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.     

Enhancing synergies between action on ocean acidification and the post-2020 global biodiversity framework

Ocean acidification is a substantial emergent threat to marine biodiversity and the goods and services it provides. Although efforts to address ocean acidification have been taken under the Convention on Biological Diversity (CBD), a far greater potential to do so exists by finding synergies between biodiversity conservation efforts and ocean acidification action. The ongoing process to develop a post-2020 global biodiversity framework offers an opportunity to ensure that opportunities for addressing ocean acidification are capitalized on and not overlooked. I argue that to achieve this, the following are needed: a technical integration of ocean acidification across the targets to be included in the post-2020 framework and a reframing of the issue as a biodiversity problem so as to highlight the synergies between existing biodiversity work and action needed to address ocean acidification. Given that the post-2020 framework is intended to establish the global biodiversity agenda for the coming decades, integration of ocean acidification will set a precedent for the other biodiversity-related conventions and encourage greater uptake of the issue across the wider international community. My approach is of direct relevance to those participating in the negotiations, both from a CBD Party perspective and the perspective of those advocating for a strong outcome to protect marine biodiversity and marine socioecological systems. My discussion of framing is relevant to those working beyond the CBD within other biodiversity-related conventions in which goals to address ocean acidification are sorely lacking.     

Effects of near‐future ocean acidification,fishing, and marine protection on a temperate coastal ecosystem

Understanding ecosystem responses to global and local anthropogenic impacts is paramount to predicting future ecosystem states. We used an ecosystem modeling approach to investigate the independent and cumulative effects of fishing, marine protection, and ocean acidification on a coastal ecosystem. To quantify the effects of ocean acidification at the ecosystem level, we used information from the peer‐reviewed literature on the effects of ocean acidification. Using an Ecopath with Ecosim ecosystem model for the Wellington south coast, including the Taputeranga Marine Reserve (MR), New Zealand, we predicted ecosystem responses under 4 scenarios: ocean acidification + fishing; ocean acidification + MR (no fishing); no ocean acidification + fishing; no ocean acidification + MR for the year 2050. Fishing had a larger effect on trophic group biomasses and trophic structure than ocean acidification, whereas the effects of ocean acidification were only large in the absence of fishing. Mortality by fishing had large, negative effects on trophic group biomasses. These effects were similar regardless of the presence of ocean acidification. Ocean acidification was predicted to indirectly benefit certain species in the MR scenario. This was because lobster (Jasus edwardsii) only recovered to 58% of the MR biomass in the ocean acidification + MR scenario, a situation that benefited the trophic groups lobsters prey on. Most trophic groups responded antagonistically to the interactive effects of ocean acidification and marine protection (46%; reduced response); however, many groups responded synergistically (33%; amplified response). Conservation and fisheries management strategies need to account for the reduced recovery potential of some exploited species under ocean acidification, nonadditive interactions of multiple factors, and indirect responses of species to ocean acidification caused by declines in calcareous predators.     

Towards improved socio-economic assessments of ocean acidification’s impacts

Ocean acidification is increasingly recognized as a component of global change that could have a wide range of impacts on marine organisms, the ecosystems they live in, and the goods and services they provide humankind. Assessment of these potential socio-economic impacts requires integrated efforts between biologists, chemists, oceanographers, economists and social scientists. But because ocean acidification is a new research area, significant knowledge gaps are preventing economists from estimating its welfare impacts. For instance, economic data on the impact of ocean acidification on significant markets such as fisheries, aquaculture and tourism are very limited (if not non-existent), and non-market valuation studies on this topic are not yet available. Our paper summarizes the current understanding of future OA impacts and sets out what further information is required for economists to assess socio-economic impacts of ocean acidification. Our aim is to provide clear directions for multidisciplinary collaborative research.     

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。     

Can ocean acidification affect population dynamics of the barnacle Semibalanus balanoides at its southern range edge?

The global ocean and atmosphere are warming. There is increasing evidence suggesting that, in addition to other environmental factors, climate change is affecting species distributions and local population dynamics. Additionally, as a consequence of the growing levels of atmospheric carbon dioxide (CO2), the oceans are taking up increasing amounts of this CO2, causing ocean pH to decrease (ocean acidification). The relative impacts of ocean acidification on population dynamics have yet to be investigated, despite many studies indicating that there will be at least a sublethal impact on many marine organisms, particularly key calcifying organisms. Using empirical data, we forced a barnacle (Semibalanus balanoides) population model to investigate the relative influence of sea surface temperature (SST) and ocean acidification on a population nearing the southern limit of its geographic distribution. Hindcast models were compared to observational data from Cellar Beach (southwestern United Kingdom). Results indicate that a declining pH trend (-0.0017 unit/yr), indicative of ocean acidification over the past 50 years, does not cause an observable impact on the population abundance relative to changes caused by fluctuations in temperature. Below the critical temperature (here T(crit) = 13.1 degrees C), pH has a more significant affect on population dynamics at this southern range edge. However, above this value, SST has the overriding influence. At lower SST, a decrease in pH (according to the National Bureau of Standards, pHNBs) from 8.2 to 7.8 can significantly decrease the population abundance. The lethal impacts of ocean acidification observed in experiments on early life stages reduce cumulative survival by approximately 25%, which again will significantly alter the population level at this southern limit. Furthermore, forecast predictions from this model suggest that combined acidification and warming cause this local population to die out 10 years earlier than would occur if there was only global warming and no concomitant decrease in pH.     

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.     

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.     

Predicting Interactions among Fishing,Ocean Warming,and Ocean Acidification in a Marine System with Whole‐Ecosystem Models

An important challenge for conservation is a quantitative understanding of how multiple human stressors will interact to mitigate or exacerbate global environmental change at a community or ecosystem level. We explored the interaction effects of fishing, ocean warming, and ocean acidification over time on 60 functional groups of species in the southeastern Australian marine ecosystem. We tracked changes in relative biomass within a coupled dynamic whole‐ecosystem modeling framework that included the biophysical system, human effects, socioeconomics, and management evaluation. We estimated the individual, additive, and interactive effects on the ecosystem and for five community groups (top predators, fishes, benthic invertebrates, plankton, and primary producers). We calculated the size and direction of interaction effects with an additive null model and interpreted results as synergistic (amplified stress), additive (no additional stress), or antagonistic (reduced stress). Individually, only ocean acidification had a negative effect on total biomass. Fishing and ocean warming and ocean warming with ocean acidification had an additive effect on biomass. Adding fishing to ocean warming and ocean acidification significantly changed the direction and magnitude of the interaction effect to a synergistic response on biomass. The interaction effect depended on the response level examined (ecosystem vs. community). For communities, the size, direction, and type of interaction effect varied depending on the combination of stressors. Top predator and fish biomass had a synergistic response to the interaction of all three stressors, whereas biomass of benthic invertebrates responded antagonistically. With our approach, we were able to identify the regional effects of fishing on the size and direction of the interacting effects of ocean warming and ocean acidification. Predicción de Interacciones entre Pesca, Calentamiento de Océanos y Acidificación de Océanos en un Sistema Marino con Modelos de Ecosistemas Completos     

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.     

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.     

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.     

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.     

Assessment and management of urbanization-induced ecological risks

The urban ecological risk incurred during the processes of urbanization has been constantly accumulating, creating a severe challenge for China to achieve sustainable urban development. At present, research on systematic evaluation of urban ecological risks is still inadequate, especially at an urban ecosystem level. In this special issue, we use Xiamen City as an example to identify the sources and receptors of urban ecological risks, to develop a methodology system of urban ecological risk assessment, and to propose a method for the management of urban ecological risks. This special issue contains 11 research articles resulting from a comprehensive research project funded by China’s National Natural Science Foundation. The innovations reported in this special issue include a framework of urban ecological risk assessment and a standardized procedure for carrying out urban ecological risk assessment using multiple stressors and endpoints.     

Metal contamination increases the sensitivity of larvae but not gametes to ocean acidification in the polychaete Pomatoceros lamarckii (Quatrefages)

Ocean acidification is not happening in isolation but against a background of chronic low-level pollution for most coastal marine environments. The reproductive and larval stages of marine invertebrates can be highly sensitive to the impacts of both environmental pollutants and ocean acidification, but very little is currently known regarding the potential impacts of combined contaminant and high CO₂ exposures on the health of marine organisms. Ocean acidification research to date has focused heavily on the responses of calcifying marine invertebrate larvae and algae, and as such the polychaetes as a group, despite their ecological importance, remain understudied. Here, we investigate the effects of elevated seawater CO₂ (pH range 8.1–7.4, plus an extreme pH of 7.2 in the sperm motility experiments), in combination with the environmental pollutant copper (0.002 μM), on the early life history stages of the intertidal polychaete Pomatoceros lamarckii from two populations. P. lamarckii sperm appear to be robust to elevated seawater CO₂. Whilst all three of the sperm motility end points measured showed a response to elevated CO₂, these responses were small and not linear. The percentage of motile sperm and sperm curvilinear velocity were significantly reduced in the lower pH treatments of 7.4 and 7.2, whereas sperm straight-line velocity (VSL) was mostly unaffected except for an increased VSL at pH 8.0. Fertilisation success was investigated using two populations from the South West (UK), one from Torquay and one from Plymouth Sound. Fertilisation success was slightly but significantly reduced at the 7.6 and 7.4 pH treatments for both populations (a 9.0 % reduction in fertilisation success from pH 8.1 to 7.4 for Torquay), but with a greater effect observed in the population from Plymouth Sound (a 13.33 % reduction in fertilisation success). No additional impact of 0.002 μM copper exposure on fertilisation success was found. Larval survival was found to be much more sensitive to elevated CO₂ than sperm function or fertilisation, and a significant interaction with copper exposure was observed. These results demonstrate the potential for polychaete larvae to be affected by predicted ocean acidification conditions and that chronic coastal pollutants, such as copper, have the potential to alter larval susceptibility to ocean acidification conditions.     

Interaction of ocean acidification and temperature; the high cost of survival in the brittlestar Ophiura ophiura

This study has demonstrated an interaction between the effect of increased ocean acidity and temperature (40 days exposure) on a number of key physiological parameters in the ophiuroid brittlestar, Ophiura ophiura. Metabolic upregulation is seen in the low pH treatments when combined with low temperature. However, this is far outweighed by the response to elevated temperature (+4.5°C). In the high temperature/low pH treatments treatments (where calcite is undersaturated) there appears to be an energetic trade-off likely in order to maintain net calcification where dissolution of calcium carbonate may occur. This energy deficit results in a ~30% reduction in the rate of arm regeneration at pH 7.3 which is predicted to be reached by the year 2300. This understanding of how O. ophiura responds to ocean acidification, taking into account an interactive effect of temperature, suggests that fitness and survival may indirectly be reduced through slower recovery from arm damage.     

Appropriate pCO2 treatments in ocean acidification experiments

Experiments in which organisms are reared in treatments simulating current and future pCO₂ concentrations are critical for ocean acidification (OA) research. The majority of OA exposure experiments use average atmospheric pCO₂ levels as a baseline treatment. We conducted an ecoregion-scale analysis of global carbon chemistry datasets. For many locales, atmospheric pCO₂ levels are not an appropriate characterization of marine carbon chemistry. We argue that atmospheric pCO₂ should be disregarded when setting baseline treatment conditions and experimental design should rely on measurements of carbon chemistry in a study subject’s habitat. As carbon chemistry conditions vary with space and time, we suggest using a range of pCO₂ values as a control rather than a single value. We illustrate this issue with data on the habitat of Euphausia pacifica, which currently lives in waters with a pCO₂ around 900 μatm, a concentration much higher than the current global atmospheric mean.     

Influence of CO<Subscript>2</Subscript>-related seawater acidification on extracellular acid–base balance in the velvet swimming crab <Emphasis Type="Italic">Necora puber</Emphasis>

We investigated the effect of different levels of hypercapnia-induced acidification (pH = 7.96, 7.31, 6.74 and 6.05) on the extracellular acid base balance of a shallow-water crustacean, the velvet swimming crab Necora puber over a period of 16 days. Any extracellular acidosis incurred was completely compensated by an increase in bicarbonate. Bicarbonate was partly, but not wholly, supplied by dissolution of the exoskeleton. This compensation was sustained for 16 days under all experimental treatments with two exceptions. First there was some evidence of extracellular acidosis in crabs after 16 days at pH = 6.74. Second at the lowest environmental pH (6.05) there was a marked uncompensated acidosis after 24 h. Necora puber appears less sensitive to low pH than many other species examined acutely. However, local acidification as a result of ocean CO₂ dispersal or leakage from geological sequestration is likely to compromise even this species.     

Microstructure of the paper nautilus (Argonauta nodosa) shell and the novel application of electron backscatter diffraction (EBSD) to address effects of ocean acidification

Electron backscatter diffraction (EBSD) is a powerful microscopic technique to characterise the crystallography of biomineralisation. Here, we use high-resolution EBSD to characterise one of the least studied shells in the ocean, the female argonaut brood chamber, and to examine the changes in shell microstructure in response to incubation in decreased pH conditions. The thin (225 μm) shell of Argonauta nodosa is magnesium calcite with an average magnesium content of ca. 5.1 Wt % MgCO₃. EBSD and scanning electron microscopy (SEM) revealed that calcification of the shell is bidirectional with formation of irregular crystalline grains. Following a 2 week incubation in a range of pH treatments (pH, 8.1–7.2), shell fragment weight decreased by dissolution in pH ≤ 7.8. EBSD and SEM revealed altered shell crystallography and microstructure at pH ≤ 7.4 due to preferential etching down crystallite grain boundaries and a change in crystalline orientation on both the inner and outer shell surfaces. Our study highlights the value of EBSD for the detailed examination of biogenic carbonates and its potential use in the field of ocean acidification research.