Effects of feeding and light intensity on the response of the coral Porites rus to ocean acidification

Recently, it has been suggested that there are conditions under which some coral species appear to be resistant to the effects of ocean acidification. To test if such resistance can be explained by environmental factors such as light and food availability, the present study investigated the effect of 3 feeding regimes crossed with 2 light levels on the response of the coral Porites rus to 2 levels of pCO2 at 28 °C. After 1, 2, and 3 weeks of incubation under experimental conditions, none of the factors-including pCO2-significantly affected area-normalized calcification and biomass-normalized calcification. Biomass also was unaffected during the first 2 weeks, but after 3 weeks, corals that were fed had more biomass per unit area than starved corals. These results suggest that P. rus is resistant to short-term exposure to high pCO2, regardless of food availability and light intensity. P. rus might therefore represent a model system for exploring the genetic basis of tolerance to OA.

Growth response of an early successional assemblage of coralline algae and benthic diatoms to ocean acidification

The sustained absorption of anthropogenically released atmospheric CO2 by the oceans is modifying seawater carbonate chemistry, a process termed ocean acidification (OA). By the year 2100, the worst case scenario is a decline in the average oceanic surface seawater pH by 0.3 units to 7.75. The changing seawater carbonate chemistry is predicted to negatively affect many marine species, particularly calcifying organisms such as coralline algae, while species such as diatoms and fleshy seaweed are predicted to be little affected or may even benefit from OA. It has been hypothesized in previous work that the direct negative effects imposed on coralline algae, and the direct positive effects on fleshy seaweeds and diatoms under a future high CO2 ocean could result in a reduced ability of corallines to compete with diatoms and fleshy seaweed for space in the future. In a 6-week laboratory experiment, we examined the effect of pH 7.60 (pH predicted to occur due to ocean acidification just beyond the year 2100) compared to pH 8.05 (present day) on the lateral growth rates of an early successional, cold-temperate species assemblage dominated by crustose coralline algae and benthic diatoms. Crustose coralline algae and benthic diatoms maintained positive growth rates in both pH treatments. The growth rates of coralline algae were three times lower at pH 7.60, and a non-significant decline in diatom growth meant that proportions of the two functional groups remained similar over the course of the experiment. Our results do not support our hypothesis that benthic diatoms will outcompete crustose coralline algae under future pH conditions. However, while crustose coralline algae were able to maintain their presence in this benthic rocky reef species assemblage, the reduced growth rates suggest that they will be less capable of recolonizing after disturbance events, which could result in reduced coralline cover under OA conditions.

Nutrient availability affects the response of juvenile corals and the endosymbionts to ocean acidification

The interactive effects of nutrient availability and ocean acidification on coral calcification were investigated using post-settlement juvenile corals of Acropora digitifera cultured in nutrient-sufficient or nutrient-depleted seawater for 4 d and then exposed to seawater with different partial pressure of carbon dioxide () conditions (38.8 or 92.5 Pa) for 10 d. After the nutrient pretreatment, corals in the high nutrient condition (HN corals) had a significantly higher abundance of endosymbiotic algae than did those in the low nutrient condition (LN corals). The high abundance of endosymbionts in HN corals was reduced as a result of subsequent seawater acidification, and the chlorophyll a per algal cell increased. The photosynthetic oxygen production rate by endosymbionts was enhanced by the acidified seawater regardless of the nutrient treatment, indicating that the reduction in endosymbiont density in HN corals due to acidification was compensated for by the increase in chlorophyll a per cell. Though the photosynthetic rate increased in the acidified conditions for both LN and HN corals, the calcification rate significantly decreased for LN corals but not for HN corals. The acquisition of nutrients from seawater, rather than the increase in alkalinity caused by photosynthesis, might effectively alleviate the negative response of coral calcification to seawater acidification, suggesting that the response of corals and their endosymbionts to ocean acidification can be influenced by nutrient conditions.

Response of benthic foraminifera to ocean acidification in their natural sediment environment: a long-term culturing experiment

Calcifying foraminifera are expected to be endangered by ocean acidification; however, the response of a complete community kept in natural sediment and over multiple generations under controlled laboratory conditions has not been constrained to date. During 6 months of incubation, foraminiferal assemblages were kept and treated in natural sediment with pCO2-enriched seawater of 430, 907, 1865 and 3247 µatm pCO2. The fauna was dominated by Ammonia aomoriensis and Elphidium species, whereas agglutinated species were rare. After 6 months of incubation, pore water alkalinity was much higher in comparison to the overlying seawater. Consequently, the saturation state of Omega calc was much higher in the sediment than in the water column in nearly all pCO2 treatments and remained close to saturation. As a result, the life cycle (population density, growth and reproduction) of living assemblages varied markedly during the experimental period, but was largely unaffected by the pCO2 treatments applied. According to the size-frequency distribution, we conclude that foraminifera start reproduction at a diameter of 250 µm. Mortality of living Ammonia aomoriensis was unaffected, whereas size of large and dead tests decreased with elevated pCO2 from 285 µm (pCO2 from 430 to 1865 µatm) to 258 µm (pCO2 3247 µatm). The total organic content of living Ammonia aomoriensis has been determined to be 4.3% of CaCO3 weight. Living individuals had a calcium carbonate production rate of 0.47 g/m**2/a, whereas dead empty tests accumulated a rate of 0.27 g /m**2/a. Although Omega calc was close to 1, approximately 30% of the empty tests of Ammonia aomoriensis showed dissolution features at high pCO2 of 3247 µatm during the last 2 months of incubation. In contrast, tests of the subdominant species, Elphidium incertum, stayed intact. Our results emphasize that the sensitivity to ocean acidification of the endobenthic foraminifera Ammonia aomoriensis in their natural sediment habitat is much lower compared to the experimental response of specimens isolated from the sediment.

Bioturbation determines the response of benthic ammonia-oxidizing microorganisms to ocean acidification

Ocean acidification (OA), caused by the dissolution of increasing concentrations of atmospheric carbon dioxide (CO2) in seawater, is projected to cause significant changes to marine ecology and biogeochemistry. Potential impacts on the microbially driven cycling of nitrogen are of particular concern. Specifically, under seawater pH levels approximating future OA scenarios, rates of ammonia oxidation (the rate-limiting first step of the nitrification pathway) have been shown to dramatically decrease in seawater, but not in underlying sediments. However, no prior study has considered the interactive effects of microbial ammonia oxidation and macrofaunal bioturbation activity, which can enhance nitrogen transformation rates. Using experimental mesocosms, we investigated the responses to OA of ammonia oxidizing microorganisms inhabiting surface sediments and sediments within burrow walls of the mud shrimp Upogebia deltaura. Seawater was acidified to one of four target pH values (pHT 7.90, 7.70, 7.35 and 6.80) in comparison with a control (pHT 8.10). At pHT 8.10, ammonia oxidation rates in burrow wall sediments were, on average, fivefold greater than in surface sediments. However, at all acidified pH values (pH < = 7.90), ammonia oxidation rates in burrow sediments were significantly inhibited (by 79-97%; p < 0.01), whereas rates in surface sediments were unaffected. Both bacterial and archaeal abundances increased significantly as pHT declined; by contrast, relative abundances of bacterial and archaeal ammonia oxidation (amoA) genes did not vary. This research suggests that OA could cause substantial reductions in total benthic ammonia oxidation rates in coastal bioturbated sediments, leading to corresponding changes in coupled nitrogen cycling between the benthic and pelagic realms.

Ocean acidification mediates photosynthetic response to UV radiation and temperature increase in the diatom Phaeodactylum tricornutum

Increasing atmospheric CO2 concentration is responsible for progressive ocean acidification, ocean warming as well as decreased thickness of upper mixing layer (UML), thus exposing phytoplankton cells not only to lower pH and higher temperatures but also to higher levels of solar UV radiation. In order to evaluate the combined effects of ocean acidification, UV radiation and temperature, we used the diatom Phaeodactylum tricornutum as a model organism and examined its physiological performance after grown under two CO2 concentrations (390 and 1000 µatm) for more than 20 generations. Compared to the ambient CO2 level (390 µatm), growth at the elevated CO2 concentration increased non-photochemical quenching (NPQ) of cells and partially counteracted the harm to PS II (photosystem II) caused by UV-A and UV-B. Such an effect was less pronounced under increased temperature levels. The ratio of repair to UV-B induced damage decreased with increased NPQ, reflecting induction of NPQ when repair dropped behind the damage, and it was higher under the ocean acidification condition, showing that the increased pCO2 and lowered pH counteracted UV-B induced harm. As for photosynthetic carbon fixation rate which increased with increasing temperature from 15 to 25 °C, the elevated CO2 and temperature levels synergistically interacted to reduce the inhibition caused by UV-B and thus increase the carbon fixation.

The modulating effect of light intensity on the response of the coccolithophore Gephyrocapsa oceanica to ocean acidification

Global change leads to a multitude of simultaneous modifications in the marine realm among which shoaling of the upper mixed layer, leading to enhanced surface layer light intensities, as well as increased carbon dioxide (CO2) concentration are some of the most critical environmental alterations for phytoplankton. In this study, we investigated the responses of growth, photosynthetic carbon fixation and calcification of the coccolithophore Gephyrocapsa oceanica to elevated inline image (51 Pa, 105 Pa, and 152 Pa) (1 Pa ~ 10 µatm) at a variety of light intensities (50-800 µmol photons/m**2/s). By fitting the light response curve, our results showed that rising inline image reduced the maximum rates for growth, photosynthetic carbon fixation and calcification. Increasing light intensity enhanced the sensitivity of these rate responses to inline image, and shifted the inline image optima toward lower levels. Combining the results of this and a previous study (Sett et al. 2014) on the same strain indicates that both limiting low inline image and inhibiting high inline image levels (this study) induce similar responses, reducing growth, carbon fixation and calcification rates of G. oceanica. At limiting low light intensities the inline image optima for maximum growth, carbon fixation and calcification are shifted toward higher levels. Interacting effects of simultaneously occurring environmental changes, such as increasing light intensity and ocean acidification, need to be considered when trying to assess metabolic rates of marine phytoplankton under future ocean scenarios.

Sea urchin response to rising pCO2 shows ocean acidification may fundamentally alter the chemistry of marine skeletons

Ocean acidification caused by an increase in pCO2 is expected to drastically affect marine ecosystem composition, yet there is much uncertainty about the mechanisms through which ecosystems may be affected. Here we studied sea urchins that are common and important grazers in the Mediterranean (Paracentrotus lividus and Arbacia lixula). Our study included a natural CO2 seep plus reference sites in the Aegean Sea off Greece. The distribution of A. lixula was unaffected by the low pH environment, whereas densities of P. lividus were much reduced. There was skeletal degradation in both species living in acidified waters compared to reference sites and remarkable increases in skeletal manganese levels (P. lividus had a 541% increase, A. lixula a 243% increase), presumably due to changes in mineral crystalline structure. Levels of strontium and zinc were also altered. It is not yet known whether such dramatic changes in skeletal chemistry will affect coastal systems but our study reveals a mechanism that may alter inter-species interactions.

Skeletal trade-offs in coralline algae in response to ocean acidification

Ocean acidification is changing the marine environment, with potentially serious consequences for many organisms. Much of our understanding of ocean acidification effects comes from laboratory experiments, which demonstrate physiological responses over relatively short timescales. Observational studies and, more recently, experimental studies in natural systems suggest that ocean acidification will alter the structure of seaweed communities. Here, we provide a mechanistic understanding of altered competitive dynamics among a group of seaweeds, the crustose coralline algae (CCA). We compare CCA from historical experiments (1981-1997) with specimens from recent, identical experiments (2012) to describe morphological changes over this time period, which coincides with acidification of seawater in the Northeastern Pacific. Traditionally thick species decreased in thickness by a factor of 2.0-2.3, but did not experience a change in internal skeletal metrics. In contrast, traditionally thin species remained approximately the same thickness but reduced their total carbonate tissue by making thinner inter-filament cell walls. These changes represent alternative mechanisms for the reduction of calcium carbonate production in CCA and suggest energetic trade-offs related to the cost of building and maintaining a calcium carbonate skeleton as pH declines. Our classification of stress response by morphological type may be generalizable to CCA at other sites, as well as to other calcifying organisms with species-specific differences in morphological types.

Ocean acidification weakens the immune response of blood clam through hampering the NF-kappa beta and toll-like receptor pathways

The impact of pCO2 driven ocean acidification on marine bivalve immunity remains poorly understood. To date, this impact has only been investigated in a few bivalve species and the underlying molecular mechanism remains unknown. In the present study, the effects of the realistic future ocean pCO2 levels (pH at 8.1, 7.8, and 7.4) on the total number of haemocyte cells (THC), phagocytosis status, blood cell types composition, and expression levels of twelve genes from the NF-kappa beta signaling and toll-like receptor pathways of a typical bottom burrowing bivalve, blood clam (Tegillarca granosa), were investigated. The results obtained showed that while both THC number and phagocytosis frequency were significantly reduced, the percentage of red and basophil granulocytes were significantly decreased and increased, respectively, upon exposure to elevated pCO2. In addition, exposure to pCO2 acidified seawater generally led to a significant down-regulation in the inducer and key response genes of NF-kappa beta signaling and toll-like receptor pathways. The results of the present study revealed that ocean acidification may hamper immune responses of the bivalve T. granosa which subsequently render individuals more susceptible to pathogens attacks such as those from virus and bacteria.

Bioenergetic trade-offs in the sea cucumber Apostichopus japonicus (Echinodermata: Holothuroidea) in response to CO2-driven ocean acidification

Ocean acidification (OA) caused by excessive CO2 is a potential ecological threat to marine organisms. The impacts of OA on echinoderms are well-documented, but there has been a strong bias towards sea urchins, and limited information is available on sea cucumbers. This work examined the effect of medium-term (60 days) exposure to three pH levels (pH 8.06, 7.72, and 7.41, covering present and future pH variability) on the bioenergetic responses of the sea cucumber, Apostichopus japonicus, an ecologically and economically important holothurian in Asian coasts. Results showed that the measured specific growth rate linearly decreased with decreased pH, leading to a 0.42 %/day decrease at pH 7.41 compared with that at pH 8.06. The impacts of pH on physiological energetics were variable: measured energy consumption and defecation rates linearly decreased with decreased pH, whereas maintenance energy in calculated respiration and excretion were not significantly affected. No shift in energy allocation pattern was observed in A. japonicus upon exposure to pH 7.72 compared with pH 8.06. However, a significant shift in energy budget occurred upon exposure to pH 7.41, leading to decreased energy intake and increased percentage of energy that was lost in feces, thereby resulting in a significantly lowered allocation into somatic growth. These findings indicate that adult A. japonicus is resilient to the OA scenario at the end of the twenty-first century, but further acidification may negatively influence the grazing capability and growth, thereby influencing its ecological functioning as an "ecosystem engineer" and potentially harming its culture output.

Differential response of two Mediterranean cold-water coral species to ocean acidification

Cold-water coral (CWC) reefs constitute one of the most complex deep-sea habitats harboring a vast diversity of associated species. Like other tropical or temperate framework builders, these systems are facing an uncertain future due to several threats, such as global warming and ocean acidification. In the case of Mediterranean CWC communities, the effect may be exacerbated due to the greater capacity of these waters to absorb atmospheric CO2 compared to the global ocean. Calcification in these organisms is an energy-demanding process, and it is expected that energy requirements will be greater as seawater pH and the availability of carbonate ions decrease. Therefore, studies assessing the effect of a pH decrease in skeletal growth, and metabolic balance are critical to fully understand the potential responses of these organisms under a changing scenario. In this context, the present work aims to investigate the medium- to long-term effect of a low pH scenario on calcification and the biochemical composition of two CWCs from the Mediterranean, Dendrophyllia cornigera and Desmophyllum dianthus. After 314 d of exposure to acidified conditions, a significant decrease of 70 % was observed in Desmophyllum dianthus skeletal growth rate, while Dendrophyllia cornigera showed no differences between treatments. Instead, only subtle differences between treatments were observed in the organic matter amount, lipid content, skeletal microdensity, or porosity in both species, although due to the high variability of the results, these differences were not statistically significant. Our results also confirmed a heterogeneous effect of low pH on the skeletal growth rate of the organisms depending on their initial weight, suggesting that those specimens with high calcification rates may be the most susceptible to the negative effects of acidification.

Physiological response of the cold-water coral Desmophyllum dianthus to thermal stress and ocean acidification

Rising temperatures and ocean acidification driven by anthropogenic carbon emissions threaten both tropical and temperate corals. However, the synergistic effect of these stressors on coral physiology is still poorly understood, in particular for cold-water corals. This study assessed changes in key physiological parameters (calcification, respiration and ammonium excretion) of the widespread cold-water coral Desmophyllum dianthus maintained for 8 months at two temperatures (ambient 12 °C and elevated 15 °C) and two pCO2 conditions (ambient 390 ppm and elevated 750 ppm). At ambient temperatures no change in instantaneous calcification, respiration or ammonium excretion rates was observed at either pCO2 levels. Conversely, elevated temperature (15 °C) significantly reduced calcification rates, and combined elevated temperature and pCO2 significantly reduced respiration rates. Changes in the ratio of respired oxygen to excreted nitrogen (O:N), which provides information on the main sources of energy being metabolized, indicated a shift from mixed use of protein and carbohydrate/lipid as metabolic substrates under control conditions, to less efficient protein-dominated catabolism under both stressors. Overall, this study shows that the physiology of D. dianthus is more sensitive to thermal than pCO2 stress, and that the predicted combination of rising temperatures and ocean acidification in the coming decades may severely impact this cold-water coral species.

Acid-base physiology response to ocean acidification of two ecologically and economically important holothuroids from contrasting habitats, Holothuria scabra and Holothuria parva

Sea cucumbers are dominant invertebrates in several ecosystems such as coral reefs, seagrass meadows and mangroves. As bioturbators, they have an important ecological role in making available calcium carbonate and nutrients to the rest of the community. However, due to their commercial value, they face overexploitation in the natural environment. On top of that, occurring ocean acidification could impact these organisms, considered sensitive as echinoderms are osmoconformers, high-magnesium calcite producers and have a low metabolism. As a first investigation of the impact of ocean acidification on sea cucumbers, we tested the impact of short-term (6 to 12 days) exposure to ocean acidification (seawater pH 7.7 and 7.4) on two sea cucumbers collected in SW Madagascar, Holothuria scabra, a high commercial value species living in the seagrass meadows, and H. parva, inhabiting the mangroves. The former lives in a habitat with moderate fluctuations of seawater chemistry (driven by day-night differences) while the second lives in a highly variable intertidal environment. In both species, pH of the coelomic fluid was significantly negatively affected by reduced seawater pH, with a pronounced extracellular acidosis in individuals maintained at pH 7.7 and 7.4. This acidosis was due to an increased dissolved inorganic carbon content and pCO2 of the coelomic fluid, indicating a limited diffusion of the CO2 towards the external medium. However, respiration and ammonium excretion rates were not affected. No evidence of accumulation of bicarbonate was observed to buffer the coelomic fluid pH. If this acidosis stays uncompensated for when facing long-term exposure, other processes could be affected in both species, eventually leading to impacts on their ecological role.

Habitat traits and food availability determine the response of marine invertebrates to ocean acidification

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 3000 µatm) 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 20 weeks, 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 5 weeks 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