Seawater carbonate chemistry and aerobic performance of coral reef fishes during experiments, 2009

Concerns about the impacts of ocean acidification on marine life have mostly focused on how reduced carbonate saturation affects calcifying organisms. Here, we show that levels of CO2-induced acidification that may be attained by 2100 could also have significant effects on marine organisms by reducing their aerobic capacity. The effects of temperature and acidification on oxygen consumption were tested in 2 species of coral reef fishes, Ostorhinchus doederleini and O. cyanosoma, from the Great Barrier Reef, Australia. The capacity for aerobic activity (aerobic scope) declined at temperatures above the summer average (29°C) and in CO2-acidified water (pH 7.8 and ~1000 ppm CO2) compared to control water (pH 8.15). Aerobic scope declined by 36 and 32% for O. doederleini and O. cyanosoma at temperatures between 29 to 32°C, whereas it declined by 33 and 47% for O. doederleini and O. cyanosoma in acidified water compared to control water. Thus, the declines in aerobic scope in acidified water were similar to those caused by a 3°C increase in water temperature. Minimum aerobic scope values of ~200 mg O2 kg-1 h-1 were attained for both species in acidified water at 32°C, compared with over 600 mg O2 kg-1 h-1 in control water at 29°C. Mortality rate increased sharply at 33°C, indicating that this temperature is close to the lethal thermal limit for both species. Acidification further increased the mortality rate of O. doederleini, but not of O. cyanosoma. These results show that coral reef fishes are sensitive to both higher temperatures and increased levels of dissolved CO2, and that the aerobic performance of some reef fishes could be significantly reduced if climate change continues unabated.

Diffusion boundary layers ameliorate the negative effects of ocean acidification on the temperate coralline macroalga Arthrocardia corymbosa

Anthropogenically-modulated reductions in pH, termed ocean acidification, could pose a major threat to the physiological performance, stocks, and biodiversity of calcifiers and may devalue their ecosystem services. Recent debate has focussed on the need to develop approaches to arrest the potential negative impacts of ocean acidification on ecosystems dominated by calcareous organisms. In this study, we demonstrate the role of a discrete (i.e. diffusion) boundary layer (DBL), formed at the surface of some calcifying species under slow flows, in buffering them from the corrosive effects of low pH seawater. The coralline macroalga Arthrocardia corymbosa was grown in a multifactorial experiment with two mean pH levels (8.05 'ambient' and 7.65 a worst case 'ocean acidification' scenario projected for 2100), each with two levels of seawater flow (fast and slow, i.e. DBL thin or thick). Coralline algae grown under slow flows with thick DBLs (i.e., unstirred with regular replenishment of seawater to their surface) maintained net growth and calcification at pH 7.65 whereas those in higher flows with thin DBLs had net dissolution. Growth under ambient seawater pH (8.05) was not significantly different in thin and thick DBL treatments. No other measured diagnostic (recruit sizes and numbers, photosynthetic metrics, %C, %N, %MgCO3) responded to the effects of reduced seawater pH. Thus, flow conditions that promote the formation of thick DBLs, may enhance the subsistence of calcifiers by creating localised hydrodynamic conditions where metabolic activity ameliorates the negative impacts of ocean acidification.

Ocean acidification alleviates low-temperature effects on growth and photosynthesis of the red alga Neosiphonia harveyi (Rhodophyta)

This study aimed to examine interactive effects between ocean acidification and temperature on the photosynthetic and growth performance of Neosiphonia harveyi. N. harveyi was cultivated at 10 and 17.5 °C at present (~380 µatm), expected future (~800 µatm), and high (~1500 µatm) pCO2. Chlorophyll a fluorescence, net photosynthesis, and growth were measured. The state of the carbon-concentrating mechanism (CCM) was examined by pH-drift experiments (with algae cultivated at 10 °C only) using ethoxyzolamide, an inhibitor of external and internal carbonic anhydrases (exCA and intCA, respectively). Furthermore, the inhibitory effect of acetazolamide (an inhibitor of exCA) and Tris (an inhibitor of the acidification of the diffusive boundary layer) on net photosynthesis was measured at both temperatures. Temperature affected photosynthesis (in terms of photosynthetic efficiency, light saturation point, and net photosynthesis) and growth at present pCO2, but these effects decreased with increasing pCO2. The relevance of the CCM decreased at 10 °C. A pCO2 effect on the CCM could only be shown if intCA and exCA were inhibited. The experiments demonstrate for the first time interactions between ocean acidification and temperature on the performance of a non-calcifying macroalga and show that the effects of low temperature on photosynthesis can be alleviated by increasing pCO2. The findings indicate that the carbon acquisition mediated by exCA and acidification of the diffusive boundary layer decrease at low temperatures but are not affected by the cultivation level of pCO2, whereas the activity of intCA is affected by pCO2. Ecologically, the findings suggest that ocean acidification might affect the biogeographical distribution of N. harveyi.

Euechinoidea and Cidaroidea respond differently to ocean acidification

The impact of the chemical changes in the ocean waters due to the increasing atmospheric CO2 depends on the ability of an organism to control extracellular pH. Among sea urchins, this seems specific to the Euechinoidea, sea urchins except Cidaroidea. However, Cidaroidea survived two ocean acidification periods: the Permian-Trias and the Cretaceous-Tertiary crises. We investigated the response of these two sea urchin groups to reduced seawater pH with the tropical cidaroid Eucidaris tribuloides, the sympatric euechinoid Tripneustes ventricosus and the temperate euechinoid Paracentrotus lividus. Both euechinoid showed a compensation of the coelomic fluid pH due to increased buffer capacity. This was linked to an increased concentration of DIC in the coelomic fluid and thus of bicarbonate ions (most probably originating from the surrounding seawater as isotopic signature of the carbon -delta 13C- was similar). On the other hand, the cidaroid showed no changes within the coelomic fluid. Moreover, the delta 13C of the coelomic fluid did not match that of the seawater and was not significantly different between the urchins from the different treatments. Feeding rate was not affected in any species. While euechinoids are able to regulate their extracellular acid-base balance, many questions are still unanswered on the costs of this capacity. On the contrary, cidaroids do not seem affected by a reduced seawater pH. Further investigations need to be undertaken to cover more species and physiological and metabolic parameters in order to determine if energy trade-offs occur and how this mechanism of compensation is distributed among sea urchins.

The photo-physiological response of a model cnidarian-dinoflagellate symbiosis to CO2-induced acidification at the cellular level

We measured the relationship between CO2-induced seawater acidification, photo-physiological performance and intracellular pH (pHi) in a model cnidarian-dinoflagellate symbiosis - the sea anemone Aiptasia sp. -under ambient (289.94 ± 12.54 µatm), intermediate (687.40 ± 25.10 µatm) and high (1459.92 ± 65.51 µatm) CO2 conditions. These treatments represented current CO2 levels, in addition to CO2 stabilisation scenarios IV and VI provided by the Intergovernmental Panel on Climate Change (IPCC). Anemones were exposed to each treatment for two months and sampled at regular intervals. At each time-point we measured a series of physiological responses: maximum dark-adapted fluorescent yield of PSII (Fv/Fm), gross photosynthetic rate, respiration rate, symbiont population density, and light-adapted pHi of both the dinoflagellate symbiont and isolated host anemone cell. We observed increases in all but one photo-physiological parameter (Pgross:R ratio). At the cellular level, increases in light-adapted symbiont pHi were observed under both intermediate and high CO2 treatments, relative to control conditions (pHi 7.35 and 7.46 versus pHi 7.25, respectively). The response of light-adapted host pHi was more complex, however, with no change observed under the intermediate CO2 treatment, but a 0.3 pH-unit increase under the high CO2 treatment (pHi 7.19 and 7.48, respectively). This difference is likely a result of a disproportionate increase in photosynthesis relative to respiration at the higher CO2 concentration. Our results suggest that, rather than causing cellular acidosis, the addition of CO2 will enhance photosynthetic performance, enabling both the symbiont and host cell to withstand predicted ocean acidification scenarios.

Ocean acidification affects growth but not nutritional quality of the seaweed Fucus vesiculosus (Phaeophyceae, Fucales)

Understanding the ecological implications of global climate change requires investigations of not only the direct effects of environmental change on species performance but also indirect effects that arise from altered species interactions. We performed CO2 perturbation experiments to investigate the effects of ocean acidification on the trophic interaction between the brown seaweed Fucus vesiculosus and the herbivorous isopod Idotea baltica. We predicted faster growth of F. vesiculosus at elevated CO2-concentrations and higher carbon content of the algal tissue. We expected that I. baltica has different consumption rates on algae that have been grown at different CO2 levels and that the isopods remove surplus carbon metabolically by enhanced respiration. Surprisingly, growth of F. vesiculosus as well as the C:N-ratio of the algal tissue were reduced at high CO2-levels. The changes in the elemental composition had no effect on the consumption rates and the respiration of the herbivores. An additional experiment showed that consumption of F. vesiculosus by the isopod Idotea emarginata was independent of ocean acidification and temperature. Our results could not reveal any effects of ocean acidification on the per capita strength of the trophic interaction between F. vesiculosus and its consumers. However, reduced growth of the algae at high CO2-concentrations might reduce the capability of the seaweed to compensate losses due to intense herbivory.

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.

CO2 and inorganic nutrient enrichment affect the performance of a calcifying green alga and its noncalcifying epiphyte

Ocean acidification studies in the past decade have greatly improved our knowledge of how calcifying organisms respond to increased surface ocean CO2 levels. It has become evident that, for many organisms, nutrient availability is an important factor that influences their physiological responses and competitive interactions with other species. Therefore, we tested how simulated ocean acidification and eutrophication (nitrate and phosphate enrichment) interact to affect the physiology and ecology of a calcifying chlorophyte macroalga (Halimeda opuntia (L.) J.V. Lamouroux) and its common noncalcifying epiphyte (Dictyota sp.) in a 4-week fully crossed multifactorial experiment. Inorganic nutrient enrichment (+NP) had a strong influence on all responses measured with the exception of net calcification. Elevated CO2 alone significantly decreased electron transport rates of the photosynthetic apparatus and resulted in phosphorus limitation in both species, but had no effect on oxygen production or respiration. The combination of CO2 and +NP significantly increased electron transport rates in both species. While +NP alone stimulated H. opuntia growth rates, Dictyota growth was significantly stimulated by nutrient enrichment only at elevated CO2, which led to the highest biomass ratios of Dictyota to Halimeda. Our results suggest that inorganic nutrient enrichment alone stimulates several aspects of H. opuntia physiology, but nutrient enrichment at a CO2 concentration predicted for the end of the century benefits Dictyota sp. and hinders its calcifying basibiont H. opuntia.

Copepod vital rates under CO2-induced acidification: a calanoid species and a cyclopoid species under short-term exposures

Although copepods have been considered tolerant against the direct influence of the ocean acidification (OA) projected for the end of the century, some recent studies have challenged this view. Here, we have examined the direct impact of short-term exposure to a pCO2/pH level relevant for the year 2100 (pHNBS, control: 8.18, low pH: 7.78), on the physiological performance of two representative marine copepods: the calanoid Acartia grani and the cyclopoid Oithona davisae. Adults of both species, from laboratory cultures, were preconditioned for four consecutive days in algal suspensions (Akashiwo sanguinea) prepared with filtered sea water pre-adjusted to the targeted pH values via CO2 bubbling. We measured the feeding and respiratory activity and reproductive output of those pre-conditioned females. The largely unaffected fatty acid composition of the prey offered between OA treatments and controls supports the absence in the study of indirect OA effects (i.e. changes of food nutritional quality). Our results show no direct effect of acidification on the vital rates examined in either copepod species. Our findings are compared with results from previous short- and long-term manipulative experiments on other copepod species.

Ocean acidification has no effect on thermal bleaching in the coral Seriatopora caliendrum

The objective of this study was to test whether elevated pCO2 predicted for the year 2100 (85.1 Pa) affects bleaching in the coral Seriatopora caliendrum (Ehrenberg 1834) either independently or interactively with high temperature (30.5 °C). Response variables detected the sequence of events associated with the onset of bleaching: reduction in the photosynthetic performance of symbionts as measured by maximum photochemical efficiency (F v/F m) and effective photochemical efficiency (delta F/F m') of PSII, declines in net photosynthesis (P net) and photosynthetic efficiency (alpha), and finally, reduced chlorophyll a and symbiont concentrations. S. caliendrum was collected from Nanwan Bay, Taiwan, and subjected to combinations of temperature (27.7 vs. 30.5 °C) and pCO2 (45.1 vs. 85.1 Pa) for 14 days. High temperature reduced values of all dependent variables (i.e., bleaching occurred), but high pCO2 did not affect Symbiodinium photophysiology or productivity, and did not cause bleaching. These results suggest that short-term exposure to 81.5 Pa pCO2, alone and in combination with elevated temperature, does not cause or affect coral bleaching.

CO2-induced ocean acidification increases anxiety in Rockfish via alteration of GABAA receptor functioning

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.

Solar UV irradiances modulate effects of ocean acidification on the Coccolithophorid Emiliania huxleyi

Emiliania huxleyi, the most abundant coccolithophorid in the oceans, is naturally exposed to solar UV radiation (UVR, 280-400 nm) in addition to photosynthetically active radiation (PAR). We investigated the physiological responses of E. huxleyi to the present day and elevated CO2 (390 vs 1000 µatm; with pH(NBS) 8.20 vs 7.86) under indoor constant PAR and fluctuating solar radiation with or without UVR. Enrichment of CO2 stimulated the production rate of particulate organic carbon (POC) under constant PAR, but led to unchanged POC production under incident fluctuating solar radiation. The production rates of particulate inorganic carbon (PIC) as well as PIC/POC ratios were reduced under the elevated CO2, ocean acidification (OA) condition, regardless of PAR levels, and the presence of UVR. However, moderate levels of UVR increased PIC production rates and PIC/POC ratios. OA treatment interacted with UVR to influence the alga's physiological performance, leading to reduced specific growth rate in the presence of UVA (315-400 nm) and decreased quantum yield, along with enhanced nonphotochemical quenching, with addition of UVB (280-315 nm). The results clearly indicate that UV radiation needs to be invoked as a key stressor when considering the impacts of ocean acidification on E. huxleyi.

The effects of water acidification, temperature and salinity on the regenerative capacity of the polychaete Diopatra neapolitana

Changes in seawater pH, temperature and salinity are expected to occur in the near future, which can be a threat to aquatic systems, mainly for marine coastal areas, and their inhabiting species. Hence, the present study proposes to evaluate the effects of temperature shifts, pH decrease and salinity changes in the tissue's regenerative capacity of the polychaete Diopatra neapolitana. This study evidenced that D. neapolitana individuals exposed to lower pH exhibited a significantly lower capacity to regenerate their body, while with the increase of temperature individuals showed a higher capacity to regenerate their tissues. Furthermore, the present work demonstrated that individuals exposed to salinities 28 and 35 did not present significant differences between them, while salinities 21 and 42 negatively influenced the regenerative capacity of D. neapolitana. At the end of regeneration, comparing all conditions, high salinity (42) seemed to have a greater impact on the regenerative capacity of individuals than the other factors, since under this condition individuals took longer to completely regenerate. Overall, this study demonstrated that variations in abiotic factors can strongly affect D. neapolitana's performance.