Coral energy reserves and calcification in a high-CO2 world at two temperatures

Rising atmospheric CO2 concentrations threaten coral reefs globally by causing ocean acidification (OA) and warming. Yet, the combined effects of elevated pCO2 and temperature on coral physiology and resilience remain poorly understood. While coral calcification and energy reserves are important health indicators, no studies to date have measured energy reserve pools (i.e., lipid, protein, and carbohydrate) together with calcification under OA conditions under different temperature scenarios. Four coral species, Acropora millepora, Montipora monasteriata, Pocillopora damicornis, Turbinaria reniformis, were reared under a total of six conditions for 3.5 weeks, representing three pCO2 levels (382, 607, 741 µatm), and two temperature regimes (26.5, 29.0°C) within each pCO2 level. After one month under experimental conditions, only A. millepora decreased calcification (-53%) in response to seawater pCO2 expected by the end of this century, whereas the other three species maintained calcification rates even when both pCO2 and temperature were elevated. Coral energy reserves showed mixed responses to elevated pCO2 and temperature, and were either unaffected or displayed nonlinear responses with both the lowest and highest concentrations often observed at the mid-pCO2 level of 607 µatm. Biweekly feeding may have helped corals maintain calcification rates and energy reserves under these conditions. Temperature often modulated the response of many aspects of coral physiology to OA, and both mitigated and worsened pCO2 effects. This demonstrates for the first time that coral energy reserves are generally not metabolized to sustain calcification under OA, which has important implications for coral health and bleaching resilience in a high-CO2 world. Overall, these findings suggest that some corals could be more resistant to simultaneously warming and acidifying oceans than previously expected.

Direct linkage between dimethyl sulfide production and microzooplankton grazing, resulting from prey composition change under high partial pressure of carbon dioxide conditions

Oceanic dimethyl sulfide (DMS) is the enzymatic cleavage product of the algal metabolite dimethylsulfoniopropionate (DMSP) and is the most abundant form of sulfur released into the atmosphere. To investigate the effects of two emerging environmental threats (ocean acidification and warming) on marine DMS production, we performed a large-scale perturbation experiment in a coastal environment. At both ambient temperature and 2 °C warmer, an increase in partial pressure of carbon dioxide (pCO2) in seawater (160-830 ppmv pCO2) favored the growth of large diatoms, which outcompeted other phytoplankton species in a natural phytoplankton assemblage and reduced the growth rate of smaller, DMSP-rich phototrophic dinoflagellates. This decreased the grazing rate of heterotrophic dinoflagellates (ubiquitous micrograzers), resulting in reduced DMS production via grazing activity. Both the magnitude and sign of the effect of pCO2 on possible future oceanic DMS production were strongly linked to pCO2-induced alterations to the phytoplankton community and the cellular DMSP content of the dominant species and its association with micrograzers.

The swimming kinematics of larval Atlantic cod, Gadus morhua L., are resilient to elevated seawater pCO2

Kinematics of swimming behavior of larval Atlantic cod, aged 12 and 27 days post-hatch (dph) and cultured under three pCO2 conditions (control-370, medium-1800, and high-4200 µatm) from March to May 2010, were extracted from swim path recordings obtained using silhouette video photography. The swim paths were analyzed for swim duration, distance and speed, stop duration, and horizontal and vertical turn angles to determine whether elevated seawater pCO2-at beyond near-future ocean acidification levels-affects the swimming kinematics of Atlantic cod larvae. There were no significant differences in most of the variables tested: the swimming kinematics of Atlantic cod larvae at 12 and 27 dph were highly resilient to extremely elevated pCO2 levels. Nonetheless, cod larvae cultured at the highest pCO2 concentration displayed vertical turn angles that were more restricted (median turn angle, 15°) than larvae in the control (19°) and medium (19°) treatments at 12 dph (but not at 27 dph). Significant reduction in the stop duration of cod larvae from the high treatment (median stop duration, 0.28 s) was also observed compared to the larvae from the control group (0.32 s) at 27 dph (but not at 12 dph). The functional and ecological significance of these subtle differences are unclear and, therefore, require further investigation in order to determine whether they are ecologically relevant or spurious.

Short-term metabolic and growth responses of the cold-water coral lophelia pertusa to ocean acidification

Cold-water corals are amongst the most three-dimensionally complex deep-sea habitats known and are associated with high local biodiversity. Despite their importance as ecosystem engineers, little is known about how these organisms will respond to projected ocean acidification. Since preindustrial times, average ocean pH has already decreased from 8.2 to ~ 8.1. Predicted CO2 emissions will decrease this by up to another 0.3 pH units by the end of the century. This decrease in pH may have a wide range of impacts upon marine life, and in particular upon calcifiers such as cold-water corals. Lophelia pertusa is the most widespread cold-water coral (CWC) species, frequently found in the North Atlantic. Data here relate to a short term data set (21 days) on metabolism and net calcification rates of freshly collected L. pertusa from Mingulay Reef Complex, Scotland. These data from freshly collected L. pertusa from the Mingulay Reef Complex will help define the impact of ocean acidification upon the growth, physiology and structural integrity of this key reef framework forming species.

Physiological and ecological variables measured at the high and low pCO2 reef sections

Experiments have shown that ocean acidification due to rising atmospheric carbon dioxide concentrations has deleterious effects on the performance of many marine organisms. However, few empirical or modelling studies have addressed the long-term consequences of ocean acidification for marine ecosystems. Here we show that as pH declines from 8.1 to 7.8 (the change expected if atmospheric carbon dioxide concentrations increase from 390 to 750 ppm, consistent with some scenarios for the end of this century) some organisms benefit, but many more lose out. We investigated coral reefs, seagrasses and sediments that are acclimatized to low pH at three cool and shallow volcanic carbon dioxide seeps in Papua New Guinea. At reduced pH, we observed reductions in coral diversity, recruitment and abundances of structurally complex framework builders, and shifts in competitive interactions between taxa. However, coral cover remained constant between pH 8.1 and ~7.8, because massive Porites corals established dominance over structural corals, despite low rates of calcification. Reef development ceased below pH 7.7. Our empirical data from this unique field setting confirm model predictions that ocean acidification, together with temperature stress, will probably lead to severely reduced diversity, structural complexity and resilience of Indo-Pacific coral reefs within this century.

Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions

Dissolution of anthropogenic CO(2) increases the partial pressure of CO(2) (pCO(2)) and decreases the pH of seawater. The rate of Fe uptake by the dominant N(2)-fixing cyanobacterium Trichodesmium declines as pH decreases in metal-buffered medium. The slower Fe-uptake rate at low pH results from changes in Fe chemistry and not from a physiological response of the organism. Contrary to previous observations in nutrient-replete media, increasing pCO(2)/decreasing pH causes a decrease in the rates of N(2) fixation and growth in Trichodesmium under low-Fe conditions. This result was obtained even though the bioavailability of Fe was maintained at a constant level by increasing the total Fe concentration at low pH. Short-term experiments in which pCO(2) and pH were varied independently showed that the decrease in N(2) fixation is caused by decreasing pH rather than by increasing pCO(2) and corresponds to a lower efficiency of the nitrogenase enzyme. To compensate partially for the loss of N(2) fixation efficiency at low pH, Trichodesmium synthesizes additional nitrogenase. This increase comes partly at the cost of down-regulation of Fe-containing photosynthetic proteins. Our results show that although increasing pCO(2) often is beneficial to photosynthetic marine organisms, the concurrent decreasing pH can affect primary producers negatively. Such negative effects can occur both through chemical mechanisms, such as the bioavailability of key nutrients like Fe, and through biological mechanisms, as shown by the decrease in N(2) fixation in Fe-limited Trichodesmium.

The impact of fluctuating light on the dinoflagellate Prorocentrum micans depends on NO3- and CO2 availability

Increasing atmospheric pCO2 and its dissolution into oceans leads to ocean acidification and warming, which reduces the thickness of upper mixing layer (UML) and upward nutrient supply from deeper layers. These events may alter the nutritional conditions and the light regime to which primary producers are exposed in the UML. In order to better understand the physiology behind the responses to the concomitant climate changes factors, we examined the impact of light fluctuation on the dinoflagellate Prorocentrum micans grown at low (1 µmol/L) or high (800 µmol/L) [NO3(-)] and at high (1000 µatm) or low (390 µatm, ambient) pCO2. The light regimes to which the algal cells were subjected were (1) constant light at a photon flux density (PFD) of either 100 (C100) or 500 (C500) µmol/m**2/s or (2) fluctuating light between 100 or 500 µmol photons/m**2/s with a frequency of either 15 (F15) or 60 (F60) min. Under continuous light, the initial portion of the light phase required the concomitant presence of high CO2 and NO3(-) concentrations for maximum growth. After exposure to light for 3h, high CO2 exerted a negative effect on growth and effective quantum yield of photosystem II (F'(v)/F'(m)). Fluctuating light ameliorated growth in the first period of illumination. In the second 3h of treatment, higher frequency (F15) of fluctuations afforded high growth rates, whereas the F60 treatment had detrimental consequences, especially when NO3(-) concentration was lower. F'(v)/F'(m) respondent differently from growth to fluctuating light: the fluorescence yield was always lower than at continuous light at 100 µmol/m**2/s, and always higher at 500 µmol/m**2/s. Our data show that the impact of atmospheric pCO2 increase on primary production of dinoflagellate depends on the availability of nitrate and the irradiance (intensity and the frequency of irradiance fluctuations) to which the cells are exposed. The impact of global change on oceanic primary producers would therefore be different in waters with different chemical and physical (mixing) properties.

Pteropod eggs released at high pCO2 lack resilience to ocean acidification

The effects of ocean acidification (OA) on the early recruitment of pteropods in the Scotia Sea, was investigated considering the process of spawning, quality of the spawned eggs and their capacity to develop. Maternal OA stress was induced on female pteropods (Limacina helicina antarctica) through exposure to present day pCO2 conditions and two potential future OA states (750??atm and 1200??atm). The eggs spawned from these females, both before and during their exposure to OA, were incubated themselves in this same range of conditions (embryonic OA stress). Maternal OA stress resulted in eggs with lower carbon content, while embryonic OA stress retarded development. The combination of maternal and embryonic OA stress reduced the percentage of eggs successfully reaching organogenesis by 80%. We propose that OA stress not only affects the somatic tissue of pteropods but also the functioning of their gonads. Corresponding in-situ sampling found that post-larval L. helicina antarctica concentrated around 600?m depth, which is deeper than previously assumed. A deeper distribution makes their exposure to waters undersaturated for aragonite more likely in the near future given that these waters are predicted to shoal from depth over the coming decades.

Ocean acidification affects the phyto-zoo plankton trophic transfer efficiency

The critical role played by copepods in ocean ecology and biogeochemistry warrants an understanding of how these animals may respond to ocean acidification (OA). Whilst an appreciation of the potential direct effects of OA, due to elevated pCO2, on copepods is improving, little is known about the indirect impacts acting via bottom-up(food quality) effects. We assessed, for the first time, the chronic effects of direct and/or indirect exposures to elevated pCO2 on the behaviour, vital rates, chemical and biochemical stoichiometry of the calanoid copepod Acartia tonsa. Bottom-up effects of elevated pCO2 caused species-specific biochemical changes to the phytoplanktonic feed, which adversely affected copepod population structure and decreased recruitment by 30 %. The direct impact of elevated pCO2 caused gender-specific respiratory responses in A.tonsa adults, stimulating an enhanced respiration rate in males (> 2-fold), and a suppressed respiratory response in females when coupled with indirect elevated pCO2 exposures. Under the combined indirect+direct exposure, carbon trophic transfer efficiency from phytoplankton-to-zooplankton declined to < 50 % of control populations, with a commensurate decrease in recruitment. For the first time an explicit role was demonstrated for biochemical stoichiometry in shaping copepod trophic dynamics. The altered biochemical composition of the CO2-exposed prey affected the biochemical stoichiometry of the copepods, which could have ramifications for production of higher tropic levels, notably fisheries. Our work indicates that the control of phytoplankton and the support of higher trophic levels involving copepods have clear potential to be adversely affected under future OA scenarios.

Ocean acidification and the loss of phenolic substances in marine plants

Rising atmospheric CO2 often triggers the production of plant phenolics, including many that serve as herbivore deterrents, digestion reducers, antimicrobials, or ultraviolet sunscreens. Such responses are predicted by popular models of plant defense, especially resource availability models which link carbon availability to phenolic biosynthesis. CO2 availability is also increasing in the oceans, where anthropogenic emissions cause ocean acidification, decreasing seawater pH and shifting the carbonate system towards further CO2 enrichment. Such conditions tend to increase seagrass productivity but may also increase rates of grazing on these marine plants. Here we show that high CO2 / low pH conditions of OA decrease, rather than increase, concentrations of phenolic protective substances in seagrasses and eurysaline marine plants. We observed a loss of simple and polymeric phenolics in the seagrass Cymodocea nodosa near a volcanic CO2 vent on the Island of Vulcano, Italy, where pH values decreased from 8.1 to 7.3 and pCO2 concentrations increased ten-fold. We observed similar responses in two estuarine species, Ruppia maritima and Potamogeton perfoliatus, in in situ Free-Ocean-Carbon-Enrichment experiments conducted in tributaries of the Chesapeake Bay, USA. These responses are strikingly different than those exhibited by terrestrial plants. The loss of phenolic substances may explain the higher-than-usual rates of grazing observed near undersea CO2 vents and suggests that ocean acidification may alter coastal carbon fluxes by affecting rates of decomposition, grazing, and disease. Our observations temper recent predictions that seagrasses would necessarily be "winners" in a high CO2 world.

Nutrient availability affects the response of the calcifying chlorophyte Halimeda opuntia (L.) J.V. Lamouroux to low pH

Atmospheric carbon dioxide emissions cause a decrease in the pH and aragonite saturation state of surface ocean water. As a result, calcifying organisms are expected to suffer under future ocean conditions, but their physiological responses may depend on their nutrient status. Because many coral reefs experience high inorganic nutrient loads or seasonal changes in nutrient availability, reef organisms in localized areas will have to cope with elevated carbon dioxide and changes in inorganic nutrients. Halimeda opuntia is a dominant calcifying primary producer on coral reefs that contributes to coral reef accretion. Therefore, we investigated the carbon and nutrient balance of H. opuntia exposed to elevated carbon dioxide and inorganic nutrients. We measured tissue nitrogen, phosphorus and carbon content as well as the activity of enzymes involved in inorganic carbon uptake and nitrogen assimilation (external carbonic anhydrase and nitrate reductase, respectively). Inorganic carbon content was lower in algae exposed to high CO2, but calcification rates were not significantly affected by CO2 or inorganic nutrients. Organic carbon was positively correlated to external carbonic anhydrase activity, while inorganic carbon showed the opposite correlation. Carbon dioxide had a significant effect on tissue nitrogen and organic carbon content, while inorganic nutrients affected tissue phosphorus and N:P ratios. Nitrate reductase activity was highest in algae grown under elevated CO2 and inorganic nutrient conditions and lowest when phosphate was limiting. In general, we found that enzymatic responses were strongly influenced by nutrient availability, indicating its important role in dictating the local responses of the calcifying primary producer H. opuntia to ocean acidification.

Seawater carbonate chemistry and settlement of a spawning coral on three common species of crustose coralline algae

Concern about the impacts of ocean acidification (OA) on ecosystem function has prompted many studies to focus on larval recruitment, demonstrating declines in settlement and early growth at elevated CO2 concentrations. Since larval settlement is often driven by particular cues governed by crustose coralline algae (CCA), it is important to determine whether OA reduces larval recruitment with specific CCA and the generality of any effects. We tested the effect of elevated CO2 on the survival and settlement of larvae from the common spawning coral Acropora selago with 3 ecologically important species of CCA, Porolithon onkodes, Sporolithon sp., and Titanoderma sp. After 3 d in no-choice laboratory assays at 447, 705, and 1214 µatm pCO2, the rates of coral settlement declined as pCO2 increased with all CCA taxa. The magnitude of the effect was highest with Titanoderma sp., decreasing by 87% from the ambient to highest CO2 treatment. In general, there were high rates of larval mortality, which were greater with the P. onkodes and Sporolithon sp. treatments (~80%) compared to the Titanoderma sp. treatment (65%). There was an increase in larval mortality as pCO2 increased, but this was variable among the CCA species. It appears that OA reduces coral settlement by rapidly altering the chemical cues associated with the CCA thalli and microbial community, and potentially by directly affecting larval viability.

Seawater carbonate chemistry and net photosynthesis, C/N ratio, growth rate, size of Ostreococcus tauri in a laboratory experiment

Phytoplankton are the basis of marine food webs, and affect biogeochemical cycles. As CO2 levels increase, shifts in the frequencies and physiology of ecotypes within phytoplankton groups will affect their nutritional value and biogeochemical function. However, studies so far are based on a few representative genotypes from key species. Here, we measure changes in cellular function and growth rate at atmospheric CO2 concentrations predicted for the year 2100 in 16 ecotypes of the marine picoplankton Ostreococcus. We find that variation in plastic responses among ecotypes is on par with published between-genera variation, so the responses of one or a few ecotypes cannot estimate changes to the physiology or composition of a species under CO2 enrichment. We show that ecotypes best at taking advantage of CO2 enrichment by changing their photosynthesis rates most should increase in relative fitness, and so in frequency in a high-CO2 environment. Finally, information on sampling location, and not phylogenetic relatedness, is a good predictor of ecotypes likely to increase in frequency in this system.

Interactive effects of ocean acidification and nitrogen limitation on the diatom Phaeodactylum tricornutum

Climate change is expected to bring about alterations in the marine physical and chemical environment that will induce changes in the concentration of dissolved CO2 and in nutrient availability. These in turn are expected to affect the physiological performance of phytoplankton. In order to learn how phytoplankton respond to the predicted scenario of increased CO2 and decreased nitrogen in the surface mixed layer, we investigated the diatom Phaeodactylum tricornutum as a model organism. The cells were cultured in both low CO2 (390 µatm) and high CO2 (1000 µatm) conditions at limiting (10 µmol/L) or enriched (110 µmol/L) nitrate concentrations. Our study shows that nitrogen limitation resulted in significant decreases in cell size, pigmentation, growth rate and effective quantum yield of Phaeodactylum tricornutum, but these parameters were not affected by enhanced dissolved CO2 and lowered pH. However, increased CO2 concentration induced higher rETRmax and higher dark respiration rates and decreased the CO2 or dissolved inorganic carbon (DIC) affinity for electron transfer (shown by higher values for K1/2 DIC or K1/2 CO2). Furthermore, the elemental stoichiometry (carbon to nitrogen ratio) was raised under high CO2 conditions in both nitrogen limited and nitrogen replete conditions, with the ratio in the high CO2 and low nitrate grown cells being higher by 45% compared to that in the low CO2 and nitrate replete grown ones. Our results suggest that while nitrogen limitation had a greater effect than ocean acidification, the combined effects of both factors could act synergistically to affect marine diatoms and related biogeochemical cycles in future oceans.

Adaptation of a globally important coccolithophore to ocean warming and acidification

Regulating intracellular pH (pHi) is critical for optimising the metabolic activity of corals, yet mechanisms involved in pH regulation and the buffering capacity within coral cells are not well understood. Our study investigated how the presence of symbiotic dinoflagellates affects the response of pHi to pCO2-driven seawater acidification in cells isolated from Pocillopora damicornis. Using the fluorescent dye BCECF-AM, in conjunction with confocal microscopy, we simultaneously characterised the response of pHi in host coral cells and their dinoflagellate symbionts, in symbiotic and non-symbiotic states under saturating light, with and without the photosynthetic inhibitor DCMU. Each treatment was run under control (pH 7.8) and CO2 acidified seawater conditions (decreasing pH from 7.8 - 6.8). After two hours of CO2 addition, by which time the external pH (pHe) had declined to 6.8, the dinoflagellate symbionts had increased their pHi by 0.5 pH units above control levels. In contrast, in both symbiotic and non-symbiotic host coral cells, 15 min of CO2 addition (0.2 pH unit drop in pHe) led to cytoplasmic acidosis equivalent to 0.4 pH units. Despite further seawater acidification over the duration of the experiment, the pHi of non-symbiotic coral cells did not change, though in host cells containing a symbiont cell the pHi recovered to control levels. This recovery was negated when cells were incubated with DCMU. Our results reveal that photosynthetic activity of the endosymbiont is tightly coupled with the ability of the host cell to recover from cellular acidosis after exposure to high CO2 / low pH.