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June 22, 2012

Contaminants and Pollution: Ocean Acidification

  • Lacoue-Labarthe, T., Martin, S., Oberhänsli, F., Teyssié, J.-L., Jeffree, R., Gattuso, J.-P., and Bustamante, P.  Temperature and pCO2 effect on the bioaccumulation of radionuclides and trace elements in the eggs of the common cuttlefish, Sepia officinalis.  Journal of Experimental Marine Biology and Ecology 413: 45-49, 2012.  
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    The increasing release of CO2 by human activities leads to ocean acidification and global warming. Both those consequences (i.e., increase in seawater pCO2 and temperature) may drastically affect the physiology of marine organisms. The effects of low pH and elevated temperature on the bioaccumulation of radionuclides (241Am, 134Cs) and trace elements (60Co, 54Mn or 75Se) were studied during the embryonic development of the common cuttlefish Sepia officinalis. The lowered accumulation of essential 60Co and 54Mn with decreasing pH was larger at 16 ºC than at 19 ºC. Se was not detected in the embryo whereas it penetrated through the eggshell, suggesting that an alternative pathway ensures the supply of this essential metal for the embryo. 241Am was totally retained by the eggshell irrespective of pH and temperature. Finally, the amount of Cs found in the peri-vitelline fluid increased with decreasing pH likely because of an enhanced swelling of the cuttlefish egg under elevated CO2.

  • Moazami-Goudarzi, M. and Colman, B.  Changes in carbon uptake mechanisms in two green marine algae by reduced seawater pH.  Journal of Experimental Marine Biology and Ecology 413: 94-99, 2012.
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    Acidification of the oceans, as a consequence of anthropogenic CO2 emissions has reduced the pH at the surface of oceans by 0.1 unit compared to pre-industrial values. The reduction of seawater pH changes the relative proportion of the inorganic carbon (Ci) species which could potentially affect the modes of Ci assimilation by marine microalgae. In this study the effects of changes in external pH on the modes of Ci uptake over the pH range 5.0 to 7.5 were determined mass spectrometrically in Stichococcus minor Naegeli and S. cylindricus Butcher et Umbauk. Both species were found to tolerate a broad range of pH from pH 5.0 to 9.5 but the optimum for growth of both species was 8.2. Both species were also found to grow over a range of salinities and are best described as brackish water species rather than marine species, since they grow over wide ranges of salinity and pH. Neither species expresses external carbonic anhydrase (CA) activity. In both species, cells grown at pH 5.0, where the bulk of dissolved inorganic carbon (DIC) is in the form of CO2, active HCO3- and CO2 uptake were absent and cells appear to take up CO2 by diffusion. However, active HCO3- uptake was present in cells of both species grown at pH 6.0, 7.0 and 7.5 but active CO2 uptake was not detectable. Cells of both species, when grown at pH 8.2, display both active CO2 uptake and active HCO3- uptake.

  • McElroy, D.J., Nguyen, H.D., and Byrne, M.  Respiratory response of the intertidal seastar Parvulastra exigua to contemporary and near-future pulses of warming and hypercapnia.  Journal of Experimental Marine Biology and Ecology 416-417: 1-7, 2012.   
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    As typical of intertidal invertebrates the asterinid seastar Parvulastra exigua experiences marked variation in environmental temperature and pH/pCO2 due to tidal exchange and diurnal patterns of photosynthesis and respiration. We characterized the temperature and pH/pCO2 conditions in the mid-intertidal, rocky-shore habitat of this species and used these data along with projections for the ocean over coming decades to define treatments in oxygen consumption experiments. The metabolic response of P. exigua to warming and acidification was dominated by temperature as the most significant factor influencing oxygen consumption. When P. exigua were exposed to intermediate pH/pCO2 (7.8/≈750 ppm) levels combined with pulses of warming occasionally experienced in nature (6 ºC above sea surface temperature), the effect of temperature on metabolism was diminished. Our results show that the metabolic response of P. exigua is resilient to current levels of stress, but may be vulnerable in the future to the interactive effects of ocean warming and acidification at levels expected under near-future climate change.

  • Fitzer, S.C., Caldwell, G.S., Close, A.J., Clare, A.S., Upstill-Goddard, R.C., and Bentley, M.G.  Ocean acidification induces multi-generational decline in copepod naupliar production with possible conflict for reproductive resource allocation.  Journal of Experimental Marine Biology and Ecology 418-419: 30-36, 2012.
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    Climate change, including ocean acidification (OA), presents fundamental challenges to marine biodiversity and sustained ecosystem health. We determined reproductive response (measured as naupliar production), cuticle composition and stage specific growth of the copepod Tisbe battagliai over three generations at four pH conditions (pH 7.67, 7.82, 7.95, and 8.06). Naupliar production increased significantly at pH 7.95 compared with pH 8.06 followed by a decline at pH 7.82. Naupliar production at pH 7.67 was higher than pH 7.82. We attribute the increase at pH 7.95 to an initial stress response which was succeeded by a hormesis-like response at pH 7.67. A multi-generational modelling approach predicted a gradual decline in naupliar production over the next 100 years (equivalent to approximately 2430 generations). There was a significant growth reduction (mean length integrated across developmental stage) relative to controls. There was a significant increase in the proportion of carbon relative to oxygen within the cuticle as seawater pH decreased. Changes in growth, cuticle composition and naupliar production strongly suggest that copepods subjected to OA-induced stress preferentially reallocate resources towards maintaining reproductive output at the expense of somatic growth and cuticle composition. These responses may drive shifts in life history strategies that favour smaller brood sizes, females and perhaps later maturing females, with the potential to profoundly destabilise marine trophodynamics.

  • Pansch, C., Nasrolahi, A., Appelhans, Y.S., and Wahl, M.  Impacts of ocean warming and acidification on the larval development of the barnacle Amphibalanus improvisus.  Journal of Experimental Marine Biology and Ecology 420-421: 48-55, 2012.
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    The world's oceans are warming and becoming more acidic. Both stressors, singly or in combination, impact marine species, and ensuing effects might be particularly serious for early life stages. To date most studies have focused on ocean acidification (OA) effects in fully marine environments, while little attention has been devoted to more variable coastal ecosystems, such as the Western Baltic Sea. Since natural spatial and temporal variability of environmental conditions such as salinity, temperature or pCO2 impose more complex stresses upon organisms inhabiting these habitats, species can be expected to be more tolerant to OA (or warming) than fully marine taxa. We present data on the variability of salinity, temperature and pH within the Kiel Fjord and on the responses of the barnacle Amphibalanus improvisus from this habitat to simulated warming and OA during its early development. Nauplii and cyprids were exposed to different temperature (12, 20 and 27 °C) and pCO2 (nominally 400, 1250 and 3250 μatm) treatments for 8 and 4  weeks, respectively. Survival, larval duration and settlement success were monitored. Warming affected larval responses more strongly than OA. Increased temperatures favored survival and development of nauplii but decreased survival of cyprids. OA had no effect upon survival of nauplii but enhanced their development at low (12 °C) and high (27 °C) temperatures. In contrast, at the intermediate temperature (20 °C), nauplii were not affected even by 3250 μatm pCO2. None of the treatments significantly affected settlement success of cyprids. These experiments show a remarkable tolerance of A. improvisus larvae to 1250 μatm pCO2, the level of OA predicted for the end of the century.

  • Amaral, V., Cabral, H.N., and Bishop, M.J.  Moderate acidification affects growth but not survival of 6-month-old oysters.  Aquatic Ecology 46(1): 119-127, 2012.
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    Oyster populations periodically exposed to runoff from acid sulfate soils (ASS) are of depressed abundance and have fewer smaller individuals than unaffected populations, despite having similar recruitment levels to unaffected sites during dry periods. We examined how the timing and duration of exposure to ASS runoff influences the growth and survival of successfully settled oysters. We predicted that among 6-month-old oysters, growth and survival would be (1) lower among individuals continuously exposed to ASS-acidified waters than those that are episodically exposed, and (2) most negatively affected during rainfall events, which enhance transport of ASS runoff to estuaries. Six-month-old Sydney rock oysters, Saccostrea glomerata, were deployed at ASS-affected and unaffected sites within each of two south-east Australian estuaries. After 10 weeks, oysters were transplanted within and across sites in an estuary and maintained in situ for another 10 weeks. Oysters that remained for 20 weeks at ASS-affected sites grew at just over half the rate of oysters at reference sites. Oysters transplanted from acidified to reference sites grew more than oysters transplanted from reference to acidified sites or oysters that remained at reference sites. Unexpectedly, overall oyster mortality was low. Greater rainfall, and hence a lower pH, is likely to have accounted for the greater impact of acidification on growth during the second 10 weeks. Where oysters recruit to a 6-month age cohort, they may be able to tolerate subsequent, moderate, acidification events. Reduced growth during acidification periods may be offset by positive growth during intervening dry periods.

  • Zeebe, R.E.  History of seawater carbonate chemistry, atmospheric CO2, and ocean acidification.  Annual Review of Earth and Planetary Sciences 40: 141-165, 2012.
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    Humans are continuing to add vast amounts of carbon dioxide (CO2) to the atmosphere through fossil fuel burning and other activities. A large fraction of the CO2 is taken up by the oceans in a process that lowers ocean pH and carbonate mineral saturation state. This effect has potentially serious consequences for marine life, which are, however, difficult to predict. One approach to address the issue is to study the geologic record, which may provide clues about what the future holds for ocean chemistry and marine organisms. This article reviews basic controls on ocean carbonate chemistry on different timescales and examines past ocean chemistry changes and ocean acidification events during various geologic eras. The results allow evaluation of the current anthropogenic perturbation in the context of Earth's history. It appears that the ocean acidification event that humans are expected to cause is unprecedented in the geologic past, for which sufficiently well-preserved records are available.

  • Catarino, A., De Ridder, C., Gonzalez, M., Gallardo, P., and Dubois, P.  Sea urchin Arbacia dufresnei (Blainville 1825) larvae response to ocean acidification.  Polar Biology 35(3): 455-461, 2012.
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    Increased atmospheric CO2 emissions are inducing changes in seawater carbon chemistry, lowering its pH, decreasing carbonate ion availability and reducing calcium carbonate saturation state. This phenomenon, known as ocean acidification, is happening at a faster rate in cold regions, i.e., polar and sub-polar waters. The larval development of Arbacia dufresnei from a sub-Antarctic population was studied at high (8.0), medium (7.7) and low (7.4) pH waters. The results show that the offspring from sub-Antarctic populations of A . dufresnei are susceptible to a development delay at low pH, with no significant increase in abnormal forms. Larvae were isometric between pH treatments. Even at calcium carbonate (CaCO3) saturation states (of both calcite and aragonite, used as proxies of the magnesium calcite) <1, skeleton deposition occurred. Polar and sub-polar sea urchin larvae can show a certain degree of resilience to acidification, also emphasizing A. dufresnei potential to poleward migrate and further colonize southern regions.

  • Franke, A. and Clemmesen, C.  Effect of ocean acidification on early life stages of Atlantic herring (Clupea harengus L.).  Biogeosciences 8(12): 3697-3707, 2011.
    Open Access >>
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    Due to atmospheric accumulation of anthropogenic CO2 the partial pressure of carbon dioxide (pCO2) in surface seawater increases and the pH decreases. This process known as ocean acidification might have severe effects on marine organisms and ecosystems. The present study addresses the effect of ocean acidification on early developmental stages, the most sensitive stages in life history, of the Atlantic herring (Clupea harengus L.). Eggs of the Atlantic herring were fertilized and incubated in artificially acidified seawater (pCO2 1260, 1859, 2626, 2903, 4635 μatm) and a control treatment (pCO2 480 μatm) until the main hatch of herring larvae occurred. The development of the embryos was monitored daily and newly hatched larvae were sampled to analyze their morphometrics, and their condition by measuring the RNA/DNA ratios. Elevated pCO2 neither affected the embryogenesis nor the hatch rate. Furthermore the results showed no linear relationship between pCO2 and total length, dry weight, yolk sac area and otolith area of the newly hatched larvae. For pCO2 and RNA/DNA ratio, however, a significant negative linear relationship was found. The RNA concentration at hatching was reduced at higher  pCO2 levels, which could lead to a decreased protein biosynthesis. The results indicate that an increased pCO2 can affect the metabolism of herring embryos negatively. Accordingly, further somatic growth of the larvae could be reduced. This can have consequences for the larval fish, since smaller and slow growing individuals have a lower survival potential due to lower feeding success and increased predation mortality. The regulatory mechanisms necessary to compensate for effects of hypercapnia could therefore lead to lower larval survival. Since the recruitment of fish seems to be determined during the early life stages, future research on the factors influencing these stages are of great importance in fisheries science.

  • Holcomb, M., Cohen, A.L., and McCorkle, D.C.  An investigation of the calcification response of the scleractinian coral Astrangia poculata to elevated pCO2 and the effects of nutrients, zooxanthellae and gender.  Biogeosciences 9(1): 29-39, 2012.
    Open Access >>
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    The effects of nutrients and pCO2 on zooxanthellate and azooxanthellate colonies of the temperate scleractinian coral Astrangia poculata (Ellis and Solander, 1786) were investigated at two different temperatures (16 °C and 24 °C). Corals exposed to elevated pCO2 tended to have lower relative calcification rates, as estimated from changes in buoyant weights. Experimental nutrient enrichments had no significant effect nor did there appear to be any interaction between pCO2 and nutrients. Elevated pCO2 appeared to have a similar effect on coral calcification whether zooxanthellae were present or absent at 16 °C. However, at 24 °C, the interpretation of the results is complicated by a significant interaction between gender and pCO2 for spawning corals. At 16 °C, gamete release was not observed, and no gender differences in calcification rates were observed – female and male corals showed similar reductions in calcification rates in response to elevated CO2 (15% and 19% respectively). Corals grown at 24 °C spawned repeatedly and male and female corals exhibited two different growth rate patterns – female corals grown at 24 °C and exposed to CO2 had calcification rates 39% lower than females grown at ambient CO2, while males showed a non-significant decline of 5% under elevated CO2. The increased sensitivity of females to elevated pCO2 may reflect a greater investment of energy in reproduction (egg production) relative to males (sperm production). These results suggest that both gender and spawning are important factors in determining the sensitivity of corals to ocean acidification, and considering these factors in future research may be critical to predicting how the population structures of marine calcifiers will change in response to ocean acidification.

  • Wall-Palmer, D., Hart, M.B., Smart, C.W., Sparks, R.S.J., LeFriant, A., Boudon, G., Deplus, C., and Komorowski, J.C.  Pteropods from the Caribbean Sea: variations in calcification as an indicator of past ocean carbonate saturation.  Biogeosciences 9(1): 309-315, 2012.
    Open Access >>
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    The aragonite shell-bearing thecosome pteropods are an important component of the oceanic plankton. However, with increasing pCO2 and the associated reduction in oceanic pH (ocean acidification), thecosome pteropods are thought to be particularly vulnerable to shell dissolution. The distribution and preservation of pteropods over the last 250 000 years have been investigated in marine sediment cores from the Caribbean Sea close to the island of Montserrat. Using the Limacina Dissolution Index (LDX), fluctuations in pteropod calcification through the most recent glacial/interglacial cycles are documented. By comparison to the oxygen isotope record (global ice volume), we show that pteropod calcification is closely linked to global changes in pCO2 and pH and is, therefore, a global signal. These data are in agreement with the findings of experiments upon living pteropods, which show that variations in pH can greatly affect aragonitic shells. The results of this study provide information which may be useful in the prediction of future changes to the pteropod assemblage caused by ocean acidification.

  • Chauvin, A., Denis, V., and Cuet, P.  Is the response of coral calcification to seawater acidification related to nutrient loading?  Coral Reefs 30(4): 911-923, 2011.
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    The effect of decreasing aragonite saturation state (ΩArag) of seawater (elevated pCO2) on calcification rates of Acropora muricata was studied using nubbins prepared from parent colonies located at two sites of La Saline reef (La Réunion Island, western Indian Ocean): a back-reef site (BR) affected by nutrient-enriched groundwater discharge (mainly nitrate), and a reef flat site (RF) with low terrigenous inputs. Protein and chlorophyll a content of the nubbins, as well as zooxanthellae abundance, were lower at RF than BR. Nubbins were incubated at ~27 °C over 2h under sunlight, in filtered seawater manipulated to get differing initial pCO2 (1,440–340 μatm), ΩArag (1.4–4.0), and dissolved inorganic carbon (DIC) concentrations (2,100–1,850 μmol kg-1). Increasing DIC concentrations at constant total alkalinity (AT) resulted in a decrease in ΩArag and an increase in pCO2. AT at the beginning of the incubations was kept at a natural level of 2,193 ± 6 μmol kg-1 (mean ± SD). Net photosynthesis (NP) and calcification were calculated from changes in pH and AT during the incubations. Calcification decrease in response to doubling pCO2 relative to preindustrial level was 22% for RF nubbins. When normalized to surface area of the nubbins, (1) NP and calcification were higher at BR than RF, (2) NP increased in high pCO2 treatments at BR compared to low pCO2 treatments, and (3) calcification was not related to ΩArag at BR. When normalized to NP, calcification was linearly related to ΩArag at both sites, and the slopes of the relationships were not significantly different. The increase in NP at BR in the high pCO2 treatments may have increased calcification and thus masked the negative effect of low ΩArag on calcification. Removing the effect of NP variations at BR showed that calcification declined in a similar manner with decreased ΩArag (increased pCO2) whatever the nutrient loading.

  • McCulloch, M. et al.  Resilience of cold-water scleractinian corals to ocean acidification: Boron isotopic systematics of pH and saturation state up-regulation.  Geochimica et Cosmochimica Acta 87: 21-34, 2012.
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    The boron isotope systematics has been determined for azooxanthellate scleractinian corals from a wide range of both deep-sea and shallow-water environments. The aragonitic coral species, Caryophyllia smithii, Desmophyllum dianthus, Enallopsammia rostrata, Lophelia pertusa, and Madrepora oculata, are all found to have relatively high δ11B compositions ranging from 23.2‰ to 28.7‰. These values lie substantially above the pH-dependent inorganic seawater borate equilibrium curve, indicative of strong up-regulation of pH of the internal calcifying fluid (pHcf), being elevated by ~0.6–0.8 units (ΔpH) relative to ambient seawater. In contrast, the deep-sea calcitic coral Corallium sp. has a significantly lower δ11B composition of 15.5‰, with a corresponding lower ΔpH value of ~0.3 units, reflecting the importance of mineralogical control on biological pH up-regulation. The solitary coral D. dianthus was sampled over a wide range of seawater pHT and shows an approximate linear correlation with ΔpHDesmo = 6.43–0.71 pHT (r2 = 0.79). An improved correlation is however found with the closely related parameter of seawater aragonite saturation state, where ΔpHDesmo = 1.09–0.14Ωarag (r2 = 0.95), indicating the important control that carbonate saturation state has on calcification. The ability to up-regulate internal pHcf, and consequently Ωcf, of the calcifying fluid is therefore a process present in both azooxanthellate and zooxanthellate aragonitic corals, and is attributed to the action of Ca2+-ATPase in modulating the proton gradient between seawater and the site of calcification. These findings also show that the boron isotopic compositions (δ11Bcarb) of aragonitic corals are highly systematic and consistent with direct uptake of the borate species within the biologically controlled extracellular calcifying medium. We also show that the relatively strong up-regulation of pH and consequent elevation of the internal carbonate saturation state (Ωcf ~8.5 to ~13) at the site of calcification by cold-water corals, facilitates calcification at or in some cases below the aragonite saturation horizon, providing a greater ability to adapt to the already low and now decreasing carbonate ion concentrations. Although providing greater resilience to the effects of ocean acidification and enhancing rates of calcification with increasing temperature, the process of internal pHcf up-regulation has an associated energetic cost, and therefore growth-rate cost, of ~10% per 0.1 pH unit decrease in seawater pHT. Furthermore, as the aragonite saturation horizon shoals with rapidly increasing pCO2 and Ωarag < 1, increased dissolution of the exposed skeleton will ultimately limit their survival in the deep oceans.

  • Ishii, M., Kosugi, N., Sasano, D., Saito, S., Midorikawa, T., and Inoue, H.Y.  Ocean acidification off the south coast of Japan: A result from time series observations of CO2 parameters from 1994 to 2008.  Journal of Geophysical Research 116(C6): art. C06022, 2011.
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    Ocean acidification resulting from increases in present and future atmospheric CO2 levels could seriously affect diverse coastal and oceanic ecosystems. In this work, we determine that a significant trend in ocean acidification is superposed on the large seasonal and interannual variabilities of acidity in surface waters off the south coast of Honshu, Japan, based on our repeated observations of partial pressure of CO2 (pCO2), total inorganic carbon (TCO2), and pH. Multiple regression analysis of TCO2 as a function of temperature, salinity, and timing of observations shows that TCO2 increased at a rate of +1.23 ± 0.40 μmol kg-1 yr-1 for the period 1994–2008, while no long-term change has been determined for total alkalinity calculated from TCO2 and pCO2 in seawater. These results indicate that pH and the aragonite saturation state (Ωarag) are decreasing at a rate of -0.020 ± 0.007 decade-1 and -0.12 ± 0.05 decade-1, respectively. If future atmospheric CO2 levels keep increasing as predicted by the Intergovernmental Panel on Climate Change emission scenario A1FI, which postulates intensive fossil fuel use associated with very rapid economic growth, a further reduction of -0.8 to -1.0 in Ωarag is likely in the next 50 years. Such a rapid reduction of Ωarag could have negative impacts on a variety of calcareous organisms.

  • Doropoulos, C., Ward, S., Diaz-Pulido, G., Hoegh-Guldberg, O., and Mumby, P.J.  Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions.  Ecology Letters 15(4): 338-346, 2012.
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    Successful recruitment in shallow reef ecosystems often involves specific cues that connect planktonic invertebrate larvae with particular crustose coralline algae (CCA) during settlement. While ocean acidification (OA) can reduce larval settlement and the abundance of CCA, the impact of OA on the interactions between planktonic larvae and their preferred settlement substrate are unknown. Here, we demonstrate that CO2 concentrations (800 and 1300 µatm) predicted to occur by the end of this century significantly reduce coral (Acropora millepora) settlement and CCA cover by ≥45%. The CCA important for inducing coral settlement (Titanoderma spp., Hydrolithon spp.) were the most deleteriously affected by OA. Surprisingly, the only preferred settlement substrate (Titanoderma) in the experimental controls was avoided by coral larvae as pCO2 increased, and other substrata selected. Our results suggest OA may reduce coral population recovery by reducing coral settlement rates, disrupting larval settlement behaviour, and reducing the availability of the most desirable coralline algal species for successful coral recruitment.

  • Maier, C., Watremez, P., Taviani, M., Weinbauer, M.G., and Gattuso, J.P.  Calcification rates and the effect of ocean acidification on Mediterranean cold-water corals.  Proceedings of the Royal Society [B] 279(1734): 1716-1723, 2012.
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    Global environmental changes, including ocean acidification, have been identified as a major threat to scleractinian corals. General predictions are that ocean acidification will be detrimental to reef growth and that 40 to more than 80 per cent of present-day reefs will decline during the next 50 years. Cold-water corals (CWCs) are thought to be strongly affected by changes in ocean acidification owing to their distribution in deep and/or cold waters, which naturally exhibit a CaCO3 saturation state lower than in shallow/warm waters. Calcification was measured in three species of Mediterranean cold-water scleractinian corals (Lophelia pertusa, Madrepora oculata and Desmophyllum dianthus) on-board research vessels and soon after collection. Incubations were performed in ambient sea water. The species M. oculata was additionally incubated in sea water reduced or enriched in CO2. At ambient conditions, calcification rates ranged between -0.01 and 0.23% d-1. Calcification rates of M. oculata under variable partial pressure of CO2 (pCO2) were the same for ambient and elevated pCO2 (404 and 867 µatm) with 0.06 ± 0.06% d-1, while calcification was 0.12 ± 0.06% d-1 when pCO2 was reduced to its pre-industrial level (285 µatm). This suggests that present-day CWC calcification in the Mediterranean Sea has already drastically declined (by 50%) as a consequence of anthropogenic-induced ocean acidification.

  • Moya, A. et al.  Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification.  Molecular Ecology 21(10): 2440-2454, 2012.
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    The impact of ocean acidification (OA) on coral calcification, a subject of intense current interest, is poorly understood in part because of the presence of symbionts in adult corals. Early life history stages of Acropora spp. provide an opportunity to study the effects of elevated CO2 on coral calcification without the complication of symbiont metabolism. Therefore, we used the Illumina RNAseq approach to study the effects of acute exposure to elevated CO2 on gene expression in primary polyps of Acropora millepora, using as reference a novel comprehensive transcriptome assembly developed for this study. Gene ontology analysis of this whole transcriptome data set indicated that CO2-driven acidification strongly suppressed metabolism but enhanced extracellular organic matrix synthesis, whereas targeted analyses revealed complex effects on genes implicated in calcification. Unexpectedly, expression of most ion transport proteins was unaffected, while many membrane-associated or secreted carbonic anhydrases were expressed at lower levels. The most dramatic effect of CO2-driven acidification, however, was on genes encoding candidate and known components of the skeletal organic matrix that controls CaCO3 deposition. The skeletal organic matrix effects included elevated expression of adult-type galaxins and some secreted acidic proteins, but down-regulation of other galaxins, secreted acidic proteins, SCRiPs and other coral-specific genes, suggesting specialized roles for the members of these protein families and complex impacts of OA on mineral deposition. This study is the first exhaustive exploration of the transcriptomic response of a scleractinian coral to acidification and provides an unbiased perspective on its effects during the early stages of calcification.

  • Ferrari, M.C.O., McCormick, M.I., Munday, P.L., Meekan, M.G., Dixson, D.L., Lönnstedt, O., and Chivers, D.P.  Effects of ocean acidification on visual risk assessment in coral reef fishes.  Functional Ecology 26(3): 553-558, 2012.
    Open Access >>
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    1. With the global increase in CO2 emissions, there is a pressing need for studies aimed at understanding the effects of ocean acidification on marine ecosystems. Several studies have reported that exposure to CO2 impairs chemosensory responses of juvenile coral reef fishes to predators. Moreover, one recent study pointed to impaired responses of reef fish to auditory cues that indicate risky locations. These studies suggest that altered behaviour following exposure to elevated CO2 is caused by a systemic effect at the neural level. 2. The goal of our experiment was to test whether juvenile damselfish Pomacentrus amboinensis exposed to different levels of CO2 would respond differently to a potential threat, the sight of a large novel coral reef fish, a spiny chromis, Acanthochromis polyancanthus, placed in a watertight bag. 3. Juvenile damselfish exposed to 440 (current day control), 550 or 700 μatm CO2 did not differ in their response to the chromis. However, fish exposed to 850 μatm showed reduced antipredator responses; they failed to show the same reduction in foraging, activity and area use in response to the chromis. Moreover, they moved closer to the chromis and lacked any bobbing behaviour typically displayed by juvenile damselfishes in threatening situations. 4. Our results are the first to suggest that response to visual cues of risk may be impaired by CO2 and provide strong evidence that the multi-sensory effects of CO2 may stem from systematic effects at the neural level.

  • Kline, D.I. et al.  A short-term in situ CO2 enrichment experiment on Heron Island (GBR).  Scientific Reports 2: art. 413, 2012.
    Open Access >>
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    Ocean acidification poses multiple challenges for coral reefs on molecular to ecological scales, yet previous experimental studies of the impact of projected CO2 concentrations have mostly been done in aquarium systems with corals removed from their natural ecosystem and placed under artificial light and seawater conditions. The Coral-Proto Free Ocean Carbon Enrichment System (CP-FOCE) uses a network of sensors to monitor conditions within each flume and maintain experimental pH as an offset from environmental pH using feedback control on the injection of low pH seawater. Carbonate chemistry conditions maintained in the -0.06 and -0.22 pH offset treatments were significantly different than environmental conditions. The results from this short-term experiment suggest that the CP-FOCE is an important new experimental system to study in situ impacts of ocean acidification on coral reef ecosystems.

  • Dickinson, G.H., Ivanina, A.V., Matoo, O.B., Pörtner, H.O., Lannig, G., Bock, C., Beniash, E., and Sokolova, I.M.  Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica.  Journal of Experimental Biology 215(1): 29-43, 2012.
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    Rising levels of atmospheric CO2 lead to acidification of the ocean and alter seawater carbonate chemistry, which can negatively impact calcifying organisms, including mollusks. In estuaries, exposure to elevated CO2 levels often co-occurs with other stressors, such as reduced salinity, which enhances the acidification trend, affects ion and acid–base regulation of estuarine calcifiers and modifies their response to ocean acidification. We studied the interactive effects of salinity and partial pressure of CO2 (PCO2) on biomineralization and energy homeostasis in juveniles of the eastern oyster, Crassostrea virginica, a common estuarine bivalve. Juveniles were exposed for 11 weeks to one of two environmentally relevant salinities (30 or 15 PSU) either at current atmospheric PCO2 (~400 μatm, normocapnia) or PCO2 projected by moderate IPCC scenarios for the year 2100 (~700–800 μatm, hypercapnia). Exposure of the juvenile oysters to elevated PCO2 and/or low salinity led to a significant increase in mortality, reduction of tissue energy stores (glycogen and lipid) and negative soft tissue growth, indicating energy deficiency. Interestingly, tissue ATP levels were not affected by exposure to changing salinity and  PCO2, suggesting that juvenile oysters maintain their cellular energy status at the expense of lipid and glycogen stores. At the same time, no compensatory upregulation of carbonic anhydrase activity was found under the conditions of low salinity and high PCO2. Metabolic profiling using magnetic resonance spectroscopy revealed altered metabolite status following low salinity exposure; specifically, acetate levels were lower in hypercapnic than in normocapnic individuals at low salinity. Combined exposure to hypercapnia and low salinity negatively affected mechanical properties of shells of the juveniles, resulting in reduced hardness and fracture resistance. Thus, our data suggest that the combined effects of elevated PCO2 and fluctuating salinity may jeopardize the survival of eastern oysters because of weakening of their shells and increased energy consumption.

  • Lohbeck, K.T., Riebesell, U., and Reusch, T.B.H.  Adaptive evolution of a key phytoplankton species to ocean acidification.  Nature Geoscience 5(5): 346-351, 2012.
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    Ocean acidification, the drop in seawater pH associated with the ongoing enrichment of marine waters with carbon dioxide from fossil fuel burning, may seriously impair marine calcifying organisms. Our present understanding of the sensitivity of marine life to ocean acidification is based primarily on short-term experiments, in which organisms are exposed to increased concentrations of CO2. However, phytoplankton species with short generation times, in particular, may be able to respond to environmental alterations through adaptive evolution. Here, we examine the ability of the world's single most important calcifying organism, the coccolithophore Emiliania huxleyi, to evolve in response to ocean acidification in two 500-generation selection experiments. Specifically, we exposed E. huxleyi populations founded by single or multiple clones to increased concentrations of CO2. Around 500 asexual generations later we assessed their fitness. Compared with populations kept at ambient CO2 partial pressure, those selected at increased partial pressure exhibited higher growth rates, in both the single- and multiclone experiment, when tested under ocean acidification conditions. Calcification was partly restored: rates were lower under increased CO2 conditions in all cultures, but were up to 50% higher in adapted compared with non-adapted cultures. We suggest that contemporary evolution could help to maintain the functionality of microbial processes at the base of marine food webs in the face of global change.

  • Nielsen, L.T., Hallegraeff, G.M., Wright, S.W., and Hansen, P.J.  Effects of experimental seawater acidification on an estuarine plankton community.  Aquatic Microbial Ecology 65(3): 271-285, 2012.
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    The atmospheric CO2 concentration is rising, and models predict that by the end of the century it will have increased to twice the amount seen at any given time during the last 15 million yr. This will cause a decrease in average surface water pH of 0.4, and planktonic protists will be among the organisms to be affected first by this change. We tested whether reduced pH (and increased free CO2) would affect plankton communities over an incubation period of 14 d. In a laboratory microcosm setup using a natural plankton community from the Derwent River estuary, Australia, 2 treatments with reduced pH (8.0 and 7.7) were compared to an unaltered control of pH 8.3. An extreme pH 6.3 was included for comparison. Measured parameters included community photosynthesis, nutrient uptake and biomass build-up as well as enumeration of 25 protist taxa and quantitative HPLC of phytoplankton pigments. A major succession was seen during the 14 d, but no effects at all were found in pH treatments 8.0 and 7.7, whereas the extreme pH 6.3 clearly affected the community for all measured parameters. Thus, it is unlikely that the investigated plankton community would be significantly affected by a pH and CO2 change as predicted for the 21st century. This has previously been found for other coastal plankton assemblages as well, and we suggest that high pH resilience is a necessity for protist species living in coastal waters with relatively large pH fluctuations.

  • Mathis, J.T. et al.  Storm-induced upwelling of high  pCO2 waters onto the continental shelf of the western Arctic Ocean and implications for carbonate mineral saturation states.  Geophysical Research Letters 39(7): art. L07606, 2012.
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    The carbon system of the western Arctic Ocean is undergoing a rapid transition as sea ice extent and thickness decline. These processes are dynamically forcing the region, with unknown consequences for CO2 fluxes and carbonate mineral saturation states, particularly in the coastal regions where sensitive ecosystems are already under threat from multiple stressors. In October 2011, persistent wind-driven upwelling occurred in open water along the continental shelf of the Beaufort Sea in the western Arctic Ocean. During this time, cold (<-1.2°C), salty (>32.4) halocline water-supersaturated with respect to atmospheric CO2 (pCO2 > 550 μatm) and undersaturated in aragonite (Ωaragonite < 1.0) was transported onto the Beaufort shelf. A single 10-day event led to the outgassing of 0.18–0.54 Tg-C and caused aragonite undersaturations throughout the water column over the shelf. If we assume a conservative estimate of four such upwelling events each year, then the annual flux to the atmosphere would be 0.72–2.16 Tg-C, which is approximately the total annual sink of CO2 in the Beaufort Sea from primary production. Although a natural process, these upwelling events have likely been exacerbated in recent years by declining sea ice cover and changing atmospheric conditions in the region, and could have significant impacts on regional carbon budgets. As sea ice retreat continues and storms increase in frequency and intensity, further outgassing events and the expansion of waters that are undersaturated in carbonate minerals over the shelf are probable.

  • Barton, A., Hales, B., Waldbusser, G.G., Langdon, C., and Feely, R.A.  The Pacific oyster, Crassostrea gigas, shows negative correlation to naturally elevated carbon dioxide levels: Implications for near-term ocean acidification effects.  Limnology and Oceanography 57(3): 698-710, 2012.
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    We report results from an oyster hatchery on the Oregon coast, where intake waters experienced variable carbonate chemistry (aragonite saturation state < 0.8 to > 3.2; pH < 7.6 to > 8.2) in the early summer of 2009. Both larval production and midstage growth (~120 to ~150 µm) of the oyster Crassostrea gigas were significantly negatively correlated with the aragonite saturation state of waters in which larval oysters were spawned and reared for the first 48h of life. The effects of the initial spawning conditions did not have a significant effect on early-stage growth (growth from D-hinge stage to ~120 µm), suggesting a delayed effect of water chemistry on larval development.

  • Stumpp, M., Trübenbach, K., Brennecke, D., Hu, M.Y., and Melzner, F.  Resource allocation and extracellular acid-base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification.  Aquatic Toxicology 110-111: 194-207, 2012.
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    Anthropogenic CO2 emission will lead to an increase in seawater pCO2 of up to 80–100Pa (800–1000μatm) within this century and to an acidification of the oceans. Green sea urchins (Strongylocentrotus droebachiensis) occurring in Kattegat experience seasonal hypercapnic and hypoxic conditions already today. Thus, anthropogenic CO2 emissions will add up to existing values and will lead to even higher pCO2 values >200Pa (>2000μatm). To estimate the green sea urchins’ potential to acclimate to acidified seawater, we calculated an energy budget and determined the extracellular acid base status of adult S. droebachiensis exposed to moderately (102–145Pa, 1007–1431μatm) and highly (284–385Pa, 2800–3800μatm) elevated seawater pCO2 for 10 and 45 days. A 45-day exposure to elevated pCO2 resulted in a shift in energy budgets, leading to reduced somatic and reproductive growth. Metabolic rates were not significantly affected, but ammonium excretion increased in response to elevated pCO2. This led to decreased O:N ratios. These findings suggest that protein metabolism is possibly enhanced under elevated pCO2 in order to support ion homeostasis by increasing net acid extrusion. The perivisceral coelomic fluid acid–base status revealed that S. droebachiensis is able to fully (intermediate pCO2) or partially (high pCO2) compensate extracellular pH (pHe) changes by accumulation of bicarbonate (maximum increases 2.5mM), albeit at a slower rate than typically observed in other taxa (10-day duration for full pHe compensation). At intermediate pCO2, sea urchins were able to maintain fully compensated pHe for 45 days. Sea urchins from the higher pCO2 treatment could be divided into two groups following medium-term acclimation: one group of experimental animals (29%) contained remnants of food in their digestive system and maintained partially compensated pHe (+2.3mM HCO3), while the other group (71%) exhibited an empty digestive system and a severe metabolic acidosis (−0.5 pH units, −2.4mM HCO3). There was no difference in mortality between the three pCO2 treatments. The results of this study suggest that S. droebachiensis occurring in the Kattegat might be pre-adapted to hypercapnia due to natural variability in pCO2 in its habitat. We show for the first time that some echinoderm species can actively compensate extracellular pH. Seawater pCO2 values of >200Pa, which will occur in the Kattegat within this century during seasonal hypoxic events, can possibly only be endured for a short time period of a few weeks. Increases in anthropogenic CO2 emissions and leakages from potential sub-seabed CO2 storage (CCS) sites thus impose a threat to the ecologically and economically important species S. droebachiensis.

  • McCarthy, A., Rogers, S.P., Duffy, S.J., and Campbell, D.A.  Elevated carbon dioxide differentially alters the photophysiology of Thalassiosira pseudonana (Bacillariophyceae) and Emiliania huxleyi (Haptophyta).  Journal of Phycology 48(3): 635-646, 2012.
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    Increasing anthropogenic carbon dioxide is causing changes to ocean chemistry, which will continue in a predictable manner. Dissolution of additional atmospheric carbon dioxide leads to increased concentrations of dissolved carbon dioxide and bicarbonate and decreased pH in ocean water. The concomitant effects on phytoplankton ecophysiology, leading potentially to changes in community structure, are now a focus of concern. Therefore, we grew the coccolithophore Emiliania huxleyi (Lohmann) W. W. Hay et H. Mohler and the diatom strains Thalassiosira pseudonana (Hust.) Hasle et Heimdal CCMP 1014 and T. pseudonana CCMP 1335 under low light in turbidostat photobioreactors bubbled with air containing 390 ppmv or 750 ppmv CO2. Increased pCO2 led to increased growth rates in all three strains. In addition, protein levels of RUBISCO increased in the coastal strains of both species, showing a larger capacity for CO2 assimilation at 750 ppmv CO2. With increased pCO2, both T. pseudonana strains displayed an increased susceptibility to PSII photoinactivation and, to compensate, an augmented capacity for PSII repair. Consequently, the cost of maintaining PSII function for the diatoms increased at increased pCO2. In E. huxleyi, PSII photoinactivation and the counter-acting repair, while both intrinsically larger than in T. pseudonana, did not change between the current and high-pCO2 treatments. The content of the photosynthetic electron transport intermediary cytochrome b6/f complex increased significantly in the diatoms under elevated pCO2, suggesting changes in electron transport function.

  • Ericson, J., Ho, M., Miskelly, A., King, C., Virtue, P., Tilbrook, B., and Byrne, M.  Combined effects of two ocean change stressors, warming and acidification, on fertilization and early development of the Antarctic echinoid Sterechinus neumayeri.  Polar Biology 35(7): 1027-1034, 2012.
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    The effects of concurrent ocean warming and acidification on Antarctic marine benthos warrant investigation as little is known about potential synergies between these climate change stressors. We examined the interactive effects of warming and acidification on fertilization and embryonic development of the ecologically important sea urchin Sterechinus neumayeri reared from fertilization in elevated temperature (+1.5°C and 3°C) and decreased pH (-0.3 and -0.5 pH units) treatments. Fertilization using gametes from multiple males and females, to represent populations of spawners, was resilient to acidification at ambient temperature (0°C). At elevated temperatures, there was a negative interactive effect of temperature and pH on percentage of fertilization (11% reduction at 3°C). For cleavage stage embryos, there was a significant, but small reduction (6%) in the percentage of normal embryos at pH 7.5. For blastulae, a 10–11% decrease in normal development occurred in the +3°C treatments across all pH levels. Our results highlight the importance of considering the impacts of both temperature and pH in assessing the life history response of S. neumayeri in a changing polar ocean. While fertilization and development to the blastula stage were robust to levels of temperature and pH change predicted over coming decades, deleterious interactive effects were evident between these stressors at levels projected to occur by 2100 and beyond.

  • Nakamura, M. and Morita, M.  Sperm motility of the scleractinian coral Acropora digitifera under preindustrial, current, and predicted ocean acidification regimes.  Aquatic Biology 15(3): 299-302, 2012.
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    Ocean acidification caused by the uptake of anthropogenic CO2 in the oceans negatively affects the early life stages of corals by reducing their calcification rate. Acidification also inhibits the sperm motility of corals, potentially affecting fertilization success. We investigated the effects of different pCO2 (partial pressure of CO2) conditions on the sperm motility of Acropora digitifera. Using a pCO2-control system, we maintained pCO2 at concentrations from preindustrial and present-day levels up to the level predicted by the year 2100 (300, 400, and 1000 ppm, respectively). Our results indicated that ocean acidification has the potential to suppress the sperm flagellar motility of A. digitifera. Furthermore, sperm motility will likely decline by ~30%, which may impact fertility, if the sensitivity of sperm motility to decreasing pH cannot adapt over a span of ~90 yr.

  • Uddin, S., Gevao, B., Al Ghadban, A.N., Nithyanandan, M., and Al Shamroukh, D.  Acidification in Arabian Gulf – Insights from pH and temperature measurements.  Journal of Environmental Monitoring 14(5): 1479-1482, 2012.
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    The detrimental effects of increasing atmospheric levels of carbon dioxide (CO2) and other greenhouse gases since the industrial revolution has led to a concerted international effort to control their release and abate the environmental and human health impacts. CO2 is removed from the atmosphere by photosynthesis of plants in the terrestrial environment and by aquatic sequestration. In the Middle East and other arid countries, terrestrial removal is minimal. The most likely removal pathway for CO2 in arid regions around the world is by aquatic sequestration. In the Middle East the major sink is the Arabian Gulf which leads to acidification of the marine environment. Biweekly pH concentration measurements in surface waters of the northern Arabian Gulf over a four year period in this study suggest that the Arabian Gulf waters are becoming increasingly acidic with time. Supporting evidence for increased CO2 sequestration comes from increased marine primary productivity over the past decade. Biological effects, such as coral bleaching, observed during this period suggest that urgent action is required to reverse the trend and protect marine life. The data highlight the fact that this semi-enclosed sea is undergoing a rapid degradation which may affect the oceanic chemistry and biogeochemical cycle much earlier than predicted for most oceanic waters.

  • Edmunds, P.J., Brown, D., and Moriarty, V.  Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia.  Global Change Biology 18(7): 2173-2183, 2012.
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    This study tested the hypothesis that the response of corals to temperature and pCO2 is consistent between taxa. Juvenile massive Porites spp. and branches of P. rus from the back reef of Moorea were incubated for 1 month under combinations of temperature (29.3 °C and 25.6 °C) and pCO2 (41.6 Pa and 81.5 Pa) at an irradiance of 599 μmol quanta m-2 s-1. Using microcosms and CO2 gas mixing technology, treatments were created in a partly nested design (tanks) with two between-plot factors (temperature and pCO2), and one within-plot factor (taxon); calcification was used as a dependent variable. pCO2 and temperature independently affected calcification, but the response differed between taxa. Massive Porites spp. was largely unaffected by the treatments, but P. rus grew 50% faster at 29.3 °C compared with 25.6 °C, and 28% slower at 81.5 Pa vs. 41.6 Pa CO2. A compilation of studies placed the present results in a broader context and tested the hypothesis that calcification for individual coral genera is independent of pH, [HCO3-], and [CO32-]. Unlike recent reviews, this analysis was restricted to studies reporting calcification in units that could be converted to nmol CaCO3 cm-2 h-1. The compilation revealed a high degree of variation in calcification as a function of pH, [HCO3-], and [CO32-], and supported three conclusions: (1) studies of the effects of ocean acidification on corals need to pay closer attention to reducing variance in experimental outcomes to achieve stronger synthetic capacity, (2) coral genera respond in dissimilar ways to pH, [HCO3-], and [CO32-], and (3) calcification of massive Porites spp. is relatively resistant to short exposures of increased pCO2, similar to that expected within 100 y.

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