Nova on Acid

Joanne Nova relies on another website call CO2Science for some of her “science”. In her latest effort Nova uses CO2Science to portray ocean acidification as something almost to embrace instead of a dangerous environmental problem that parallels global warming.

Sadly Nova and CO2Science try to deceive you with conducting poor science and a strange kind of analysis in which they document a number of scientific papers and count the number of species affected by higher levels of acidification. They classify the data by the “Type of Organism” (Bivalves, Bryozoans, Corals, Crustacean, Echinoderms, Echinoderms, Fish, Gastropods, Macroalgae, Netamodes, Phytoplankton, Seagrass), and also by “life characteristics” (Calcification, Metabolism, Growth, Fertility, Survival).

Sounds like a good approach, but there are numerous and very obvious problems with their analysis – let’s look closer.

Is Growth a Good Thing?

CO2Science group all growth as if it’s a good thing, when in some cases the opposite is true. For example their Heterosigma akashiwo [Marine Raphidophyte] contains positive growth data an is included as beneficial in CO2Science’s graphs. What’s the problem with that? The journal reference is a dead giveaway, A comparison of future increased CO2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae

Nova and CO2Science want you to believe an increase in harmful algae is a good thing. This highlights another serious problem with CO2Science’s analysis, a lack of understanding in what they are looking at and a lack of diligence in their analysis process. To them it’s just “numbers”. Fortunately we needn’t rely upon CO2Sciences interpretations, the experts conducting the research, who have a greater understanding of the impact give us their knowledgeable insight into the real changes we can expect. You can read their educated summaries for every single paper included in CO2Science’s database – I’ve listed them all below.

Characteristic A does not compensate for Characteristic B

By reducing the study to “just numbers” CO2Science miss an obvious point. They believe that a positive value in one characteristic will offset a negative characteristic in another. They think growing faster somehow makes up for being dead; that having a faster metabolism will somehow make up for reduced fertility.

It’s obvious that each characteristic should be considered in light of each other. It’s no good being bigger if you’re dead or if you can’t reproduce.

CO2Science are Simplistic

Another problem with Co2Science’s approach of “reducing papers to mere numbers” is that they don’t consider the interaction between different species. One species may get bigger, stronger whilst others may get weaker thus changing the ecological balance in a relatively short amount of time.

As science understands, the picture is much more complex than, “did fish X grow faster, if Yes, this must be a good thing”. Real science is more complicated than Nova science, perhaps that helps Nova convince stupid people that prefer things as simple as possible, but the research carried out by individuals in their field of expertise understand the complexity better than you or I and obviously better than Nova.

Nova’s simple approach of “There will be winners and losers” completely ignores the loss of biodiversity this will bring.

CO2Science Hides the Decline

CO2Science uses the paper of Tans 2009 to estimate pH levels. Once again CO2Science are deceptive and only present the higher ph Levels Tans calculates. CO2Science hides Tans’ higher estimate of carbon use (and lower estimate of pH levels) from their graph by Photoshopping the graph from Tans research paper in their own version of “hide the decline”.

The pH estimates CO2Science uses are ones on a planet where humans don’t exploit Shale oil, bitumen or heavy oil. Unfortunately we humans are exploiting Shale Oil, we are exploiting bitumen and we are exploiting heavy oil.

Tans 2009’s figures make no allowance for tapping undiscovered coal and oil. Nor does it take into consideration carbon permafrost which will be released as the planet warms.

This is not a poor reflection of Tans, because he does acknowledge these problems in trying to estimate exactly what pH level we will reach. Uncertainty in determining this measure is NOT reassuring as Nova would like you naively believe.

Deceptive Graphing

This is really a nit-pick, but something you should be aware of when looking at the graphs produced by CO2Science basic “reduction to numbers only” analysis. A doubling of a characteristic is just as dramatic as a halving of that characteristic, however when plotted on CO2Science’s graph an increase of 100% will appear more dramatic than a reduction of 50% because it will be further spaced from the X-axis.

But there are already so many problems with their simplistic approach that this is the least of their worries.

1103 ‘studies’ – That’s a lot, right?

Nova says “1103 studies on acidification say there’s no need to panic”. 1,103 sounds convincing – that’s a lot of papers BUT, surprise, surprise, Nova and CO2Science are being deceptive. These are not actually 1,103 papers, but 1,103 “numbers” from only 74 papers.

So do the 74 papers represent the current science on ocean acidification? Are CO2Science’s papers purposefully skewed in one area, or does it represent all facets of ocean acidification studies? How many papers are there in total?

CO2Science only have one paper on fish fertility, is this really good representation for this field? A Google Scholar search finds numerous papers that are not covered in CO2Science’s analysis, within a few hours I have found dozens of papers that highlight concern about ocean acidification that are not in CO2Science’s database.

Here’s a list of dozens CO2Science choose to ignore.

Are CO2Science’s 74 papers saying Ocean Acidification is nothing to worry about? Further below I’ve listed all 74 papers along with their abstract or conclusion. The experts disagree with Nova and CO2Science – I am not surprised.

The 74 Papers

If you take the time to examine the papers that CO2Science cites, almost all of them say that acidification has a detrimental impact even though CO2Science will categorise them as having a positive effect. Some of the papers which CO2Science might categorise as “growth” relate to harmful algae which is not beneficial to the ecosystem. Some of the reports are on the effect of adding iron in an attempt to accelerate CO2 take-up.

Bamber, R.N. 1987. The effects of acidic sea water on young carpet-shell clams Venerupis decussata (L.) (Mollusca : Veneracea). Journal of Experimental Marine Biology and Ecology 108: 241-260.

Young carpet-shell clams Venerupis decussata (L.) were maintained in sea water over a pH range of 3.5 to 8.2 (control), for periods from 8 to 30 days. Shell dissolution occurred at pH 7.55. At pH < 7.0 feeding was inhibited, and both tissue and shell growth were significantly reduced. There were 50% mortalities over the time scale of the experiment at pH 6.5, with smaller (3–4 mm) clams more sensitive than larger (7–9 mm) clams. The animals showed reduced activity at pH<6.0, with abnormal feeding behaviour, exhibited by hyper-extension of the siphons; greater time spent with the valves closed at these pH levels may have marginally reduced the deleterious effects. It is concluded that pH levels below those found naturally in the sea are intolerable to young V. decussata.

Bamber, R.N. 1990. The effects of acidic seawater on three species of lamellibranch mollusc. Journal of Experimental Marine Biology and Ecology 143: 181-191.

Three species of commercial bivalve mollusc, Ostrea edulis, Crassostrea gigas and Mytilus edulis, were maintained in seawater over a pH range of 5.4–8.2 (control), normally for 30 days. Significant mortalities occurred in C. gigas at pH <6, in M. edulis at pH <6.6, in O. edulis young at pH 6.9 (after 60 days) and spat at pH <7 after 18 days. Survival at a given pH level reduced with time of exposure and with increased temperature, and increased with size of animal. Growth suppression, tissue weight loss, reduced shell size, shell dissolution and suppressed feeding activity occurred at pH 7. Abnormal behaviour analogous to narcosis (excessive shell gaping, torpor) occurred at pH 6.5, possibly attributable to CO2 excess. These and other collated results confirm that seawater at pH <7 is intolerable to bivalve molluscs.

Batten, S.D. and Bamber, R.N. 1996. The effects of acidified seawater on the polychaete Nereis virens Sars, 1835. Marine Pollution Bulletin 32 : 283-287.

The ragworm Nereis virens was maintained in seawater over a pH range of 5.1–8.1 (control). At 18°C the worms were active and demonstrated deleterious effects at pH =6.5 within 10 days, shown by mortality, burrowing activity and dry weight; survivors below pH 6 showed significantly reduced glycogen levels, indicating that stored reserves were needed to maintain metabolism within this short period. At 9°C the worms were comparatively inactive, showing no significant mortalities over 30 days; again, body weight was significantly depressed below pH 6.5. Glycogen levels gave the clearest indication of stress, with a significant decline below pH 6.5. It is concluded that such low pH levels are deleterious to N. virens, and also that monitoring body glycogen levels gives a useful indication of stress over timescales where whole animal responses may be poorly indicative.

Bechmann, R.K., Taban, I.C., Westerlund, S., Godal, B.F., Arnberg, M., Vingen, S., Ingvarsdottir, A. and Baussant, T. 2011. Effects of ocean acidification on early life stages of shrimp (Pandalus borealis) and mussel (Mytilus edulis). Journal of Toxicology and Environmental Health, Part A 74: 424-438.

Ocean acidification (OA) resulting from anthropogenic emissions of carbon dioxide (CO2) has already lowered and is predicted to further lower surface ocean pH. There is a particular need to study effects of OA on organisms living in cold-water environments due to the higher solubility of CO2 at lower temperatures. Mussel larvae (Mytilus edulis) and shrimp larvae (Pandalus borealis) were kept under an ocean acidification scenario predicted for the year 2100 (pH 7.6) and compared against identical batches of organisms held under the current oceanic pH of 8.1, which acted as a control. The temperature was held at a constant 10°C in the mussel experiment and at 5°C in the shrimp experiment. There was no marked effect on fertilization success, development time, or abnormality to the D-shell stage, or on feeding of mussel larvae in the low-pH (pH 7.6) treatment. Mytilus edulis larvae were still able to develop a shell in seawater undersaturated with respect to aragonite (a mineral form of CaCO3), but the size of low-pH larvae was significantly smaller than in the control. After 2 mo of exposure the mussels were 28% smaller in the pH 7.6 treatment than in the control. The experiment with Pandalus borealis larvae ran from 1 through 35 days post hatch. Survival of shrimp larvae was not reduced after 5 wk of exposure to pH 7.6, but a significant delay in zoeal progression (development time) was observed.

Berge, J.A., Bjerkeng, B., Pettersen, O., Schaanning, M.T. and Oxnevad, S. 2006. Effects of increased sea water concentrations of CO2 on growth of the bivalve Mytilus edulis L. Chemosphere 62 : 681-687.

It has been proposed that emission of anthropogenic carbon dioxide to the atmosphere will lead to increased concentrations of CO2 in sea water corresponding to a decrease of pH of several tenths of pH units. An experiment was performed to test the effects of increased sea water concentrations of CO2 on shell growth of the blue mussel Mytilus edulis. The experiment was performed in aquaria continuously flushed with sea water spiked with CO2 to provide five different levels of pH between 6.7 and control sea water with a pH of 8.1. The shell length of the mussels was measured at the start and end of the 44 days experimental period. No mortality was observed during the first 23 days of the experiment. The growth increment in mm was much larger for small mussels than for large mussels, but relative growth profile as function of pH was more similar in the two size groups; observed differences may be random variation between samples. The experiments showed that CO2 induced reduction of pH affects the growth of M. edulis negatively. There was a strong and statistically significant decrease in growth at the lowest pH values, with virtually no growth at pH = 6.7 and reduced growth at pH = 7.1. The effect seems to set in between pH 7.4 and 7.1; at mean pH levels 7.4 and 7.6 the growth increments were not significantly different from growth at normal pH 8.1.

Brennand, H.S., Soars, N. Dworjanyn, S.A., Davis, A.R. and Byrne, M. 2010. Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS ONE 5 : e11372. doi:10.1371/journal.pone.0011372.

This study of the effects of ocean warming and CO2 driven acidification on development and calcification of marine invertebrate larvae reared in experimental conditions from the outset of development (fertilization) shows the positive and negative effects of these stressors. In simultaneous exposure to stressors the dwarfing effects of acidification were dominant. Reduction in size of sea urchin larvae in a high PCO2 ocean would likely impair their performance with negative consequent effects for benthic adult populations.

Byrne, M., Ho, M., Selvakumaraswamy, P., Nguyen, H.D., Dworjanyn, S. A. and Davis, A.R. 2009. Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proceedings of the Royal Society B 276 : 1883-1888.

Global warming is causing ocean warming and acidification. The distribution of Heliocidaris erythrogramma coincides with the eastern Australia climate change hot spot, where disproportionate warming makes marine biota particularly vulnerable to climate change. In keeping with near-future climate change scenarios, we determined the interactive effects of warming and acidification on fertilization and development of this echinoid. Experimental treatments (20–26°C, pH 7.6–8.2) were tested in all combinations for the ‘business-as-usual’ scenario, with 20°C/pH 8.2 being ambient. Percentage of fertilization was high (>89%) across all treatments. There was no difference in percentage of normal development in any pH treatment. In elevated temperature conditions, +4°C reduced cleavage by 40 per cent and +6°C by a further 20 per cent. Normal gastrulation fell below 4 per cent at +6°C. At 26°C, development was impaired. As the first study of interactive effects of temperature and pH on sea urchin development, we confirm the thermotolerance and pH resilience of fertilization and embryogenesis within predicted climate change scenarios, with negative effects at upper limits of ocean warming. Our findings place single stressor studies in context and emphasize the need for experiments that address ocean warming and acidification concurrently. Although ocean acidification research has focused on impaired calcification, embryos may not reach the skeletogenic stage in a warm ocean.

Byrne, M., Ho, M., Wong, E., Soars, N.A., Selvakumaraswamy, P., Shepard-Brennand, H., Dworjanyn, S.A. and Davis, A.R. 2011. Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean. Proceedings of the Royal Society B 278 : 2376-2383.

The most fragile skeletons produced by benthic marine calcifiers are those that larvae and juveniles make to support their bodies. Ocean warming, acidification, decreased carbonate saturation and their interactive effects are likely to impair skeletogenesis. Failure to produce skeleton in a changing ocean has negative implications for a diversity of marine species. We examined the interactive effects of warming and acidification on an abalone (Haliotis coccoradiata) and a sea urchin (Heliocidaris erythrogramma) reared from fertilization in temperature and pH/pCO2 treatments in a climatically and regionally relevant setting. Exposure of ectodermal (abalone) and mesodermal (echinoid) calcifying systems to warming (+2°C to 4°C) and acidification (pH 7.6–7.8) resulted in unshelled larvae and abnormal juveniles. Haliotis development was most sensitive with no interaction between stressors. For Heliocidaris, the percentage of normal juveniles decreased in response to both stressors, although a +2°C warming diminished the negative effect of low pH. The number of spines produced decreased with increasing acidification/pCO2, and the interactive effect between stressors indicated that a +2°C warming reduced the negative effects of low pH. At +4°C, the developmental thermal tolerance was breached. Our results show that projected near-future climate change will have deleterious effects on development with differences in vulnerability in the two species.

Crim, R.N., Sunday, J.M. and Harley, C.D.G. 2011. Elevated seawater CO2 concentrations impair larval development and reduce larval survival in endangered northern abalone (Haliotis kamtschatkana). Journal of Experimental Marine Biology and Ecology 400: 272-277.

Increasing levels of anthropogenic carbon dioxide in the world’s oceans are resulting in a decrease in the availability of carbonate ions and a drop in seawater pH. This process, known as ocean acidification, is a potential threat to marine populations via alterations in survival and development. To date, however, little research has examined the effects of ocean acidification on rare or endangered species. To begin to assess the impacts of acidification on endangered northern abalone (Haliotis kamtschatkana) populations, we exposed H. kamtschatkana larvae to various levels of CO2 [400 ppm (ambient), 800 ppm, and 1800 ppm CO2] and measured survival, settlement, shell size, and shell development. Larval survival decreased by ca. 40% in elevated CO2 treatments relative to the 400 ppm control. However, CO2 had no effect on the proportion of surviving larvae that metamorphosed at the end of the experiment. Larval shell abnormalities became apparent in approximately 40% of larvae reared at 800 ppm CO2, and almost all larvae reared at 1800 ppm CO2 either developed an abnormal shell or lacked a shell completely. Of the larvae that did not show shell abnormalities, shell size was reduced by 5% at 800 ppm compared to the control. Overall, larval development of H. kamtschatkana was found to be sensitive to ocean acidification. Near future levels of CO2 will likely pose a significant additional threat to this species, which is already endangered with extinction due in part to limited reproductive output and larval recruitment.

Cullen, J.T. and Sherrell, R.M. 2005. Effects of Dissolved Carbon Dioxide, Zinc, and Manganese on the Cadmium to Phosphorus Ratio in Natural Phytoplankton Assemblages. Limnology and Oceanography 50 : 1193-1204.

We report the results of a field study, in productive waters off California, of the factors that control the particulate cadmium (Cd) : phosphorus (P) composition of natural assemblages of marine phytoplankton, the dominant vector of both elements to the deep ocean. Controlled shipboard incubation experiments (;2–4 d) demonstrated that while manipulation of pCO2 and dissolved zinc (Zn) and manganese (Mn) concentrations had little effect on the species composition or C : nitrogen (N) : P ratios of natural, diatom-dominated phytoplankton assemblages, their Cd : P ratio was negatively correlated to each of these variables. The particulate Cd : P ratios of phytoplankton were two to five times higher for cells grown at low pCO2 than for cells acclimated to growth at pCO2 at or above atmospheric equilibrium values. Addition of Zn to incubations at five- to 20-fold above background concentrations decreased Cd uptake and phytoplankton Cd : P ratios across pCO2 and Mn treatments and suppressed short term Cd uptake rates by a factor of approximately two to four, compared to controls. A broad pattern of Mn suppression of Cd uptake was also evident in our incubations. We propose that natural variability in surface water pCO2 and dissolved Zn and Mn, related to water mass history and biological drawdown, likely govern the degree of Cd uptake and, therefore, the evolution of the dissolved Cd : PO4 ratio in recently upwelled, high-productivity surface waters.

Czerny, J., Barcelos e Ramos, J. and Riebesell, U. 2009. Influence of elevated CO2 concentrations on cell division and nitrogen fixation rates in the bloom-forming cyanobacterium Nodularia spumigena. Biogeosciences Discussions 6 : 4279-4304.

The surface ocean currently absorbs about one-fourth of the CO2 emitted to the atmosphere from human activities. As this CO2 dissolves in seawater, it reacts with seawater to form carbonic acid, increasing ocean acidity and shifting the partitioning of inorganic carbon species towards increased CO2 at the expense of CO32- concentrations. While the decrease in [CO32-] and/or increase in [H+] has been found to adversely affect many calcifying organisms, some photosynthetic organisms appear to benefit from increasing [CO2]. Among these is the cyanobacterium Trichodesmium, a predominant diazotroph (nitrogen-fixing) in large parts of the oligotrophic oceans, which responded with increased carbon and nitrogen fixation at elevated pCO2. With the mechanism underlying this CO2 stimulation still unknown, the question arises whether this is a common response of diazotrophic cyanobacteria. In this study we therefore investigate the physiological response of Nodularia spumigena, a heterocystous bloom-forming diazotroph of the Baltic Sea, to CO2-induced changes in seawater carbonate chemistry. N. spumigena reacted to seawater acidification/carbonation with reduced cell division rates and nitrogen fixation rates, accompanied by significant changes in carbon and phosphorus quota and elemental composition of the formed biomass. Possible explanations for the contrasting physiological responses of Nodularia compared to Trichodesmium may be found in the different ecological strategies of non-heterocystous (Trichodesmium) and heterocystous (Nodularia) cyanobacteria.

De Bodt, C., Van Oostende, N., Harlay, J., Sabbe, K. and Chou, L. 2010. Individual and interacting effects of pCO2 and temperature on Emiliania huxleyi calcification: study of the calcite production, the coccolith morphology and the coccosphere size. Biogeosciences 7 : 1401-1412.

The impact of ocean acidification and increased water temperature on marine ecosystems, in particular those involving calcifying organisms, has been gradually recognised. We examined the individual and combined effects of increased pCO(2) (180 ppmV CO2, 380 ppmV CO2 and 750 ppmV CO2 corresponding to past, present and future CO2 conditions, respectively) and temperature (13 degrees C and 18 degrees C) during the exponential growth phase of the coccolithophore E. huxleyi using batch culture experiments. We showed that cellular production rate of Particulate Organic Carbon (POC) increased from the present to the future CO2 treatments at 13 degrees C. A significant effect of pCO(2) and of temperature on calcification was found, manifesting itself in a lower cellular production rate of Particulate Inorganic Carbon (PIC) as well as a lower PIC:POC ratio at future CO2 levels and at 18 degrees C. Coccosphere-sized particles showed a size reduction with both increasing temperature and CO2 concentration. The influence of the different treatments on coccolith morphology was studied by categorizing SEM coccolith micrographs. The number of well-formed coccoliths decreased with increasing pCO(2) while temperature did not have a significant impact on coccolith morphology. No interacting effects of pCO(2) and temperature were observed on calcite production, coccolith morphology or on coccosphere size. Finally, our results suggest that ocean acidification might have a larger adverse impact on coccolithophorid calcification than surface water warming.

Dupont, S., Havenhand, J., Thorndyke, W., Peck, L. and Thorndyke, M. 2008. Near-future level of CO2-driven ocean acidificationradically affects larval survival and development inthe brittlestar Ophiothrix fragilis. Marine Ecology Progress Series 373 :285-294.

The world’s oceans are slowly becoming more acidic. In the last 150 yr, the pH of the oceans has dropped by ~0.1 units, which is equivalent to a 25% increase in acidity. Modelling predicts the pH of the oceans to fall by 0.2 to 0.4 units by the year 2100. These changes will have significant effects on marine organisms, especially those with calcareous skeletons such as echinoderms. Little is known about the possible long-term impact of predicted pH changes on marine invertebrate larval development. Here we predict the consequences of increased CO2 (corresponding to pH drops of 0.2 and 0.4 units) on the larval development of the brittlestar Ophiothrix fragilis, which is a keystone species occurring in high densities and stable populations throughout the shelf seas of northwestern Europe (eastern atlantic). Acidification by 0.2 units induced 100% larval mortality within 8 d while control larvae showed 70% survival over the same period. Exposure to low pH also resulted in a temporal decrease in larval size as well as abnormal development and skeletogenesis (abnormalities, asymmetry, altered skeletal proportions). If oceans continue to acidify as expected, ecosystems of the Atlantic dominated by this keystone species will be seriously threatened with major changes in many key benthic and pelagic ecosystems. Thus, it may be useful to monitor O. fragilis populations and initiate conservation if needed.

Dupont, S., Lundve, B. and Thorndyke, M. 2010 Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. Journal of Experimental Zoology 314B: 382-389.

Ocean acidification (OA) is believed to be a major threat for near-future marine ecosystems, and that the most sensitive organisms will be calcifying organisms and the free-living larval stages produced by most benthic marine species. In this respect, echinoderms are one of the taxa most at risk. Earlier research on the impact of near-future OA on echinoderm larval stages showed negative effects, such as a decreased growth rate, increased mortality, and developmental abnormalities. However, all the long-term studies were performed on planktotrophic larvae while alternative life-history strategies, such as nonfeeding lecithotrophy, were largely ignored. Here, we show that lecithotrophic echinoderm larvae and juveniles are positively impacted by ocean acidification. When cultured at low pH, larvae and juveniles of the sea star Crossaster papposus grow faster with no visible affects on survival or skeletogenesis. This suggests that in future oceans, lecithotrophic species may be better adapted to deal with the threat of OA compared with planktotrophic ones with potentially important consequences at the ecosystem level. For example, an increase in populations of the top predator C. papposus will likely have huge consequences for community structure. Our results also highlight the importance of taking varying life-history strategies into account when assessing the impacts of climate change, an approach that also provides insight into understanding the evolution of life-history strategies. J. Exp. Zool. (Mol. Dev. Evol.) 314B:382–389, 2010. © 2010 Wiley-Liss, Inc.

Findlay, H.S., Kendall, M.A., Spicer, J.I. and Widdicombe, S. 2010. Post-larval development of two intertidal barnacles at elevated CO2 and temperature. Marine Biology 157 : 725-735.

Ocean acidification and global warming are occurring concomitantly, yet few studies have investigated how organisms will respond to increases in both temperature and CO2. Intertidal microcosms were used to examine growth, shell mineralogy and survival of two intertidal barnacle post-larvae, Semibalanus balanoides and Elminius modestus, at two temperatures (14 and 19°C) and two CO2 concentrations (380 and 1,000 ppm), fed with a mixed diatom-flagellate diet at 15,000 cells ml-1 with flow rate of 10 ml-1 min-1. Control growth rates, using operculum diameter, were 14 ± 8 µm day-1 and 6 ± 2 µm day-1 for S. balanoides and E. modestus, respectively. Subtle, but significant decreases in E. modestus growth rate were observed in high CO2 but there were no impacts on shell calcium content and survival by either elevated temperature or CO2. S. balanoides exhibited no clear alterations in growth rate but did show a large reduction in shell calcium content and survival under elevated temperature and CO2. These results suggest that a decrease by 0.4 pH(NBS) units alone would not be sufficient to directly impact the survival of barnacles during the first month post-settlement. However, in conjunction with a 4–5°C increase in temperature, it appears that significant changes to the biology of these organisms will ensue.

Fine, M. and Tchernov, D. 2007. Scleractinian coral species survive and recover from decalcification. Science 315 : 1811.

Anthropogenic-driven accumulation of carbon dioxide in the atmosphere and projected ocean acidification have raised concerns regarding the eventual impact on coral reefs. This study demonstrates that skeleton-producing corals grown in acidified experimental conditions are able to sustain basic life functions, including reproductive ability, in a sea anemone-like form and will resume skeleton building when reintroduced to normal modern marine conditions. These results support the existence of physiological refugia, allowing corals to alternate between nonfossilizing soft-body ecophenotypes and fossilizing skeletal forms in response to changes in ocean chemistry. This refugia, however, does not undermine the threats to reef ecosystems in a high carbon dioxide world.

Foss, A., Røsnes,B.A. and Øiestad, V. 2003. Graded environmental hypercapnia in juvenile spotted wolffish (Anarhichas minor Olafsen): effects on growth, food conversion efficiency and nephrocalcinosis. Aquaculture 220 : 607-617.

Growth performance and food conversion efficiency (FCE) were investigated in juvenile spotted wolffish (Anarhichas minor Olafsen), mean (S.D.) initial weight 15.7 (4.8) g, reared at four levels of carbon dioxide (CO2(aq)) for 10 weeks at 6 °C and 33‰. CO2 levels averaged 1.1 (control), 18.1 (low), 33.5 (medium) and 59.4 (high) mg l-1, with corresponding pH values of 8.10, 6.98, 6.71 and 6.45, respectively. In addition, kidneys from sampled fish were examined macroscopically for gross signs of calcareous deposits, i.e. nephrocalcinosis, at the start and end of the experiment. Growth was significantly reduced at the highest concentration (P<0.0001), as compared to all other groups, while no overall differences in growth rate or mean weight were seen in the range of 1.1–33.5 mg CO2 l-1 at the end of the experiment. Daily feeding rates and total food consumption were reduced at the highest concentration (P<0.001), whereas food conversion efficiency did not vary significantly between groups. Plasma chloride levels displayed a significant decrease with increasing CO2 levels, from 151.3 mmol l-1 (1.1 mg CO2 l-1) to 128.3 mmol l-1 (59.4 mg CO2 l-1) at the end of the experiment, whereas plasma osmolality in the high CO2 group was significantly higher compared to the control group at the end of the experiment (371.4 and 350.8 mOsmol kg-1, respectively). Nephrocalcinosis was observed in all groups at the end of the experiment, but was most pronounced in the medium and high CO2 group.

Fu, F.-X., Mulholland, M.R., Garcia, N.S., Beck, A., Bernhardt, P.W., Warner, M.E., Sanudo-Wilhelmy, S.A. and Hutchins, D.A. 2008. Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera. Limnology and Oceanography 53 : 2472-2484.

We examined the physiological responses of steady-state iron (Fe)-replete and Fe-limited cultures of the biogeochemically critical marine unicellular diazotrophic cyanobacterium Crocosphaera at glacial (19 Pa; 190 ppm), current (39 Pa; 380 ppm), and projected year 2100 (76 Pa; 750 ppm) CO2 levels. Rates of N2 and CO2 fixation and growth increased in step with increasing partial pressure of CO2 (pCO2), but only under Fe-replete conditions. N2 and carbon fixation rates at 75 Pa CO2 were 1.4–1.8-fold and 1.2–2.0-fold higher, respectively, relative to those at present day and glacial pCO2 levels. In Fe-replete cultures, cellular Fe and molybdenum quotas varied threefold and were linearly related to N2 fixation rates and to external pCO2. However, N2 fixation and trace metal quotas were decoupled from pCO2 in Fe-limited Crocosphaera. Higher CO2 and Fe concentrations both resulted in increased cellular pigment contents and affected photosynthesis vs. irradiance parameters. If these results also apply to natural Crocosphaera populations, anthropogenic CO2 enrichment could substantially increase global oceanic N2 and CO2 fixation, but this effect may be tempered by Fe availability. Possible biogeochemical consequences may include elevated inputs of new nitrogen to the ocean and increased potential for Fe and/or phosphorus limitation in the future high-CO2 ocean, and feedbacks to atmospheric pCO2 in both the near future and over glacial to interglacial timescales.

Fu, F.-X., Warner, M.E., Zhang, Y., Feng, Y. and Hutchins, D.A. 2007. Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). Journal of Phycology 43 : 485–496.

Little is known about the combined impacts of future CO2 and temperature increases on the growth and physiology of marine picocyanobacteria. We incubated Synechococcus and Prochlorococcus under present-day (380 ppm) or predicted year-2100 CO2 levels (750 ppm), and under normal versus elevated temperatures (+4°C) in semicontinuous cultures. Increased temperature stimulated the cell division rates of Synechococcus but not Prochlorococcus. Doubled CO2 combined with elevated temperature increased maximum chl a–normalized photosynthetic rates of Synechococcus four times relative to controls. Temperature also altered other photosynthetic parameters (a, Fmax, Ek, and ) in Synechococcus, but these changes were not observed for Prochlorococcus. Both increased CO2 and temperature raised the phycobilin and chl a content of Synechococcus, while only elevated temperature increased divinyl chl a in Prochlorococcus. Cellular carbon (C) and nitrogen (N) quotas, but not phosphorus (P) quotas, increased with elevated CO2 in Synechococcus, leading to ~20% higher C:P and N:P ratios. In contrast, Prochlorococcus elemental composition remained unaffected by CO2, but cell volume and elemental quotas doubled with increasing temperature while maintaining constant stoichiometry. Synechococcus showed a much greater response to CO2 and temperature increases for most parameters measured, compared with Prochlorococcus. Our results suggest that global change could influence the dominance of Synechococcus and Prochlorococcus ecotypes, with likely effects on oligotrophic food-web structure. However, individual picocyanobacteria strains may respond quite differently to future CO2 and temperature increases, and caution is needed when generalizing their responses to global change in the ocean.

Fu, F.-X., Zhang, Y., Warner, M.E., Feng, Y., Sun, J. and Hutchins, D.A. 2008. A comparison of future increased CO2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae 7 : 76-90.

Very little is known about how global anthropogenic changes will affect major harmful algal bloom groups. Shifts in the growth and physiology of HAB species like the raphidophyte Heterosigma akashiwo and the dinoflagellate Prorocentrum minimum due to rising CO2 and temperature could alter their relative abundance and environmental impacts in estuaries where both form blooms, such as the Delaware Inland Bays (DIB). We grew semi-continuous cultures of sympatric DIB isolates of these two species under four conditions: (1) 20 °C and 375 ppm CO2 (ambient control), (2) 20 °C and 750 ppm CO2 (high CO2), (3) 24 °C and 375 ppm CO2 (high temperature), and (4) 24 °C and 750 ppm CO2 (combined). Elevated CO2 alone or in concert with temperature stimulated Heterosigma growth, but had no significant effect on Prorocentrum growth. PBmax (the maximum biomass-normalized light-saturated carbon fixation rate) in Heterosigma was increased only by simultaneous CO2 and temperature increases, whereas PBmax in Prorocentrum responded significantly to CO2 enrichment, with or without increased temperature. CO2 and temperature affected photosynthetic parameters a, Fmax, Ek, and in both species. Increased temperature decreased and increased the Chl a content of Heterosigma and Prorocentrum, respectively. CO2 availability and temperature had pronounced effects on cellular quotas of C and N in Heterosigma, but not in Prorocentrum. Ratios of C:P and N:P increased with elevated carbon dioxide in Heterosigma but not in Prorocentrum. These changes in cellular nutrient quotas and ratios imply that Heterosigma could be more vulnerable to N limitation but less vulnerable to P-limitation than Prorocentrum under future environmental conditions. In general, Heterosigma growth and physiology showed a much greater positive response to elevated CO2 and temperature compared to Prorocentrum, consistent with what is known about their respective carbon acquisition mechanisms. Hence, rising temperature and CO2 either alone or in combination with other limiting factors could significantly alter the relative dominance of these two co-existing HAB species over the next century.

Gao, K., Aruga, Y., Asada, K., Ishihara, T., Akano, T. and Kiyohara, M. 1991. Enhanced growth of the red alga Porphyra yezoensis Ueda in high CO2 concentrations. Journal of Applied Phycology 3 : 355-362.

Leafy thalli of the red algaPorphyra yezoensis Ueda, initiated from conchospores released from free-living conchocelis, were cultured using aeration with high CO2. It was found that the higher the CO2 concentration, the faster the growth of the thalli. Aeration with elevated CO2 lowered pH in dark, but raised pH remarkably in light with the thalli, because the photosynthetic conversion of HCO 3 – to OH- and CO2 proceeded much faster than the dissociation of hydrated CO2 releasing H+. Photosynthesis of the alga was found to be enhanced in the seawater of elevated dissolved inorganic carbon (DIC, CO2 + HCO 3 – + CO 3 – ). It is concluded that the increased pH in the light resulted in the increase of DIC in the culture media, thus enhancing photosynthesis and growth. The relevance of the results to removal of atmospheric CO2 by marine algae is discussed.

Gattuso, J.-P., Frankignoulle, M., Bourge, I., Romaine, S. and Buddemeier, R.W. 1998. Effect of calcium carbonate saturation of seawater on coral calcification. Global and Planetary Change 18 : 37-46.

The carbonate chemistry of seawater is usually not considered to be an important factor influencing calcium-carbonate-precipitation by corals because surface seawater is supersaturated with respect to aragonite. Recent reports, however, suggest that it could play a major role in the evolution and biogeography of recent corals. We investigated the calcification rates of five colonies of the zooxanthellate coral Stylophora pistillata in synthetic seawater using the alkalinity anomaly technique. Changes in aragonite saturation from 98% to 585% were obtained by manipulating the calcium concentration. The results show a nonlinear increase in calcification rate as a function of aragonite saturation level. Calcification increases nearly 3-fold when aragonite saturation increases from 98% to 390%, i.e., close to the typical present saturation state of tropical seawater. There is no further increase of calcification at saturation values above this threshold. Preliminary data suggest that another coral species, Acropora sp., displays a similar behaviour. These experimental results suggest: (1) that the rate of calcification does not change significantly within the range of saturation levels corresponding to the last glacial-interglacial cycle, and (2) that it may decrease significantly in the future as a result of the decrease in the saturation level due to anthropogenic release of CO2 into the atmosphere. Experimental studies that control environmental conditions and seawater composition provide unique opportunities to unravel the response of corals to global environmental changes.

Gazeau, F., Gattuso, J.-P., Dawber, C., Pronker, A.E., Peene, F., Peene, J., Heip, C.H.R. and Middelburg, J.J. 2010. Effect of ocean acidification on the early life stages of the blue mussel Mytilus edulis. Biogeosciences 7 : 2051-2060.

Several experiments have shown a decrease of growth and calcification of organisms at decreased pH levels. There is a growing interest to focus on early life stages that are believed to be more sensitive to environmental disturbances such as hypercapnia. Here, we present experimental data, acquired in a commercial hatchery, demonstrating that the growth of planktonic mussel (Mytilus edulis) larvae is significantly affected by a decrease of pH to a level expected for the end of the century. Even though there was no significant effect of a 0.25–0.34 pH unit decrease on hatching and mortality rates during the first 2 days of development nor during the following 13-day period prior to settlement, final shells were respectively 4.5±1.3 and 6.0±2.3% smaller at pHNBS~7.8 (pCO2~1100–1200 µatm) than at a control pHNBS of ~8.1 (pCO2~460–640 µatm). Moreover, a decrease of 12.0±5.4% of shell thickness was observed after 15d of development. More severe impacts were found with a decrease of ~0.5 pHNBS unit during the first 2 days of development which could be attributed to a decrease of calcification due to a slight undersaturation of seawater with respect to aragonite. Indeed, important effects on both hatching and D-veliger shell growth were found. Hatching rates were 24±4% lower while D-veliger shells were 12.7±0.9% smaller at pHNBS~7.6 (pCO2~1900 µatm) than at a control pHNBS of ~8.1 (pCO2~540 µatm). Although these results show that blue mussel larvae are still able to develop a shell in seawater undersaturated with respect to aragonite, the observed decreases of hatching rates and shell growth could lead to a significant decrease of the settlement success. As the environmental conditions considered in this study do not necessarily reflect the natural conditions experienced by this species at the time of spawning, future studies will need to consider the whole larval cycle (from fertilization to settlement) under environmentally relevant conditions in order to investigate the potential ecological and economical losses of a decrease of this species fitness in the field.

Gazeau, F., Quiblier, C., Jansen, J.M., Gattuso, J.-P., Middelburg, J.J. and Heip, C.H.R. 2007. Impact of elevated CO2 on shellfish calcification. Geophysical Research Letters 34, L07603, doi:10.1029/2006GL028554.

Ocean acidification resulting from human emissions of carbon dioxide has already lowered and will further lower surface ocean pH. The consequent decrease in calcium carbonate saturation potentially threatens calcareous marine organisms. Here, we demonstrate that the calcification rates of the edible mussel (Mytilus edulis) and Pacific oyster (Crassostrea gigas) decline linearly with increasing pCO2. Mussel and oyster calcification may decrease by 25 and 10%, respectively, by the end of the century, following the IPCC IS92a scenario (~740 ppmv in 2100). Moreover, mussels dissolve at pCO2 values exceeding a threshold value of ~1800 ppmv. As these two species are important ecosystem engineers in coastal ecosystems and represent a large part of worldwide aquaculture production, the predicted decrease of calcification in response to ocean acidification will probably have an impact on coastal biodiversity and ecosystem functioning as well as potentially lead to significant economic loss.

Gooding, R.A., Harley, C.D.G. and Tang, E. 2009. Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proceedings of the National Academy of Sciences 106: 9316-9321.

Anthropogenic climate change poses a serious threat to biodiversity. In marine environments, multiple climate variables, including temperature and CO2 concentration ([CO2]), are changing simultaneously. Although temperature has well-documented ecological effects, and many heavily calcified marine organisms experience reduced growth with increased [CO2], little is known about the combined effects of temperature and [CO2], particularly on species that are less dependent on calcified shells or skeletons. We manipulated water temperature and [CO2] to determine the effects on the sea star Pisaster ochraceus, a keystone predator. We found that sea star growth and feeding rates increased with water temperature from 5 °C to 21 °C. A doubling of current [CO2] also increased growth rates both with and without a concurrent temperature increase from 12 °C to 15 °C. Increased [CO2] also had a positive but nonsignificant effect on sea star feeding rates, suggesting [CO2] may be acting directly at the physiological level to increase growth rates. As in past studies of other marine invertebrates, increased [CO2] reduced the relative calcified mass in sea stars, although this effect was observed only at the lower experimental temperature. The positive relationship between growth and [CO2] found here contrasts with previous studies, most of which have shown negative effects of [CO2] on marine species, particularly those that are more heavily calcified than P. ochraceus. Our findings demonstrate that increased [CO2] will not have direct negative effects on all marine invertebrates, suggesting that predictions of biotic responses to climate change should consider how different types of organisms will respond to changing climatic variables.

Gordillo, F.J.L, Jimenez, C., Figueroa, F.L. and Niell, F.X. 2003. Influence of elevated CO2 and nitrogen supply on the carbon assimilation performance and cell composition of the unicellular alga Dunaliella viridis. Physiologia Plantarum 119 : 513-518.

The carbon assimilation efficiency and the internal composition of the chlorophyte Dunaliella viridis have been studied under conditions of current (0.035%) and enriched (1%) levels of CO2, with and without N limitation (supplied as nitrate). Results show that both photosynthesis and growth rates are enhanced by high CO2, but the strategy of acclimation also involves the light harvesting machinery and the nutritional metabolism in an N supply dependent manner. D. viridis carried out a qualitative rather than a quantitative acclimation of the light harvesting system leading to increased PSII quantum yields. Total internal C decreased as a consequence of either active growth or organic carbon release to the external medium. The latter process allowed photosynthetic electron transport to proceed at higher rates than under normal CO2 conditions, and maintained the internal C:N balance in a narrow range (under N sufficiency). N limitation generally prevented the effects of high CO2, with some exceptions such as the photosynthetic O2 evolution rate.

Hare, C.E., Leblanc, K., DiTullio, G.R., Kudela, R.M. Zhang, Y., Lee, P.A., Riseman, S. and Hutchins, D.A. 2007. Consequences of increased temperature and CO2 for phytoplankton community structure in the Bering Sea. Marine Ecology Progress Series 352 : 9-16.

Global climate change is predicted to have large effects on the ocean that could cause shifts in current algal community structure, major nutrient cycles, and carbon export. The Bering Sea is already experiencing changes in sea surface temperature (SST), unprecedented algal blooms, and alterations to trophic level dynamics. We incubated phytoplankton communities from 2 Bering Sea regimes under conditions of elevated SST and/or partial pressure of carbon dioxide (pCO2) similar to predicted values for 2100. In our ‘greenhouse ocean’ simulations, maximum biomass-normalized photosynthetic rates increased 2.6 to 3.5 times and community composition shifted away from diatoms and towards nanophytoplankton. These changes were driven largely by elevated temperature, with secondary effects from increased pCO2. If these results are indicative of future climate responses, community shifts towards nanophytoplankton dominance could reduce the ability of the Bering Sea to maintain the productive diatom-based food webs that currently support one of the world’s most productive fisheries.

Iglesias-Rodriguez, M.D., Halloran, P.R., Rickaby, R.E.M., Hall, I.R., Colmenero-Hidalgo, E., Gittins, J.R., Green, D.R.H., Tyrrell, T., Gibbs, S.J., von Dassow, P., Rehm, E., Armbrust, E.V. and Boessenkool, K.P. 2008. Phytoplankton calcification in a high-CO2 world. Science 320 : 336-340.

Ocean acidification in response to rising atmospheric CO2 partial pressures is widely expected to reduce calcification by marine organisms. From the mid-Mesozoic, coccolithophores have been major calcium carbonate producers in the world’s oceans, today accounting for about a third of the total marine CaCO3 production. Here, we present laboratory evidence that calcification and net primary production in the coccolithophore species Emiliania huxleyi are significantly increased by high CO2 partial pressures. Field evidence from the deep ocean is consistent with these laboratory conclusions, indicating that over the past 220 years there has been a 40% increase in average coccolith mass. Our findings show that coccolithophores are already responding and will probably continue to respond to rising atmospheric CO2 partial pressures, which has important implications for biogeochemical modeling of future oceans and climate.

Ivers, O., Romero, J. and Perez, M. 1997. Effects of pH on seagrass photosynthesis: a laboratory and field assessment. Aquatic Botany 59 : 185-194.

The effects of pH changes on photosynthesis in three Mediterranean seagrass species were assessed by combining laboratory experiments with field records of pH. The response of photosynthesis to increasing pH was examined under laboratory conditions. Posidonia oceanica and Cymodocea nodosa showed a linear decrease in photosynthetic rates with pH; values at pH 8.8 were 25–80% of those obtained at pH 8.2. Zostera noltii was much less sensitive to pH increase than the other two species, maintaining high photosynthetic rates up to pH 8.8 and showing a significant reduction only at pH 9. Daily changes in pH over the seagrass meadows showed a maximum amplitude of ca. 0.5 pH units. However, the maximum daily values of pH were reached towards the end of the daily period of photosynthesis, and hence the estimated reduction in photosynthesis caused by the rising pH was relatively small (13–17%), in very shallow (i.e. 1 m deep or less) P. oceanica and C. nodosa meadows, and even less (about 4%) in deeper areas.

Jury, C.P., Whitehead, R.F. and Szmant, A.M. 2010. Effects of variations in carbonate chemistry on the calcification rates of Madracis auretenra (= Madracis mirabilis sensu Wells,1973): bicarbonate concentrations best predict calcification rates. Global Change Biology 16 : 1632-1644.

Physiological data and models of coral calcification indicate that corals utilize a combination of seawater bicarbonate and (mainly) respiratory CO2 for calcification, not seawater carbonate. However, a number of investigators are attributing observed negative effects of experimental seawater acidification by CO2 or hydrochloric acid additions to a reduction in seawater carbonate ion concentration and thus aragonite saturation state. Thus, there is a discrepancy between the physiological and geochemical views of coral biomineralization. Furthermore, not all calcifying organisms respond negatively to decreased pH or saturation state. Together, these discrepancies suggest that other physiological mechanisms, such as a direct effect of reduced pH on calcium or bicarbonate ion transport and/or variable ability to regulate internal pH, are responsible for the variability in reported experimental effects of acidification on calcification. To distinguish the effects of pH, carbonate concentration and bicarbonate concentration on coral calcification, incubations were performed with the coral Madracis auretenra (= Madracis mirabilis sensu Wells, 1973) in modified seawater chemistries. Carbonate parameters were manipulated to isolate the effects of each parameter more effectively than in previous studies, with a total of six different chemistries. Among treatment differences were highly significant. The corals responded strongly to variation in bicarbonate concentration, but not consistently to carbonate concentration, aragonite saturation state or pH. Corals calcified at normal or elevated rates under low pH (7.6–7.8) when the seawater bicarbonate concentrations were above 1800 μm. Conversely, corals incubated at normal pH had low calcification rates if the bicarbonate concentration was lowered. These results demonstrate that coral responses to ocean acidification are more diverse than currently thought, and question the reliability of using carbonate concentration or aragonite saturation state as the sole predictor of the effects of ocean acidification on coral calcification.

Kikkawa, T., Ishimatsu, A. and Kita, J. 2003. Acute CO2 tolerance during the early developmental stages of four marine teleosts. Environmental Toxicology 18 : 375-382.

Ocean sequestration of CO2 is proposed as a possible measure to mitigate climate changes caused by increasing atmospheric concentrations of the gas, but its impact on the marine ecosystem is unknown. We investigated the acute lethal effect of CO2 during the early developmental stages of four marine teleosts: red sea bream (Pagrus major), Japanese whiting (Sillago japonica), Japanese flounder (Paralichthys olivaceus), and eastern little tuna (Euthynnus affinis). The percentages of larvae that hatched and survived were not affected by exposure to water with a PCO2 of 1.0 kPa (= 7.5 mmHg) within 24 h. Median lethal PCO2 values for a 360-min exposure were 1.4 kPa (cleavage), 5.1 kPa (embryo), 7.3 kPa (preflexion), 4.2 kPa (flexion), 4.6 kPa (postflexion), and 2.5 kPa (juvenile) for red sea bream; 2.4 kPa (cleavage), 4.9 kPa (embryo), 5.9 kPa (preflexion), 6.1 kPa (flexion), 4.1 kPa (postflexion), and 2.7 kPa (juvenile) for Japanese whiting; 2.8 kPa (cleavage) and > 7.0 kPa (young) for Japanese flounder; and 11.8 kPa (cleavage) for eastern little tuna. Red sea bream and Japanese whiting of all ontogenetic stages had similar susceptibilities to CO2: the most susceptible stages were cleavage and juvenile, whereas the most tolerant stages were preflexion and flexion.

Kim,J.-M., Lee, K., Shin, K., Kang, J.-H., Lee, H.-W., Kim, M., Jang,P.-G. and Jang, M.-C. 2006. The effect of seawater CO2 concentration ongrowth of a natural phytoplankton assemblage in a controlled mesocosmexperiment. Limnology and Oceanography 51 : 1629-1636.

We examine the effects of seawater pCO2 concentration of 25, 41, and 76 kPa (250, 400, and 750 matm) on the growth rate of a natural assemblage of mixed phytoplankton obtained from a carefully controlled, 14-d mesocosm experiment. Throughout the experiment period, in all enclosures, two phytoplankton taxa (microflagellates and cryptomonads) and two diatom species (Skeletonema costatum and Nitzschia spp.) account for approximately 90% of the phytoplankton community. During the nutrient-replete period from day 9 to day 14 populations of Skeletonema costatum and Nitzschia spp. increased substantially; however, only Skeletonema costatum showed an increase in growth rate with increasing seawater pCO2. Not all diatom species in Korean coastal waters are sensitive to seawater pCO2 under nutrient-replete conditions.

Krief, S., Hendy, E.J., Fine, M., Yam, R., Meibom, A., Foster, G.L. and Shemesh, A. 2010. Physiological and isotopic responses of scleractinian corals to ocean acidificiation. Geochimica et Cosmochimica Acta 74 : 4988-5001.

Uptake of anthropogenic CO2 by the oceans is altering seawater chemistry with potentially serious consequences for coral reef ecosystems due to the reduction of seawater pH and aragonite saturation state (Oarag). The objectives of this long-term study were to investigate the viability of two ecologically important reef-building coral species, massive Porites sp. and Stylophora pistillata, exposed to high pCO2 (or low pH) conditions and to observe possible changes in physiologically related parameters as well as skeletal isotopic composition. Fragments of Porites sp. and S. pistillata were kept for 6–14 months under controlled aquarium conditions characterized by normal and elevated pCO2 conditions, corresponding to pHT values of 8.09, 7.49, and 7.19, respectively. In contrast with shorter, and therefore more transient experiments, the long experimental timescale achieved in this study ensures complete equilibration and steady state with the experimental environment and guarantees that the data provide insights into viable and stably growing corals. During the experiments, all coral fragments survived and added new skeleton, even at seawater Oarag < 1, implying that the coral skeleton is formed by mechanisms under strong biological control. Measurements of boron (B), carbon (C), and oxygen (O) isotopic composition of skeleton, C isotopic composition of coral tissue and symbiont zooxanthellae, along with physiological data (such as skeletal growth, tissue biomass, zooxanthellae cell density, and chlorophyll concentration) allow for a direct comparison with corals living under normal conditions and sampled simultaneously. Skeletal growth and zooxanthellae density were found to decrease, whereas coral tissue biomass (measured as protein concentration) and zooxanthellae chlorophyll concentrations increased under high pCO2 (low pH) conditions. Both species showed similar trends of d11B depletion and d18O enrichment under reduced pH, whereas the d13C results imply species-specific metabolic response to high pCO2 conditions. The skeletal d11B values plot above seawater d11B vs. pH borate fractionation curves calculated using either the theoretically derived aB value of 1.0194 (Kakihana et al. (1977) Bull. Chem. Soc. Jpn.50, 158) or the empirical aB value of 1.0272 (Klochko et al. (2006) EPSL248, 261). However, the effective aB must be greater than 1.0200 in order to yield calculated coral skeletal d11B values for pH conditions where Oarag ? 1. The d11B vs. pH offset from the seawater d11B vs. pH fractionation curves suggests a change in the ratio of skeletal material laid down during dark and light calcification and/or an internal pH regulation, presumably controlled by ion-transport enzymes. Finally, seawater pH significantly influences skeletal d13C and d18O. This must be taken into consideration when reconstructing paleo-environmental conditions from coral skeletons.

Kübler, J.E., Johnston, A.M. and Raven, J.A. 1999. The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata. Plant, Cell and Environment 22: 1303-1310.

We grew a non-bicarbonate using red seaweed, Lomentaria articulata (Huds.) Lyngb., in media aerated with four O2 concentrations between 10 and 200% of current ambient [O2] and four CO2 concentrations between 67 and 500% of current ambient [CO2], in a factorial design, to determine the effects of gas composition on growth and physiology. The relative growth rate of L. articulata increased with increasing [CO2] up to 200% of current ambient [CO2] but was unaffected by [O2]. The relative growth enhancement, on a carbon basis, was 52% with a doubling of [CO2] but fell to 23% under 5× ambient [CO2]. Plants collected in winter responded more extremely to [CO2] than did plants collected in the summer, although the overall pattern was the same. Discrimination between stable carbon isotopes (Δ13C) increased with increasing [CO2] as would be expected for diffusive CO2 acquisition. Tissue C and N were inversely related to [CO2]. Growth in terms of biomass appeared to be limited by conversion of photosynthate to new biomass rather than simply by diffusion of CO2, suggesting that non-bicarbonate-using macroalgae, such as L. articulata, may not be directly analogous to C3 higher plants in terms of their responses to changing gas composition.

Kurihara, H. and Shirayama, Y. 2004. Effects of increased atmospheric CO2 on sea urchin early development. Marine Ecology Progress Series 274 : 161-169.

Increased carbon dioxide (CO2) concentration in the atmosphere will change the balance of the components of carbonate chemistry and reduce the pH at the ocean surface. Here, we report the effects of increased CO2 concentration on the early development of the sea urchins Hemicentrotus pulcherrimus and Echinometra mathaei. We examined the fertilization, early cleavage, and pluteus larval stage to evaluate the impact of elevated CO2 concentration on fertilization rate, cleavage rate, developmental speed, and pluteus larval morphology. Furthermore, we compared the effects of CO2 and HCl at the same pH in an attempt to elucidate any differences between the two. We found that fertilization rate, cleavage rate, developmental speed, and pluteus larval size all tended to decrease with increasing CO2 concentration. Furthermore, CO2-seawater had a more severe effect than HCl-seawater on the fertilization rate. By contrast, the effects on cleavage rate, developmental speed, and pluteus larval morphology were similar for CO2- and HCl-seawater. Our results suggest that both decreased pH and altered carbonate chemistry affect the early development and life history of marine animals, implying that increased seawater CO2 concentration will seriously alter marine ecosystems. The effects of CO2 itself on marine organisms therefore requires further clarification.

Kurihara, H., Shimode, S. and Shirayama Y. 2004. Effects of raised CO2 concentration on the egg production rate and early development of two marine copepods (Acartia steueri and Acartia erythraea). Marine Pollution Bulletin 49 : 721-727.

Direct injection of CO2 into the deep ocean is receiving increasing attention as a way to mitigate increasing atmospheric CO2 concentration. To assess the potential impact of the environmental change associated with CO2 sequestration in the ocean, we studied the lethal and sub-lethal effects of raised CO2 concentration in seawater on adult and early stage embryos of marine planktonic copepods. We found that the reproduction rate and larval development of copepods are very sensitive to increased CO2 concentration. The hatching rate tended to decrease, and nauplius mortality rate to increase, with increased CO2 concentration. These results suggest that the marine copepod community will be negatively affected by the disposal of CO2. This could decrease on the carbon export flux to the deep ocean and change the biological pump. Clearly, further studies are needed to determine whether ocean CO2 injection is an acceptable strategy to reduce anthropogenic CO2.

Kuroyanagi, A., Kawahata, H., Suzuki, A., Fujita, K. and Irie, T. 2009. Impacts of ocean acidification on large benthic foraminifers: Results from laboratory experiments. Marine Micropaleontology 73 : 190-195.

Ocean acidification has become recognized recently to be a major threat to calcifying organisms. Previous studies have reported that calcification rates of calcareous marine organisms (e.g., corals, foraminifers, coccolithophores, pteropods, mussels, and oysters) change in response to lowering pH levels even in waters oversaturated with respect to calcium carbonate. However, the impact of ocean acidification on large benthic foraminifers, which are major contributors to organic and inorganic carbon production in coral reefs, is still unclear. In this study, we cultured asexually-produced individuals of Marginopora kudakajimensis under four different pH conditions to examine the effects of lowering pH on their growth rates. Experimental results indicate that growth rate, measured by shell diameter, shell weight, and the number of chambers added, generally decreased with lowering pH after 10 weeks of culture. Shell weight was most closely dependent upon pH, suggesting that fossil shell weight can be more useful for reconstruction of paleo-pH changes. The relationship between the shell weight and shell size also showed significant differences among the four pH conditions. Between pH 8.3 and 7.7 (NBS scale), the tendency of the growth rate of M. kudakajimensis to decrease with pH was consistent with that of most other calcifying organisms. However, the calcification/growth rates at pH 7.9 and ~ 8.2 (present seawater value, control) were not significantly different, and other organisms also display a nonlinear response to elevated pCO2 at around this pH range. These results suggest that 1) they already may have experienced a reduction in growth in natural environments since pre-industrial times and 2) although the seawater CO2 system of reef water shows great variation, the calcification rate of these large foraminifers should remain at the present level at pH 7.9–8.2. However, at around pH 7.7, their calcification rate would decline steeply, which would probably preclude their survival.

Langdon, C. and Atkinson, M.J. 2005. Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. Journal of Geophysical Research 110, C09S07, doi:10.1029/2004JC002576.

An investigation was conducted to determine the effects of elevated pCO2 on the net production and calcification of an assemblage of corals maintained under near-natural conditions of temperature, light, nutrient, and flow. Experiments were performed in summer and winter to explore possible interactions between seasonal change in temperature and irradiance and the effect of elevated pCO2. Particular attention was paid to interactions between net production and calcification because these two processes are thought to compete for the same internal supply of dissolved inorganic carbon (DIC). A nutrient enrichment experiment was performed because it has been shown to induce a competitive interaction between photosynthesis and calcification that may serve as an analog to the effect of elevated pCO2. Net carbon production, NPC, increased with increased pCO2 at the rate of 3 ± 2% (µmol CO2aq kg-1)-1. Seasonal change of the slope NPC-[CO2aq] relationship was not significant. Calcification (G) was strongly related to the aragonite saturation state O a . Seasonal change of the G-O a relationship was not significant. The first-order saturation state model gave a good fit to the pooled summer and winter data: G = (8 ± 1 mmol CaCO3 m-2 h-1)(O a – 1), r 2 = 0.87, P = 0.0001. Both nutrient and CO2 enrichment resulted in an increase in NPC and a decrease in G, giving support to the hypothesis that the cellular mechanism underlying the decrease in calcification in response to increased pCO2 could be competition between photosynthesis and calcification for a limited supply of DIC.

Langenbuch, M. and Pörtner, H.O. 2004. High sensitivity to chronically elevated CO2 levels in a eurybathic marine sipunculid. Aquatic Toxicology 70 : 55-61.

CO2 levels are expected to rise (a) in surface waters of the oceans as atmospheric accumulation continues or (b) in the deep sea, once industrial CO2 dumping is implemented. These scenarios suggest that CO2 will become a general stress factor in aquatic environments. The mechanisms of sensitivity to CO2 as well as adaptation capacity of marine animals are insufficiently understood. Here, we present data obtained in Sipunculus nudus, a sediment-dwelling marine worm that is able to undergo drastic metabolic depression to survive regular exposure to elevated CO2 levels within its natural habitat. We investigated animal survival and the proximate biochemical body composition during long-term CO2 exposure. Results indicate an unexpected and pronounced sensitivity characterized by the delayed onset of enhanced mortality at CO2 levels within the natural range of concentrations. Therefore, the present study contrasts the previously assumed high-CO2 tolerance of animals adapted to temporary hypercapnia. As a consequence, we expect future loss of species and, thereby, detrimental effects on marine benthic ecosystems with as yet poorly defined critical thresholds of long-term tolerance to CO2.

Langer, G., Geisen, M., Baumann, K.-H., Kläs, J., Riebesell, U.,Thoms, S. and Young, J.R. 2006. Species-specific responses of calcifying algae to changing seawater carbonate chemistry. Geochemistry Geophysics Geosystems 7, Q09006, doi:10.1029/2005GC001227.

Uptake of half of the fossil fuel CO2 into the ocean causes gradual seawater acidification. This has been shown to slow down calcification of major calcifying groups, such as corals, foraminifera, and coccolithophores. Here we show that two of the most productive marine calcifying species, the coccolithophores Coccolithus pelagicus and Calcidiscus leptoporus, do not follow the CO2-related calcification response previously found. In batch culture experiments, particulate inorganic carbon (PIC) of C. leptoporus changes with increasing CO2 concentration in a nonlinear relationship. A PIC optimum curve is obtained, with a maximum value at present-day surface ocean pCO2 levels (~360 ppm CO2). With particulate organic carbon (POC) remaining constant over the range of CO2 concentrations, the PIC/POC ratio also shows an optimum curve. In the C. pelagicus cultures, neither PIC nor POC changes significantly over the CO2 range tested, yielding a stable PIC/POC ratio. Since growth rate in both species did not change with pCO2, POC and PIC production show the same pattern as POC and PIC. The two investigated species respond differently to changes in the seawater carbonate chemistry, highlighting the need to consider species-specific effects when evaluating whole ecosystem responses. Changes of calcification rate (PIC production) were highly correlated to changes in coccolith morphology. Since our experimental results suggest altered coccolith morphology (at least in the case of C. leptoporus) in the geological past, coccoliths originating from sedimentary records of periods with different CO2 levels were analyzed. Analysis of sediment samples was performed on six cores obtained from locations well above the lysocline and covering a range of latitudes throughout the Atlantic Ocean. Scanning electron micrograph analysis of coccolith morphologies did not reveal any evidence for significant numbers of incomplete or malformed coccoliths of C. pelagicus and C. leptoporus in last glacial maximum and Holocene sediments. The discrepancy between experimental and geological results might be explained by adaptation to changing carbonate chemistry.

Langer, G., Nehrke, G., Probert, I., Ly, J. and Ziveri, P. 2009. Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6 : 2637-2646.

Four strains of the coccolithophore Emiliania huxleyi (RCC1212, RCC1216, RCC1238, RCC1256) were grown in dilute batch culture at four CO2 levels ranging from ∼200 µatm to ∼1200 µatm. Growth rate, particulate organic carbon content, and particulate inorganic carbon content were measured, and organic and inorganic carbon production calculated. The four strains did not show a uniform response to carbonate chemistry changes in any of the analysed parameters and none of the four strains displayed a response pattern previously described for this species. We conclude that the sensitivity of different strains of E. huxleyi to acidification differs substantially and that this likely has a genetic basis. We propose that this can explain apparently contradictory results reported in the literature.

Lannig, G., Eilers, S., Portner, H.O., Sokolova, I.M. and Bock, C. 2010. Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas – changes in metabolic pathways and thermal response. Marine Drugs 8 : 2318-2339.

Climate change with increasing temperature and ocean acidification (OA) poses risks for marine ecosystems. According to Pörtner and Farrell [1], synergistic effects of elevated temperature and CO2-induced OA on energy metabolism will narrow the thermal tolerance window of marine ectothermal animals. To test this hypothesis, we investigated the effect of an acute temperature rise on energy metabolism of the oyster, Crassostrea gigas chronically exposed to elevated CO2 levels (partial pressure of CO2 in the seawater ~0.15 kPa, seawater pH ~ 7.7). Within one month of incubation at elevated PCO2 and 15 °C hemolymph pH fell (pHe = 7.1 ± 0.2 (CO2-group) vs. 7.6 ± 0.1 (control)) and PeCO2 values in hemolymph increased (0.5 ± 0.2 kPa (CO2-group) vs. 0.2 ± 0.04 kPa (control)). Slightly but significantly elevated bicarbonate concentrations in the hemolymph of CO2-incubated oysters ([HCO-3]e = 1.8 ± 0.3 mM (CO2-group) vs. 1.3 ± 0.1 mM (control)) indicate only minimal regulation of extracellular acid-base status. At the acclimation temperature of 15 °C the OA-induced decrease in pHe did not lead to metabolic depression in oysters as standard metabolism rates (SMR) of CO2-exposed oysters were similar to controls. Upon acute warming SMR rose in both groups, but displayed a stronger increase in the CO2-incubated group. Investigation in isolated gill cells revealed a similar temperature-dependence of respiration between groups. Furthermore, the fraction of cellular energy demand for ion regulation via Na+/K+-ATPase was not affected by chronic hypercapnia or temperature. Metabolic profiling using 1H-NMR spectroscopy revealed substantial changes in some tissues following OA exposure at 15 °C. In mantle tissue alanine and ATP levels decreased significantly whereas an increase in succinate levels was observed in gill tissue. These findings suggest shifts in metabolic pathways following OA-exposure. Our study confirms that OA affects energy metabolism in oysters and suggests that climate change may affect populations of sessile coastal invertebrates such as mollusks.

Leclercq N., Gattuso J.-P. and Jaubert J. 2002. Primary production, respiration, and calcification of a coral reef mesocosm under increased CO2 partial pressure. Limnology and Oceanography 47 : 558-564.

The effect of increased CO2 partial pressure (pCO2) on the community metabolism (primary production, respiration, and calcification) of a coral community was investigated over periods ranging from 9 to 30 d. The community was set up in an open-top mesocosm within which pCO2 was manipulated (411, 647, and 918 µatm). The effect of increased pCO2 on the rate of calcification of the sand area of the mesocosm was also investigated. The net community primary production (NCP) did not change significantly with respect to pCO2 and was 5.1 ± 0.9 mmol $O_2\> m^{-2}\> h^{-1}$. Dark respiration (R) increased slightly during the experiment at high pCO2, but this did not affect significantly the NCP : R ratio (1.0 ± 0.2). The rate of calcification exhibited the trend previously reported; it decreased as a function of increasing pCO2 and decreasing aragonite saturation state. This re-emphasizes the predictions that reef calcification is likely to decrease during the next century. The dissolution process of calcareous sand does not seem to be affected by open seawater carbonate chemistry; rather, it seems to be controlled by the biogeochemistry of sediment pore water.

Levitan, O., Rosenberg, G., Setlik, I., Setlikova, E., Grigel, J., Klepetar, J., Prasil, O. and Berman-Frank, I. 2007. Elevated CO2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Global Change Biology 13 : 531-538.

The increases in atmospheric pCO2 over the last century are accompanied by higher concentrations of CO2(aq) in the surface oceans. This acidification of the surface ocean is expected to influence aquatic primary productivity and may also affect cyanobacterial nitrogen (N)-fixers (diazotrophs). No data is currently available showing the response of diazotrophs to enhanced oceanic CO2(aq). We examined the influence of pCO2 [preindustrial~250 ppmv (low), ambient~400, future~900 ppmv (high)] on the photosynthesis, N fixation, and growth of Trichodesmium IMS101. Trichodesmium spp. is a bloom-forming cyanobacterium contributing substantial inputs of ‘new N’ to the oligotrophic subtropical and tropical oceans. High pCO2 enhanced N fixation, C : N ratios, filament length, and biomass of Trichodesmium in comparison with both ambient and low pCO2 cultures. Photosynthesis and respiration did not change significantly between the treatments. We suggest that enhanced N fixation and growth in the high pCO2 cultures occurs due to reallocation of energy and resources from carbon concentrating mechanisms (CCM) required under low and ambient pCO2. Thus, in oceanic regions, where light and nutrients such as P and Fe are not limiting, we expect the projected concentrations of CO2 to increase N fixation and growth of Trichodesmium. Other diazotrophs may be similarly affected, thereby enhancing inputs of new N and increasing primary productivity in the oceans.

Marchant, H.K., Calosi, P. and Spicer, J.I. 2010. Short-term exposure to hypercapnia does not compromise feeding, acid-base balance or respiration of Patella vulgata but surprisingly is accompanied by radula damage. Journal of the Marine Biological Association of the United Kingdom 90:1379-1384.

The effect of short-term (5 days) exposure to CO2-acidified seawater (year 2100 predicted values, ocean pH = 7.6) on key aspects of the function of the intertidal common limpet Patella vulgata (Gastropoda: Patellidae) was investigated. Changes in extracellular acid–base balance were almost completely compensated by an increase in bicarbonate ions. A concomitant increase in haemolymph Ca2+ and visible shell dissolution implicated passive shell dissolution as the bicarbonate source. Analysis of the radula using SEM revealed that individuals from the hypercapnic treatment showed an increase in the number of damaged teeth and the extent to which such teeth were damaged compared with controls. As radula teeth are composed mainly of chitin, acid dissolution seems unlikely, and so the proximate cause of damage is unknown. There was no hypercapnia-related change in metabolism (O2 uptake) or feeding rate, also discounting the possibility that teeth damage was a result of a CO2-related increase in grazing. We conclude that although the limpet appears to have the physiological capacity to maintain its extracellular acid–base balance, metabolism and feeding rate over a 5 days exposure to acidified seawater, radular damage somehow incurred during this time could still compromise feeding in the longer term, in turn decreasing the top-down ecosystem control that P. vulgata exerts over rocky shore environments.

Marubini, F. and Atkinson, M.J. 1999. Effects of lowered pH and elevated nitrate on coral calcification. Marine Ecology Progress Series 188 :117–121.

Both CO2 chemistry and nutrient concentrations of seawater affect coral calcification. The relative effects of these factors on growth of corals were studied using coral tips or ‘nubbins’ of the hermatypic coral Porites compressa. Coral nubbins were grown over 5 wk in different combinations of pCO2 (760 and 3980 µatm), HCO3- (1670 and 1520 µM), CO32- (110 and 20 µM), and NO3- (0.42 to 5.66 µM). The pCO2 was increased and CO32- decreased by adding HCl to normal seawater; NO3- was increased by adding KNO3 to ambient seawater. Corals growing in seawater at a reduced pH of 7.2 calcified at half the rate of control corals at pH 8.0, indicating that coral growth is strongly dependent on the concentration of CO32- ions in seawater. Reduction of calcification from lowered pH and CO32- was greater than reduction from nitrate additions. Corals in low pH treatments recovered their initial calcification rates within 2 d of re-introduction to ambient seawater, indicating the effects of CO2 chemistry are immediate and reversible. Changes in calcification from increases in atmospheric CO2, and hence decreases in CO32-, may be larger than local effects from elevated nutrients.

Marubini, F., Ferrier-Pagès, C., Furla, P., and Allemand, D. 2008. Coral calcification responds to seawater acidification: a working hypothesis towards a physiological mechanism. Coral Reefs 27 : 491-499.

The decrease in the saturation state of seawater, O, following seawater acidification, is believed to be the main factor leading to a decrease in the calcification of marine organisms. To provide a physiological explanation for this phenomenon, the effect of seawater acidification was studied on the calcification and photosynthesis of the scleractinian tropical coral Stylophora pistillata. Coral nubbins were incubated for 8 days at three different pH (7.6, 8.0, and 8.2). To differentiate between the effects of the various components of the carbonate chemistry (pH, CO32-, HCO3-, CO2, O), tanks were also maintained under similar pH, but with 2-mM HCO3- added to the seawater. The addition of 2-mM bicarbonate significantly increased the photosynthesis in S. pistillata, suggesting carbon-limited conditions. Conversely, photosynthesis was insensitive to changes in pH and pCO2. Seawater acidification decreased coral calcification by ca. 0.1-mg CaCO3 g-1 d-1 for a decrease of 0.1 pH units. This correlation suggested that seawater acidification affected coral calcification by decreasing the availability of the CO32- substrate for calcification. However, the decrease in coral calcification could also be attributed either to a decrease in extra- or intracellular pH or to a change in the buffering capacity of the medium, impairing supply of CO32- from HCO3-.

Melzner, F., Göbel, S., Langenbuch, M., Gutowska, M.A., Pörtner, H.-O. and Lucassen, M. 2009. Swimming performance in Atlantic Cod (Gadus morhua) following long-term (4–12 months) acclimation to elevated seawater PCO2. AquaticToxicology 92 : 30-37.

Anthropogenic CO2 emissions lead to chronically elevated seawater CO2 partial pressures (hypercapnia). The induced ocean acidification will very likely be a relevant factor shaping future marine environments. CO2 exposure concomitantly challenges the animal’s capacity of acid-base and ionic regulation as well as the ability to maintain energy metabolism and calcification. Under conditions of acute hypercapnia, numerous studies have revealed a broad range of tolerance levels displayed by various marine taxa. Thus, it is well known that, in contrast to many marine invertebrates, most teleost fish are able to fully compensate acid-base disturbances in short-term experiments (hours to several days). In order to determine whether marine fish are able to preserve aerobic scope following long-term incubation to elevated CO2, we exposed two groups of Atlantic Cod for 4 and 12 months to 0.3 and 0.6 kPa PCO2, respectively. Measurements of standard and active metabolic rates, critical swimming speeds and aerobic scope of long-term incubated cod showed no deviations from control values, indicating that locomotory performance is not compromised by the different levels of chronic hypercapnia. While the maintenance of high activity levels is supported by a 2-fold increased Na+/K+-ATPase protein expression and 2-fold elevated Na+/K+-ATPase activity in the 12 month incubated fish (0.6 kPa PCO2), no such elevation in Na+/K+-ATPase activity could be observed in the group treated with 0.3 kPa PCO2. Owing to the relevance of Na+/K+-ATPase as a general indicator for ion regulatory capacity, these results point at an adjustment of enzymatic activity to cope with the CO2 induced acid-base load at 0.6 kPa PCO2 while under milder hypercapnic conditions the ‘standard’ Na+/K+-ATPase capacity might still be sufficient to maintain acid-base status.

Michaelidis, B., Ouzounis, C., Paleras, A. and Portner, H.O. 2005. Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology Progress Series 293 : 109–118.

In the context of future scenarios of progressive accumulation of anthropogenic CO2 in marine surface waters, the present study addresses the effects of long-term hypercapnia on a Mediterranean bivalve, Mytilus galloprovincialis. Sea-water pH was lowered to a value of 7.3 by equilibration with elevated CO2 levels. This is close to the maximum pH drop expected in marine surface waters during atmospheric CO2 accumulation. Intra- and extracellular acid–base parameters as well as changes in metabolic rate and growth were studied under both normocapnia and hypercapnia. Long-term hypercapnia caused a permanent reduction in haemolymph pH. To limit the degree of acidosis, mussels increased haemolymph bicarbonate levels, which are derived mainly from the dissolution of shell CaCO3. Intracellular pH in various tissues was at least partly compensated; no deviation from control values occurred during long-term measurements in whole soft-body tissues. The rate of oxygen consumption fell significantly, indicating a lower metabolic rate. In line with previous reports, a close correlation became evident between the reduction in extracellular pH and the reduction in metabolic rate of mussels during hypercapnia. Analysis of frequency histograms of growth rate revealed that hypercapnia caused a slowing of growth, possibly related to the reduction in metabolic rate and the dissolution of shell CaCO3 as a result of extracellular acidosis. In addition, increased nitrogen excretion by hypercapnic mussels indicates the net degradation of protein, thereby contributing to growth reduction. The results obtained in the present study strongly indicate that a reduction in sea-water pH to 7.3 may be fatal for the mussels. They also confirm previous observations that a reduction in sea-water pH below 7.5 is harmful for shelled molluscs.

Morita, M., Suwa, R., Iguchi, A., Nakamura, M., Shimada, K., Sakai, K. and Suzuki, A. 2010. Ocean acidification reduces sperm flagellar motility in broadcast spawning reef invertebrates. Zygote 18 : 103-107.

Ocean acidification is now recognized as a threat to marine ecosystems; however, the effect of ocean acidification on fertilization in marine organisms is still largely unknown. In this study, we focused on sperm flagellar motility in broadcast spawning reef invertebrates (a coral and a sea cucumber). Below pH 7.7, the pH predicted to occur within the next 100 years, sperm flagellar motility was seriously impaired in these organisms. Considering that sperm flagellar motility is indispensable for transporting the paternal haploid genome for fertilization, fertilization taking place in seawater may decline in the not too distant future. Urgent surveys are necessary for a better understanding of the physiological consequences of ocean acidification on sperm flagellar motility in a wide range of marine invertebrates.

Moulin, L., Catarino, A.I., Claessens, T. and Dubois, P. 2011. Effects of seawater acidification on early development of the intertidal sea urchin Paracentroutus lividus (Lamarck 1816). Marine Pollution Bulletin 62 : 48-54.

The effect of pH ranging from 8.0 to 6.8 (total scale – pHT) on fertilization, cleavage and larval development until pluteus stage was assessed in an intertidal temperate sea urchin. Gametes were obtained from adults collected in two contrasting tide pools, one showing a significant nocturnal pH decrease (lowest pHT = 7.4) and another where pH was more stable (lowest pHT = 7.8). The highest pHT at which significant effects on fertilization and cleavage were recorded was 7.6. On the contrary, larval development was only affected below pHT 7.4, a value equal or lower than that reported for several subtidal species. This suggests that sea urchins inhabiting stressful intertidal environments produce offspring that may better resist future ocean acidification. Moreover, at pHT 7.4, the fertilization rate of gametes whose progenitors came from the tide pool with higher pH decrease was significantly higher, indicating a possible acclimatization or adaptation of gametes to pH stress.

Munday, P.L., Donelson, J.M., Dixson, D.L. and Endo, G.G.K. 2009. Effects of ocean acidification on the early life history of a tropical marine fish. Proceedings of the Royal Society B 276 : 3275-3283.

Little is known about how fishes and other non-calcifying marine organisms will respond to the increased levels of dissolved CO2 and reduced sea water pH that are predicted to occur over the coming century. We reared eggs and larvae of the orange clownfish, Amphiprion percula, in sea water simulating a range of ocean acidification scenarios for the next 50–100 years (current day, 550, 750 and 1030 ppm atmospheric CO2). CO2 acidification had no detectable effect on embryonic duration, egg survival and size at hatching. In contrast, CO2 acidification tended to increase the growth rate of larvae. By the time of settlement (11 days post-hatching), larvae from some parental pairs were 15 to 18 per cent longer and 47 to 52 per cent heavier in acidified water compared with controls. Larvae from other parents were unaffected by CO2 acidification. Elevated CO2 and reduced pH had no effect on the maximum swimming speed of settlement-stage larvae. There was, however, a weak positive relationship between length and swimming speed. Large size is usually considered to be advantageous for larvae and newly settled juveniles. Consequently, these results suggest that levels of ocean acidification likely to be experienced in the near future might not, in isolation, significantly disadvantage the growth and performance of larvae from benthic-spawning marine fishes.

Ohde, S. and Hossain, M.M.M. 2004. Effect of CaCO3 (aragonite) saturation state of seawater on calcification of Porites coral. Geochemical Journal 38 : 613–621.

Using living corals collected from Okinawan coral reefs, laboratory experiments were performed to investigate the relationship between coral calcification and aragonite saturation state (Omega) of seawater at 25 degreesC. Calcification rate of a massive coral Porites lutea cultured in a beaker showed a linear increase with increasing Omega(aragonit) values (1.08-7.77) of seawater. The increasing trend of calcification rate (c) for Omega is expressed as an equation, c = aOmega + b (a, b: constants). When Omega was larger than similar to4, the coral samples calcified during nighttime, indicating an evidence of dark calcification. This study strongly suggests that calcification of Porites lutea depends on Omega of ambient seawater. A decrease in saturation state of seawater due to increased pCO(2) may decrease reef-building capacity of corals through reducing calcification rate of corals.

Palacios, S.L. and Zimmerman, R.C. 2007. Response of eelgrass Zostera marina to CO2 enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Marine Ecology Progress Series 344 : 1-13.

Projected increases in dissolved aqueous concentrations of carbon dioxide [CO2(aq)] may have significant impacts on photosynthesis of CO2-limited organisms such as seagrasses. Short-term CO2(aq) enrichment increases photosynthetic rates and reduces light requirements for growth and survival of individual eelgrass Zostera marina L. shoots growing in the laboratory under artificial light regimes for at least 45 d. This study examined the effects of long-term CO2(aq) enrichment on the performance of eelgrass growing under natural light-replete (33% surface irradiance) and light-limited (5% surface irradiance) conditions for a period of 1 yr. Eelgrass shoots were grown at 4 CO2(aq) concentrations in outdoor flow-through seawater aquaria bubbled with industrial flue gas containing approximately 11% CO2. Enrichment with CO2(aq) did not alter biomass-specific growth rates, leaf size, or leaf sugar content of above-ground shoots in either light treatment. CO2(aq) enrichment, however, led to significantly higher reproductive output, below-ground biomass and vegetative proliferation of new shoots in light-replete treatments. This suggests that increasing the CO2 content of the atmosphere and ocean surface will increase the area-specific productivity of seagrass meadows. CO2(aq) enrichment did not affect the performance of shoots grown under light limitation, suggesting that the transition from carbon- to light-limited growth followed Liebig’s Law. This study also demonstrated that direct injection of industrial flue gas could significantly increase eelgrass productivity; this might prove useful for restoration efforts in degraded environments. The broader effects of CO2(aq) enrichment on the function of natural seagrass meadows, however, require further study before deliberate CO2 injection could be considered as an engineering solution to the problem of seagrass habitat degradation.

Parra, G and Yúfera, M. 2002. Tolerance response to water pH in larvae of two marine fish species, gilthead seabream, Sparus aurata (L.) and Senegal sole, Solea senegalensis (Kaup), during development. Aquaculture Research 33 : 747-752.

Gilthead seabream, Sparus aurata (L.) and Senegal sole, Solea senegalensis (Kaup) are two fish of primary importance in Mediterranean aquaculture. In the present study, the larvae of these species were exposed to different rearing-water pH during 24 h to examine their tolerance. The 24-h pHL50 values were calculated with low and high pH values at 7, 20 and 32 days after hatching (DAH) in S. senegalensis larvae, and 12, 20 and 52 DAH in S. aurata larvae. Low 24-h pHL50 values ranged between 4.88 and 5.76, whereas high 24-h pHL50 values ranged between 8.94 and 9.57 in S. senegalensis larvae. S. aurata larvae showed values of low 24-h pHL50 that ranged between 4.82 and 5.55, whereas values of high 24-h pHL50 ranged between 8.66 and 9.26. Both species showed similar tolerance response at all the tested ages. The high 24-h pHL50 values found were close to pH values that eventually can be reached in the rearing tanks. The pH should be carefully controlled in rearing water during the first development stages of both species.

Ries, J.B., Cohen, A.L. and McCorkle, D.C. 2009. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37 : 1131-1134.

Anthropogenic elevation of atmospheric carbon dioxide (pCO2) is making the oceans more acidic, thereby reducing their degree of saturation with respect to calcium carbonate (CaCO3). There is mounting concern over the impact that future CO2-induced reductions in the CaCO3 saturation state of seawater will have on marine organisms that construct their shells and skeletons from this mineral. Here, we present the results of 60 d laboratory experiments in which we investigated the effects of CO2-induced ocean acidification on calcification in 18 benthic marine organisms. Species were selected to span a broad taxonomic range (crustacea, cnidaria, echinoidea, rhodophyta, chlorophyta, gastropoda, bivalvia, annelida) and included organisms producing aragonite, low-Mg calcite, and high-Mg calcite forms of CaCO3. We show that 10 of the 18 species studied exhibited reduced rates of net calcification and, in some cases, net dissolution under elevated pCO2. However, in seven species, net calcification increased under the intermediate and/or highest levels of pCO2, and one species showed no response at all. These varied responses may reflect differences amongst organisms in their ability to regulate pH at the site of calcification, in the extent to which their outer shell layer is protected by an organic covering, in the solubility of their shell or skeletal mineral, and in the extent to which they utilize photosynthesis. Whatever the specific mechanism(s) involved, our results suggest that the impact of elevated atmospheric pCO2 on marine calcification is more varied than previously thought.

Ries, J.B., Cohen, A.L. and McCorkle, D.C. 2010. A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29 : 661-674.

Anthropogenic elevation of atmospheric pCO2 is predicted to cause the pH of surface seawater to decline by 0.3–0.4 units by 2100 AD, causing a 50% reduction in seawater [CO3 2-] and undersaturation with respect to aragonite in high-latitude surface waters. We investigated the impact of CO2-induced ocean acidification on the temperate scleractinian coral Oculina arbuscula by rearing colonies for 60 days in experimental seawaters bubbled with air-CO2 gas mixtures of 409, 606, 903, and 2,856 ppm pCO2, yielding average aragonite saturation states (OA) of 2.6, 2.3, 1.6, and 0.8. Measurement of calcification (via buoyant weighing) and linear extension (relative to a 137Ba/138Ba spike) revealed that skeletal accretion was only minimally impaired by reductions in OA from 2.6 to 1.6, although major reductions were observed at 0.8 (undersaturation). Notably, the corals continued accreting new skeletal material even in undersaturated conditions, although at reduced rates. Correlation between rates of linear extension and calcification suggests that reduced calcification under OA = 0.8 resulted from reduced aragonite accretion, rather than from localized dissolution. Accretion of pure aragonite under each OA discounts the possibility that these corals will begin producing calcite, a less soluble form of CaCO3, as the oceans acidify. The corals’ nonlinear response to reduced OA and their ability to accrete new skeletal material in undersaturated conditions suggest that they strongly control the biomineralization process. However, our data suggest that a threshold seawater [CO3 2-] exists, below which calcification within this species (and possibly others) becomes impaired. Indeed, the strong negative response of O. arbuscula to OA = 0.8 indicates that their response to future pCO2-induced ocean acidification could be both abrupt and severe once the critical OA is reached.

Rodolfo-Metalpa, R., Lombardi, C., Cocito, S., Hall-Spencer, J.M. and Gambi, M.C. 2010. Effects of ocean acidification and high temperatures on the bryozoan Myriapora truncate at natural CO2 vents. Marine Ecology 31 : 447-456.

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.

Rodolfo-Metalpa, R., Martin, S., Ferrier-Pagès, C. and Gattuso, J.-P. 2010. Response of the temperate coral Cladocora caespitosa to mid- and long-term exposure to pCO2 and temperature levels projected for the year 2100 AD. Biogeosciences 7 : 289-300.

Atmospheric CO2 partial pressure (pCO2) is expected to increase to 700 μatm or more by the end of the present century. Anthropogenic CO2 is absorbed by the oceans, leading to decreases in pH and the CaCO3 saturation state (Ω) of the seawater. Elevated pCO2 was shown to drastically decrease calcification rates in tropical zooxanthellate corals. Here we show, using the Mediterranean zooxanthellate coral Cladocora caespitosa, that an increase in pCO2, in the range predicted for 2100, does not reduce its calcification rate. Therefore, the conventional belief that calcification rates will be affected by ocean acidification may not be widespread in temperate corals. Seasonal change in temperature is the predominant factor controlling photosynthesis, respiration, calcification and symbiont density. An increase in pCO2, alone or in combination with elevated temperature, had no significant effect on photosynthesis, photosynthetic efficiency and calcification. The lack of sensitivity C. caespitosa to elevated pCO2 might be due to its slow growth rates, which seem to be more dependent on temperature than on the saturation state of calcium carbonate in the range projected for the end of the century.

Schneider, K. and Erez, J. 2006. The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnology and Oceanography 51 : 1284-1293.

The rise in atmospheric CO2 has caused significant decrease in sea surface pH and carbonate ion (CO3-2) concentration. This decrease has a negative effect on calcification in hermatypic corals and other calcifying organisms. We report the results of three laboratory experiments designed specifically to separate the effects of the different carbonate chemistry parameters (pH, CO3-2, CO2 [aq], total alkalinity [AT], and total inorganic carbon [CT]) on the calcification, photosynthesis, and respiration of the hermatypic coral Acropora eurystoma. The carbonate system was varied to change pH (7.9-8.5), without changing CT; CT was changed keeping the pH constant, and CT was changed keeping the pCO2 constant. In all of these experiments, calcification (both light and dark) was positively correlated with CO3-2 concentration, suggesting that the corals are not sensitive to pH or CT but to the CO3-2 concentration. A decrease of ~30% in the CO3-2 concentration (which is equivalent to a decrease of about 0.2 pH units in seawater) caused a calcification decrease of about 50%. These results suggest that calcification in today’s ocean (pCO2 = 370 ppm) is lower by ~20% compared with preindustrial time (pCO2 = 280 ppm). An additional decrease of ~35% is expected if atmospheric CO2 concentration doubles (pCO2 = 560 ppm). In all of these experiments, photosynthesis and respiration did not show any significant response to changes in the carbonate chemistry of seawater. Based on this observation, we propose a mechanism by which the photosynthesis of symbionts is enhanced by coral calcification at high pH when CO2(aq) is low. Overall it seems that photosynthesis and calcification support each other mainly through internal pH regulation, which provides CO3-2 ions for calcification and CO2(aq) for photosynthesis.

Sciandra, A., Harlay, J., Lefèvre, D., Lemee, R., Rimmelin, P., Denis, M. and Gattuso, J.-P. 2003. Response of coccolithophorid Emiliania huxleyi to elevated partial pressure of CO2 under nitrogen limitation. Marine Ecology Progress Series 261 : 111-122.

Precipitation of calcium carbonate by phytoplankton in the photic oceanic layer is an important process regulating the carbon cycling and the exchange Of CO2 at the ocean-atmosphere interface. Previous experiments have demonstrated that, under nutrient-sufficient conditions, doubling the partial pressure Of CO2 (pCO(2)) in seawater-a likely scenario for the end of the century-can significantly decrease both the rate of calcification by coccolithophorids and the ratio of inorganic to organic carbon production. The present work investigates the effects of high pCO(2) on calcification by the coccolithophore Emiliania huxleyi (Strain TW1) grown under nitrogen-limiting conditions, a situation that can also prevail in the ocean. Nitrogen limitation was achieved in NO3-limited continuous cultures renewed at the rate of 0.5 d(-1) and exposed to a saturating light level. pCO(2) was increased from 400 to 700 ppm and controlled by bubbling CO2-rich or CO2-free air into the cultures. The pCO(2) shift has a rapid effect on cell physiology that occurs within 2 cell divisions subsequent to the perturbation. Net calcification rate (C) decreased by 25% and, in contrast to previous studies with N-replete cultures, gross community production (GCP) and dark community respiration (DCR) also decreased. These results suggest that increasing pCO(2) has no noticeable effect on the calcification/photosynthesis ratio (C/P) when cells of E. huxleyi are NO3-limited.

Shirayama, Y. and Thornton, H. 2005. Effect of increased atmospheric CO2 on shallow water marine benthos. Journal of Geophysical Research 110, C09S08, doi:10.1029/2004JC002618.

The decision to sequester CO2 in the deep ocean should ultimately be based not only upon what would happen to deep sea marine biota but also upon what would happen to surface organisms if nothing were done to limit atmospheric CO2. Thus such a decision should be based on a proper understanding of long-term chronic effects, from the global-scale perturbation in near-surface ocean CO2, in addition to acute effects, from large local increases in CO2 caused by purposeful sequestration. Here we focus on the long-term chronic effects of CO2 on shallow water benthic organisms that have calcium carbonate shells. With two duplicate 6 month manipulative experiments, we demonstrate that a 200 ppm increase in CO2 adversely affects the growth of both gastropods and sea urchins. Thus even moderate increases in atmospheric CO2 that could well be reached by the middle of this century will adversely affect shallow water marine benthic organisms. This provides another reason, beyond concerns for climate, to enhance efforts to limit increases in atmospheric CO2 to the lowest possible levels.

Surif, M.B. and Raven, J.A. 1989. Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta): ecological and taxonomic implication. Oecologia 78 : 97-105.

Characteristics of inorganic carbon assimilation by photosynthesis in seawater were investigated in six species of the Fucales (five Fucaceae, one Cystoseiraceae) and four species of the Laminariales (three Laminariaceae, one Alariaceae) from Arbroath, Scotland. All of the algae tested could photosynthesise faster at high external pH values than the uncatalysed conversion of HCO 3 – to CO2 can occur, i.e. can use external HCO 3 – . They all had detectable extracellular carbonic anhydrase activity, suggesting that HCO 3 – use could involve catalysis of external CO2 production, a view supported to some extent by experiments with an inhibitor of carbonic anhydrase. All of the algae tested had CO2 compensation concentrations at pH 8 which were lower than would be expected from diffusive entry of CO2 supplying RUBISCO as the initial carboxylase, consistent with the operation of energized entry of HCO 3 – and / or CO2 acting as a CO2 concentrating mechanism. Quantitative differences among the algae examined were noted with respect to characteristics of inorganic C assimilation. The most obvious distinction was between the eulittoral Fucaceae, which are emersed for part of, or most of, the tidal cycle, and the other three families (Cystoseiraceae, Laminariaceae, Alariaceae) whose representatives are essentially continually submersed. The Fucaceae examined are able to photosynthesise at high pH values, and have lower CO2 compensation concentrations, and lower K1/2 values for inorganic C use in photosynthesis, at pH 8, than the other algae tested. Furthermore, the Fucaceae are essentially saturated with inorganic C for photosynthesis at the normal seawater concentration at pH 8 and 10°C. These characteristics are consistent with the dominant role of a CO2 concentrating mechanism in CO2 acquisition by these plants. Other species tested have characteristcs which suggest a less effective HCO 3 – use and CO2 concentrating mechanism, with the Laminariaceae being the least effective; unlike the Fucaceae, photosynthesis by these algae is not saturated with inorganic C in normal seawater. Taxonomic and ecological implications of these results are considered in relation to related data in the literature.

Swanson, A.K and Fox, C.H. 2007. Altered kelp (Laminariales) phlorotannins and growth under elevated carbon dioxide and ultraviolet-B treatments can influence associated intertidal food webs. Global Change Biology 13 : 1696-1709.

Due to the importance of brown algae, such as kelp (Laminariales, Phaeophyta), within most cool nearshore environments, any direct responses of kelp to multiple global changes could alter the integrity of future coastal marine systems. Fifty-five-day manipulation of carbon dioxide (CO2) and ultraviolet light (UVB) within outdoor sea-tanks, approximating past, present and two predicted future levels, examined the direct influences on Saccharina latissima (=Laminaria saccharina) and Nereocystis luetkeana development and biochemistry, as well as the indirect influences on a marine herbivore (Tegula funebralis; Gastropoda, Mollusca) and on naturally occurring intertidal detritivores. Kelp species displayed variable directional (negative and positive growth) and scale responses to CO2 and UVB manipulations, which was influenced by interactions. Kelp phlorotannin (phenolic) production in blade tissues was induced by elevated UVB levels, and especially enhanced (additively) by elevated CO2, further suggesting that some actively growing kelp species are carbon limited in typical nearshore environments. Negative indirect effects upon detritivore consumers fed CO2-manipulated kelp blade tissues were detected, however, no statistical relationships existed among UVB-treated tissues, and test herbivores did not distinguish between phlorotannin-altered CO2: UVB-treated kelp blade tissues. Results suggest that past and future conditions differentially benefit these kelp species, which implies a potential for shifts in species abundance and community composition. Higher CO2 conditions can indirectly impede marine decay processes delaying access to recycled trace nutrients, which may be disruptive to the seasonal regrowth of algae and/or higher trophic levels of nearshore ecosystems.

Takeda, T. and Itazawa, Y. 1983. Possibility of applying anesthesia by carbon dioxide in the transportation of live fish. Bulletin of the Japanese Society of Scientific Fisheries 29: 725-731. – Online reference not found.

Talmage, S.C. and Gobler, C.J. 2010. Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proceedings of the National Academy of Sciences, USA 107: 17246-17251.

The combustion of fossil fuels has enriched levels of CO2 in the world’s oceans and decreased ocean pH. Although the continuation of these processes may alter the growth, survival, and diversity of marine organisms that synthesize CaCO3 shells, the effects of ocean acidification since the dawn of the industrial revolution are not clear. Here we present experiments that examined the effects of the ocean’s past, present, and future (21st and 22nd centuries) CO2 concentrations on the growth, survival, and condition of larvae of two species of commercially and ecologically valuable bivalve shellfish (Mercenaria mercenaria and Argopecten irradians). Larvae grown under near preindustrial CO2 concentrations (250 ppm) displayed significantly faster growth and metamorphosis as well as higher survival and lipid accumulation rates compared with individuals reared under modern day CO2 levels. Bivalves grown under near preindustrial CO2 levels displayed thicker, more robust shells than individuals grown at present CO2 concentrations, whereas bivalves exposed to CO2 levels expected later this century had shells that were malformed and eroded. These results suggest that the ocean acidification that has occurred during the past two centuries may be inhibiting the development and survival of larval shellfish and contributing to global declines of some bivalve populations.

Thom, R.M. 1996. CO2-enrichment effects on eelgrass (Zostera marina L) and bull kelp ( Nereocystis luetkeana (Mert) P & R). Water Air and Soil Pollution 88 : 383-391.

I investigated the effect of CO2-enrichment on productivity of two aquatic plant species [Zostera marina L., Nereocystis luetkeana (Mert.) P. & R.] that form significant components of coastal ecosystems in the Pacific Northwest. Short-term (i.e., 2-hr) experiments showed that doubling CO2 resulted in up to a 2.5-fold increase in Zostera net apparent productivity (NAP). Nereocystis NAP was increased 2.2 – 2.8 fold. In experiments involving seven enrichment treatments, NAP increased with increasing CO2 between ambient (1.0×) and 2.5× CO2 in both Zostera and Nereocystis. Nereocystis and Zostera NAP was lowest at highest (i.e., 5×) CO2 concentrations. In growth experiments, mean growth rate of Zostera increased with increasing CO2 during one of the two trials. I conclude that increasing CO2 in the surface waters of the coastal ocean would predictably result in increased NAP of these two species. These results supplement limited published data showing that shallow estuarine and marine systems are vulnerable to increased carbon dioxide.

Tortell, P. D., Payne, C.D. Li, Y., Trimborn, S. Rost, B., Smith, W.O., Riesselman, C., Dunbar, R.B., Sedwick, P. and DiTullio, G.R. 2008. CO2 sensitivity of Southern Ocean phytoplankton. Geophysical Research Letters 35, L04605, doi:10.1029/2007GL032583.

The Southern Ocean exerts a strong impact on marine biogeochemical cycles and global air-sea CO2 fluxes. Over the coming century, large increases in surface ocean CO2 levels, combined with increased upper water column temperatures and stratification, are expected to diminish Southern Ocean CO2 uptake. These effects could be significantly modulated by concomitant CO2-dependent changes in the region’s biological carbon pump. Here we show that CO2 concentrations affect the physiology, growth and species composition of phytoplankton assemblages in the Ross Sea, Antarctica. Field results from in situ sampling and ship-board incubation experiments demonstrate that inorganic carbon uptake, steady-state productivity and diatom species composition are sensitive to CO2 concentrations ranging from 100 to 800 ppm. Elevated CO2 led to a measurable increase in phytoplankton productivity, promoting the growth of larger chain-forming diatoms. Our results suggest that CO2 concentrations can influence biological carbon cycling in the Southern Ocean, thereby creating potential climate feedbacks.

Waldbusser, G.G., Voigt, E.P., Bergschneider, H., Green, M.A., and Newell, R.I.E. 2011. Biocalcification in the Eastern Oyster (Crassostrea virginica) in relation to long-term trends in Chesapeake Bay pH. Estuaries and Coasts 34 : 221-231.

Anthropogenic carbon dioxide (CO2) emissions reduce pH of marine waters due to the absorption of atmospheric CO2 and formation of carbonic acid. Estuarine waters are more susceptible to acidification because they are subject to multiple acid sources and are less buffered than marine waters. Consequently, estuarine shell forming species may experience acidification sooner than marine species although the tolerance of estuarine calcifiers to pH changes is poorly understood. We analyzed 23 years of Chesapeake Bay water quality monitoring data and found that daytime average pH significantly decreased across polyhaline waters although pH has not significantly changed across mesohaline waters. In some tributaries that once supported large oyster populations, pH is increasing. Current average conditions within some tributaries however correspond to values that we found in laboratory studies to reduce oyster biocalcification rates or resulted in net shell dissolution. Calcification rates of juvenile eastern oysters, Crassostrea virginica, were measured in laboratory studies in a three-way factorial design with 3 pH levels, two salinities, and two temperatures. Biocalcification declined significantly with a reduction of ∼0.5 pH units and higher temperature and salinity mitigated the decrease in biocalcification.

Walther, K., Anger, K. and Pörtner, H.O. 2010. Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54° vs. 79° N). Marine Ecology Progress Series 417 : 159-170.

The combined effects of predicted ocean acidification and global warming on the larvae of the cold-eurythermal spider crab Hyas araneus L. were investigated in 2 populations: a southernmost around Helgoland (North Sea, 54°N) and a northernmost at Svalbard (North Atlantic, 79°N). Larvae were exposed at temperatures of 3, 9 and 15°C to present day normocapnia (380 ppm CO2) and to CO2 conditions predicted for the near or medium-term future (710 ppm by the year 2100, 3000 ppm by 2300 and beyond). Larval development time, growth and C/N ratio were studied in the larval stages Zoea I, II, and Megalopa. Permanent differences in instar duration between both populations were detected in all stages, likely as a result of evolutionary temperature adaptation. With the exception of Zoea II at 3°C and under all CO2 conditions, development in all instars from Svalbard was delayed compared to those from Helgoland. Most prominently, development was much longer and fewer specimens morphosed to the first crab instar in the Megalopa from Svalbard than from Helgoland. Enhanced CO2 levels (particularly 3000 ppm) extended the duration of larval development and reduced larval growth (measured as dry mass) and fitness (decreasing C/N ratio, a proxy of the lipid content). Such effects were strongest in the zoeal stages of Svalbard larvae, and during the Megalopa instar of Helgoland larvae. The high sensitivity of megalopae from the Svalbard population to warming and of those from Helgoland to enhanced CO2 levels suggests that this larval instar is a physiologically sensitive bottleneck within the life cycle of H. araneus.

Wood, H.L., Spicer, J.I., Lowe, D.M. and Widdicombe, S. 2010. Interaction of ocean acidification and temperature; the high cost of survival in the brittlestar Ophiura ophiura. Marine Biology 157 : 2001-2013.

This study has demonstrated an interaction between the effect of increased ocean acidity and temperature (40days 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 (+4.5C). 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.

Wu, Y., Gao, K. and Riebesell, U. 2010. CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7 : 2915-2923.

CO2/pH perturbation experiments were carried out under two different pCO2 levels (39.3 and 101.3 Pa) to evaluate effects of CO2-induced ocean acidification on the marine diatom Phaeodactylum tricornutum. After acclimation (>20 generations) to ambient and elevated CO2 conditions (with corresponding pH values of 8.15 and 7.80, respectively), growth and photosynthetic carbon fixation rates of high CO2 grown cells were enhanced by 5% and 12%, respectively, and dark respiration stimulated by 34% compared to cells grown at ambient CO2. The half saturation constant (Km) for carbon fixation (dissolved inorganic carbon, DIC) increased by 20% under the low pH and high CO2 condition, reflecting a decreased affinity for HCO3– or/and CO2 and down-regulated carbon concentrating mechanism (CCM). In the high CO2 grown cells, the electron transport rate from photosystem II (PSII) was photoinhibited to a greater extent at high levels of photosynthetically active radiation, while non-photochemical quenching was reduced compared to low CO2 grown cells. This was probably due to the down-regulation of CCM, which serves as a sink for excessive energy. The balance between these positive and negative effects on diatom productivity will be a key factor in determining the net effect of rising atmospheric CO2 on ocean primary production.

Zippay, M.L. and Hofmann, G.E. 2010. Effect of pH on gene expression and thermal tolerance of early life history stages of red abalone (Haliotis rufescens). Journal of Shellfish Research 29 : 429-439.

A growing body of research on calcifying marine invertebrates suggests that ocean acidification will have deleterious effects on development and various physiological processes in these organisms. In laboratory experiments designed to mimic seawater chemistry in future oceans, we examined the effect of pH reduction, driven by the carbon dioxide (CO2) acidification of seawater, on larvae of the red abalone, Haliotis rufescens. Following development under CO2-acidified conditions, we measured 2 indicators of physiological response to low pH in 4 stages of larval development: (1) tolerance of acute thermal challenges and (2) quantitative real-time polymerase chain reaction-determined expression of 2 genes involved in shell formation (engrailed and ap24). The results showed that low pH (pH 7.87 vs. pH 8.05 for control treatments) had a significant effect and decreased larval thermal tolerance for some developmental stages (pretorsion and late veliger), but not for others (posttorsion and premetamorphic veligers). In contrast to the thermal tolerance data, decreased pH did not affect the expression pattern of the 2 shell formation genes in any of the abalone larval stages. The results indicate larval stages were differentially sensitive to low pH conditions and this variability may play into the resilience of individual species to withstand environmental change in the longer term.

Zou, D. and Gao, K. 2009. Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48 : 510–517.

The red seaweed Gracilaria lemaneiformis (Bory) Weber-van Bosse (Gigartinales, Rhodophyta) from Nanao Island, Shantou, China, was cultured at 370 and 700 µl l−1 CO2 in aeration and at intermediate (160 µmol photons m−2 s−1) and low (30 µmol photons m−2 s−1) irradiance levels in order to examine the influences of the elevated atmospheric CO2 concentrations on growth, photosynthetic performance and some biochemical components in this commercially important species. Relative growth rate (RGR) was significantly higher in G. lemaneiformis thalli grown using CO2-enriched air with respect to nonenriched air when the algae were subjected to intermediate irradiance. However, RGR was similar between these two CO2 treatments when the algae were grown under the low-irradiance condition. Extra CO2 in the culture decreased phycobiliprotein (PB, including phycoerythrin, PE, and phycocyanin, PC) contents of G. lemaneiformis thalli at the higher growth irradiance. However, chlorophyll a (Chl a) and soluble protein contents were unchanged by the CO2 levels in culture. Both PB and Chl a contents were higher in G. lemaneiformis thalli grown at the lower irradiance than at the higher irradiance, regardless of the CO2 levels in culture. The parameters for photosynthetic responses to irradiance and inorganic carbon were mostly not altered with the increase of CO2 concentrations in culture. However, light-saturated photosynthetic rates (Pmax) and apparent carboxylating efficiencies (ACE), expressed per unit Chl a, were significantly higher in algae grown at the intermediate irradiance compared to the low irradiance. Photosynthetic rate was reduced by an increase in pH of seawater from 8.2 to 9.1, and it was also strongly inhibited by the external carbonic anhydrase inhibitor acetazolamide (AZ) in G. lemaneiformis thalli grown at each CO2 and irradiance condition. Moreover, pH compensation points were not affected by the growth conditions. These results suggested that G. lemaneiformis under both growth conditions had a similar capacity of the photosynthetic utilization of external pool in seawater. However, ACE decreased in G. lemaneiformis thalli grown at the low irradiance with respect to the higher irradiance implied that the transport of Ci towards Rubisco within the cell was weakened. Taken together, the data showed that an increase of CO2 was less effective on G. lemaneiformis than the irradiance levels. We concluded that CO2 affected photosynthesis and growth performance when light was not the limiting factor.

Note: I have done my utmost to visit every single page in CO2Science’s “database of deception”. If new items are added, please let me know by posting here and I will continue to update this list.

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5 Responses to “Nova on Acid”

  1. Michael Says:

    That’s an impressive rebuttal of co2 and Nova. It’s a shame there are so many idiots willing to take them at face value.

  2. geeaye Says:

    I really wish you had not listed all abstracts in this way… maybe on a separate page with a warning. Length is not an indicator of argument virility.

    • itsnotnova Says:

      Thanks for your thoughts and I agree that length alone is not an indicator of virility.

      The content on this page is about 0.5 MB, by contrast Nova’s original post is more than three times this amount so I assume it’s more the layout that inconveniences you rather than the bandwidth.

      It took me a long time to compile and I purposely wanted it out on display exactly like this. I gathered the extracts for every single piece CO2Science used and highlighted the negative and positive aspects in each.

      I feel this, along with the other arguments I present do give my argument “virility”, irrespective of length or girth.

  3. Bernard J. Says:

    Heh, I for one am quite chuffed to see those abstracts so listed, and I appreciate the amount of work involved in doing so.

    The list supports the point of the whole post, and I would beg to differ – the length of the list does indicate the high strength (“virility”?!) of the argument against Joanne Codling’s silliness.

    If it’s just a matter of not having the bandwidth to download the text, simply hit the ‘back’ button. Or perhaps “geeaye” wishes that the abstracts had not been listed because they are so devastating to Codling’s case…?

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