Ocean acidification: Separating evidence from judgment – A reply to Dupont et al.

Recently ocean acidification as a major threat for marine species has moved from a consensus statement into a much discussed and even challenged conception. A simple meta-analysis of Hendriks et al. (2010) showed that based on results of pooled experimental evidence, marine biota may turn out to be more resistant than hitherto believed. Dupont et al. (in press) indicate the importance of evaluating the most vulnerable stages in the life cycle of organisms instead of only adult stages. Here we evaluate additional material, composed of experimental evidence of the effect of ocean acidification on marine organisms during adult, larval, and juvenile stages, and show that the observed effects are within the range predicted by Hendriks et al. (2010). Species-specific differences and a wide variance in the reaction of organisms might obscure patterns of differences between life stages. Future research should be aimed to clarify underlying mechanisms to define the effect ocean acidification will have on marine biodiversity. Conveying scientific evidence along with an open acknowledgment of uncertainties to help separate evidence from judgment should not harm the need to act to mitigate ocean acidification and should pave the road for robust progress in our understanding of how ocean acidification impacts biota of the ocean.     

Global change ecotoxicology: Identification of early life history bottlenecks in marine invertebrates,variable species responses and variable experimental approaches

Climate change is a threat to marine biota because increased atmospheric CO₂ is causing ocean warming, acidification, hypercapnia and decreased carbonate saturation. These stressors have toxic effects on invertebrate development. The persistence and success of populations requires all ontogenetic stages be completed successfully and, due to their sensitivity to environmental stressors, developmental stages may be a population bottleneck in a changing ocean. Global change ecotoxicology is being used to identify the marine invertebrate developmental stages vulnerable to climate change. This overview of research, and the methodologies used, shows that most studies focus on acidification, with few studies on ocean warming, despite a long history of research on developmental thermotolerance. The interactive effects of stressors are poorly studied. Experimental approaches differ among studies. Fertilization in many species exhibits a broad tolerance to warming and/or acidification, although different methodologies confound inter-study comparisons. Early development is susceptible to warming and most calcifying larvae are sensitive to acidification/increased pCO₂. In multistressor studies moderate warming diminishes the negative impact of acidification on calcification in some species. Development of non-calcifying larvae appears resilient to near-future ocean change. Although differences in species sensitivities to ocean change stressors undoubtedly reflect different tolerance levels, inconsistent handling of gametes, embryos and larvae probably influences different research outcomes. Due to the integrative ‘developmental domino effect’, life history responses will be influenced by the ontogenetic stage at which experimental incubations are initiated. Exposure to climate change stressors from early development (fertilization where possible) in multistressor experiments is needed to identify ontogenetic sensitivities and this will be facilitated by more consistent methodologies.     

Boldness in a deep sea hermit crab to simulated tactile predator attacks is unaffected by ocean acidification

Despite rapidly growing interest in the effects of ocean acidification on marine animals, the ability of deep-sea animals to acclimate or adapt to reduced pH conditions has received little attention. Deep-sea species are generally thought to be less tolerant of environmental variation than shallow-living species because they inhabit relatively stable conditions for nearly all environmental parameters. To explore whether deep-sea hermit crabs (Pagurus tanneri) can acclimate to ocean acidification over several weeks, we compared behavioral “boldness,” measured as time taken to re-emerge from shells after a simulated predatory attack by a toy octopus, under ambient (pH ～7.6) and expected future (pH ～7.1) conditions. The boldness measure for crab behavioral responses did not differ between different pH treatments, suggesting that future deep-sea acidification would not influence anti-predatory behavior. However, we did not examine the effects of olfactory cues released by predators that may affect hermit crab behavior and could be influenced by changes in the ocean carbonate system driven by increasing CO₂ levels.     

Relative influences of ocean acidification and temperature on intertidal barnacle post-larvae at the northern edge of their geographic distribution

The Arctic Ocean and its associated ecosystems face numerous challenges over the coming century. Increasing atmospheric CO₂ is causing increasing warming and ice melting as well as a concomitant change in ocean chemistry (“ocean acidification”). As temperature increases it is expected that many temperate species will expand their geographic distribution northwards to follow this thermal shift; however with the addition of ocean acidification this transition may not be so straightforward. Here we investigate the potential impacts of ocean acidification and climate change on populations of an intertidal species, in this case the barnacle Semibalanus balanoides, at the northern edge of its range. Growth and development of metamorphosing post-larvae were negatively impacted at lower pH (pH 7.7) compared to the control (pH 8.1) but were not affected by elevated temperature (+4 °C). The mineral composition of the shells did not alter under any of the treatments. The combination of reduced growth and maintained mineral content suggests that there may have been a change in the energetic balance of the exposed animals. In undersaturated conditions more mineral is expected to dissolve from the shell and hence more energy would be required to maintain the mineral integrity. Any energy that would normally be invested into growth could be reallocated and hence organisms growing in lowered pH grow slower and end up smaller than individuals grown in higher pH conditions. The idea of reallocation of resources under different conditions of pH requires further investigation. However, there could be long-term implications on the fitness of these barnacles, which in turn may prevent them from successfully colonising new areas.     

The Effects of Ocean Acidification on Feeding and Contest Behaviour by the Beadlet Anemone <Emphasis Type="Italic">Actinia equina</Emphasis>

Increasing concentrations of atmospheric carbon dioxide are causing oceanic pH to decline worldwide, a phenomenon termed ocean acidification. Mounting experimental evidence indicates that near-future levels of CO₂ will affect calcareous invertebrates such as corals, molluscs and gastropods, by reducing their scope for calcification. Despite extensive research into ocean acidification in recent years, the effects on non-calcifying anthozoans, such as sea anemones, remain little explored. In Western Europe, intertidal anemones such as Actinia equina are abundant, lower trophic-level organisms that function as important ecosystem engineers. Changes to behaviours of these simple predators could have implications for intertidal assemblages. This investigation identified the effects of reduced seawater pH on feeding and contest behaviour by A. equina. Video footage was recorded for A. equina feeding at current-day seawater (pH 8.1), and the least (pH 7.9) and most (pH 7.6) severe end-of-century predictions. Footage was also taken of contests over ownership of space between anemones exposed to reduced pH and those that were not. No statistically significant differences were identified in feeding duration or various aspects of contest behaviour including initiating, winning, inflating acrorhagi, inflicting acrorhagial peels and contest duration. Multivariate analyses showed no effect of pH on a combination of these variables. This provides contrast with other studies where anemones with symbiotic algae thrive in areas of natural increased acidity. Thus, novel experiments using intraspecific contests and resource-holding potential may prove an effective approach to understand sub-lethal consequences of ocean acidification for A. equina, other sea anemones and more broadly for marine ecosystems.     

Effects of ocean acidification and high temperatures on the bryozoan Myriapora truncata at natural CO2 vents

There are serious concerns that ocean acidification will combine with the effects of global warming to cause major shifts in marine ecosystems, but there is a lack of field data on the combined ecological effects of these changes due to the difficulty of creating large‐scale, long‐term exposures to elevated CO₂ and temperature. Here we report the first coastal transplant experiment designed to investigate the effects of naturally acidified seawater on the rates of net calcification and dissolution of the branched calcitic bryozoan Myriapora truncata (Pallas, 1766). Colonies were transplanted to normal (pH 8.1), high (mean pH 7.66, minimum value 7.33) and extremely high CO₂ conditions (mean pH 7.43, minimum value 6.83) at gas vents off Ischia Island (Tyrrhenian Sea, Italy). The net calcification rates of live colonies and the dissolution rates of dead colonies were estimated by weighing after 45 days (May–June 2008) and after 128 days (July–October) to examine the hypothesis that high CO₂ levels affect bryozoan growth and survival differently during moderate and warm water conditions. In the first observation period, seawater temperatures ranged from 19 to 24 °C; dead M. truncata colonies dissolved at high CO₂ levels (pH 7.66), whereas live specimens maintained the same net calcification rate as those growing at normal pH. In extremely high CO₂ conditions (mean pH 7.43), the live bryozoans calcified significantly less than those at normal pH. Therefore, established colonies of M. truncata seem well able to withstand the levels of ocean acidification predicted in the next 200 years, possibly because the soft tissues protect the skeleton from an external decrease in pH. However, during the second period of observation a prolonged period of high seawater temperatures (25–28 °C) halted calcification both in controls and at high CO₂, and all transplants died when high temperatures were combined with extremely high CO₂ levels. Clearly, attempts to predict the future response of organisms to ocean acidification need to consider the effects of concurrent changes such as the Mediterranean trend for increased summer temperatures in surface waters. Although M. truncata was resilient to short‐term exposure to high levels of ocean acidification at normal temperatures, our field transplants showed that its ability to calcify at higher temperatures was compromised, adding it to the growing list of species now potentially threatened by global warming.     

Physiological Responses of the Mediterranean Subtidal Alga <Emphasis Type="Italic">Peyssonnelia squamaria</Emphasis> to Elevated CO<Subscript>2</Subscript>

The ecological consequences of ocean acidification are unclear due to varying physiological properties of macroalgae and species-specific responses. Therefore, in the present study, we used a laboratory culture experiment to analyse the eco-physiological responses of the Mediterranean subtidal red alga Peyssonnelia squamaria to CO₂-induced lower pH. Our results showed an increase in the photosynthetic performance and growth rate of P. squamaria, despite the reduction in CaCO₃ content in the low pH treatment. According to our results, we believe that samples exposed to elevated CO₂ could be regulated own nitrogen metabolism to support increased growth rate and it may be down-regulated nitrate uptake. As a result, we hypothesize that P. squamaria may benefit from ocean acidification.     

Seasonal and inter-annual variability of air–sea CO2 fluxes and seawater carbonate chemistry in the Southern North Sea

A 3D coupled biogeochemical–hydrodynamic model (MIRO-CO₂&CO) is implemented in the English Channel (ECH) and the Southern Bight of the North Sea (SBNS) to estimate the present-day spatio-temporal distribution of air–sea CO₂ fluxes, surface water partial pressure of CO₂ (pCO₂) and other components of the carbonate system (pH, saturation state of calcite (Ω_ca) and of aragonite (Ω_ar)), and the main drivers of their variability. Over the 1994–2004 period, air–sea CO₂ fluxes show significant inter-annual variability, with oscillations between net annual CO₂ sinks and sources. The inter-annual variability of air–sea CO₂ fluxes simulated in the SBNS is controlled primarily by river loads and changes of biological activities (net autotrophy in spring and early summer, and net heterotrophy in winter and autumn), while in areas less influenced by river inputs such as the ECH, the inter-annual variations of air–sea CO₂ fluxes are mainly due to changes in sea surface temperature and in near-surface wind strength and direction. In the ECH, the decrease of pH, of Ω_ca and of Ω_ar follows the one expected from the increase of atmospheric CO₂ (ocean acidification), but the decrease of these quantities in the SBNS during the considered time period is faster than the one expected from ocean acidification alone. This seems to be related to a general pattern of decreasing nutrient river loads and net ecosystem production (NEP) in the SBNS. Annually, the combined effect of carbon and nutrient loads leads to an increase of the sink of CO₂ in the ECH and the SBNS, but the impact of the river loads varies spatially and is stronger in river plumes and nearshore waters than in offshore waters. The impact of organic and inorganic carbon (C) inputs is mainly confined to the coast and generates a source of CO₂ to the atmosphere and low pH, of Ω_ca and of Ω_ar values in estuarine plumes, while the impact of nutrient loads, highest than the effect of C inputs in coastal nearshore waters, also propagates offshore and, by stimulating primary production, drives a sink of atmospheric CO₂ and higher values of pH, of Ω_ca and of Ω_ar.     

Numerical Simulation of Biological Impact Caused by Direct Injection of Carbon Dioxide in the Ocean

The direct injection of CO₂ in the deep ocean is a promising way to mitigate global warming. One of the uncertainties in this method, however, is its impact on marine organisms in the near field before CO₂ is diluted widely in the ocean. Since field experiments cost enormously, computational simulations are expected to show detailed information on the dilution process near injection points and its impact on marine organisms. In general, the LC50 concept is widely applied for testing the acute impact of a toxic agent on organisms. As a biological impact model we therefore consider mortality, which reflects recent laboratory experiments on zooplankton at various concentrations of CO₂. Here we regard the sigmoid-transformed mortality as a linear function of time in the logarithmic scale, and not just of the concentration of CO₂ in the logarithmic scale. This model was installed in a computational simulation code for the reconstruction of small-scale ocean turbulence. The results suggest that the biological effect is not significant when the ship speed is 4 knots and CO₂ is injected at 0.1 ton/sec in the form of a spray through 100 nozzles provided vertically on a pipe at 10 m intervals. It is therefore considered that the moving-ship method is effective for direct CO₂ injection. This revised version was published online in July 2006 with corrections to the Cover Date.     

Acidification at the Surface in the East Sea: A Coupled Climate-carbon Cycle Model Study

This modeling study investigates the impacts of increasing atmospheric CO₂ concentration on acidification in the East Sea. A historical simulation for the past three decades (1980 to 2010) was performed using the Hadley Centre Global Environmental Model (version 2), a coupled climate model with atmospheric, terrestrial and ocean cycles. As the atmospheric CO₂ concentration increased, acidification progressed in the surface waters of the marginal sea. The acidification was similar in magnitude to observations and models of acidification in the global ocean. However, in the global ocean, the acidification appears to be due to increased in-situ oceanic CO₂ uptake, whereas local processes had stronger effects in the East Sea. pH was lowered by surface warming and by the influx of water with higher dissolved inorganic carbon (DIC) from the northwestern Pacific. Due to the enhanced advection of DIC, the partial pressure of CO₂ increased faster than in the overlying air; consequently, the in-situ oceanic uptake of CO₂ decreased.     

Effects of low pCO2 conditions on sea urchin larval size

Ocean acidification results from an increase in the concentrations of atmospheric carbon dioxide (CO₂) impacts on marine calcifying species, which is predicted to become more pronounced in the future. By the end of this century, atmospheric pCO₂ levels will have doubled relative to the pre‐industrial levels of 280 ppm. However, the effects of pre‐industrial pCO₂ levels on marine organisms remain largely unknown. In this study, we investigated the effects of pre‐industrial pCO₂ conditions on the size of the pluteus larvae of sea urchins, which are known to be vulnerable to ocean acidification. The larval size of Hemicentrotus pulcherrimus significantly increased when reared at pre‐industrial pCO₂ level relative to the present one, and the size of Anthocidaris crassispina larvae decreased as the pCO₂ levels increased from the pre‐industrial level to the near future ones after 3 days' exposure. In this study, it is suggested that echinoid larvae responded to pre‐industrial pCO₂ levels. Ocean acidification may be affecting some sensitive marine calcifiers even at the present pCO₂ level.     

Effects of CO<Subscript>2</Subscript> Enrichment on Marine Phytoplankton

Rising atmospheric CO₂ and deliberate CO₂ sequestration in the ocean change seawater carbonate chemistry in a similar way, lowering seawater pH, carbonate ion concentration and carbonate saturation state and increasing dissolved CO₂ concentration. These changes affect marine plankton in various ways. On the organismal level, a moderate increase in CO₂ facilitates photosynthetic carbon fixation of some phytoplankton groups. It also enhances the release of dissolved carbohydrates, most notably during the decline of nutrient-limited phytoplankton blooms. A decrease in the carbonate saturation state represses biogenic calcification of the predominant marine calcifying organisms, foraminifera and coccolithophorids. On the ecosystem level these responses influence phytoplankton species composition and succession, favouring algal species which predominantly rely on CO₂ utilization. Increased phytoplankton exudation promotes particle aggregation and marine snow formation, enhancing the vertical flux of biogenic material. A decrease in calcification may affect the competitive advantage of calcifying organisms, with possible impacts on their distribution and abundance. On the biogeochemical level, biological responses to CO₂ enrichment and the related changes in carbonate chemistry can strongly alter the cycling of carbon and other bio-active elements in the ocean. Both decreasing calcification and enhanced carbon overproduction due to release of extracellular carbohydrates have the potential to increase the CO₂ storage capacity of the ocean. Although the significance of such biological responses to CO₂ enrichment becomes increasingly evident, our ability to make reliable predictions of their future developments and to quantify their potential ecological and biogeochemical impacts is still in its infancy. This revised version was published online in July 2006 with corrections to the Cover Date.     

海洋酸化模拟控制系统及其在珊瑚生理研究中的应用

Due to the elevated atmospheric carbon dioxide, ocean acidification(OA) has recently emerged as a research theme in marine biology due to an expected deleterious effect of altered seawater chemistry on calcification. A system simulating future OA scenario is crucial for OA-related studies. Here, we designed an OA-simulated system(OASys) with three solenoid-controlled CO2 gas channels. The OASys can adjust the pH of the seawater by bubbling CO2 gas into seawaters via feedback systems. The OASys is very simple in structure with an integrated design and is new-user friendly with the instruction. Moreover, the OASys can monitor and record real-time pH values and can maintain pH levels within 0.02 pH unit. In a 15-d experiment, the OASys was applied to simulate OA in which the expected target pH values were 8.00, 7.80 and 7.60 to study the calcifying response of Galaxea fascicularis. The results showed daily mean seawater pH values held at pH 8.00±0.01, 7.80±0.01 and 7.61±0.01 over15 d. Correspondingly, the coral calcification of G. fascicularis gradually decreased with reduced pH.     

The effects of elevated-CO2 on physiological performance of Bryopsis plumosa

An increase in the level of atmospheric carbon dioxide (CO2) and the resultant rise in CO2 in seawater alter the inorganic carbon concentrations of seawater. This change, known as ocean acidification, ...     

A Eulerian-Eulerian Physical-Biological Impact Model of Zooplankton Injury Due to CO<Subscript>2</Subscript> Ocean Sequestration

To study the biological impacts of CO₂ ocean sequestration on floating marine organisms, a full Eulerian-Eulerian scheme model has been developed in a large-eddy simulation (LES) version using one-way coupling of the equations of seawater flow to the transport equations of the bio-scalar variables. Special attention was paid to deriving the transport equation, involving non-conservative scalars to describe the degree of injury to floating organisms due to the change in the pH environment resulting from CO₂ dissolution. The source terms of the transport equations of bio-scalar variables are based on experimental data on zooplankton activities affected by lower pH seawater, allowing construction of empirical sub-models of three kinds of floating marine organisms: Gaidius variabilis, Paraeuchaeta Birostrata, and Multi-organisms. An example is given to show the applicability of the model to the assessment of the biological impact of CO₂ sequestration in the ocean. Given an initial CO₂ droplet diameter of 8.0 mm and an injection rate of 1.0 kg/sec, the model simulation predicts that the zooplanktons lose approximately 90% of their activity when the lowest pH inside the plume decreases from 7.57 to 5.61. These injured zooplanktons then recovered gradually to their normal state within two hours due to dilution of the plume. This revised version was published online in July 2006 with corrections to the Cover Date.     

What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification?

Ocean acidification has been proposed as a major threat for marine biodiversity. Hendriks et al. [Hendriks, I.E., Duarte, C.M., Alvarez, M., 2010. Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuarine, Coastal and Shelf Science, doi:10.1016/j.ecss.2009.11.022.] proposed an alternative view and suggested, based on a meta-analysis, that marine biota may be far more resistant to ocean acidification than hitherto believed. However, such a meta-analytical approach can mask more subtle features, for example differing sensitivities during the life-cycle of an organism. Using a similar metric on an echinoderm database, we show that key bottlenecks present in the life-cycle (e.g. larvae being more vulnerable than adults) and responsible for driving the whole species response may be hidden in a global meta-analysis. Our data illustrate that any ecological meta-analysis should be hypothesis driven, taking into account the complexity of biological systems, including all life-cycle stages and key biological processes. Available data allow us to conclude that near-future ocean acidification can/will have dramatic negative impact on some marine species, including echinoderms, with likely consequences at the ecosystem level.     

Perspectives on Biological Research for CO<Subscript>2</Subscript> Ocean Sequestration

Feasibility studies recently suggest that sequestration of anthropogenic CO₂ in the deep ocean could help reduce the atmospheric CO₂ concentration. However, implementation of this strategy could have a significant environmental impact on marine organisms. This has highlighted the urgent need of further studies concerning the biological impact of CO₂ ocean sequestration. In this paper we summarize the recent literature reporting on the biological impact of CO₂ and discuss the research work required for the future. Although fundamental research of the effect of CO₂ on marine organisms before the practical consideration of CO₂ ocean sequestration was limited, laboratory and field studies concerning biological impacts have been increasing after the first international workshop in 1991 discussing CO₂ ocean sequestration. Acute impacts of CO₂ ocean sequestration could be determined by laboratory and field experiments and assessed by simulation models as described by the following papers in this section. On the other hand, chronic effects of CO₂ ocean sequestration, those directly related to the marine ecosystem, would be difficult to verify by means of experiments and to assess using ecosystem models. One of the practical solutions for this issue implies field experiments starting with controlled small scale and eventually to a large scale of CO₂ injection intended to determine ecosystem alteration. This revised version was published online in July 2006 with corrections to the Cover Date.     

Model Simulations of Carbon Sequestration in the Northwest Pacific by Direct Injection

The direct disposal of CO₂ into the ocean interior represents a possible means to help mitigate rising levels of atmospheric CO₂. Here, we use three different versions of an ocean general circulation model (OGCM) to simulate the direct injection of liquid CO₂ near Tokyo. Our results confirm that direct injection can sequester large amounts of CO₂ from the atmosphere when disposal is made at sufficient depth (80–100% of the carbon injected at 3000 m remains in the ocean after 500 years) but show that the calculated efficiency is rather sensitive to the choice of physical model. Moreover, we show, for the first time in an OGCM and under a reasonable set of economic assumptions, that sequestration effectiveness is quite high for even shallow injections. However, the severe acidification that accompanies injection and the impossibility of effectively monitoring injected plumes argue against the large-scale viability of this technology. Our coarse-grid models show that injection at the rate of 0.1 Pg-C/yr lowers pH near the site of injection by as much as 0.7–1.0 pH-unit. Such pH anomalies would be much larger in more finely gridded models (and in reality) and have potential to severely harm deep-sea organisms. We also show that, after several hundred years, one would effectively need to survey the entire ocean in order to accurately verify the inventory of injected carbon. These results suggest that while retention may be sufficient to justify disposal costs, other practical problems will limit or at best delay widespread deployment of this technology.     

海洋酸化对马氏珠母贝受精及早期发育的影响

自2010年7月1日至3日,在pH值为8.1、7.7和7.4条件下研究了海洋酸化对马氏珠母贝(Pinctada martensii Dunker)受精及早期发育的影响。结果显示,海洋酸化对不同pH值下马氏珠母贝的受精率无显著影响。pH8.1、pH 7.7和pH 7.4试验组幼虫的壳长、壳高的值逐渐增大,pH 8.1组幼虫的壳长、壳高的值大于同期其他两组的值,且在实验的第24、36、48小时与其他两组同期幼虫的壳长、壳高的值差异显著,这表明海洋酸化显著影响马氏珠母贝幼虫的生长。实验期间,pH 8.1试验组幼虫的存活率和畸形率没有显著变化,而pH 7.7和pH 7.4组幼虫的存活率显著低于pH 8.1组。pH 7.4组幼虫的畸形率显著高于同期pH 8.1和pH 7.7组幼虫的畸形率,表明在海洋酸化的环境中幼虫的发育受到影响。本文将为海洋酸化的相关研究提供基础数据。     

Effect of ocean acidification on coastal phytoplankton composition and accompanying organic nitrogen production

The effect of ocean acidification, caused by the increase in pCO₂ in seawater, on phytoplankton population and on related organic nitrogen production was experimentally examined by use of a natural coastal microbial population. pCO₂ and pH were controlled by aeration with air in which pCO₂ was at the current level (control), for which ambient air was used, and with air in which pCO₂ was ??800?? and ??1200?? ppm, in 500-L culture vessels. The experiment was continued for 15?days after addition of the inorganic nutrients such as nitrate, phosphate, and silicate. During most of the experimental period, a minor increase in phytoplankton biomass was noted, probably because of low irradiance, an increase in phytoplankton biomass was observed at the end of the experiment. Flow cytometric and microscopic observations revealed that this increase was because of Chrysochromulina sp. (Haptophyceae). The growth of Chrysochromulina sp. was most obvious in the control vessel, and tended to be obscured by increasing pCO₂ (decrease in pH), indicating the possibility that ocean acidification inhibits the growth of specific phytoplankton groups, for example Chrysochromulina sp. Production of particulate organic nitrogen (PON), determined by the ¹⁵N tracer method, also diminished under acidified conditions compared with that at the current level.