The response of two ecologically important Antarctic invertebrates (Sterechinus neumayeri and Parborlasia corrugatus) to reduced seawater pH: effects on fertilisation and embryonic development

Ocean acidification, or the lowering of seawater pH, is caused by sequestration of atmospheric CO₂ into the oceans. This study investigated the effects of present-day pH 8.0, predicted ocean surface pH for the years 2100 and 2300 (pH 7.7 and pH 7.3, respectively) and an extreme pH (pH 7.0) on fertilisation and embryogenesis in the Antarctic nemertean worm Parborlasia corrugatus and sea urchin Sterechinus neumayeri. Fertilisation success was not affected by pH in P. corrugatus across a range of sperm concentrations. Fertilisation success in S. neumayeri declined significantly in pH 7.0 and 7.3 seawater, but only at a low sperm concentration. Seawater pH had no effect on the rate of egg cleavage in S. neumayeri, or the proportion of abnormal embryos 1-day post-fertilisation. P. corrugatus embryogenesis was also relatively robust to pH changes, with a significant effect detected only when the seawater pH was decreased to 7.0. While fertilisation and early cell division were relatively robust, later development through to the gastrula was sensitive to pH. In S. neumayeri, an effect of pH on development was evident by the gastrula stage, while there were significantly more abnormal P. corrugatus embryos in pH 7.0 up to the blastula stage, and in pH 7.0 and pH 7.3 at the coeloblastula stage. Our results are similar to the observations on other marine invertebrate species where fertilisation and early embryonic development are generally robust to lowered seawater pH, while the older coeloblastula and gastrula stages are more responsive. We also found no evidence to suggest that Antarctic species are more adversely affected by lower seawater pH compared with the findings for non-Antarctic counterparts. We conclude that in the two species we examined, near-future decreases in pH (decreases of ≈0.3–0.5 pH units) may not have a significant effect on fertilisation and early embryogenesis, while predicted longer term decreases (decreases of ≈0.7–0.77 pH units) could reduce fertilisation success in S. neumayeri if sperm concentrations are low and may increase abnormalities in P. corrugatus during later embryogenesis.     

Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis

Anthropogenic CO₂ emissions are acidifying the world’s oceans. A growing body of evidence demonstrates that ocean acidification can impact survival, growth, development and physiology of marine invertebrates. Here, we tested the impact of long-term (up to 16 months) and trans-life-cycle (adult, embryo/larvae and juvenile) exposure to elevated pCO₂ (1,200 μatm, compared to control 400 μatm) on the green sea urchin Strongylocentrotus droebachiensis. Female fecundity was decreased 4.5-fold when acclimated to elevated pCO₂ for 4 months during reproductive conditioning, while no difference was observed in females acclimated for 16 months. Moreover, adult pre-exposure for 4 months to elevated pCO₂ had a direct negative impact on subsequent larval settlement success. Five to nine times fewer offspring reached the juvenile stage in cultures using gametes collected from adults previously acclimated to high pCO₂ for 4 months. However, no difference in larval survival was observed when adults were pre-exposed for 16 months to elevated pCO₂. pCO₂ had no direct negative impact on juvenile survival except when both larvae and juveniles were raised in elevated pCO₂. These negative effects on settlement success and juvenile survival can be attributed to carry-over effects from adults to larvae and from larvae to juveniles. Our results support the contention that adult sea urchins can acclimate to moderately elevated pCO₂ in a matter of a few months and that carry-over effects can exacerbate the negative impact of ocean acidification on larvae and juveniles.     

CO2 leakage simulation: effects of the pH decrease on fertilisation and larval development of Paracentrotus lividus and sediment metals toxicity

Carbon capture and storage has become a new mitigation option to reduce anthropogenic CO₂ emissions. The effects of the CO₂-related acidification, associated with unpredictable leaks of CO₂ during the operational phases were studied using the Paracentrotus lividus sea urchin-liquid-phase-assays (fertilisation and embryo-larval development tests). Besides to the direct effects of the CO₂-associated pH decrease, the possible effects on marine sediment toxicity were studied by exposing the urchin larvae to elutriate of sediments with different metals concentration, which were subjected to various pH treatments. The resulted median toxic effect pH ranged from 6.33?±?0.02 and 6.91?±?0.01 for the egg fertilisation, and between 6.66?±?0.03 and 7.16?±?0.01 for the larval development assays. Concentrations of Co, Zn, As, Cu, and Fe were detected in the sediment elutriates. For all the sediment elutriates tested the amount of the dissolved Zn increased in parallel with the pH reductions. Correlated effects of acidification, biological response, and the presence of dissolved metals were observed in this work evidencing that the most important factor controlling the reduction of egg fertilisation and larval development success was the combined effects of the reduction of pH and the presence of the contaminants (mainly Zn, Co, and As).     

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.     

Impact of ocean acidification in the metabolism and swimming behavior of the dolphinfish (Coryphaena hippurus) early larvae

Since the industrial revolution, [CO₂]_atm has increased from 280 μatm to levels now exceeding 380 μatm and is expected to rise to 730–1,020 μatm by the end of this century. The consequent changes in the ocean’s chemistry (e.g., lower pH and availability of the carbonate ions) are expected to pose particular problems for marine organisms, especially in the more vulnerable early life stages. The aim of this study was to investigate how the future predictions of ocean acidification may compromise the metabolism and swimming capabilities of the recently hatched larvae of the tropical dolphinfish (Coryphaena hippurus). Here, we show that the future environmental hypercapnia (ΔpH 0.5; 0.16 % CO₂, ~1,600 μatm) significantly (p < 0.05) reduced oxygen consumption rate up to 17 %. Moreover, the swimming duration and orientation frequency also decreased with increasing pCO₂ (50 and 62.5 %, respectively). We argue that these hypercapnia-driven metabolic and locomotory challenges may potentially influence recruitment, dispersal success, and the population dynamics of this circumtropical oceanic top predator.     

The physiological and molecular responses of larvae from the reef-building coral Pocillopora damicornis exposed to near-future increases in temperature and pCO2

Given the threats of greenhouse gas emissions and a changing climate to marine ecosystems, there is an urgent need to better understand the response of not only adult corals, which are particularly sensitive to environmental changes, but also their larvae, whose mechanisms of acclimation to both temperature increases and ocean acidification are not well understood. Brooded larvae from the reef coral Pocillopora damicornis collected from Nanwan Bay, Southern Taiwan, were exposed to ambient or elevated temperature (25 or 29 °C) and pCO₂ (415 or 635 μatm) in a factorial experiment for 9 days, and a variety of physiological and molecular parameters were measured. Respiration and rubisco protein expression decreased in larvae exposed to elevated temperature, while those incubated at high pCO₂ were larger in size. Collectively, these findings highlight the complex metabolic and molecular responses of this life history stage and the need to integrate our understanding across multiple levels of biological organization. Our results also suggest that for this pocilloporid larval life stage, the impacts of elevated temperature are likely a greater threat under near-future predictions for climate change than ocean acidification.     

海洋酸化对鱼类感觉和行为影响的研究进展

海洋酸化是指大气增多的二氧化碳(CO2)溶解于海水而导致海水p H值降低的过程。海洋酸化将改变海水碳酸盐平衡体系,使依赖于原化学环境的多种海洋生物乃至生态系统面临巨大威胁。海洋酸化对钙质生物影响的研究最早引起大家关注,而海洋鱼类具有较完善的酸碱调节机制,大家普遍认为酸化对其影响不大。但在过去的5年中,不少实验证明海洋酸化会影响海洋鱼类仔稚鱼的感觉和行为,减弱其野外的生存能力及增加被捕食率,很可能将威胁自然种群补给量和影响全球的渔业资源量。本文从嗅觉、听觉、视觉及高级意识和相关行为角度,综述近几年海洋酸化对鱼类感觉和行为影响的研究进展,介绍了鱼类神经行为生物学的研究,为全面了解和预测海洋酸化的生态、经济和社会效应提供科学依据。     

Within- and transgenerational effects of ocean acidification on life history of marine three-spined stickleback (Gasterosteus aculeatus)

Some studies have demonstrated that elevated CO₂ concentrations in ocean waters negatively impact metabolism and development of marine fish. Particularly, early developmental stages are probably more susceptible to ocean acidification due to insufficient regulations of their acid-base balance. Transgenerational acclimation can be an important mechanism to mediate impacts of increased CO₂ on marine species, yet very little is known about the potential of parental effects in teleosts. Therefore, transgenerational effects were investigated on life history in juvenile three-spined sticklebacks Gasterosteus aculeatus by acclimating parents (collected in April 2012, 55°03′N, 8°44′E) and offspring to ambient (~400 µatm) and elevated (~1,000 µatm) CO₂ levels and measured parental fecundity as well as offspring survival, growth and otolith characteristics. Exposure to elevated CO₂ concentrations led to an increase in clutch size in adults as well as increased juvenile survival and growth rates between 60 and 90 days post-hatch and enlarged otolith areas compared with fish from ambient CO₂ concentrations. Moreover, transgenerational effects were observed in reduced survival and body size 30 days post-hatch as well as in enlarged otoliths at the end of the experiment, when fathers or both parents were acclimated to the high-CO₂ environment. These results may suggest that elevated CO₂ concentrations had rather positive effects on life-history traits of three-spined sticklebacks, but that parental acclimation can modify these effects without improving offspring fitness. Although the mechanistic basis of such transgenerational acclimation remains unclear, selective gradients within generations seem to determine the direction of transgenerational effects.     

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.     

Structural and functional vulnerability to elevated pCO2 in marine benthic communities

The effect of elevated pCO₂/low pH on marine invertebrate benthic biodiversity, community structure and selected functional responses which underpin ecosystem services (such as community production and calcification) was tested in a medium-term (30 days) mesocosm experiment in June 2010. Standardised intertidal macrobenthic communities, collected (50.3567°N, 4.1277°W) using artificial substrate units (ASUs), were exposed to one of seven pH treatments (8.05, 7.8. 7.6, 7.4, 7.2, 6.8 and 6.0). Community net calcification/dissolution rates, as well as changes in biomass, community structure and diversity, were measured at the end of the experimental period. Communities showed significant changes in structure and reduced diversity in response to reduced pH: shifting from a community dominated by calcareous organisms to one dominated by non-calcareous organisms around either pH 7.2 (number of individuals and species) or pH 7.8 (biomass). These results were supported by a reduced total weight of CaCO₃ structures in all major taxa at lowered pH and a switch from net calcification to net dissolution around pH 7.4 (Ω_calc = 0.78, Ω_ara = 0.5). Overall community soft tissue biomass did not change with pH and high mortality was observed only at pH 6.0, although molluscs and arthropods showed significant decreases in soft tissue. This study supports and refines previous findings on how elevated pCO₂ can induce changes in marine biodiversity, underlined by differential vulnerability of different phyla. In addition, it shows significant elevated pCO₂-/low pH-dependent changes in fundamental community functional responses underpinning changes in ecosystem services.     

Populations of the Sydney rock oyster, Saccostrea glomerata, vary in response to ocean acidification

Acidifying oceans are predicted to fundamentally alter marine ecosystems. Over the next century, acute studies suggest that the impacts of climate change on marine organisms and ecosystems may be catastrophic. To date, however, little is known about whether the response of marine organisms varies within a species and whether this provides a potential ??adaptive capacity??. Here, we show that selectively bred lines of the ecologically and economically important estuarine mollusc, the Sydney rock oyster Saccostrea glomerata, are more resilient to ocean acidification than the wild populations. When reared at elevated pCO₂, we found a 25% reduction in shell growth of the selectively bred population of the Sydney rock oyster, Saccostrea glomerata, compared to a 64% reduction in shell growth of wild populations. This study shows that there are significantly different sensitivities to ocean acidification even within the same species, providing preliminary evidence that selective breeding may be a solution for important aquaculture industries to overcome the future effects of ocean acidification.     

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.     

Ocean acidification induces budding in larval sea urchins

Ocean acidification (OA), the reduction of ocean pH due to hydration of atmospheric CO₂, is known to affect growth and survival of marine invertebrate larvae. Survival and transport of vulnerable planktonic larval stages play important roles in determining population dynamics and community structures in coastal ecosystems. Here, we show that larvae of the purple urchin, Strongylocentrotus purpuratus, underwent high-frequency budding (release of blastula-like particles) when exposed to elevated pCO₂ level (>700 μatm). Budding was observed in >50 % of the population and was synchronized over short periods of time (~24 h), suggesting this phenomenon may be previously overlooked. Although budding can be a mechanism through which larval echinoids asexually reproduce, here, the released buds did not develop into viable clones. OA-induced budding and the associated reduction in larval size suggest new hypotheses regarding physiological and ecological tradeoffs between short-term benefits (e.g. metabolic savings and predation escape) and long-term costs (e.g. tissue loss and delayed development) in the face of climate change.     

Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei

Effects of acclimation to projected near-future ocean acidification (OA) conditions on physiology, reproduction and development were investigated in the tropical sea urchin Echinometra mathaei. Following 6 weeks in control or one of the three elevated pCO₂ (pH_NIST 7.5–8.1; pCO₂ ~485–1,770 μatm) conditions, adult urchins exhibited a slight decline of growth in low pH treatments and moderately reduced respiration at intermediate levels. At 7 weeks, gametes from adults were used to produce larvae that were reared in their respective parental treatments. To assess whether larvae from acclimated parents are more resilient to elevated pCO₂ than those not acclimated, larvae from control animals were also reared in the elevated pCO₂ treatments. There was no difference in female ‘spawnability’ and oocyte size between treatments, but male spawning ability was reduced in increased pCO₂ conditions. In elevated pCO₂ treatments, the percentage of normal larvae and larval size decreased in the progeny of control- and elevated pCO₂-acclimated parents, and arm asymmetry increased. Thus, acclimation of the parents did not make the progeny more resilient or sensitive to OA effects. Negative effects of increased pCO₂ on reproduction and development may impact on recruitment and population maintenance of this species.     

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.     

Tough as a rock-boring urchin: adult Echinometra sp. EE from the Red Sea show high resistance to ocean acidification over long-term exposures

Ocean acidification, a process caused by the continuous rise of atmospheric CO₂ levels, is expected to have a profound impact on marine invertebrates. Findings of the numerous studies conducted in this field indicate high variability in species responses to future ocean conditions. This study aimed at understanding the effects of long-term exposure to elevated pCO₂ conditions on the performance of adult Echinometra sp. EE from the Gulf of Aqaba (Red Sea). During an 11-month incubation under high pCO₂ (1,433 μatm, pH_NBS 7.7) and control (435 μatm, pH_NBS 8.1) conditions, we examined the urchins’ somatic and gonadal growth, gametogenesis and skeletal microstructure. Somatic and gonadal growths were exhibited with no significant differences between the treatments. In addition, all urchins in the experiment completed a full reproductive cycle, typical of natural populations, with no detectable impact of increased pCO₂ on the timing, duration or progression of the cycle. Furthermore, scanning electron microscopy imaging of urchin tests and spines revealed no signs of the usual observed effects of acidosis, such as skeletal dissolution, widened stereom pores or non-smoothed structures. Our results, which yielded no significant impact of the high pCO₂ treatment on any of the examined processes in the urchins studied, suggest high resistance of adult Echinometra sp. EE to near future ocean acidification conditions. With respect to other findings in this area, the outcome of this study provides an example of the complicated and diverse responses of echinoids to the predicted environmental changes.     

Ocean acidification reduces biomineralization-related gene expression in the sea urchin, Hemicentrotus pulcherrimus

Although recent studies have demonstrated that calcification in a wide range of marine organisms is profoundly affected by CO₂-induced ocean acidification, the mechanism of this phenomenon is still unclear. To clarify the effects of ocean acidification on the calcification process at the molecular level, we evaluated the expression of three biomineralization-related genes in the sea urchin Hemicentrotus pulcherrimus exposed under control, 1,000, and 2,000?ppm CO₂ from egg to pluteus larval stage. We found that the expression of the gene msp130, which is proposed to transport Ca²⁺ to the calcification site, is suppressed by increased CO₂ at pluteus larval stage. Meanwhile, expression of the spicule protein matrix genes SM30 and SM50 was apparently not affected. The results suggest that the combined effects of ocean acidification on the expression of skeletogenesis-related genes as well as the change in seawater carbonate chemistry affect the biomineralization ability of sea urchins.     

Spatio-temporal variability of polychaete colonization at volcanic CO2 vents indicates high tolerance to ocean acidification

Ocean acidification is predicted to have negative effects on marine biota, resulting in the loss of biodiversity and changes in marine ecosystem structure and function. However, some species and life stages may be capable of thriving in low pH conditions, either due to their natural ability to tolerate stressful low pH–high pCO₂ conditions and/or alteration of species interactions caused by changes in pH profiles, or due to evolutionary trade-offs. A better understanding of which species may be capable of tolerating ocean acidification can guide future research into the mechanisms for physiological and ecological resilience to future carbon dioxide (CO₂) conditions. We investigated the colonization of selected polychaete species along a pH gradient originating from shallow, coastal volcanic CO₂ vents (Ischia, Italy). Colonization was quantified by exposing artificial invertebrate collectors attached to the substratum for 30 days during different periods of the year (late spring, fall and late winter). Three species, Amphiglena mediterranea, Platynereis dumerilii and Syllis prolifera, were present and abundant along the gradient throughout the year. All three species were significantly more abundant in the most acidified areas, confirming their high tolerance and capacity to cope with very low pH. Abundances of all three species were compared to data previously collected via collectors suspended in the water column. More individuals were found in the collectors attached to the substratum, suggesting that abundances may have previously been underestimated. This is likely due to the close proximity of these collectors with the natural rocky substratum. All three species exhibited similar temporal variability, consistent with their life cycle and reproductive biology. Our results demonstrate high tolerance of the species for low and variable pH and corroborate their use as robust models to explore the capacity to cope with low pH–high pCO₂ conditions, both in the natural vent systems and in the laboratory.     

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.