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February 20, 2014

Ocean Acidification - Part III

  • Findlay, H.S., Hennige, S.J., Wicks, L.C., Navas, J.M., Woodward, E.M., and Roberts, J.M.  Fine-scale nutrient and carbonate system dynamics around cold-water coral reefs in the northeast Atlantic.  Scientific Reports 4: art. 3671, 2014.
    Open Access >>   
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    Ocean acidification has been suggested as a serious threat to the future existence of cold-water corals (CWC). However, there are few fine-scale temporal and spatial datasets of carbonate and nutrients conditions available for these reefs, which can provide a baseline definition of extant conditions. Here we provide observational data from four different sites in the northeast Atlantic that are known habitats for CWC. These habitats differ by depth and by the nature of the coral habitat. At depths where CWC are known to occur across these sites the dissolved inorganic carbon ranged from 2088 to 2186 μmol kg-1, alkalinity ranged from 2299 to 2346 μmol kg-1, and aragonite Ω ranged from 1.35 to 2.44. At two sites fine-scale hydrodynamics caused increased variability in the carbonate and nutrient conditions over daily time-scales. The observed high level of variability must be taken into account when assessing CWC sensitivities to future environmental change.

  • Watson, S.-A., Lefevre, S., McCormick, M.I., Domenici, P., Nilsson, G.E., and Munday, P.L.  Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels.  Proceedings of the Royal Society of London [B] 281(1774): art. 20132377, 2014.
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    Ocean acidification poses a range of threats to marine invertebrates; however, the potential effects of rising carbon dioxide (CO2) on marine invertebrate behaviour are largely unknown. Marine gastropod conch snails have a modified foot and operculum allowing them to leap backwards rapidly when faced with a predator, such as a venomous cone shell. Here, we show that projected near-future seawater CO2 levels (961 µatm) impair this escape behaviour during a predator–prey interaction. Elevated-CO2 halved the number of snails that jumped from the predator, increased their latency to jump and altered their escape trajectory. Physical ability to jump was not affected by elevated-CO2 indicating instead that decision-making was impaired. Antipredator behaviour was fully restored by treatment with gabazine, a GABA antagonist of some invertebrate nervous systems, indicating potential interference of neurotransmitter receptor function by elevated-CO2, as previously observed in marine fishes. Altered behaviour of marine invertebrates at projected future CO2 levels could have potentially far-reaching implications for marine ecosystems.

  • Fabricius, K.E., De'Ath, G., Noonan, S., and Uthicke, S.  Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities.  Proceedings of the Royal Society of London [B] 281(1775): art. 20132479, 2014.
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    The ecological effects of ocean acidification (OA) from rising atmospheric carbon dioxide (CO2) on benthic marine communities are largely unknown. We investigated in situ the consequences of long-term exposure to high CO2 on coral-reef-associated macroinvertebrate communities around three shallow volcanic CO2 seeps in Papua New Guinea. The densities of many groups and the number of taxa (classes and phyla) of macroinvertebrates were significantly reduced at elevated CO2 (425–1100 µatm) compared with control sites. However, sensitivities of some groups, including decapod crustaceans, ascidians and several echinoderms, contrasted with predictions of their physiological CO2 tolerances derived from laboratory experiments. High CO2 reduced the availability of structurally complex corals that are essential refugia for many reef-associated macroinvertebrates. This loss of habitat complexity was also associated with losses in many macroinvertebrate groups, especially predation-prone mobile taxa, including crustaceans and crinoids. The transition from living to dead coral as substratum and habitat further altered macroinvertebrate communities, with far more taxa losing than gaining in numbers. Our study shows that indirect ecological effects of OA (reduced habitat complexity) will complement its direct physiological effects and together with the loss of coral cover through climate change will severely affect macroinvertebrate communities in coral reefs.

  • Hamilton, T.J., Holcombe, A., and Tresguerres, M.  CO2-induced ocean acidification increases anxiety in Rockfish via alteration of GABAA receptor functioning.  Proceedings of the Royal Society of London [B]  281(1775): art. 20132509, 2014.
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    The average surface pH of the ocean is dropping at a rapid rate due to the dissolution of anthropogenic CO2, raising concerns for marine life. Additionally, some coastal areas periodically experience upwelling of CO2-enriched water with reduced pH. Previous research has demonstrated ocean acidification (OA)-induced changes in behavioural and sensory systems including olfaction, which is due to altered function of neural gamma-aminobutyric acid type A (GABAA) receptors. Here, we used a camera-based tracking software system to examine whether OA-dependent changes in GABAA receptors affect anxiety in juvenile Californian rockfish (Sebastes diploproa). Anxiety was estimated using behavioural tests that measure light/dark preference (scototaxis) and proximity to an object. After one week in OA conditions projected for the next century in the California shore (1125 ± 100 µatm, pH 7.75), anxiety was significantly increased relative to controls (483 ± 40 µatm CO2, pH 8.1). The GABAA-receptor agonist muscimol, but not the antagonist gabazine, caused a significant increase in anxiety consistent with altered Cl- flux in OA-exposed fish. OA-exposed fish remained more anxious even after 7 days back in control seawater; however, they resumed their normal behaviour by day 12. These results show that OA could severely alter rockfish behaviour; however, this effect is reversible.

  • Allan, B.J.M., Miller, G.M., McCormick, M.I., Domenici, P., and Munday, P.L.  Parental effects improve escape performance of juvenile reef fish in a high-CO2 world.  Proceedings of the Royal Society of London [B] 281(1777): art. 20132179, 2014.
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    Rising CO2 levels in the oceans are predicted to have serious consequences for many marine taxa. Recent studies suggest that non-genetic parental effects may reduce the impact of high CO2 on the growth, survival and routine metabolic rate of marine fishes, but whether the parental environment mitigates behavioural and sensory impairment associated with high CO2 remains unknown. Here, we tested the acute effects of elevated CO2 on the escape responses of juvenile fish and whether such effects were altered by exposure of parents to increased CO2 (transgenerational acclimation). Elevated CO2 negatively affected the reactivity and locomotor performance of juvenile fish, but parental exposure to high CO2 reduced the effects in some traits, indicating the potential for acclimation of behavioural impairment across generations. However, acclimation was not complete in some traits, and absent in others, suggesting that transgenerational acclimation does not completely compensate the effects of high CO2 on escape responses.

  • Williams, G.J. et al.  Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease.  Proceedings of the Royal Society of London [B] 281(1778): art. 20133069, 2014.
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    Diseases threaten the structure and function of marine ecosystems and are contributing to the global decline of coral reefs. We currently lack an understanding of how climate change stressors, such as ocean acidification (OA) and warming, may simultaneously affect coral reef disease dynamics, particularly diseases threatening key reef-building organisms, for example crustose coralline algae (CCA). Here, we use coralline fungal disease (CFD), a previously described CCA disease from the Pacific, to examine these simultaneous effects using both field observations and experimental manipulations. We identify the associated fungus as belonging to the subphylum Ustilaginomycetes and show linear lesion expansion rates on individual hosts can reach 6.5 mm per day. Further, we demonstrate for the first time, to our knowledge, that ocean-warming events could increase the frequency of CFD outbreaks on coral reefs, but that OA-induced lowering of pH may ameliorate outbreaks by slowing lesion expansion rates on individual hosts. Lowered pH may still reduce overall host survivorship, however, by reducing calcification and facilitating fungal bio-erosion. Such complex, interactive effects between simultaneous extrinsic environmental stressors on disease dynamics are important to consider if we are to accurately predict the response of coral reef communities to future climate change.

  • Sanford, E., Gaylord, B., Hettinger, A., Lenz, E.A., Meyer, K., and Hill, T.M.  Ocean acidification increases the vulnerability of native oysters to predation by invasive snails.  Proceedings of the Royal Society of London [B] 281(1778): art. 20132681, 2014.
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    There is growing concern that global environmental change might exacerbate the ecological impacts of invasive species by increasing their per capita effects on native species. However, the mechanisms underlying such shifts in interaction strength are poorly understood. Here, we test whether ocean acidification, driven by elevated seawater pCO2, increases the susceptibility of native Olympia oysters to predation by invasive snails. Oysters raised under elevated pCO2 experienced a 20% increase in drilling predation. When presented alongside control oysters in a choice experiment, 48% more high-CO2 oysters were consumed. The invasive snails were tolerant of elevated CO2 with no change in feeding behaviour. Oysters raised under acidified conditions did not have thinner shells, but were 29–40% smaller than control oysters, and these smaller individuals were consumed at disproportionately greater rates. Reduction in prey size is a common response to environmental stress that may drive increasing per capita effects of stress-tolerant invasive predators.

  • Collins, S., Rost, B., and Rynearson, T.A.  Evolutionary potential of marine phytoplankton under ocean acidification.  Evolutionary Applications 7(1): 140-155, 2014.
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    Marine phytoplankton have many obvious characters, such as rapid cell division rates and large population sizes, that give them the capacity to evolve in response to global change on timescales of weeks, months or decades. However, few studies directly investigate if this adaptive potential is likely to be realized. Because of this, evidence of to whether and how marine phytoplankton may evolve in response to global change is sparse. Here, we review studies that help predict evolutionary responses to global change in marine phytoplankton. We find limited support from experimental evolution that some taxa of marine phytoplankton may adapt to ocean acidification, and strong indications from studies of variation and structure in natural populations that selection on standing genetic variation is likely. Furthermore, we highlight the large body of literature on plastic responses to ocean acidification available, and evolutionary theory that may be used to link plastic and evolutionary responses. Because of the taxonomic breadth spanned by marine phytoplankton, and the diversity of roles they fill in ocean ecosystems and biogeochemical cycles, we stress the necessity of treating taxa or functional groups individually.

  • Gianguzza, P., Visconti, G., Gianguzza, F., Vizzini, S., Sarà, G., and Dupont, S.  Temperature modulates the response of the thermophilous sea urchin Arbacia lixula early life stages to CO2-driven acidification.  Marine Environmental Research 93: 70-77, 2014.
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    The increasing abundances of the thermophilous black sea urchin Arbacia lixula in the Mediterranean Sea are attributed to the Western Mediterranean warming. However, few data are available on the potential impact of this warming on A.lixula in combination with other global stressors such as ocean acidification. The aim of this study is to investigate the interactive effects of increased temperature and of decreased pH on fertilization and early development of A.lixula. This was tested using a fully crossed design with four temperatures (20, 24, 26 and 27 °C) and two pH levels (pHNBS 8.2 and 7.9). Temperature and pH had no significant effect on fertilization and larval survival (2d) for temperature <27 °C. At 27 °C, the fertilization success was very low (<1%) and all larvae died within 2d. Both temperature and pH had effects on the developmental dynamics. Temperature appeared to modulate the impact of decreasing pH on the % of larvae reaching the pluteus stage leading to a positive effect (faster growth compared to pH 8.2) of low pH at 20 °C, a neutral effect at 24 °C and a negative effect (slower growth) at 26 °C. These results highlight the importance of considering a range of temperatures covering today and the future environmental variability in any experiment aiming at studying the impact of ocean acidification.

  • Asnaghi, V., Mangialajo, L., Gattuso, J.-P., Francour, P., Privitera, D., and Chiantore, M.  Effects of ocean acidification and diet on thickness and carbonate elemental composition of the test of juvenile sea urchins.  Marine Environmental Research 93: 78-84, 2014.
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    Continuous anthropogenic CO2 emissions to the atmosphere and uptake by the oceans will cause a reduction of seawater pH and saturation state (Ω) of CaCO3 minerals from which marine calcifiers build their shells and skeletons. Sea urchins use the most soluble form of calcium carbonate, high-magnesium calcite, to build their skeleton, spines and grazing apparatus. In order to highlight the effects of increased pCO2 on the test thickness and carbonate elemental composition of juvenile sea urchins and potential differences in their responses linked to the diet, we performed a laboratory experiment on juvenile Paracentrotus lividus, grazing on calcifying (Corallina elongata) and non-calcifying (Cystoseira amentacea, Dictyota dichotoma) macroalgae, under different pH (corresponding to pCO2 values of 390, 550, 750 and 1000 µatm). Results highlighted the importance of the diet in determining sea urchin size irrespectively of the pCO2 level, and the relevance of macroalgal diet in modulating urchin Mg/Ca ratio. The present study provides relevant clues both in terms of the mechanism of mineral incorporation and in terms of bottom-up processes (algal diet) affecting top-down ones (fish predation) in rocky subtidal communities.

  • Gobler, C.J., DePasquale, E.L., Griffith, A.W., and Baumann, H.  Hypoxia and acidification have additive and synergistic negative effects on the growth, survival, and metamorphosis of early life stage bivalves.  PLoS ONE 9(1): art. e83648, 2014.
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    Low oxygen zones in coastal and open ocean ecosystems have expanded in recent decades, a trend that will accelerate with climatic warming. There is growing recognition that low oxygen regions of the ocean are also acidified, a condition that will intensify with rising levels of atmospheric CO2. Presently, however, the concurrent effects of low oxygen and acidification on marine organisms are largely unknown, as most prior studies of marine hypoxia have not considered pH levels. We experimentally assessed the consequences of hypoxic and acidified water for early life stage bivalves (bay scallops, Argopecten irradians, and hard clams, Mercenaria mercenaria), marine organisms of significant economic and ecological value and sensitive to climate change. In larval scallops, experimental and naturally-occurring acidification (pH, total scale = 7.4–7.6) reduced survivorship (by >50%), low oxygen (30–50 µM) inhibited growth and metamorphosis (by >50%), and the two stressors combined produced additively negative outcomes. In early life stage clams, however, hypoxic waters led to 30% higher mortality, while acidified waters significantly reduced growth (by 60%). Later stage clams were resistant to hypoxia or acidification separately but experienced significantly (40%) reduced growth rates when exposed to both conditions simultaneously. Collectively, these findings demonstrate that the consequences of low oxygen and acidification for early life stage bivalves, and likely other marine organisms, are more severe than would be predicted by either individual stressor and thus must be considered together when assessing how ocean animals respond to these conditions both today and under future climate change scenarios.

  • Domenici, P., Allan, B.J.M., Watson, S.-A., McCormick, M.I., and Munday, P.L.  Shifting from right to left: the combined effect of elevated CO2 and temperature on behavioural lateralization in a coral reef fish.  PLoS ONE 9(1): art. e87969, 2014.
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    Recent studies have shown that elevated CO2 can affect the behaviour of larval and juvenile fishes. In particular, behavioural lateralization, an expression of brain functional asymmetries, is affected by elevated CO2 in both coral reef and temperate fishes. However, the potentially interacting effects of rising temperatures and CO2 on lateralization are unknown. Here, we tested the combined effect of near-future elevated-CO2 concentrations (930 µatm) and temperature variation on behavioural lateralization of a marine damselfish, Pomacentrus wardi. Individuals exposed to one of four treatments (two CO2 levels and two temperatures) were observed in a detour test where they made repeated decisions about turning left or right. Individuals exposed to current CO2 and ambient temperature levels showed a significant right-turning bias at the population level. This biased was reversed (i.e. to the left side) in fish exposed to the elevated-CO2 treatment. Increased temperature attenuated this effect, resulting in lower values of relative lateralization. Consequently, rising temperature and elevated CO2 may have different and interactive effects on behavioural lateralization and therefore future studies on the effect of climate change on brain functions need to consider both these critical variables in order to assess the potential consequences for the ecological interactions of marine fishes.

  • Johnson, M.D., Moriarty, V.W., and Carpenter, R.C.  Acclimatization of the crustose coralline alga Porolithon onkodes to variable pCO2.  PLoS ONE 9(2): art. e87678, 2014.
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    Ocean acidification (OA) has important implications for the persistence of coral reef ecosystems, due to potentially negative effects on biomineralization. Many coral reefs are dynamic with respect to carbonate chemistry, and experience fluctuations in pCO2 that exceed OA projections for the near future. To understand the influence of dynamic pCO2 on an important reef calcifier, we tested the response of the crustose coralline alga Porolithon onkodes to oscillating pCO2. Individuals were exposed to ambient (400 µatm), high (660 µatm), or variable pCO2 (oscillating between 400/660 µatm) treatments for 14 days. To explore the potential for coralline acclimatization, we collected individuals from low and high pCO2 variability sites (upstream and downstream respectively) on a back reef characterized by unidirectional water flow in Moorea, French Polynesia. We quantified the effects of treatment on algal calcification by measuring the change in buoyant weight, and on algal metabolism by conducting sealed incubations to measure rates of photosynthesis and respiration. Net photosynthesis was higher in the ambient treatment than the variable treatment, regardless of habitat origin, and there was no effect on respiration or gross photosynthesis. Exposure to high pCO2 decreased P. onkodes calcification by >70%, regardless of the original habitat. In the variable treatment, corallines from the high variability habitat calcified 42% more than corallines from the low variability habitat. The significance of the original habitat for the coralline calcification response to variable, high pCO2 indicates that individuals existing in dynamic pCO2 habitats may be acclimatized to OA within the scope of in situ variability. These results highlight the importance of accounting for natural pCO2 variability in OA manipulations, and provide insight into the potential for plasticity in habitat and species-specific responses to changing ocean chemistry.

  • Sett, S., Bach, L.T., Schulz, K.G., Koch-Klavsen, S., Lebrato, M., and Riebesell, U.  Temperature modulates coccolithophorid sensitivity of growth, photosynthesis and calcification to increasing seawater pCO2.  PLoS ONE 9(2): art. e88308, 2014.
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    Increasing atmospheric CO2 concentrations are expected to impact pelagic ecosystem functioning in the near future by driving ocean warming and acidification. While numerous studies have investigated impacts of rising temperature and seawater acidification on planktonic organisms separately, little is presently known on their combined effects. To test for possible synergistic effects we exposed two coccolithophore species, Emiliania huxleyi and Gephyrocapsa oceanica, to a CO2 gradient ranging from ~0.5–250 µmol kg-1 (i.e. ~20–6000 µatm pCO2) at three different temperatures (i.e. 10, 15, 20°C for E. huxleyi and 15, 20, 25°C for G. oceanica). Both species showed CO2-dependent optimum-curve responses for growth, photosynthesis and calcification rates at all temperatures. Increased temperature generally enhanced growth and production rates and modified sensitivities of metabolic processes to increasing CO2. CO2 optimum concentrations for growth, calcification, and organic carbon fixation rates were only marginally influenced from low to intermediate temperatures. However, there was a clear optimum shift towards higher CO2 concentrations from intermediate to high temperatures in both species. Our results demonstrate that the CO2 concentration where optimum growth, calcification and carbon fixation rates occur is modulated by temperature. Thus, the response of a coccolithophore strain to ocean acidification at a given temperature can be negative, neutral or positive depending on that strain's temperature optimum. This emphasizes that the cellular responses of coccolithophores to ocean acidification can only be judged accurately when interpreted in the proper eco-physiological context of a given strain or species. Addressing the synergistic effects of changing carbonate chemistry and temperature is an essential step when assessing the success of coccolithophores in the future ocean.

  • Waldbusser, G.G. and Salisbury, J.E.  Ocean acidification in the coastal zone from an organism's perspective: multiple system parameters, frequency domains, and habitats.  Annual Review of Marine Science 6(1): 221-247, 2014.
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    Multiple natural and anthropogenic processes alter the carbonate chemistry of the coastal zone in ways that either exacerbate or mitigate ocean acidification effects. Freshwater inputs and multiple acid–base reactions change carbonate chemistry conditions, sometimes synergistically. The shallow nature of these systems results in strong benthic–pelagic coupling, and marine invertebrates at different life history stages rely on both benthic and pelagic habitats. Carbonate chemistry in coastal systems can be highly variable, responding to processes with temporal modes ranging from seconds to centuries. Identifying scales of variability relevant to levels of biological organization requires a fuller characterization of both the frequency and magnitude domains of processes contributing to or reducing acidification in pelagic and benthic habitats. We review the processes that contribute to coastal acidification with attention to timescales of variability and habitats relevant to marine bivalves.

  • Traving, S.J., Clokie, M.R.J., and Middelboe, M.  Increased acidification has a profound effect on the interactions between the cyanobacterium Synechococcus sp. WH7803 and its viruses.  FEMS Microbiology Ecology 87(1): 133-141, 2014.
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    Increased anthropogenic CO2 emissions are expected to cause a drop in oceanic pH of c. 0.4 units within this century. According to current assessments, the consequences of this are limited for oceanic Cyanobacteria, and absent for viruses. We investigated the effect of pH on the life history of cyanophage S-PM2 and its host, Synechococcus sp. WH7803, at current pH concentrations and at predicted future concentrations. We identified significant negative effects of decreasing pH on Synechococcus growth rate, with profound negative implications for S-PM2 biogenesis and its infection cycle. The duration of the S-PM2 eclipse period increased significantly with decreasing pH. In contrast, the latent period was shorter at pH 7.6 than at pH 8, coinciding with a reduction in S-PM2 burst size from 20.1 ± 3.2 progeny phages per cell at pH 8 to 5.68 ± 4.4 progeny phages per cell at pH 7.6. At pH 7, there was no detectable progeny release. The extracellular stage of S-PM2 was insensitive to pH changes, but sensitive to light, with significant loss in infectivity (0.35–0.38 day-1) at relatively low irradiances (>130 μmol photon m-2 s-1). Overall, the results suggest that pH has significant influence on cyanobacterial growth with important implications for the interactions between Cyanobacteria and their viruses.

  • Sunday, J.M., Calosi, P., Dupont, S., Munday, P.L, Stillman, J.H., and Reusch, T.B.H.  Evolution in an acidifying ocean.  Trends in Ecology & Evolution 29(2): 117-125, 2014.
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    Ocean acidification poses a global threat to biodiversity, yet species might have the capacity to adapt through evolutionary change. Here we summarize tools available to determine species' capacity for evolutionary adaptation to future ocean change and review the progress made to date with respect to ocean acidification. We focus on two key approaches: measuring standing genetic variation within populations and experimental evolution. We highlight benefits and challenges of each approach and recommend future research directions for understanding the modulating role of evolution in a changing ocean.

  • Sewell, M.A., Millar, R.B., Yu, P.C., Kapsenberg, L., and Hofmann, G.E.  Ocean acidification and fertilization in the Antarctic sea urchin Sterechinus neumayeri: the importance of polyspermy.  Environmental Science & Technology 48(1): 713-722, 2014.
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    Ocean acidification (OA), the reduction of the seawater pH as a result of increasing levels of atmospheric CO2, is an important climate change stressor in the Southern Ocean and Antarctic. We examined the impact of OA on fertilization success in the Antarctic sea urchin Sterechinus neumayeri using pH treatment conditions reflective of the current and near-future "pH seascape" for this species: current (control: pH 8.052, 384.1 μatm of pCO2), a high CO2 treatment approximating the 0.2–0.3 unit decrease in pH predicted for 2100 (high CO2: pH 7.830, 666.0 μatm of pCO2), and an intermediate medium CO2 (pH 7.967, 473.4 μatm of pCO2). Using a fertilization kinetics approach and mixed-effect models, we observed significant variation in the OA response between individual male/female pairs (N = 7) and a significant population-level increase (70–100%) in tb (time for a complete block to polyspermy) at medium and high CO2, a mechanism that potentially explains the higher levels of abnormal development seen in OA conditions. However, two pairs showed higher fertilization success with CO2 treatment and a nonsignificant effect. Future studies should focus on the mechanisms and levels of interindividual variability in OA response, so that we can consider the potential for selection and adaptation of organisms to a future ocean.

  • Duarte, C., Navarro, J.M., Acuña, K., Torres, R., Manríquez, P.H., Lardies, M.A., Vargas, C.A., Lagos, N.A., and Aguilera, V.  Combined effects of temperature and ocean acidification on the juvenile individuals of the mussel Mytilus chilensis.  Journal of Sea Research 85: 308-314, 2014.
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    Anthropogenic CO2 emissions have led to increasing global mean temperatures (a process called global warming) and ocean acidification. Because both processes are occurring simultaneously, to better understand their consequences on marine species their combined effects must be experimentally evaluated. The aim of this study was to evaluate for the first time the combined effects of ocean acidification and water temperature increase on the total calcification rate, growth rate and survival of juvenile individuals of the mytilid mussel Mytilus chilensis (Hupe). Two temperature levels (12 and 16 ºC) and three nominal CO2 concentrations (390, 700 and 1000 ppm of CO2) were used. We found that the net rate of calcium deposition and total weight were not significantly affected by temperature, but were negatively affected by the levels of CO2. The interactive effects of temperature and CO2 levels affected only the shell dissolution, but this process was not important for the animal's net calcification. These results suggest that individuals of M. chilensis are able to overcome increased temperatures, but not increments of CO2 levels. It is well known that mussels influence their physical and biological surroundings. Therefore, the negative effects of a CO2 increase could have significant ecological consequences, mainly in those habitats where this group is dominant in terms of abundance and biomass. Finally, taking into account that this species inhabit a wide geographic range, with contrasting environmental conditions (e.g., temperature, salinity and, pH), further studies are needed to evaluate the intraspecific variability in the responses of this species to different environmental stressors.

  • Diaz-Pulido, G., Nash, M.C., Anthony, K.R.N., Bender, D., Opdyke, B.N., Reyes-Nivia, C., and Troitzsch, U.  Greenhouse conditions induce mineralogical changes and dolomite accumulation in coralline algae on tropical reefs.  Nature Communications 5: art. 3310, 2014.
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    Human-induced ocean acidification and warming alter seawater carbonate chemistry reducing the calcification of reef-building crustose coralline algae (CCA), which has implications for reef stability. However, due to the presence of multiple carbonate minerals with different solubilities in seawater, the algal mineralogical responses to changes in carbonate chemistry are poorly understood. Here we demonstrate a 200% increase in dolomite concentration in living CCA under greenhouse conditions of high pCO2 (1,225 µatm) and warming (30 ºC). Aragonite, in contrast, increases with lower pCO2 (296 µatm) and low temperature (28 ºC). Mineral changes in the surface pigmented skeleton are minor and dolomite and aragonite formation largely occurs in the white crust beneath. Dissolution of high-Mg-calcite and particularly the erosive activities of endolithic algae living inside skeletons play key roles in concentrating dolomite in greenhouse treatments. As oceans acidify and warm in the future, the relative abundance of dolomite in CCA will increase.

  • Mattsdotter Björk, M., Fransson, A., Torstensson, A., and Chierici, M.  Ocean acidification state in western Antarctic surface waters: controls and interannual variability.  Biogeosciences 11(1): 57-73, 2014.
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    During four austral summers (December to January) from 2006 to 2010, we investigated the surface-water carbonate system and its controls in the western Antarctic Ocean. Measurements of total alkalinity (AT), pH and total inorganic carbon (CT) were investigated in combination with high-frequency measurements on sea-surface temperature (SST), salinity and Chl a. In all parameters we found large interannual variability due to differences in sea-ice concentration, physical processes and primary production. The main result from our observations suggests that primary production was the major control on the calcium carbonate saturation state (Ω) in austral summer for all years. This was mainly reflected in the covariance of pH and Chl a. In the sea-ice-covered parts of the study area, pH and Ω were generally low, coinciding with low Chl a concentrations. The lowest pH in situ and lowest aragonite saturation (ΩAr ~ 1.0) were observed in December 2007 in the coastal Amundsen and Ross seas near marine outflowing glaciers. These low Ω and high pH values were likely influenced by freshwater dilution. Comparing 2007 and 2010, the largest ΩAr difference was found in the eastern Ross Sea, where ΩAr was about 1.2 units lower in 2007 than in 2010. This was mainly explained by differences in Chl a (i.e primary production). In 2010 the surface water along the Ross Sea shelf was the warmest and most saline, indicating upwelling of nutrient and CO2-rich sub-surface water, likely promoting primary production leading to high Ω and pH. Results from multivariate analysis agree with our observations showing that changes in Chl a had the largest influence on the ΩAr variability. The future changes of ΩAr were estimated using reported rates of the oceanic uptake of anthropogenic CO2, combined with our data on total alkalinity, SST and salinity (summer situation). Our study suggests that the Amundsen Sea will become undersaturated with regard to aragonite about 40 yr sooner than predicted by models.

  • Popova, E.E., Yool, A., Aksenov, Y., Coward, A.C., and Anderson, T.R.  Regional variability of acidification in the Arctic: a sea of contrasts.  Biogeosciences 11(2): 293-308, 2014.
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    The Arctic Ocean is a region that is particularly vulnerable to the impact of ocean acidification driven by rising atmospheric CO2, with potentially negative consequences for calcifying organisms such as coccolithophorids and foraminiferans. In this study, we use an ocean-only general circulation model, with embedded biogeochemistry and a comprehensive description of the ocean carbon cycle, to study the response of pH and saturation states of calcite and aragonite to rising atmospheric pCO2 and changing climate in the Arctic Ocean. Particular attention is paid to the strong regional variability within the Arctic, and, for comparison, simulation results are contrasted with those for the global ocean. Simulations were run to year 2099 using the RCP8.5 (an Inter-governmental Panel on Climate Change (IPCC) Fifth Assessment Report (AR5) scenario with the highest concentrations of atmospheric CO2). The separate impacts of the direct increase in atmospheric CO2 and indirect effects via impact of climate change (changing temperature, stratification, primary production and freshwater fluxes) were examined by undertaking two simulations, one with the full system and the other in which atmospheric CO2 was prevented from increasing beyond its preindustrial level (year 1860). Results indicate that the impact of climate change, and spatial heterogeneity thereof, plays a strong role in the declines in pH and carbonate saturation (Ω) seen in the Arctic. The central Arctic, Canadian Arctic Archipelago and Baffin Bay show greatest rates of acidification and Ω decline as a result of melting sea ice. In contrast, areas affected by Atlantic inflow including the Greenland Sea and outer shelves of the Barents, Kara and Laptev seas, had minimal decreases in pH and Ω because diminishing ice cover led to greater vertical mixing and primary production. As a consequence, the projected onset of undersaturation in respect to aragonite is highly variable regionally within the Arctic, occurring during the decade of 2000–2010 in the Siberian shelves and Canadian Arctic Archipelago, but as late as the 2080s in the Barents and Norwegian seas. We conclude that, for future projections of acidification and carbonate saturation state in the Arctic, regional variability is significant and needs to be adequately resolved, with particular emphasis on reliable projections of the rates of retreat of the sea ice, which are a major source of uncertainty.

  • Hendriks, I.E., Olsen, Y.S., Ramajo, L., Basso, L., Steckbauer, A., Moore, T.S., Howard, J., and Duarte, C.M.  Photosynthetic activity buffers ocean acidification in seagrass meadows.  Biogeosciences 11(2): 333-346, 2014.
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    Macrophytes growing in shallow coastal zones characterised by intense metabolic activity have the capacity to modify pH within their canopy and beyond. We observed diel pH changes in shallow (5–12 m) seagrass (Posidonia oceanica) meadows spanning 0.06 pH units in September to 0.24 units in June. The carbonate system (pH, DIC, and aragonite saturation state (ΩAr)) and O2 within the meadows displayed strong diel variability driven by primary productivity, and changes in chemistry were related to structural parameters of the meadow, in particular, the leaf surface area available for photosynthesis (LAI). LAI was positively correlated to mean, max and range pHNBS and max and range ΩAr. In June, vertical mixing (as Turbulent Kinetic Energy) influenced max and min ΩAr, while in September there was no effect of hydrodynamics on the carbonate system within the canopy. Max and range ΩAr within the meadow showed a positive trend with the calcium carbonate load of the leaves, pointing to a possible link between structural parameters, ΩAr and carbonate deposition. Calcifying organisms, e.g. epiphytes with carbonate skeletons, may benefit from the modification of the carbonate system by the meadow. There is, however, concern for the ability of seagrasses to provide modifications of similar importance in the future. The predicted decline of seagrass meadows may alter the scope for alteration of pH within a seagrass meadow and in the water column above the meadow, particularly if shoot density and biomass decline, on which LAI is based. Organisms associated with seagrass communities may therefore suffer from the loss of pH buffering capacity in degraded meadows.

  • Evans, W., Mathis, J.T., and Cross, J.N.  Calcium carbonate corrosivity in an Alaskan inland sea.  Biogeosciences 11(2): 365-379, 2014.
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    Ocean acidification is the hydrogen ion increase caused by the oceanic uptake of anthropogenic CO2, and is a focal point in marine biogeochemistry, in part, because this chemical reaction reduces calcium carbonate (CaCO3) saturation states (Ω) to levels that are corrosive (i.e., Ω ≤ 1) to shell-forming marine organisms. However, other processes can drive CaCO3 corrosivity; specifically, the addition of tidewater glacial melt. Carbonate system data collected in May and September from 2009 through 2012 in Prince William Sound (PWS), a semienclosed inland sea located on the south-central coast of Alaska and ringed with fjords containing tidewater glaciers, reveal the unique impact of glacial melt on CaCO3 corrosivity. Initial limited sampling was expanded in September 2011 to span large portions of the western and central sound, and included two fjords proximal to tidewater glaciers: Icy Bay and Columbia Bay. The observed conditions in these fjords affected CaCO3 corrosivity in the upper water column (<50 m) in PWS in two ways: (1) as spring-time formation sites of mode water with near-corrosive Ω levels seen below the mixed layer over a portion of the sound, and (2) as point sources for surface plumes of glacial melt with corrosive Ω levels (Ω for aragonite and calcite down to 0.60 and 1.02, respectively) and carbon dioxide partial pressures (pCO2) well below atmospheric levels. CaCO3 corrosivity in glacial melt plumes is poorly reflected by pCO2 or pHT, indicating that either one of these carbonate parameters alone would fail to track Ω in PWS. The unique Ω and pCO2 conditions in the glacial melt plumes enhances atmospheric CO2 uptake, which, if not offset by mixing or primary productivity, would rapidly exacerbate CaCO3 corrosivity in a positive feedback. The cumulative effects of glacial melt and air–sea gas exchange are likely responsible for the seasonal reduction of Ω in PWS, making PWS highly sensitive to increasing atmospheric CO2 and amplified CaCO3 corrosivity.

  • van Hooidonk, R., Maynard, J.A., Manzello, D., and Planes, S.  Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs.  Global Change Biology 20(1): 103-112, 2014.
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    Coral reefs and the services they provide are seriously threatened by ocean acidification and climate change impacts like coral bleaching. Here, we present updated global projections for these key threats to coral reefs based on ensembles of IPCC AR5 climate models using the new Representative Concentration Pathway (RCP) experiments. For all tropical reef locations, we project absolute and percentage changes in aragonite saturation state (Ωarag) for the period between 2006 and the onset of annual severe bleaching (thermal stress >8 degree heating weeks); a point at which it is difficult to believe reefs can persist as we know them. Severe annual bleaching is projected to start 10–15 years later at high-latitude reefs than for reefs in low latitudes under RCP8.5. In these 10–15 years, Ωarag keeps declining and thus any benefits for high-latitude reefs of later onset of annual bleaching may be negated by the effects of acidification. There are no long-term refugia from the effects of both acidification and bleaching. Of all reef locations, 90% are projected to experience severe bleaching annually by 2055. Furthermore, 5% declines in calcification are projected for all reef locations by 2034 under RCP8.5, assuming a 15% decline in calcification per unit of Ωarag. Drastic emissions cuts, such as those represented by RCP6.0, result in an average year for the onset of annual severe bleaching that is ~20 years later (2062 vs. 2044). However, global emissions are tracking above the current worst-case scenario devised by the scientific community, as has happened in previous generations of emission scenarios. The projections here for conditions on coral reefs are dire, but provide the most up-to-date assessment of what the changing climate and ocean acidification mean for the persistence of coral reefs.

  • Chivers, D.P., McCormick, M.I., Nilsson, G.E., Munday, P.L, Watson, S.-A., Meekan, M.G., Mitchell, M.D., Corkill, K.C., and Ferrari, M.C.O.  Impaired learning of predators and lower prey survival under elevated CO2: a consequence of neurotransmitter interference.  Global Change Biology 20(2): 515-522, 2014.
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    Ocean acidification is one of the most pressing environmental concerns of our time, and not surprisingly, we have seen a recent explosion of research into the physiological impacts and ecological consequences of changes in ocean chemistry. We are gaining considerable insights from this work, but further advances require greater integration across disciplines. Here, we showed that projected near-future CO2 levels impaired the ability of damselfish to learn the identity of predators. These effects stem from impaired neurotransmitter function; impaired learning under elevated CO2 was reversed when fish were treated with gabazine, an antagonist of the GABA-A receptor – a major inhibitory neurotransmitter receptor in the brain of vertebrates. The effects of CO2 on learning and the link to neurotransmitter interference were manifested as major differences in survival for fish released into the wild. Lower survival under elevated CO2, as a result of impaired learning, could have a major influence on population recruitment.

  • Eggers, S.L., Lewandowska, A.M., Barcelos e Ramos, J., Blanco-Ameijeiras, S., Gallo, F., and Matthiessen, B.  Community composition has greater impact on the functioning of marine phytoplankton communities than ocean acidification.  Global Change Biology 20(3): 713-723, 2014.
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    Ecosystem functioning is simultaneously affected by changes in community composition and environmental change such as increasing atmospheric carbon dioxide (CO2) and subsequent ocean acidification. However, it largely remains uncertain how the effects of these factors compare to each other. Addressing this question, we experimentally tested the hypothesis that initial community composition and elevated CO2 are equally important to the regulation of phytoplankton biomass. We full-factorially exposed three compositionally different marine phytoplankton communities to two different CO2 levels and examined the effects and relative importance (w²) of the two factors and their interaction on phytoplankton biomass at bloom peak. The results showed that initial community composition had a significantly greater impact than elevated CO2 on phytoplankton biomass, which varied largely among communities. We suggest that the different initial ratios between cyanobacteria, diatoms, and dinoflagellates might be the key for the varying competitive and thus functional outcome among communities. Furthermore, the results showed that depending on initial community composition elevated CO2 selected for larger sized diatoms, which led to increased total phyto-plankton biomass. This study highlights the relevance of initial community composition, which strongly drives the functional outcome, when assessing impacts of climate change on ecosystem functioning. In particular, the increase in phytoplankton biomass driven by the gain of larger sized diatoms in response to elevated CO2 potentially has strong implications for nutrient cycling and carbon export in future oceans.

  • Frieder, C. A., Gonzalez, J. P., Bockmon, E. E., Navarro, M. O., and Levin, L. A.  Can variable pH and low oxygen moderate ocean acidification outcomes for mussel larvae?  Global Change Biology 20(3): 754-764, 2014.
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    Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O2]) levels. In controlled-laboratory experiments we explored the interactive effects of pH, [O2], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis. Survivorship of larvae was unaffected by low pH, low [O2], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH, larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus. Low [O2] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O2] reflective of their environment (80–260 μmol kg-1). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses.

  • Pansch, C., Schaub, I., Havenhand, J., and Wahl, M.  Habitat traits and food availability determine the response of marine invertebrates to ocean acidification.  Global Change Biology 20(3): 765-777, 2014.
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    Energy availability and local adaptation are major components in mediating the effects of ocean acidification (OA) on marine species. In a long-term study, we investigated the effects of food availability and elevated pCO2 (ca. 400, 1000 and 3000μatm) on growth of newly settled Amphibalanus (Balanus) improvisus to reproduction, and on their offspring. We also compared two different populations, which were presumed to differ in their sensitivity to pCO2 due to differing habitat conditions: Kiel Fjord, Germany (Western Baltic Sea) with naturally strong pCO2 fluctuations, and the Tjärnö Archipelago, Sweden (Skagerrak) with far lower fluctuations. Over 20weeks, survival, growth, reproduction and shell strength of Kiel barnacles were all unaffected by elevated pCO2, regardless of food availability. Moulting frequency and shell corrosion increased with increasing pCO2 in adults. Larval development and juvenile growth of the F1 generation were tolerant to increased pCO2, irrespective of parental treatment. In contrast, elevated pCO2 had a strong negative impact on survival of Tjärnö barnacles. Specimens from this population were able to withstand moderate levels of elevated pCO2 over 5weeks when food was plentiful but showed reduced growth under food limitation. Severe levels of elevated pCO2 negatively impacted growth of Tjärnö barnacles in both food treatments. We demonstrate a conspicuously higher tolerance to elevated pCO2 in Kiel barnacles than in Tjärnö barnacles. This tolerance was carried over from adults to their offspring. Our findings indicate that populations from fluctuating pCO2 environments are more tolerant to elevated pCO2 than populations from more stable pCO2 habitats. We furthermore provide evidence that energy availability can mediate the ability of barnacles to withstand moderate CO2 stress. Considering the high tolerance of Kiel specimens and the possibility to adapt over many generations, near future OA alone does not seem to present a major threat for A. improvisus.

  • Chung, W.-S., Marshall, N.J., Watson, S.-A., Munday, P.L., and Nilsson, G.E.  Ocean acidification slows retinal function in a damselfish through interference with GABAA receptors.  Journal of Experimental Biology 217(3): 323-326, 2014.
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    Vision is one of the most efficient senses used by animals to catch prey and avoid predators. Therefore, any deficiency in the visual system could have important consequences for individual performance. We examined the effect of CO2 levels projected to occur by the end of this century on retinal responses in a damselfish, by determining the threshold of its flicker electroretinogram (fERG). The maximal flicker frequency of the retina was reduced by continuous exposure to elevated CO2, potentially impairing the capacity of fish to react to fast events. This effect was rapidly counteracted by treatment with a GABA antagonist (gabazine), indicating that GABAA receptor function is disrupted by elevated CO2. In addition to demonstrating the effects of elevated CO2 on fast flicker fusion of marine fishes, our results show that the fish retina could be a model system to study the effects of high CO2 on neural processing.

  • Rosa, R. et al.  Differential impacts of ocean acidification and warming on winter and summer progeny of a coastal squid (Loligo vulgaris).  Journal of Experimental Biology 217(4): 518-525, 2014.
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    Little is known about the capacity of early life stages to undergo hypercapnic and thermal acclimation under the future scenarios of ocean acidification and warming. Here, we investigated a comprehensive set of biological responses to these climate change-related variables (2°C above winter and summer average spawning temperatures and ΔpH  = 0.5 units) during the early ontogeny of the squid Loligo vulgaris. Embryo survival rates ranged from 92% to 96% under present-day temperature (13–17°C) and pH (8.0) scenarios. Yet, ocean acidification (pH 7.5) and summer warming (19°C) led to a significant drop in the survival rates of summer embryos (47%, P < 0.05). The embryonic period was shortened by increasing temperature in both pH treatments (P < 0.05). Embryo growth rates increased significantly with temperature under present-day scenarios, but there was a significant trend reversal under future summer warming conditions (P < 0.05). Besides pronounced premature hatching, a higher percentage of abnormalities was found in summer embryos exposed to future warming and lower pH (P < 0.05). Under the hypercapnic scenario, oxygen consumption rates decreased significantly in late embryos and newly hatched paralarvae, especially in the summer period (P < 0.05). Concomitantly, there was a significant enhancement of the heat shock response (HSP70/HSC70) with warming in both pH treatments and developmental stages. Upper thermal tolerance limits were positively influenced by acclimation temperature, and such thresholds were significantly higher in late embryos than in hatchlings under present-day conditions (P < 0.05). In contrast, the upper thermal tolerance limits under hypercapnia were higher in hatchlings than in embryos. Thus, we show that the stressful abiotic conditions inside the embryo's capsules will be exacerbated under near-future ocean acidification and summer warming scenarios. The occurrence of prolonged embryogenesis along with lowered thermal tolerance limits under such conditions is expected to negatively affect the survival success of squid early life stages during the summer spawning period, but not winter spawning.

  • Zhang, H., Cheung, S.G., and Shin, P.K.S.  The larvae of congeneric gastropods showed differential responses to the combined effects of ocean acidification, temperature and salinity.  Marine Pollution Bulletin 79(1-2): 39-46, 2014.
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    The tolerance and physiological responses of the larvae of two congeneric gastropods, the intertidal Nassarius festivus and subtidal Nassarius conoidalis, to the combined effects of ocean acidification (pCO2 at 380, 950, 1250 ppm), temperature (15, 30 °C) and salinity (10, 30 psu) were compared. Results of three-way ANOVA on cumulative mortality after 72-h exposure showed significant interactive effects in which mortality increased with pCO2 and temperature, but reduced at higher salinity for both species, with higher mortality being obtained for N. conoidalis. Similarly, respiration rate of the larvae increased with temperature and pCO2 level for both species, with a larger percentage increase for N. conoidalis. Larval swimming speed increased with temperature and salinity for both species whereas higher pCO2 reduced swimming speed in N. conoidalis but not N. festivus. The present findings indicated that subtidal congeneric species are more sensitive than their intertidal counterparts to the combined effects of these stressors.

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