Seawater carbonate chemistry and concentration boundary layers around complex assemblages of macroalgae in a laboratory experiment

Metabolic processes have the potential to modulate the effects of ocean acidification (OA) in nearshore macroalgal beds. We investigated whether natural mixed assemblages of the articulate coralline macroalgae Arthrocardia corymbosa and understory crustose coralline algae (CCA) altered pH and O2 concentrations within and immediately above their canopies. In a unidirectional flume, we tested the effect of water velocity (0-0.1 m/s), bulk seawater pH (ambient pH 8.05, and pH 7.65), and irradiance (photosynthetically saturating light and darkness) on pH and O2 concentration gradients, and the derived concentration boundary layer (CBL) thickness. At bulk seawater pH 7.65 and slow velocities (0 and 0.015 m/s), pH at the CCA surface increased to 7.90-8.00 in the light. Although these manipulations were short term, this indicates a potential daytime buffering capacity that could alleviate the effects of OA. Photosynthetic activity also increased O2 concentrations at the surface of the CCA. However, this moderating capacity was flow dependent; the CBL thickness decreased from an average of 26.8 mm from the CCA surface at 0.015 m/s to 4.1 mm at 0.04 m/s. The reverse trends occurred in the dark, with respiration causing pH and O2 concentrations to decrease at the CCA surface. At all flow velocities the CBL thicknesses (up to 68 mm) were much greater than those previously published, indicating that the presence of canopies can alter the CBL substantially. In situ, the height of macroalgal canopies can be an order of magnitude larger than those used here, indicating that the degree of buffering to OA will be context dependent.

Seawater carbonate chemistry, thickness and carbonate elemental composition of the test of juvenile sea urchins in a laboratory experiment

Ocean surface CO2 levels are increasing in line with rising atmospheric CO2 and could exceed 900 µatm by year 2100, with extremes above 2000 µatm in some coastal habitats. The imminent increase in ocean pCO2 is predicted to have negative consequences for marine fishes, including reduced aerobic performance, but variability among species could be expected. Understanding interspecific responses to ocean acidification is important for predicting the consequences of ocean acidification on communities and ecosystems. In the present study, the effects of exposure to near-future seawater CO2 (860 µatm) on resting (M O2rest) and maximum (M O2max) oxygen consumption rates were determined for three tropical coral reef fish species interlinked through predator-prey relationships: juvenile Pomacentrus moluccensis and Pomacentrus amboinensis, and one of their predators: adult Pseudochromis fuscus. Contrary to predictions, one of the prey species, P. amboinensis, displayed a 28-39% increase in M O2max after both an acute and four-day exposure to near-future CO2 seawater, while maintaining M O2rest. By contrast, the same treatment had no significant effects on M O2rest or M O2max of the other two species. However, acute exposure of P. amboinensis to 1400 and 2400 µatm CO2 resulted in M O2max returning to control values. Overall, the findings suggest that: (1) the metabolic costs of living in a near-future CO2 seawater environment were insignificant for the species examined at rest; (2) the M O2max response of tropical reef species to near-future CO2 seawater can be dependent on the severity of external hypercapnia; and (3) near-future ocean pCO2 may not be detrimental to aerobic scope of all fish species and it may even augment aerobic scope of some species. The present results also highlight that close phylogenetic relatedness and living in the same environment, does not necessarily imply similar physiological responses to near-future CO2.

Seawater carbonate chemistry and larval growth response of the Portuguese oyster (Crassostrea angulata) in a laboratory experiment

Rising anthropogenic carbon dioxide (CO2) dissolving into coastal waters is decreasing the pH and carbonate ion concentration, thereby lowering the saturation state of calcium carbonate (CaCO3) minerals through a process named ocean acidification (OA). The unprecedented threats posed by such low pH on calcifying larvae of several edible oyster species have not yet been fully explored. Effects of low pH (7.9, 7.6, 7.4) on the early growth phase of Portuguese oyster (Crassostrea angulata) veliger larvae was examined at ambient salinity (34 ppt) and the low-salinity (27 ppt) treatment. Additionally, the combined effect of pH (8.1, 7.6), salinity (24 and 34 ppt) and temperature (24 °C and 30 °C) was examined using factorial experimental design. Surprisingly, the early growth phase from hatching to 5-day-old veliger stage showed high tolerance to pH 7.9 and pH 7.6 at both 34 ppt and 27 ppt. Larval shell area was significantly smaller at pH 7.4 only in low-salinity. In the 3-factor experiment, shell area was affected by salinity and the interaction between salinity and temperature but not by other combinations. Larvae produced the largest shell at the elevated temperature in low-salinity, regardless of pH. Thus the growth of the Portuguese oyster larvae appears to be robust to near-future pH level (> 7.6) when combined with projected elevated temperature and low-salinity in the coastal aquaculture zones of South China Sea.

Seawater carbonate chemistry, Acropora digitifera growth and skeletal U/Ca ratios during experiments, 2011

The impact of ocean acidification caused by the increasing atmospheric CO2 has been studied in marine calcifiers, including hermatypic corals. However, the effect of elevated pCO2 on the early developmental life-cycle stage of corals has been little studied. In this study, we reared polyps of Acropora digitifera in seawater at pHT 6.55, 7.31, 7.64, 7.77, and 8.03, controlled by CO2 bubbling. We measured the dry weights of polyp skeletons after the 40-d experiment to investigate the relationship between the seawater aragonite saturation state and polyp growth. In addition, we measured skeletal U/Ca ratio to estimate their pH dependence. Skeletal weights of coral polyps increased with the aragonite saturation state and reached an apparent saturation plateau above pH 7.77. U/Ca ratios had a strong inverse relationship with pH and a negligible relationship with skeletal growth rate (polyp weight), suggesting that skeletal U/Ca could be useful for reconstructing paleo-pH.

Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification

Ocean acidification (OA) and its associated decline in calcium carbonate saturation states is one of the major threats that tropical coral reefs face this century. Previous studies of the effect of OA on coral reef calcifiers have described a wide variety of outcomes for studies using comparable partial pressure of CO2 (pCO2) ranges, suggesting that key questions remain unresolved. One unresolved hypothesis posits that heterogeneity in the response of reef calcifiers to high pCO2 is a result of regional-scale variation in the responses to OA. To test this hypothesis, we incubated two coral taxa (Pocillopora damicornis and massive Porites) and two calcified algae (Porolithon onkodes and Halimeda macroloba) under 400, 700 and 1000 µatm pCO2 levels in experiments in Moorea (French Polynesia), Hawaii (USA) and Okinawa (Japan), where environmental conditions differ. Both corals and H. macroloba were insensitive to OA at all three locations, while the effects of OA on P. onkodes were location-specific. In Moorea and Hawaii, calcification of P. onkodes was depressed by high pCO2, but for specimens in Okinawa, there was no effect of OA. Using a study of large geographical scale, we show that resistance to OA of some reef species is a constitutive character expressed across the Pacific.

Seawater carbonate chemistry, pigments and proteins during experiments with phytoplankton, 2010

In the high-nutrient, low-chlorophyll waters of the Gulf of Alaska, microcosm manipulation experiments were used to assess the effect of CO2 on growth and primary production under iron-limited and iron-replete conditions. As expected, iron had a strong effect on growth and photosynthesis. A modest and variable stimulation of growth and biomass production by CO2 (high CO2: 77-122 Pa; low CO2: 11-17 Pa) was observed under both iron-replete and iron-limited conditions, though near the limit of precision of our measurements in slow-growing low-iron experiments. Physiological acclimations responsible for the changes in growth were assessed. Under iron-limited conditions, growth stimulation at high CO2 appeared to result from an increase in photosynthetic efficiency, which we attribute to energy savings from down-regulation of the carbon concentrating mechanisms. In some cases, iron-rich photosynthetic proteins (PsbA, PsaC, and cytochrome b6) were down-regulated at elevated CO2in iron-limited controls. Under iron-replete conditions, there was an increase in growth rate and biomass at high CO2 in some experiments. This increase was unexpectedly supported by reductions in cellular carbon loss, most likely decreased respiration. We speculate that this effect may be due to acclimation to decreased pH rather than high CO2. The variability in responses to CO2 among experiments did not appear to be caused by differences in phytoplankton community structure and may reflect the sensitivity of the net response of phytoplankton to antagonistic effects of the several parameters that co-vary with CO2.

Seawater carbonate chemistry and toxicity of Pseudo-nitzschia fraudulenta in a laboratory experiment

Anthropogenic CO2 is progressively acidifying the ocean, but the responses of harmful algal bloom species that produce toxins that can bioaccumulate remain virtually unknown. The neurotoxin domoic acid is produced by the globally-distributed diatom genus Pseudo-nitzschia. This toxin is responsible for amnesic shellfish poisoning, which can result in illness or death in humans and regularly causes mass mortalities of marine mammals and birds. Domoic acid production by Pseudo-nitzschia cells is known to be regulated by nutrient availability, but potential interactions with increasing seawater CO2 concentrations are poorly understood. Here we present experiments measuring domoic acid production by acclimatized cultures of Pseudo-nitzschia fraudulenta that demonstrate a strong synergism between projected future CO2 levels (765 ppm) and silicate-limited growth, which greatly increases cellular toxicity relative to growth under modern atmospheric (360 ppm) or pre-industrial (200 ppm) CO2 conditions. Cellular Si:C ratios decrease with increasing CO2, in a trend opposite to that seen for domoic acid production. The coastal California upwelling system where this species was isolated currently exhibits rapidly increasing levels of anthropogenic acidification, as well as widespread episodic silicate limitation of diatom growth. Our results suggest that the current ecosystem and human health impacts of toxic Pseudo-nitzschia blooms could be greatly exacerbated by future ocean acidification and 'carbon fertilization' of the coastal ocean.

Seawater carbonate chemistry and protein content, respiration, symbiodinium densities, survivorship of Pocillopora damicornis larvae in a laboratory experiment

Efforts to evaluate the response of coral larvae to global climate change (GCC) and ocean acidification (OA) typically employ short experiments of fixed length, yet it is unknown how the response is affected by exposure duration. In this study, we exposed larvae from the brooding coral Pocillopora damicornis to contrasts of temperature (24.00 °C [ambient] versus 30.49 °C) and pCO2 (49.4 Pa versus 86.2 Pa) for varying periods (1-5 days) to test the hypothesis that exposure duration had no effect on larval response as assessed by protein content, respiration, Symbiodinium density, and survivorship; exposure times were ecologically relevant compared to representative pelagic larval durations (PLD) for corals. Larvae differed among days for all response variables, and the effects of the treatment were relatively consistent regardless of exposure duration for three of the four response variables. Protein content and Symbiodinium density were unaffected by temperature and pCO2, but respiration increased with temperature (but not pCO2) with the effect intensifying as incubations lengthened. Survival, however, differed significantly among treatments at the end of the study, and by the 5th day, 78% of the larvae were alive and swimming under ambient temperature and ambient pCO2, but only 55-59% were alive in the other treatments. These results demonstrate that the physiological effects of temperature and pCO2 on coral larvae can reliably be detected within days, but effects on survival require > or = 5 days to detect. The detection of time-dependent effects on larval survivorship suggests that the influence of GCC and OA will be stronger for corals having long PLDs.

Seawater carbonate chemistry and Globigerinoides sacculifer biological processes during experiments, 2010

The effect of carbonate ion concentration ([CO3]) on calcification rates estimated from shell size and weight was investigated in the planktonic foraminifera Orbulina universa and Globigerinoides sacculifer. Experiments on G. sacculifer were conducted under two irradiance levels (35 and 335 µmol photons m-2 s-1). Calcification was ca. 30% lower under low light than under high light, irrespective of the [CO3]. Both O. universa and G. sacculifer exhibited reduced final shell weight and calcification rate under low [CO3]. For the [CO3] expected at the end of the century, the calcification rates of these two species are projected to be 6 to 13% lower than the present conditions, while the final shell weights are reduced by 20 to 27% for O. universa and by 4 to 6% for G. sacculifer. These results indicate that ocean acidification would impact on calcite production by foraminifera and may decrease the calcite flux contribution from these organisms.

Seawater carbonate chemistry and processes during experiments with crabs Chionoecetes tanneri and Cancer magister, 2007

Rising levels of atmospheric carbon dioxide could be curbed by large-scale sequestration of CO2 in the deep sea. Such a solution requires prior assessment of the impact of hypercapnic, acidic seawater on deep-sea fauna. Laboratory studies were conducted to assess the short-term hypercapnic tolerance of the deep-sea Tanner crab Chionoecetes tanneri, collected from 1000 m depth in Monterey Canyon off the coast of central California, USA. Hemolymph acid- base parameters were monitored over 24 h of exposure to seawater equilibrated with ~1% CO2 (seawater PCO2 ~6 torr or 0.8 kPa, pH 7.1), and compared with those of the shallow-living Dungeness crab Cancer magister. Short-term hypercapnia-induced acidosis in the hemolymph of Chionoecetes tanneri was almost uncompensated, with a net 24 h pH reduction of 0.32 units and a net bicarbonate accumulation of only 3 mM. Under simultaneous hypercapnia and hypoxia, short-term extracellular acidosis in Chionoecetes tanneri was completely uncompensated. In contrast, Cancer magister fully recovered its hemolymph pH over 24 h of hypercapnic exposure by net accumulation of 12 mM bicarbonate from the surrounding medium. The data support the hypothesis that deep-sea animals, which are adapted to a stable environment and exhibit reduced metabolic rates, lack the short-term acid-base regulatory capacity to cope with the acute hypercapnic stress that would accompany large-scale CO2 sequestration. Additionally, the data indicate that sequestration in oxygen-poor areas of the ocean would be even more detrimental to deep-sea fauna.

Seawater carbonate chemistry and coral (Acropora digitifera and Acropora tenuis) algal infection rate, survival and surface area of plyps during experiments, 2009

Ocean acidification, caused by increased atmospheric carbon dioxide (CO2) concentrations, is currently an important environmental problem. It is therefore necessary to investigate the effects of ocean acidification on all life stages of a wide range of marine organisms. However, few studies have examined the effects of increased CO2 on early life stages of organisms, including corals. Using a range of pH values (pH 7.3, 7.6, and 8.0) in manipulative duplicate aquarium experiments, we have evaluated the effects of increased CO2 on early life stages (larval and polyp stages) of Acropora spp. with the aim of estimating CO2 tolerance thresholds at these stages. Larval survival rates did not differ significantly between the reduced pH and control conditions. In contrast, polyp growth and algal infection rates were significantly decreased at reduced pH levels compared to control conditions. These results suggest that future ocean acidification may lead to reduced primary polyp growth and delayed establishment of symbiosis. Stress exposure experiments using longer experimental time scales and lower levels of CO2 concentrations than those used in this study are needed to establish the threshold of CO2 emissions required to sustain coral reef ecosystems.

Seawater carbonate chemistry, physiology, morphology of larval sea urchins, Strongylocentrotus purpuratus in a laboratory experiment

Ocean warming and ocean acidification, both consequences of anthropogenic production of CO2, will combine to influence the physiological performance of many species in the marine environment. In this study, we used an integrative approach to forecast the impact of future ocean conditions on larval purple sea urchins (Strongylocentrotus purpuratus) from the northeast Pacific Ocean. In laboratory experiments that simulated ocean warming and ocean acidification, we examined larval development, skeletal growth, metabolism and patterns of gene expression using an orthogonal comparison of two temperature (13°C and 18°C) and pCO2 (400 and 1100 µatm) conditions. Simultaneous exposure to increased temperature and pCO2 significantly reduced larval metabolism and triggered a widespread downregulation of histone encoding genes. pCO2 but not temperature impaired skeletal growth and reduced the expression of a major spicule matrix protein, suggesting that skeletal growth will not be further inhibited by ocean warming. Importantly, shifts in skeletal growth were not associated with developmental delay. Collectively, our results indicate that global change variables will have additive effects that exceed thresholds for optimized physiological performance in this keystone marine species.

Seawater carbonate chemistry and boron incorporation of planktic foraminifer Orbulina universa during experiments, 2011

Culture experiments with living planktic foraminifers reveal that the ratio of boron to calcium (B/Ca) in Orbulina universa increases from 56 to 92 µmol mol-1 when pH is raised from 7.61 +/- 0.02 to 8.67 +/- 0.03 (total scale). Across this pH range, the abundances of carbonate, bicarbonate, and borate ions also change (+ 530, - 500, and + 170 µmol kg-1, respectively). Thus specific carbonate system control(s) on B/Ca remain unclear, complicating interpretation of paleorecords. B/Ca in cultured O. universa also increases with salinity (55-72 µmol mol-1 from 29.9-35.4 per mil) and seawater boron concentration (62-899 µmol mol-1 from 4-40 ppm B), suggesting that these parameters may need to be taken into account for paleorecords spanning large salinity changes (~ 2 per mil) and for samples grown in seawater whose boron concentration ([B]SW) differs from modern by more than 0.25 ppm. While our results are consistent with the predominant incorporation of the charged borate species B(OH)4 into foraminiferal calcite, the behavior of the partition coefficient KD (defined as [B/Ca]calcite/B(OH)4/HCO3seawater) cannot be explained by borate incorporation alone, and suggests the involvement of other pH-sensitive ions such as CO3 For a given increase in seawater B(OH)4, the corresponding increase in B/Ca is stronger when B(OH)4 is raised by increasing [B]SW than when it is raised by increasing pH. These results suggest that B incorporation controls should be reconsidered. Additional insight is gained from laser-ablation ICP-MS profiles, which reveal variable B/Ca distributions within individual shells.