ambient Cu and Zn concentrations. The results highlight the complexity of internal and external pathways that govern the uptake of heavy metals into the molluscan shell and suggest that the shell of N. lapillus could be a suitable archive for a targeted investigation of Pb pollution in the intertidal zone.

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Metabolic rate allometry in intertidal mussels across environmental gradients: the role of coastal carbonate system parameters in mediating the effects of latitude and temperature

Graphical abstract


  • Latitude and temperature do not explain intertidal mussel metabolic rate allometry.
  • Carbonate system parameters also have effects on size and metabolic rate.
  • Observed allometric variation is best explained by a structural equation model.
  • Metabolic rate allometry is modulated by multiple environmental stressors.


We assess the role of direct and indirect effects of coastal environmental drivers (including the parameters of the carbonate system) on energy expenditure (MR) and body mass (M) of the intertidal mussel, Perumytilus purpuratus, across 10 populations distributed over 2800 km along the Southern Eastern Pacific (SEP) coast. We find biogeographic and local variation in carbonate system variables mediates the effects of latitude and temperature on metabolic rate allometry along the SEP coast. Also, the fitted Piecewise Structural Equation models (PSEM) have greater predictive ability (conditional R2 = 0.95) relative to the allometric scaling model (R2 = 0.35). The largest standardized coefficients for MR and M were determined by the influence of temperature and latitude, followed by pCO2, pH, total alkalinity, and salinity. Thus, physiological diversity of P. purpuratus along the SEP coast emerges as the result of direct and indirect effects of biogeographic and local environmental variables.

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Camouflage and exploratory avoidance of newborn cuttlefish under warming and acidification

Ocean warming and acidification have been shown to elicit deleterious effects on cephalopod mollusks, especially during early ontogeny, albeit effects on behavior remain largely unexplored. This study aimed to evaluate, for the first time, the effect of end-of-the-century projected levels of ocean warming (W; + 3 °C) and acidification (A; 980 µatm pCO2) on Sepia officinalis hatchlings’ exploratory behavior and ability to camouflage in different substrate complexities (sand and black and white gravel). Cuttlefish were recorded in open field tests, from which mobility and exploratory avoidance behavior data were obtained. Latency to camouflage was registered remotely, and pixel intensity of body planes and background gravel were extracted from photographs. Hatching success was lowered under A and W combined (AW; 72.7%) compared to control conditions (C; 98.8%). Motion-related behaviors were not affected by the treatments. AW delayed camouflage response in the gravel substrate compared to W alone. Moreover, cuttlefish exhibited a higher contrast and consequently a stronger disruptive pattern under W, with no changes in background matching. These findings suggest that, although climate change may elicit relevant physiological challenges to cuttlefish, camouflage and mobility of these mollusks are not undermined under the ocean of tomorrow. 

Continue reading ‘Camouflage and exploratory avoidance of newborn cuttlefish under warming and acidification’

Variation in the behavioral tolerance of congeneric marine snails to low-pH exposure

The ocean is acidifying, with multiple consequences for coastal organisms. However, species may differ in their sensitivities. Some taxa may find future conditions mildly stressful or even advantageous, while others will persist only through acclimatization or genetic adaptation. An open question is whether such variation in the sensitivity of species to ocean acidification relates to their evolutionary histories of exposure to reduced pH. Here, we explored this unknown through an investigation of differences in pH tolerance of 2 shoreline gastropods, the black turban snail Tegula funebralis and its congener, the brown turban snail T. brunnea. These species occupy distinct vertical distributions on rocky shores, each subject to different extremes in low pH. We assayed the extent to which low pH degrades the flight behavior of each species in response to the predatory sea star Pisaster ochraceus. Across a range of pH, the tidepool-inhabiting T. funebralis exhibited less behavioral disruption than T. brunnea at any given pH value but also experienced impairment at a pH characteristic of the present-day minimum in its habitat (7.1 pH). The latter pattern suggests T. funebralis operates near what may be a fixed tolerance limit to low pH. T. funebralis also exhibited hints of elevated intraspecific variation in its behaviors, which could imply scope for selection to act. Deeper-dwelling T. brunnea, in contrast, showed little sensitivity to present-day pH minima found where it lives (7.6 pH) and displayed less variation upon which selection might operate. These results provide a initial framework for investigations into the capacity of species of differing evolutionary histories to cope with future ocean acidification.

Continue reading ‘Variation in the behavioral tolerance of congeneric marine snails to low-pH exposure’

Phenotypic plasticity in economically and ecologically important bivalves in response to changing environments

Marine bivalves are ecologically important, providing ecosystem services like filtering water, stabilizing substrate, and creating hard structure for epibionts. Cultured bivalves are also economically important, supporting thousands of aquaculture jobs nationwide and providing valuable protein sources for our growing human population. However, recent shifts in the environment such as temperature, ocean acidification, hypoxia, and extreme environmental variation have greatly affected bivalve physiology, reproduction, and survival across multiple lifestages. Bivalves in the Northeast Pacific are increasingly vulnerable climate change related stressors like intensifying upwelling and weather extremes, defined stratification, and unique geography which causes distinct spatial and seasonal variation. I seek to investigate if higher degrees of phenotypic plasticity and parental carryover will have the potential to improve bivalve’s fitness and tolerance as climate change progresses. My goal is to evaluate plastic capacity by taking a multi-method approach to assessing the physiological metrics of several important bivalve species, using both field and laboratory experiments. Early lifestages are greatly influenced by parental environmental history leading to carryover effects, favoring phenotypes that have a higher likelihood of surviving. In addition to natural selection in the wild, commercial and restoration aquaculturists may select for beneficial phenotypes in adults and offspring which would yield the most desirable characteristics. In our experiment, I focus on three different species: the purple-hinge rock scallop Crassadoma gigantea, the Mediterranean mussels Mytilus galloprovincialis, and the Olympia oyster Ostrea lurida. By choosing a suite of native and non-native, inter- and subtidal species, I hope to obtain a broad snapshot of physiological responses to help restore vulnerable species and maximize quality of farmed product. Chapter 1 examines physiological responses of the scallop C. gigantea to climate change related stressors in the laboratory. I conducted a full factorial laboratory experiment, manipulating pCO2 and temperature to mimic current and future ocean acidification and warming levels. After six weeks of acclimation, I found that stressors reduced shell strength and periostracum (outer shell layer) density. Only acidification affected lipids, and fatty acid content varied between treatments. I was the first to quantify microbial composition of a bivalve under multiple stressors and I found differences in the microbiome, especially with temperature stress. Chapter 2 explores physiological responses of C. gigantea and M. galloprovincialis in a six-month field acclimatation experiment. Shellfish were deployed in cages in Puget Sound, Washington at either 5 or 30 m below the surface. I found that environmental gradients varied seasonally and spatially and affected growth, shell strength, and isotopic signatures. There were differences between the two species, namely with shell strength and δ13C. I found that no one depth or time period yielded the most desirable traits for culturing, and I highlight the concerning patterns in Puget Sound’s most productive region. In Chapter 3, I took my research one step further by introducing a spatial component to a one-year field experiment. I outplanted O. lurida in cages at 5 m depth in three different locations in Puget Sound, one of which also had a 20 m depth. Each of these locations had an oceanographic monitoring buoy which allowed me to couple physiological data with high-resolution environmental data. I spawned the oysters to test parental carryover and found evidence in growth rates of larvae, which when acclimated to high temperatures, mirrored their parents. Interestingly, larval survival did not coincide with growth, and through respirometry, I found that 20°C may be a bottleneck for this lifestage. Adult oyster growth, isotopic signatures, and gametogenesis were affected by both seasonal and spatial field conditions. Metabolic responses to pH and temperature depending on recent acclimatization history. This research shows evidence of strong adaptive plasticity which was demonstrated by energetic trade-offs and parental carryover. Chapter 4 acclimatized M. galloprovincialis in the field in a similar fashion to O. lurida. Growth, shell strength, and isotopes were all affected by season and site. Similar to oysters, acute metabolic rate of each site and season was affected differently between pH and temperature. Shellfish covered in Chapter 3/4 have a high degree of plasticity and results are useful to restoration (oyster) and commercial (mussel) aquaculturists to create selective breeding programs that will withstand climate change. Results of this dissertation demonstrate the rapid degree of phenotypic plasticity and capacity for parental carryover in field and laboratory setting though a wide array of physiological analysis. Outcomes of this research add to the limited but growing body of literature about multiple-stressors and field experiments, and indents to assist aquaculturists as climate change progresses.

Continue reading ‘Phenotypic plasticity in economically and ecologically important bivalves in response to changing environments’

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