Impacts of ocean acidification on marine shelled molluscs

Over the next century, elevated quantities of atmospheric CO₂ are expected to penetrate into the oceans, causing a reduction in pH (?0.3/?0.4 pH unit in the surface ocean) and in the concentration of carbonate ions (so-called ocean acidification). Of growing concern are the impacts that this will have on marine and estuarine organisms and ecosystems. Marine shelled molluscs, which colonized a large latitudinal gradient and can be found from intertidal to deep-sea habitats, are economically and ecologically important species providing essential ecosystem services including habitat structure for benthic organisms, water purification and a food source for other organisms. The effects of ocean acidification on the growth and shell production by juvenile and adult shelled molluscs are variable among species and even within the same species, precluding the drawing of a general picture. This is, however, not the case for pteropods, with all species tested so far, being negatively impacted by ocean acidification. The blood of shelled molluscs may exhibit lower pH with consequences for several physiological processes (e.g. respiration, excretion, etc.) and, in some cases, increased mortality in the long term. While fertilization may remain unaffected by elevated pCO₂, embryonic and larval development will be highly sensitive with important reductions in size and decreased survival of larvae, increases in the number of abnormal larvae and an increase in the developmental time. There are big gaps in the current understanding of the biological consequences of an acidifying ocean on shelled molluscs. For instance, the natural variability of pH and the interactions of changes in the carbonate chemistry with changes in other environmental stressors such as increased temperature and changing salinity, the effects of species interactions, as well as the capacity of the organisms to acclimate and/or adapt to changing environmental conditions are poorly described.     

Impact of ocean acidification on marine ecosystems: educational challenges and innovations

Population growth and social/technological developments have resulted in the buildup of carbon dioxide (CO₂) in the atmosphere and oceans to the extent that we now see changes in the earth’s climate and ocean chemistry. Ocean acidification is one consequence of these changes, and it is known with certainty that it will continue to increase as we emit more CO₂ into the atmosphere. Ocean acidification is a global issue likely to impact marine organisms, food webs and ecosystems and to be most severely experienced by the people who depend on the goods and services the ocean provides at regional and local levels. However, research is in its infancy and the available data on biological impacts are complex (e.g., species-specific response). Educating future generations on the certainties and uncertainties of the emerging science of ocean acidification and its complex consequences for marine species and ecosystems can provide insights that will help assessing the need to mitigate and/or adapt to future global change. This article aims to present different educational approaches, the different material available and highlight the future challenges of ocean acidification education for both educators and marine biologists.     

Effects of ocean acidification, temperature and nutrient regimes on the appendicularian Oikopleura dioica: a mesocosm study

Increasing pCO₂ is hypothesized to induce shifts in plankton communities toward smaller cells, reduced carbon export rates and increased roles of gelatinous zooplankton. Appendicularians, among the most numerous pan-global “gelatinous” zooplankton, continuously produce filter-feeding houses, shortcutting marine food webs by ingesting submicron particles, and their discarded houses contribute significantly to carbon fluxes. We present a first mesocosm-scale study on the effects of temperature, pCO₂ and bloom structures on the appendicularian, Oikopleura dioica. There were effects of temperature and nutrients on phytoplankton communities. No shifts in functional phytoplankton groups, nor changes in particle sizes/morphotypes, known to impact appendicularian feeding, were observed under manipulated pCO₂ conditions. However, appendicularian abundance was positively correlated with increased pCO₂, temperature and nutrient levels, consistent with hypotheses concerning gelatinous zooplankton in future oceans. This suggests appendicularians will play more important roles in marine pelagic communities and vertical carbon transport under projected ocean acidification and elevated temperature scenarios.     

Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents

We present the first study of the effects of ocean acidification on settlement of benthic invertebrates and microfauna. Artificial collectors were placed for 1 month along pH gradients at CO₂ vents off Ischia (Tyrrhenian Sea, Italy). Seventy-nine taxa were identified from six main taxonomic groups (foraminiferans, nematodes, polychaetes, molluscs, crustaceans and chaetognaths). Calcareous foraminiferans, serpulid polychaetes, gastropods and bivalves showed highly significant reductions in recruitment to the collectors as pCO₂ rose from normal (336–341 ppm, pH 8.09–8.15) to high levels (886–5,148 ppm) causing acidified conditions near the vents (pH 7.08–7.79). Only the syllid polychaete Syllis prolifera had higher abundances at the most acidified station, although a wide range of polychaetes and small crustaceans was able to settle and survive under these conditions. A few taxa (Amphiglena mediterranea, Leptochelia dubia, Caprella acanthifera) were particularly abundant at stations acidified by intermediate amounts of CO₂ (pH 7.41–7.99). These results show that increased levels of CO₂ can profoundly affect the settlement of a wide range of benthic organisms.     

Health and population-dependent effects of ocean acidification on the marine isopod Idotea balthica

Three populations of the grazing isopod Idotea balthica were exposed to high CO₂ treatment for a period of 20 days to investigate the effect of ocean acidification (OA) on animal health and immunocompetence. The results of the populations from more saline habitats were comparable and showed a 60–80 % decrease in immune response as a result of the high CO₂ treatment. Analysis of protein carbonyls showed no treatment effect, indicating that short-term OA does not increase oxidative protein damage. Meanwhile, the third tested population from the lower saline Baltic Sea had higher background protein carbonyl levels. Ocean acidification in addition to this resulted in 100 % mortality. The results of this study show that OA reduced immunocompetence of this marine isopod. In addition, populations and individuals in poor health are potentially at greater risk to succumb under OA.     

Seasonal variation in the effects of ocean warming and acidification on a native bryozoan, Celleporaria nodulosa

Ocean warming and acidification are co-occurring stressors likely to affect marine biota through climate-driven change to the ocean. We investigated the effects of increased temperature and lowered pH, solely and in combination, on the growth of the endemic Australian bryozoan, Celleporaria nodulosa. Two temperatures and three pH levels were fully crossed in experimental treatments performed in winter 2008 (August) and summer 2009 (February/March). Fragments of C. nodulosa colonies (clones) were collected from Coffs Harbour, NSW, Australia, (30°18′S, 153°09′E) and elongation of colonies was assessed periodically over a 12-day incubation period. Lowered pH in winter significantly decreased growth. Elevated temperatures during the summer significantly impeded the growth of bryozoan colonies, possibly masking the effect of ocean acidification and discovering a maximal thermal tolerance at around 27 °C for C. nodulosa. The effects of decreased pH and increased temperature may be seasonally dependent and particularly acute during the summer months. Thermal stress may in fact be the initial stressor before ocean acidification, negatively affecting organisms in such a way that they are unable to survive before feeling the effects of ocean acidification.     

Simulating the fate of Florida Snowy Plovers with sea-level rise: Exploring research and management priorities with a global uncertainty and sensitivity analysis perspective

Changes in coastal habitats due to sea-level rise provide an uncertain, yet significant threat to shoreline dependent birds. Rising sea levels can cause habitat fragmentation and loss which can result in considerable reduction in their foraging and nesting areas. Computational models and their algorithmic assumptions play an integral role in exploring potential mitigation responses to uncertain and potentially adverse ecological outcomes. The presence of uncertainty in metapopulation models is widely acknowledged but seldom considered in their development and evaluation, specifically the effects of uncertain model inputs on the model outputs. This paper was aimed to (1) quantify the contribution of each uncertain input factor to the uncertainty in the output of a metapopulation model which evaluated the effects of long-term sea-level rise on the population of Snowy Plovers (Charadrius alexandrinus) found in the Gulf Coast of Florida, and (2) determine the ranges of model inputs that produced a specific output for the purpose of formulating environmental management decisions. This was carried out by employing global sensitivity and uncertainty analysis (GSA) using two generic (model independent) methods, the qualitative screening Morris method and a quantitative variance-based Sobol’ method coupled with Monte Carlo filtering. The analyses were applied to three density dependence scenarios: assuming a ceiling-type density dependence, assuming a contest-type density dependence, and assuming that density dependence is uncertain as to being ceiling- or contest-dependent. The sources of uncertainty in the outputs depended strongly on the type of density dependence considered in the model. In general, uncertainty in the outputs highly depended on the uncertainty in stage matrix elements (fecundity, adult survival, and juvenile survival), dispersal rate from central areas with low current populations (the “Big Bend” area of Florida) to the northern, panhandle populations, the maximum growth rate, and density dependence type. Our results showed that increasing the maximum growth rate to a value of 1.2 or larger will increase the final average population of Snowy Plovers assuming a contest-type density dependence. Results suggest that studies that further quantify which density dependence relationship best describes Snowy Plover population dynamics should be conducted since this is the main driver of uncertainty in model outcomes. Furthermore, investigating the presence of Snowy Plovers in the Big Bend region may be important for providing connection between the panhandle and peninsula populations.     

The effect of ocean acidification on early algal colonization stages at natural CO2 vents

Marine algae exhibit different responses to ocean acidification, suggesting that a decrease in pH does not always favour marine photosynthetic organisms. In order to understand the effect of acidification on algal community development, early colonization stages were investigated using carbon dioxide vents around the Castello Aragonese (Ischia, Italy) as a natural laboratory. Settlement tiles were placed in zones with different pH (normal, medium and low), and species composition and coverage measured after 2, 3 and 4 months of deployment. The number of species decreased by 4 and 18 % at medium and low pH zones, respectively (P < 0.05). The structure of the algal assemblage differed between pH zones during the 4 months of the experiment, due to the addition and/or replacement of new species. This leads to a change in the succession of morphological forms as soft crustose algae replaced calcareous species, and turf species were dominant in cover; more complex thalli started to occur only at medium pH. These results support previous findings that ocean acidification will induce changes in benthic algal communities.     

One size fits all: stability of metabolic scaling under warming and ocean acidification in echinoderms

Responses by marine species to ocean acidification (OA) have recently been shown to be modulated by external factors including temperature, food supply and salinity. However the role of a fundamental biological parameter relevant to all organisms, that of body size, in governing responses to multiple stressors has been almost entirely overlooked. Recent consensus suggests allometric scaling of metabolism with body size differs between species, the commonly cited ‘universal’ mass scaling exponent (b) of ¾ representing an average of exponents that naturally vary. One model, the Metabolic-Level Boundaries hypothesis, provides a testable prediction: that b will decrease within species under increasing temperature. However, no previous studies have examined how metabolic scaling may be directly affected by OA. We acclimated a wide body-mass range of three common NE Atlantic echinoderms (the sea star Asterias rubens, the brittlestars Ophiothrix fragilis and Amphiura filiformis) to two levels of pCO₂ and three temperatures, and metabolic rates were determined using closed-chamber respirometry. The results show that contrary to some models these echinoderm species possess a notable degree of stability in metabolic scaling under different abiotic conditions; the mass scaling exponent (b) varied in value between species, but not within species under different conditions. Additionally, we found no effect of OA on metabolic rates in any species. These data suggest responses to abiotic stressors are not modulated by body size in these species, as reflected in the stability of the metabolic scaling relationship. Such equivalence in response across ontogenetic size ranges has important implications for the stability of ecological food webs.     

Effects of ocean acidification on the early developmental stages of the horned turban,Turbo cornutus

To estimate the impact of CO₂-driven ocean acidification on the early life stages of gastropods, the effects of increased partial pressure of seawater carbon dioxide (pCO₂) (800–2,000 μatm) on the early developmental stages and larval shell length of the commercially important gastropod, the horned turban snail, Turbo cornutus were investigated. Increase in experimental seawater pCO₂ had an increasingly negative impact on the early developmental rate; the proportion of embryos or larvae displaying retarded development increased at higher pCO₂. The proportion of embryos that developed to the 4-cell stage at 2 h after fertilization decreased linearly with increasing pCO₂. At ~1,000 μatm pCO₂, retarded development was observed in ~50 % of larvae. No embryos developed to the 4-cell stage at 2,000 μatm pCO₂ within 2 h of fertilization. A similar trend continued until 24–26 h after fertilization; the proportion of larvae attaining veliger stage by 24–26 h also decreased with increasing pCO₂. The shell length of T. cornutus veligers decreased gradually as seawater pCO₂ increased, but markedly decreased in seawater under nearly unsaturated and unsaturated conditions (≤1.04) of the aragonite saturation state (Ω _aragonite). The results indicate that increased pCO₂ seawater has a progressive and acute effect on embryonic and larval T. cornutus, and imply that the extended early developmental period and/or the downsized larval shell produced by ocean acidification will have a negative impact on survival, settlement and recruitment well into the future.     

Impact of ocean acidification on escape performance of the king scallop, Pecten maximus, from Norway

The ongoing process of ocean acidification already affects marine life, and according to the concept of oxygen and capacity limitation of thermal tolerance, these effects may be intensified at the borders of the thermal tolerance window. We studied the effects of elevated CO₂ concentrations on clapping performance and energy metabolism of the commercially important scallop Pecten maximus. Individuals were exposed for at least 30 days to 4 °C (winter) or to 10 °C (spring/summer) at either ambient (0.04 kPa, normocapnia) or predicted future PCO₂ levels (0.11 kPa, hypercapnia). Cold-exposed (4 °C) groups revealed thermal stress exacerbated by PCO₂ indicated by a high mortality overall and its increase from 55 % under normocapnia to 90 % under hypercapnia. We therefore excluded the 4 °C groups from further experimentation. Scallops at 10 °C showed impaired clapping performance following hypercapnic exposure. Force production was significantly reduced although the number of claps was unchanged between normocapnia- and hypercapnia-exposed scallops. The difference between maximal and resting metabolic rate (aerobic scope) of the hypercapnic scallops was significantly reduced compared with normocapnic animals, indicating a reduction in net aerobic scope. Our data confirm that ocean acidification narrows the thermal tolerance range of scallops resulting in elevated vulnerability to temperature extremes and impairs the animal’s performance capacity with potentially detrimental consequences for its fitness and survival in the ocean of tomorrow.     

Effects of feeding and light intensity on the response of the coral Porites rus to ocean acidification

Recently, it has been suggested that there are conditions under which some coral species appear to be resistant to the effects of ocean acidification. To test if such resistance can be explained by environmental factors such as light and food availability, the present study investigated the effect of 3 feeding regimes crossed with 2 light levels on the response of the coral Porites rus to 2 levels of pCO₂ at 28 °C. After 1, 2, and 3 weeks of incubation under experimental conditions, none of the factors—including pCO₂—significantly affected area-normalized calcification and biomass-normalized calcification. Biomass also was unaffected during the first 2 weeks, but after 3 weeks, corals that were fed had more biomass per unit area than starved corals. These results suggest that P. rus is resistant to short-term exposure to high pCO₂, regardless of food availability and light intensity. P. rus might therefore represent a model system for exploring the genetic basis of tolerance to OA.     

Escape performance of temperate king scallop,Pecten maximus under ocean warming and acidification

Among bivalves, scallops are exceptional due to their capacity to escape from predators by swimming which is provided by rapid and strong claps that are produced by the phasic muscle interspersed with tonic muscle contractions. Based on the concept of oxygen and capacity-limited thermal tolerance, the following hypothesis was tested: ocean warming and acidification (OWA) would induce disturbances in aerobic metabolic scope and extracellular acid-case status and impair swimming performance in temperate scallops. Following long-term incubation under near-future OWA scenarios [20 vs. 10 °C (control) and 0.112 kPa CO₂ (hypercapnia) vs. 0.040 kPa CO₂ (normocapnic control)], the clapping performance and metabolic rates (MR) were measured in resting (RMR) and fatigued (maximum MR) king scallops, Pecten maximus, from Roscoff, France. Exposure to OA, either alone or combined with warming, left MR and swimming parameters such as the total number of claps and clapping forces virtually unchanged. Only the duration of the escape response was affected by OA which caused earlier exhaustion in hyper- than in normocapnic scallops at 10 °C. While maximum MR was unaffected, warm exposure increased RMR in both normocapnic and hypercapnic P. maximus resulting in similar Q ₁₀ values of ~2.2. The increased costs of maintenance and the observation of strongly reduced haemolymph PO₂ levels indicate that at 20 °C scallops have reached the upper thermal pejus range with unbalanced capacities for aerobic energy metabolism. As a consequence, warming to 20 °C decreased mean phasic force during escape performance until fatigue. The observed prolonged recovery time in warm incubated scallops might be a consequence of elevated metabolic costs at reduced oxygen availability in the warmth.     

Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification

Climate change driven ocean acidification and hypercapnia may have a negative impact on fertilization in marine organisms because of the narcotic effect these stressors exert on sperm. In contrast, warmer, less viscous water may have a positive influence on sperm swimming speed and so ocean warming may enhance fertilization. To address questions on future vulnerabilities we examined the interactive effects of near-future ocean warming and ocean acidification/hypercapnia on fertilization in intertidal and shallow subtidal echinoids (Heliocidaris erythrogramma, H. tuberculata, Tripneustes gratilla, Centrostephanus rodgersii), an asteroid (Patiriella regularis) and an abalone (Haliotis coccoradiata). Batches of eggs from multiple females were fertilized by sperm from multiple males in all combinations of three temperature and three \textpH/P_\textCO2 {\text{pH}}/P_{{{\text{CO}}_{2} }} treatments. Experiments were placed in the setting of projected near-future conditions for southeast Australia, an ocean change hot spot. There was no significant effect of warming and acidification on the percentage of fertilization. These results indicate that fertilization in these species is robust to temperature and \textpH/P_\textCO2 {\text{pH}}/P_{{{\text{CO}}_{2} }} fluctuation. This may reflect adaptation to the marked fluctuation in temperature and pH that characterises their shallow water coastal habitats. Efforts to identify potential impacts of ocean change to the life histories of coastal marine invertebrates are best to focus on more vulnerable embryonic and larval stages because of their long time in the water column where seawater chemistry and temperature have a major impact on development.