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Vulnerability of pteropod (Limacina helicina) to ocean acidification: Shell dissolution occurs despite an intact organic layer
... OA represents a significant threat to calcifying marine organisms, particularly shelled molluscs (Gazeau et al. 2013), some of which serve important roles in pelagic food webs and the export of carbon to the deep ocean (Berner and Honjo 1981;Hunt et al. 2008). Planktonic, highly motile gastropod larvae and adult thecosome pteropods may be especially sensitive to changes in ocean chemistry due to their thin shells and incomplete protection of the outer organic layer of their shells (periostracum), resulting in rapid dissolution of the aragonite shell matrix under low aragonite saturation state (Ω arag ; e.g., Bednaršek et al. 2012bBednaršek et al. , 2016Gazeau et al. 2013). Pteropods in particular serve as one of the first bioindicators of OA in pelagic marine ecosystems (Bednaršek et al. 2012a(Bednaršek et al. , 2014a(Bednaršek et al. , 2016. ...
... Planktonic, highly motile gastropod larvae and adult thecosome pteropods may be especially sensitive to changes in ocean chemistry due to their thin shells and incomplete protection of the outer organic layer of their shells (periostracum), resulting in rapid dissolution of the aragonite shell matrix under low aragonite saturation state (Ω arag ; e.g., Bednaršek et al. 2012bBednaršek et al. , 2016Gazeau et al. 2013). Pteropods in particular serve as one of the first bioindicators of OA in pelagic marine ecosystems (Bednaršek et al. 2012a(Bednaršek et al. , 2014a(Bednaršek et al. , 2016. ...
... Aragonite dissolution in shelled molluscs such as L. helicina occurs over the surface of the entire shell rather than simply at the oldest, inner whorls or along the newest, growing edge (Bednaršek et al. 2012b). The periostracum, an outer organic layer of the shell, exists as a barrier between the mineral layers of the shell and ambient seawater (Harper 2000;Peck et al. 2016), but does not provide sufficient protection against chemical dissolution under OA conditions (Bednaršek et al. 2016). Although shell dissolution can occur despite an intact periostracum, the local thinning or degradation of this protective veneer can further exacerbate dissolution damage at discrete sites on the shell surface (Gazeau et al. 2013;Bednaršek et al. 2016)-a process similar to that seen in nassariid gastropods (Garilli et al. 2015). ...
Ocean acidification (OA) increases aragonite shell dissolution in calcifying marine organisms. It has been proposed that bacteria associated with molluscan shell surfaces in situ could damage the periostracum and reduce its protective function against shell dissolution. However, the influence of bacteria on shell dissolution under OA conditions is unknown. In this study, dissolution in dead shells from gastropod larvae and adult pteropods (Limacina helicina) was examined following a 5-day incubation under a range of aragonite saturation states (Ωarag; values ranging from 0.5 to 1.8) both with and without antibiotics. Gastropod and pteropod specimens were collected from Puget Sound, Washington (48°33′19″N, 122°59′49″W and 47°41′11″N, 122°25′23″W, respectively), preserved, stored, and then treated in August 2015. Environmental scanning electron microscopy (ESEM) was used to determine the severity and extent of dissolution, which was scored as mild, severe, or summed (mild + severe) dissolution. Shell dissolution increased with decreasing Ωarag. In gastropod larvae, there was a significant interaction between the effects of antibiotics and Ωarag on severe dissolution, indicating that microbes could mediate certain types of dissolution among shells under low Ωarag. In L. helicina, there were no significant interactions between the effects of antibiotics and Ωarag on dissolution. These findings suggest that bacteria may differentially influence the response of some groups of shelled planktonic gastropods to OA conditions. This is the first assessment of the microbial–chemical coupling of dissolution in shells of either gastropod larvae or adult L. helicina under OA.
... We prepared each individual by removing the organic layer using a combination of protocols (Bednaršek et al., 2012b(Bednaršek et al., , 2016a. Briefly, pteropods were transferred from 100% to 70% and 50% ethanol in gradual steps, rinsed thoroughly with DI water, exposed to diluted bleach (5% sodium hypochlorite) for a treatment of approximately 30 min that was subsequently rinsed with DI water for 2-3 times to clean the shell surface, and subsequent air-dried for 12 h. ...
... The GoA is more likely to experience severe spring and summertime dissolution of pteropod shells compared to the same period in the Bering Sea. Our data show that thinner shells, along with dissolution uniformly distributed around the shell surface, are evidence of an impact related to lower ar cumulative exposure (Bednaršek et al., 2016a). This is opposite to the conclusion from Peck et al. (2016); namely that dissolution only occurs if the periostracum is damaged or if imposed through predation pressure. ...
Exposure to the impact of ocean acidification (OA) is increasing in high-latitudinal productive habitats. Pelagic calcifying snails (pteropods), a significant component of the diet of economically important fish, are found in high abundance in these regions. Pteropods have thin shells that readily dissolve at low aragonite saturation state (Ωar), making them susceptible to OA. Here, we conducted a first integrated risk assessment for pteropods in the Eastern Pacific subpolar gyre, the Gulf of Alaska (GoA), Bering Sea, and Amundsen Gulf. We determined the risk for pteropod populations by integrating measures of OA exposure, biological sensitivity, and resilience. Exposure was based on physical-chemical hydrographic observations and regional biogeochemical model outputs, delineating seasonal and decadal changes in carbonate chemistry conditions. Biological sensitivity was based on pteropod morphometrics and shell-building processes, including shell dissolution, density and thickness. Resilience and adaptive capacity were based on species diversity and spatial connectivity, derived from the particle tracking modeling. Extensive shell dissolution was found in the central and western part of the subpolar gyre, parts of the Bering Sea, and Amundsen Gulf. We identified two distinct morphotypes: L. helicina helicina and L. helicina pacifica, with high-spired and flatter shells, respectively. Despite the presence of different morphotypes, genetic analyses based on mitochondrial haplotypes identified a single species, without differentiation between the morphological forms, coinciding with evidence of widespread spatial connectivity. We found that shell morphometric characteristics depends on omega saturation state (Ωar); under Ωar decline, pteropods build flatter and thicker shells, which is indicative of a certain level of phenotypic plasticity. An integrated risk evaluation based on multiple approaches assumes a high risk for pteropod population persistence with intensification of OA in the high latitude eastern North Pacific because of their known vulnerability, along with limited evidence of species diversity despite their connectivity and our current lack of sufficient knowledge of their adaptive capacity. Such a comprehensive understanding would permit improved prediction of ecosystem change relevant to effective fisheries resource management, as well as a more robust foundation for monitoring ecosystem health and investigating OA impacts in high-latitudinal habitats.
... Lastly, although the effects of pH on calcification in Limacina spp. have been well documented [13,16,20,21,[65][66][67], there remains an ongoing debate regarding the ability for Limacina spp. to utilize internal shell repair mechanisms to minimize the deleterious impacts of ocean acidification [65,68,69]. However, this study along with the transcriptome study presented by Koh et al. [22] suggests that all forms of Limacina helicina are challenged to maintain calcification in low pH conditions. ...
... Lastly, although the effects of pH on calcification in Limacina spp. have been well documented [13,16,20,21,[65][66][67], there remains an ongoing debate regarding the ability for Limacina spp. to utilize internal shell repair mechanisms to minimize the deleterious impacts of ocean acidification [65,68,69]. However, this study along with the transcriptome study presented by Koh et al. [22] suggests that all forms of Limacina helicina are challenged to maintain calcification in low pH conditions. ...
Background
Ocean acidification (OA), a change in ocean chemistry due to the absorption of atmospheric CO2 into surface oceans, challenges biogenic calcification in many marine organisms. Ocean acidification is expected to rapidly progress in polar seas, with regions of the Southern Ocean expected to experience severe OA within decades. Biologically, the consequences of OA challenge calcification processes and impose an energetic cost.
Results
In order to better characterize the response of a polar calcifier to conditions of OA, we assessed differential gene expression in the Antarctic pteropod, Limacina helicina antarctica. Experimental levels of pCO2 were chosen to create both contemporary pH conditions, and to mimic future pH expected in OA scenarios. Significant changes in the transcriptome were observed when juvenile L. h. antarctica were acclimated for 21 days to low-pH (7.71), mid-pH (7.9) or high-pH (8.13) conditions. Differential gene expression analysis of individuals maintained in the low-pH treatment identified down-regulation of genes involved in cytoskeletal structure, lipid transport, and metabolism. High pH exposure led to increased expression and enrichment for genes involved in shell formation, calcium ion binding, and DNA binding. Significant differential gene expression was observed in four major cellular and physiological processes: shell formation, the cellular stress response, metabolism, and neural function. Across these functional groups, exposure to conditions that mimic ocean acidification led to rapid suppression of gene expression.
Conclusions
Results of this study demonstrated that the transcriptome of the juvenile pteropod, L. h. antarctica, was dynamic and changed in response to different levels of pCO2. In a global change context, exposure of L. h. antarctica to the low pH, high pCO2 OA conditions resulted in a suppression of transcripts for genes involved in key physiological processes: calcification, metabolism, and the cellular stress response. The transcriptomic response at both acute and longer-term acclimation time frames indicated that contemporary L. h. antarctica may not have the physiological plasticity necessary for adaptation to OA conditions expected in future decades. Lastly, the differential gene expression results further support the role of shelled pteropods such as L. h. antarctica as sentinel organisms for the impacts of ocean acidification.
Electronic supplementary material
The online version of this article (10.1186/s12864-017-4161-0) contains supplementary material, which is available to authorized users.
... This was contested but until today not ultimately disproved, because in the study of Peck, Tarling, Manno, Harper, and Tynan (2016) all pteropod shells that appeared pristine were examined untreated, a pretreated control group demonstrating artificial damage was missing, and the authors conclude from the pattern of breaches and dissolution they found that dissolution only happened where the periostracum was/must have been breached. Therefore, based on our results, this may support the opinion that it is recommendable to remove the periostracum prior dissolution assessment (Bednaršek, Tarling, Bakker, Fielding, Cohen, et al. 2012;Bednaršek et al. 2016). However, it has never been demonstrated that the periostracum is completely removed under H 2 O 2 and KOH exposure, and unfortunately, the irrefutable demonstration of the efficacy of this method is hardly possible. ...
Aragonite undersaturation (Ωar < 1) events are projected to rapidly increase in frequency and duration in the Antarctic Weddell Sea by 2050. Thecosome pteropods (pelagic snails) are bioindicators of ocean acidification (OA) because their aragonite shell dissolves easily at low Ωar saturation states. Here, we describe the shell dissolution state of the pteropod Limacina helicina antarctica in relation to the water column Ωar in the southern Weddell Sea during austral summer 2018 as benchmark for future monitoring of ongoing OA. Ωar depth profiles at the sampling sites were consistently close to or in the range of threshold levels (Ωar ∼ 1.1–1.3) for pteropod shell dissolution. Pteropods contributed up to 69% of total mesozooplankton biomass, and their distribution correlated positively with Ωar and chlorophyll a concentration. When analyzed with scanning electron microscopy, 78% of the investigated shells exhibited dissolution, and 50–69% showed the more severe Type II dissolution exceeding current projections of pteropod shell dissolution for the Southern Ocean. But importantly, in our study, only two specimens had the most severe Type III dissolution. Dissolution often co‐occurred with and occurred in scratch marks of unclear origin supporting notions that an intact periostracum protects the shell from dissolution. Where dissolution occurred in the absence of scratches or absence of evidence of periostracum breaches, microscale/nanoscale breaches may have been an important pathway for dissolution commencement supporting recent findings of a reduction of the organic shell content caused by low Ωar/low pH. The dissolution benchmark we provide here allows future application of pteropods as early‐warning indicators of presumably progressing OA in the Weddell Sea.
... Various studies agree that the extreme sensitivity of pteropods to low ar , low pH stress is related to their energetics metabolism, pointing toward the trade-off processes underlined by their insufficient energy budget (e.g., Riebesell, 2012, 2017;Seibel et al., 2012;Bednaršek et al., 2016b;Peck et al., 2018). Based on the numerous lines of evidence, and as previously demonstrated for numerous other taxa (Lesser, 2006;, oxidative stress biomarkers offer important insights into bioenergetic requirements for pteropods under exposure to multiple stressors. ...
Understanding the interactive effects of multiple stressors on pelagic mollusks associated with global climate change is especially important in highly productive coastal ecosystems of the upwelling regime, such as the California Current System (CCS). Due to temporal overlap between a marine heatwave, an El Niño event, and springtime intensification of the upwelling, pteropods of the CCS were exposed to co-occurring increased temperature, low Ωar and pH, and deoxygenation. The variability in the natural gradients during NOAA’s WCOA 2016 cruise provided a unique opportunity for synoptic study of chemical and biological interactions. We investigated the effects of in situ multiple drivers and their interactions across cellular, physiological, and population levels. Oxidative stress biomarkers were used to assess pteropods’ cellular status and antioxidant defenses. Low aragonite saturation state (Ωar) is associated with significant activation of oxidative stress biomarkers, as indicated by increased levels of lipid peroxidation (LPX), but the antioxidative activity defense might be insufficient against cellular stress. Thermal stress in combination with low Ωar additively increases the level of LPX toxicity, while food availability can mediate the negative effect. On the physiological level, we found synergistic interaction between low Ωar and deoxygenation and thermal stress (Ωar:T, O2:T). On the population level, temperature was the main driver of abundance distribution, with low Ωar being a strong driver of secondary importance. The additive effects of thermal stress and low Ωar on abundance suggest a negative effect of El Niño at the population level. Our study clearly demonstrates Ωar and temperature are master variables in explaining biological responses, cautioning the use of a single parameter in the statistical analyses. High quantities of polyunsaturated fatty acids are susceptible to oxidative stress because of LPX, resulting in the loss of lipid reserves and structural damage to cell membranes, a potential mechanism explaining extreme pteropod sensitivity to low Ωar. Accumulation of oxidative damage requires metabolic compensation, implying energetic trade-offs under combined thermal and low Ωar and pH stress. Oxidative stress biomarkers can be used as early-warning signal of multiple stressors on the cellular level, thereby providing important new insights into factors that set limits to species’ tolerance to in situ multiple drivers.
... Observations of rapid pteropod shell dissolution have been accounted for by the thin periostracum covering pteropod shells allowing dissolution to occur beneath it 13 . However, a recent study finding that pteropods exposed to seasonally undersaturated waters were only vulnerable to shell dissolution where the periostracum had been damaged 14 opened debate on the effectiveness of the pteropod periostracum 15,16 . Accepting the notion that intact pteropod periostracum is effective in impeding dissolution, once damaged, for example, scratched by a predator or weakened by microbes, the underlying shell structure is no longer protected and exposure of aragonite to waters of Ω Ar ≤ 1 can lead to progressive shell dissolution 14 . ...
The dissolution of the delicate shells of sea butterflies, or pteropods, has epitomised discussions regarding ecosystem vulnerability to ocean acidification over the last decade. However, a recent demonstration that the organic coating of the shell, the periostracum, is effective in inhibiting dissolution suggests that pteropod shells may not be as susceptible to ocean acidification as previously thought. Here we use micro-CT technology to show how, despite losing the entire thickness of the original shell in localised areas, specimens of polar species Limacina helicina maintain shell integrity by thickening the inner shell wall. One specimen collected within Fram Strait with a history of mechanical and dissolution damage generated four times the thickness of the original shell in repair material. The ability of pteropods to repair and maintain their shells, despite progressive loss, demonstrates a further resilience of these organisms to ocean acidification but at a likely metabolic cost.
... Ocean acidification may present a physiological challenge to biogenic calcification, and many species, such as the shell-forming pteropods, are proposed to be negatively impacted by this shift in ocean chemistry (Comeau et al., 2009;Kroeker et al., 2010;Maas et al., 2015;Byrne, 2011;Lischka et al., 2011;Fabry et al., 2008). Recently, pteropods in general have been proposed as an indicator species for the progression and impacts of ocean acidification in the world oceans; however, there are possible difficulties with attributing visible shell damage with true physiological stress (Peck et al., 2015;Bednaršek et al., 2016;Peck et al., 2016). Since pteropods are ecologically significant in many regions, more information regarding the physiological response to future ocean conditions will benefit an international research community seeking to use Limacina as an indicator species in both polar and temperate marine sciences (Bednaršek et al., 2012a(Bednaršek et al., , 2012b(Bednaršek et al., , 2012cComeau et al., 2009;Fabry et al., 2009). ...
The pteropod Limacina helicina antarctica is a dominant member of the zooplankton assemblage in the Antarctic marine ecosystem, and is part of a relatively simple food web in nearshore marine Antarctic waters. As a shelled pteropod, Limacina has been suggested as a candidate sentinel organism for the impacts of ocean acidification, due to the potential for shell dissolution in undersaturated waters. In this study, our goal was to develop a transcriptomic resource for Limacina that would support mechanistic studies to explore the physiological response of Limacina to abiotic stressors such as ocean acidification and ocean warming. To this end, RNA sequencing libraries were prepared from Limacina that had been exposed to a range of pH levels and an elevated temperature to maximize the diversity of expressed genes. RNA sequencing (RNA-seq) was conducted on an Illumina NextSeq500 which produced 339,000,000 150 bp paired-end reads. The de novo transcriptome was produced using Trinity and annotation of the assembled transcriptome resulted in the identification of 81,229 transcripts in 137 KEGG pathways. This RNA-seq effort resulted in a transcriptome for the Antarctic pteropod, Limacina helicina antarctica, that is a major resource for an international marine science research community studying these pelagic molluscs in a global change context.
The passive dissolution of anthropogenically produced CO2 into the ocean system is reducing ocean pH and changing a suite of chemical equilibria, with negative consequences for some marine organisms, in particular those that bear calcium carbonate shells. Although our monitoring of these chemical changes has improved, we have not developed effective tools to translate observations, which are typically of the pH and carbonate saturation state, into ecologically relevant predictions of biological risks. One potential solution is to develop bioindicators: biological variables with a clear relationship to environmental risk factors that can be used for assessment and management. Thecosomatous pteropods are a group of pelagic shelled marine gastropods, whose biological responses to CO2 have been suggested as potential bioindicators of ocean acidification owing to their sensitivity to acidification in both the laboratory and the natural environment. Using five CO2 exposure experiments, occurring across four seasons and running for up to 15 days, we describe a consistent relationship between saturation state, shell transparency and duration of exposure, as well as identify a suite of genes that could be used for biological monitoring with further study. We clarify variations in thecosome responses due to seasonality, resolving prior uncertainties and demonstrating the range of their phenotypic plasticity. These biomarkers of acidification stress can be implemented into ecosystem models and monitoring programmes in regions where pteropods are found, whilst the approach will serve as an example for other regions on how to bridge the gap between point-based chemical monitoring and biologically relevant assessments of ecosystem health.
The pteropod Limacina helicina has become an important bioindicator species for the negative impacts of ocean acidification (OA) on marine ecosystems. However, pteropods diversified during earlier high CO2 periods in Earth history and currently inhabit regions that are naturally corrosive to their shells, suggesting that they possess mechanisms to survive unfavourable conditions. Recent work, which is still under considerable debate, has proposed that the periostracum, a thin organic coating on the outer shell, protects pteropods from shell dissolution. Here, we provide direct evidence that shows that damage to the L. helicina periostracum results in dissolution of the underlying shell when exposed to corrosive water for ∼8 d, while an intact periostracum protects the shell from dissolution under the same conditions. This important first line of defence suggests that pteropods are more resistant to OA-induced shell dissolution than is generally accepted.
Coastal-estuarine habitats are rapidly changing due to global climate change, with impacts influenced by the variability of carbonate chemistry conditions. However, our understanding of the responses of ecologically and economically important calcifiers to pH variability and temporal variation is limited, particularly with respect to shell-building processes. We investigated the mechanisms driving biomineralogical and physiological responses in juveniles of introduced (Pacific; Crassostrea gigas) and native (Olympia; Ostrea lurida) oysters under flow-through experimental conditions over a six-week period that simulate current and future conditions: static control and low pH (8.0 and 7.7); low pH with fluctuating (24-h) amplitude (7.7 ± 0.2 and 7.7 ± 0.5); and high-frequency (12-h) fluctuating (8.0 ± 0.2) treatment. The oysters showed physiological tolerance in vital processes, including calcification, respiration, clearance, and survival. However, shell dissolution significantly increased with larger amplitudes of pH variability compared to static pH conditions, attributable to the longer cumulative exposure to lower pH conditions, with the dissolution threshold of pH 7.7 with 0.2 amplitude. Moreover, the high-frequency treatment triggered significantly greater dissolution, likely because of the oyster's inability to respond to the unpredictable frequency of variations. The experimental findings were extrapolated to provide context for conditions existing in several Pacific coastal estuaries, with time series analyses demonstrating unique signatures of pH predictability and variability in these habitats, indicating potentially benefiting effects on fitness in these habitats. These implications are crucial for evaluating the suitability of coastal habitats for aquaculture, adaptation, and carbon dioxide removal strategies.
Climate change impacts are pronounced at high latitudes, where warming, reduced sea-ice-cover, and ocean acidification affect marine ecosystems. We review climate change impacts on two major gateways into the Arctic: the Bering and Chukchi seas in the Pacific and the Barents Sea and Fram Strait in the Atlantic. We present scenarios of how changes in the physical environment and prey resources may affect commercial fish populations and fisheries in these high-latitude systems to help managers and stakeholders think about possible futures. Predicted impacts include shifts in the spatial distribution of boreal species, a shift from larger, lipid-rich zooplankton to smaller, less nutritious prey, with detrimental effects on fishes that depend on high-lipid prey for overwinter survival, shifts from benthic- to pelagic-dominated food webs with implications for upper trophic levels, and reduced survival of commercially important shellfish in waters that are increasingly acidic. Predicted changes are expected to result in disruptions to existing fisheries, the emergence of new fisheries, new challenges for managing transboundary stocks, and possible conflicts among resource users. Some impacts may be irreversible, more severe, or occur more frequently under anthropogenic climate change than impacts associated with natural variability, posing additional management challenges.
We compare physiological responses of the crustacean copepod Calanus pacificus and pelagic pteropod mollusk Limacina helicina to ocean temperatures and pH by measuring biomarkers of oxidative stress, antioxidant defences, and the activity of the respiratory electron transport system in organisms collected on the 2016 West Coast Ocean Acidification cruise in the California Current System. Copepods and pteropods exhibited strong but divergent responses in the same habitat; copepods had higher oxygen-reactive absorbance capacity, glutathione-S-transferase, and total glutathione content. The ratio between reduced to oxidised glutathione was higher in copepods than in pteropods, indicating lower oxidative stress in copepods. Pteropods showed higher activities of glutathione reductase, catalase, and lipid peroxidation, indicating increased antioxidant defences and oxidative stress. Thus, the antioxidant defence system of the copepods has a greater capacity to respond to oxidative stress, while pteropods already face severe stress and show limited capacity to deal with further changes. The results suggest that copepods have higher adaptive potential, owing to their stronger vertical migration behaviour and efficient glutathione metabolism, whereas pteropods run the risk of oxidative stress and mortality under high CO2 conditions. Our results provide a unique dataset and evidence of stress-inducing mechanisms behind pteropod ocean acidification responses.
Early life stages of marine calcifiers are particularly vulnerable to climate change. In the Southern Ocean aragonite undersaturation events and areas of rapid warming already occur and are predicted to increase in extent. Here, we present the first study to successfully hatch the polar pteropod Limacina helicina antarctica and observe the potential impact of exposure to increased temperature and aragonite undersaturation resulting from ocean acidification (OA) on the early life stage survival and shell morphology. High larval mortality (up to 39%) was observed in individuals exposed to perturbed conditions. Warming and OA induced extensive shell malformation and dissolution, respectively, increasing shell fragility. Furthermore, shell growth decreased, with variation between treatments and exposure time. Our results demonstrate that short-term exposure through passing through hotspots of OA and warming poses a serious threat to pteropod recruitment and long-term population viability.
Electronic supplementary material
The online version of this article (10.1007/s00227-017-3261-3) contains supplementary material, which is available to authorized users.
The gymnosome (unshelled) pteropod Clione limacina is a pelagic predatory mollusc found in polar and sub-polar regions. It has been studied for its distinctive swimming behavior and as an obligate predator on the closely related thecosome (shelled) pteropods. As concern about ocean acidification increases, it becomes useful to compare the physiological responses of closely-related calcifying and non-calcifying species to acidification. The goals of this study were thus to generate a reference transcriptome for Clione limacina, to expose individuals to CO2 for a period of 3days, and to explore differential patterns of gene expression. Our Trinity assembly contained 300,994 transcripts of which ~26% could be annotated. In total, only 41 transcripts were differentially expressed following the CO2 treatment, consistent with a limited physiological response of this species to short-term CO2 exposure. The differentially expressed genes identified in our study were largely distinct from those identified in previous studies of thecosome pteropods, although some similar transcripts were identified, suggesting that comparison of these transcriptomes and responses may provide insight into differences in responses to ocean acidification among phylogenetically and functionally distinct molluscan lineages.
Scarred shells of polar pteropod Limacina helicina collected from the Greenland Sea in June 2012 reveal a history of damage, most likely failed predation, in earlier life stages. Evidence of shell fracture and subsequent re-growth is commonly observed in specimens recovered from the sub-Arctic and further afield. However, at one site within sea-ice on the Greenland shelf, shells that had been subject to mechanical damage were also found to exhibit considerable dissolution. It was evident that shell dissolution was localised to areas where the organic, periostracal sheet that covers the outer shell had been damaged at some earlier stage during the animal's life. Where the periostracum remained intact, the shell appeared pristine with no sign of dissolution. Specimens which appeared to be pristine following collection were incubated for four days. Scarring of shells that received periostracal damage during collection only became evident in specimens that were incubated in waters undersaturated with respect to aragonite, Ω Ar≤1. While the waters from which the damaged specimens were collected at the Greenland Sea sea-ice margin were not Ω Ar≤1, the water column did exhibit the lowest Ω Ar values observed in the Greenland and Barents Seas, and was likely to have approached Ω Ar≤1 during the winter months. We demonstrate that L. helicina shells are only susceptible to dissolution where both the periostracum has been breached and the aragonite beneath the breach is exposed to waters of Ω Ar≤1. Exposure of multiple layers of aragonite in areas of deep dissolution indicate that, as with many molluscs, L. helicina is able to patch up dissolution damage to the shell by secreting additional aragonite internally and maintain their shell. We conclude that, unless breached, the periostracum provides an effective shield for pteropod shells against dissolution in waters Ω Ar≤1, and when dissolution does occur the animal has an effective means of self-repair. We suggest that future studies of pteropod shell condition are undertaken on specimens from which the periostracum has not been removed in preparation.
We tested the sensitivity of the vertical distributions and shell dissolution patterns of thecosome pteropods to spatial gradients associated with an eddy-associated front in the southern California Current System. The aragonite saturation horizon (Omega(arag) = 1.0) shoaled from > 200 to <75 m depth across the front. The vertical distribution of thecosome pteropods tracked these changes, with all 5 species showing reduced occurrence at depths below 100 m where waters were less saturated with respect to aragonite. Shell dissolution patterns of the numerically dominant thecosome Limacina helicina corresponded to the cross-frontal changes in Omega(arag) saturation state. Severe shell dissolution ( categorized here as Type II and Type III) was low in near-surface waters where Omega(arag) > 1.4, while peak dissolution occurred in depths where Omega(arag) = 1.0 to 1.4. Vertical habitat compression and increased shell dissolution may be expected to accompany future shoaling of waters that are undersaturated with respect to aragonite.
Excessive CO2 in the present-day ocean-atmosphere system is causing ocean acidification, and is likely to cause a severe biodiversity decline in the future, mirroring effects in many past mass extinctions. Fossil records demonstrate that organisms surviving such events were often smaller than those before, a phenomenon called the Lilliput effect. Here, we show that two gastropod species adapted to acidified seawater at shallow-water CO2 seeps were smaller than those found in normal pH conditions and had higher mass-specific energy consumption but significantly lower whole-animal metabolic energy demand. These physiological changes allowed the animals to maintain calcification and to partially repair shell dissolution. These observations of the long-term chronic effects of increased CO2 levels forewarn of changes we can expect in marine ecosystems as CO2 emissions continue to rise unchecked, and support the hypothesis that ocean acidification contributed to past extinction events. The ability to adapt through dwarfing can confer physiological advantages as the rate of CO2 emissions continues to increase.
Thecosome pteropods are abundant upper-ocean zooplankton that build aragonite shells. Ocean acidification results in the lowering of aragonite saturation levels in the surface layers, and several incubation studies have shown that rates of calcification in these organisms decrease as a result. This study provides a weight-specific net calcification rate function for thecosome pteropods that includes both rates of dissolution and calcification over a range of plausible future aragonite saturation states (Ωar). We measured gross dissolution in the pteropod Limacina helicina antarctica in the Scotia Sea (Southern Ocean) by incubating living specimens across a range of aragonite saturation states for a maximum of 14 days. Specimens started dissolving almost immediately upon exposure to undersaturated conditions (Ωar∼0.8), losing 1.4% of shell mass per day. The observed rate of gross dissolution was different from that predicted by rate law kinetics of aragonite dissolution, in being higher at Ωar levels slightly above 1 and lower at Ωar levels of between 1 and 0.8. This indicates that shell mass is affected by even transitional levels of saturation, but there is, nevertheless, some partial means of protection for shells when in undersaturated conditions. A function for gross dissolution against Ωar derived from the present observations was compared to a function for gross calcification derived by a different study, and showed that dissolution became the dominating process even at Ωar levels close to 1, with net shell growth ceasing at an Ωar of 1.03. Gross dissolution increasingly dominated net change in shell mass as saturation levels decreased below 1. As well as influencing their viability, such dissolution of pteropod shells in the surface layers will result in slower sinking velocities and decreased carbon and carbonate fluxes to the deep ocean.
We tested whether the thecosome pteropod Limacina helicina from Puget Sound, an urbanized estuary in the northwest continental US, experiences shell dissolution and altered mortality rates when exposed to the high CO2, low aragonite saturation state (Ωa) conditions that occur in Puget Sound and the northeast Pacific Ocean. Five, week-long experiments were conducted in which we incubated pteropods collected from Puget Sound in four carbon chemistry conditions: current summer surface (∼460-500 µatm CO2, Ωa≈1.59), current deep water or surface conditions during upwelling (∼760 and ∼1600-1700 µatm CO2, Ωa≈1.17 and 0.56), and future deep water or surface conditions during upwelling (∼2800-3400 µatm CO2, Ωa≈0.28). We measured shell condition using a scoring regime of five shell characteristics that capture different aspects of shell dissolution. We characterized carbon chemistry conditions in statistical analyses with Ωa, and conducted analyses considering Ωa both as a continuous dataset and as discrete treatments. Shell dissolution increased linearly as aragonite saturation state decreased. Discrete treatment comparisons indicate that shell dissolution was greater in undersaturated treatments compared to oversaturated treatments. Survival increased linearly with aragonite saturation state, though discrete treatment comparisons indicated that survival was similar in all but the lowest saturation state treatment. These results indicate that, under starvation conditions, pteropod survival may not be greatly affected by current and expected near-future aragonite saturation state in the NE Pacific, but shell dissolution may. Given that subsurface waters in Puget Sound's main basin are undersaturated with respect to aragonite in the winter and can be undersaturated in the summer, the condition and persistence of the species in this estuary warrants further study.
Few studies to date have demonstrated widespread biological impacts of ocean acidification (OA) under conditions currently found in the natural environment. From a combined survey of physical and chemical water properties and biological sampling along the Washington-Oregon-California coast in August 2011, we show that large portions of the shelf waters are corrosive to pteropods in the natural environment. We show a strong positive correlation between the proportion of pteropod individuals with severe shell dissolution damage and the percentage of undersaturated water in the top 100 m with respect to aragonite. We found 53% of onshore individuals and 24% of offshore individuals on average to have severe dissolution damage. Relative to pre-industrial CO2 concentrations, the extent of undersaturated waters in the top 100 m of the water column has increased over sixfold along the California Current Ecosystem (CCE). We estimate that the incidence of severe pteropod shell dissolution owing to anthropogenic OA has doubled in near shore habitats since pre-industrial conditions across this region and is on track to triple by 2050. These results demonstrate that habitat suitability for pteropods in the coastal CCE is declining. The observed impacts represent a baseline for future observations towards understanding broader scale OA effects.
Increasing atmospheric carbon dioxide levels are causing ocean
acidification, compromising the ability of some marine organisms to
build and maintain support structures as the equilibrium state of
inorganic carbon moves away from calcium carbonate. Few marine organisms
tolerate conditions where ocean pH falls significantly below today's
value of about 8.1 and aragonite and calcite saturation values below 1
(refs 5, 6). Here we report dense clusters of the vent mussel
Bathymodiolus brevior in natural conditions of pH values between 5.36
and 7.29 on northwest Eifuku volcano, Mariana arc, where liquid carbon
dioxide and hydrogen sulphide emerge in a hydrothermal setting. We find
that both shell thickness and daily growth increments in shells from
northwest Eifuku are only about half those recorded from mussels living
in water with pH>7.8. Low pH may therefore also be implicated in
metabolic impairment. We identify four-decade-old mussels, but suggest
that the mussels can survive for so long only if their protective shell
covering remains intact: crabs that could expose the underlying calcium
carbonate to dissolution are absent from this setting. The mussels'
ability to precipitate shells in such low-pH conditions is remarkable.
Nevertheless, the vulnerability of molluscs to predators is likely to
increase in a future ocean with low pH.
The carbonate chemistry of the surface ocean is rapidly changing with ocean acidification, a result of human activities. In the upper layers of the Southern Ocean, aragonite—a metastable form of calcium carbonate with rapid dissolution kinetics—may become undersaturated by 2050. Aragonite undersaturation is likely to affect aragonite-shelled organisms, which can dominate surface water communities in polar regions. Here we present analyses of specimens of the pteropod Limacina helicina antarctica that were extracted live from the Southern Ocean early in 2008. We sampled from the top 200m of the water column, where aragonite saturation levels were around 1, as upwelled deep water is mixed with surface water containing anthropogenic CO2. Comparing the shell structure with samples from aragonite-supersaturated
regions elsewhere under a scanning electron microscope, we found severe levels of shell dissolution in the undersaturated region alone. According to laboratory incubations of intact samples with a range of aragonite saturation levels, eight days of incubation in aragonite saturation levels of 0.94–1.12 produces equivalent levels of dissolution. As deep-water upwelling and CO2 absorption by surface waters is likely to increase as a result of human activities, we conclude that upper ocean regions where aragonite-shelled organisms are
affected by dissolution are likely to expand.
Anthropogenic ocean acidification is likely to have negative effects on marine calcifying organisms, such as shelled pteropods, by promoting dissolution of aragonite shells. Study of shell dissolution requires an accurate and sensitive method for assessing shell damage. Shell dissolution was induced through incubations in CO2‐enriched seawater for 4 and 14 days. We describe a procedure that allows the level of dissolution to be assessed and classified into three main types: Type I with partial dissolution of the prismatic layer; Type II with exposure of underlying crossed‐lamellar layer, and Type III, where crossed‐lamellar layer shows signs of dissolution. Levels of dissolution showed a good correspondence to the incubation conditions, with the most severe damage found in specimens held for 14 days in undersaturated condition (Ω ~ 0.8). This methodology enables the response of small pelagic calcifiers to acidified conditions to be detected at an early stage, thus making pteropods a valuable bioindicator of future ocean acidification.
Excessive CO2 in the present-day ocean–atmosphere system is causing ocean acidification, and is likely to cause a severe biodiversity decline in the future, mirroring effects in many past mass extinctions. Fossil records demonstrate that organisms surviving such events were often smaller than those before, a phenomenon called the Lilliput effect. Here, we show that two gastropod species adapted to acidified seawaterat shallow-water CO2 seeps were smaller than those found in normal pH conditions and had higher mass-specific energy consumption but significantly lower whole-animal metabolic energy demand. These physiological changes allowed the animals to maintain calcification and to partially repair shell dissolution. These observations of the long-term chronic effects of increased CO2 levels forewarn of changes we can expect in marine ecosystems as CO2 emissions continue to rise unchecked, and support the hypothesis that ocean acidification contributed to past extinction events. The ability to adapt through dwarfing can confer physiological advantages as the rate of CO2 emissions contines to increase
Determines the effects of the three most commonly used reagents, H2O2, NaOCl (commercial Clorox), and NaOH, on both the organic and mineral components of carbonate skeletons. -from Authors
We show that death by dissolution is an important size-dependent mortality factor for juvenile bivalves. Utilizing a new experimental design, we were able to replicate saturation states in sediments after values frequently encountered by Mercenaria mercenaria in coastal deposits (Omega(aragonite) = 0.4 and 0.6). When 0.2-mm M. mercenaria were reared in sediments at Omega(aragonite) = 0.4 and 0.6, significant daily losses of living individuals occurred (14.0% and 14.4% d(-1), respectively), relative to supersaturated-control sediments (3.9% d(-1)). For 0.4-mm M. mercenaria, significant mortality occurred under the most undersaturated conditions (Omega(aragonite) = 0.4, mortality = 9.6% d(-1)), although mortality at Omega(aragonite) = 0.6 was not significant (mortality = 2.7% d(-1); control-saturated mortality = 0.2% d(-1)). For the largest size- class investigated, 0.6 mm, we show significant mortality for clams under the most undersaturated sediments (Omega(aragonite) = 0.4, 2.8% d(-1)). To test if buffered sediments would increase survivorship of juvenile bivalves during periods of recruitment, we manually manipulated sediment saturation state by adding crushed Mya arenaria shell to a mud flat in West Bath, Maine, U.S. A. Although we increased the average sediment saturation state within retrieved cores from Omega = 0.25 +/- 0.01 to only 0.53 +/- 0.06, numbers of live M. arenaria in buffered sediment increased almost three-fold in 2 weeks. Buffering muds against the metabolic acids that cause lowered saturation states may represent a potentially important management strategy to decrease dissolution mortality.
Outer organic layer and internal repair mechanism protects pteropod Limacina helicina from ocean acidification
- S Lischka
Lischka, S., et al., 2011. Impact of ocean acidification and elevated temperatures on
early juveniles pteropod Limacina helicina. Biogeosci. Discuss. 7 (6), 8214.
Peck, V., et al., 2016. Outer organic layer and internal repair mechanism protects
pteropod Limacina helicina from ocean acidification. Deep Sea Research II 127,
41-52.