Description: Ocean acidification (OA) research seeks to understand how marine ecosystems and global elemental cycles will respond to changes in seawater carbonate chemistry in combination with other environmental perturbations such as warming, eutrophication, and deoxygenation. Here, we discuss the effectiveness and limitations of current research approaches used to address this goal. A diverse combination of approaches is essential to decipher the consequences of OA to marine organisms, communities, and ecosystems. Consequently, the benefits and limitations of each approach must be considered carefully. Major research challenges involve experimentally addressing the effects of OA in the context of large natural variability in seawater carbonate system parameters and other interactive variables, integrating the results from different research approaches, and scaling results across different temporal and spatial scales.

Description: The impact of anthropogenic ocean acidification (OA) on marine ecosystems is a vital concern facing marine scientists and managers of ocean resources. Euthecosomatous pteropods (holoplanktonic gastropods) represent an excellent sentinel for indicating exposure to anthropogenic OA because of the sensitivity of their aragonite shells to the OA conditions less favorable for calcification. However, an integration of observations, experiments and modelling efforts is needed to make accurate predictions of how these organisms will respond to future changes to their environment. Our understanding of the underlying organismal biology and life history is far from complete and must be improved if we are to comprehend fully the responses of these organisms to the multitude of stressors in their environment beyond OA. This review considers the present state of research and understanding of euthecosomatous pteropod biology and ecology of these organisms and considers promising new laboratory methods, advances in instrumentation (such as molecular, trace elements, stable isotopes, palaeobiology alongside autonomous sampling platforms, CT scanning and high-quality video recording) and novel field-based approaches (i.e. studies of upwelling and CO2 vent regions) that may allow us to improve our predictive capacity of their vulnerability and/or resilience. In addition to playing a critical ecological and biogeochemical role, pteropods can offer a significant value as an early-indicator of anthropogenic OA. This role as a sentinel species should be developed further to consolidate their potential use within marine environmental management policy making.

Description: The diversity of life in the sea is critical to the health of ocean ecosystems that support living resources and therefore essential to the economic, nutritional, recreational, and health needs of billions of people. Yet there is evidence that the biodiversity of many marine habitats is being altered in response to a changing climate and human activity. Understanding this change, and forecasting where changes are likely to occur, requires monitoring of organism diversity, distribution, abundance, and health. It requires a minimum of measurements including productivity and ecosystem function, species composition, allelic diversity, and genetic expression. These observations need to be complemented with metrics of environmental change and socio-economic drivers. However, existing global ocean observing infrastructure and programs often do not explicitly consider observations of marine biodiversity and associated processes. Much effort has focused on physical, chemical and some biogeochemical measurements. Broad partnerships, shared approaches, and best practices are now being organized to implement an integrated observing system that serves information to resource managers and decision-makers, scientists and educators, from local to global scales. This integrated observing system of ocean life is now possible due to recent developments among satellite, airborne, and in situ sensors in conjunction with increases in information system capability and capacity, along with an improved understanding of marine processes represented in new physical, biogeochemical, and biological models.

Description: Interpreting the vulnerability of pelagic calcifiers to ocean acidification (OA) is enhanced by an understanding of their critical thresholds and how these thresholds are modified by other climate change stressors (e.g., warming). To address this need, we undertook a three-part data synthesis for pteropods, one of the calcifying zooplankton group. We conducted the first meta-analysis and threshold analysis of literature characterizing pteropod responses to OA and warming by synthetizing dataset comprising of 2,097 datapoints. Meta-analysis revealed the extent to which responses among studies conducted on differing life stages and disparate geographies could be integrated into a common analysis. The results demonstrated reduced calcification, growth, development, and survival to OA with increased magnitude of sensitivity in the early life stages, under prolonged duration, and with the concurrent exposure of OA and warming, but not species-specific sensitivity. Second, breakpoint analyses identified OA thresholds for several endpoints: dissolution (mild and severe), calcification, egg development, shell growth, and survival. Finally, consensus by a panel of pteropod experts was used to verify thresholds and assign confidence scores for five endpoints with a sufficient signal: noise ratio to develop life-stage specific, duration-dependent thresholds. The range of aragonite saturation state from 1.5–0.9 provides a risk range from early warning to lethal impacts, thus providing a rigorous basis for vulnerability assessments to guide climate change management responses, including an evaluation of the efficacy of local pollution management. In addition, meta-analyses with OA, and warming shows increased vulnerability in two pteropod processes, i.e., shell dissolution and survival, and thus pointing toward increased threshold sensitivity under combined stressor effect.

Description: Estuaries are recognized as one of the habitats most vulnerable to coastal ocean acidification due to seasonal extremes and prolonged duration of acidified conditions. This is combined with co-occurring environmental stressors such as increased temperature and low dissolved oxygen. Despite this, evidence of biological impacts of ocean acidification in estuarine habitats is largely lacking. By combining physical, biogeochemical, and biological time-series observations over relevant seasonal-to-interannual time scales, this study is the first to describe both the spatial and temporal variation of biological response in the pteropod Limacina helicina to estuarine acidification in association with other stressors. Using clustering and principal component analyses, sampling sites were grouped according to their distribution of physical and biogeochemical variables over space and time. This identified the most exposed habitats and time intervals corresponding to the most severe negative biological impacts across three seasons and three years. We developed a cumulative stress index as a means of integrating spatial-temporal OA variation over the organismal life history. Our findings show that over the 2014–2016 study period, the severity of low aragonite saturation state combined with the duration of exposure contributed to overall cumulative stress and resulted in severe shell dissolution. Seasonally-variable estuaries such as the Salish Sea (Washington, U.S.A.) predispose sensitive organisms to more severe acidified conditions than those of coastal and open-ocean habitats, yet the sensitive organisms persist. We suggest potential environmental factors and compensatory mechanisms that allow pelagic calcifiers to inhabit less favorable habitats and partially offset associated stressors, for instance through food supply, increased temperature, and adaptation of their life history. The novel metric of cumulative stress developed here can be applied to other estuarine environments with similar physical and chemical dynamics, providing a new tool for monitoring biological response in estuaries under pressure from accelerating global change.

Description: Pteropods are a group of holoplanktonic gastropods for which global biomass distribution patterns remain poorly resolved. The aim of this study was to collect and synthesize existing pteropod (Gymnosomata, Thecosomata and Pseudothecosomata) abundance and biomass data, in order to evaluate the global distribution of pteropod carbon biomass, with a particular emphasis on its seasonal, temporal and vertical patterns. We collected 25 902 data points from several online databases and a number of scientific articles. The biomass data has been gridded onto a 360 x 180° grid, with a vertical resolution of 33 WOA depth levels. Data has been converted to NetCDF format. Data were collected between 1951-2010, with sampling depths ranging from 0-1000 m. Pteropod biomass data was either extracted directly or derived through converting abundance to biomass with pteropod specific length to weight conversions. In the Northern Hemisphere (NH) the data were distributed evenly throughout the year, whereas sampling in the Southern Hemisphere was biased towards the austral summer months. 86% of all biomass values were located in the NH, most (42%) within the latitudinal band of 30-50° N. The range of global biomass values spanned over three orders of magnitude, with a mean and median biomass concentration of 8.2 mg C l-1 (SD = 61.4) and 0.25 mg C l-1, respectively for all data points, and with a mean of 9.1 mg C l-1 (SD = 64.8) and a median of 0.25 mg C l-1 for non-zero biomass values. The highest mean and median biomass concentrations were located in the NH between 40-50° S (mean biomass: 68.8 mg C l-1 (SD = 213.4) median biomass: 2.5 mg C l-1) while, in the SH, they were within the 70-80° S latitudinal band (mean: 10.5 mg C l-1 (SD = 38.8) and median: 0.2 mg C l-1). Biomass values were lowest in the equatorial regions. A broad range of biomass concentrations was observed at all depths, with the biomass peak located in the surface layer (0-25 m) and values generally decreasing with depth. However, biomass peaks were located at different depths in different ocean basins: 0-25 m depth in the N Atlantic, 50-100 m in the Pacific, 100-200 m in the Arctic, 200-500 m in the Brazilian region and 〉500 m in the Indo-Pacific region. Biomass in the NH was relatively invariant over the seasonal cycle, but more seasonally variable in the SH. The collected database provides a valuable tool for modellers for the study of ecosystem processes and global biogeochemical cycles.

Description: 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. Due to temporal overlap between an El Niño event and springtime intensification of the upwelling, pteropods of the California Current System 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. OA stress induced 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 (chorolophyll) 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). Since this co-incides with the conditions in the natural settings, we can expect non-linear impact on physiological responses. 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 low Ωar on abundance suggest 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. Because pteropods contain high quantities of polyunsaturated fatty acids, oxidative stress causes LPX, resulting in the loss of lipid reserves and structural damage of cell membranes; corroborating pteropods' extreme sensitivity to OA. Accumulation of oxidative damage requires metabolic compensation, implying energetic trade-offs under combined thermal and OA stress. Oxidative stress biomarkers can be used as an early-warning signal of multiple stress on the cellular level, thereby providing important new insights into factors that set limits to species' tolerance of multiple drivers in the natural environment, especially when mechanistically linked though energetic implications.

Description: The pteropod Limacina helicina frequently experiences seasonal exposure to corrosive conditions (Omega arag  〈 1) along the US West Coast and is recognized as one of the species most susceptible to ocean acidification (OA). Yet, little is known about their capacity to acclimatize to such conditions. We collected pteropods in the California Current Ecosystem (CCE) that differed in the severity of exposure to Omega arag conditions in the natural environment. Combining field observations, high-CO2 perturbation experiment results, and retrospective ocean transport simulations, we investigated biological responses based on histories of magnitude and duration of exposure to Omega arag  〈 1. Our results suggest that both exposure magnitude and duration affect pteropod responses in the natural environment. However, observed declines in calcification performance and survival probability under high CO2 experimental conditions do not show acclimatization capacity or physiological tolerance related to history of exposure to corrosive conditions. Pteropods from the coastal CCE appear to be at or near the limit of their physiological capacity, and consequently, are already at extinction risk under projected acceleration of OA over the next 30 years. Our results demonstrate that Omega arag  exposure history largely determines pteropod response to experimental conditions and is essential to the interpretation of biological observations and experimental results.