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.

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.

Seawater carbonate chemistry and energy status in the periwinkle Littorina littorea during experiments, 2011

In the future, marine organisms will face the challenge of coping with multiple environmental changes associated with increased levels of atmospheric Pco2, such as ocean warming and acidification. To predict how organisms may or may not meet these challenges, an in-depth understanding of the physiological and biochemical mechanisms underpinning organismal responses to climate change is needed. Here, we investigate the effects of elevated Pco2 and temperature on the whole-organism and cellular physiology of the periwinkle Littorina littorea. Metabolic rates (measured as respiration rates), adenylate energy nucleotide concentrations and indexes, and end-product metabolite concentrations were measured. Compared with values for control conditions, snails decreased their respiration rate by 31% in response to elevated Pco2 and by 15% in response to a combination of increased Pco2 and temperature. Decreased respiration rates were associated with metabolic reduction and an increase in end-product metabolites in acidified treatments, indicating an increased reliance on anaerobic metabolism. There was also an interactive effect of elevated Pco2 and temperature on total adenylate nucleotides, which was apparently compensated for by the maintenance of adenylate energy charge via AMP deaminase activity. Our findings suggest that marine intertidal organisms are likely to exhibit complex physiological responses to future environmental drivers, with likely negative effects on growth, population dynamics, and, ultimately, ecosystem processes.

Tolerance of juvenile Mytilus galloprovincialis to experimental seawater acidification

Coastal ocean acidification is expected to interfere with the physiology of marine bivalves. In this work, the effects of acidification on the physiology of juvenile mussels Mytilus galloprovincialis were tested by means of controlled CO2 perturbation experiments. The carbonate chemistry of natural (control) seawater was manipulated by injecting CO2 to attain 2 reduced pH levels: -0.3 and -0.6 pH units as compared with the control seawater. After 78 d of exposure, we found that the absorption efficiency and ammonium excretion rate of juveniles were inversely related to pH. Significant differences among treatments were not observed in clearance, ingestion and respiration rates. Coherently, the maximal scope for growth and tissue dry weight were observed in mussels exposed to the pH reduction delta pH=-0.6, suggesting that M. galloprovincialis could be tolerant to CO2 acidification, at least in the highly alkaline coastal waters of Ria Formosa (SW Portugal).

Future CO2-induced ocean acidification mediates the physiological performance of a green tide alga Ulva prolifera

The oceans take up more than 1 million tons of CO2 from the air per hour, about one-quarter of the anthropogenically released amount, leading to disrupted seawater chemistry due to increasing CO2 emissions. Based on the fossil fuel-intensive CO2 emission scenario (A1F1; Houghton et al., 2001), the H+ concentration or acidity of surface seawater will increase by about 150% (pH drop by 0.4) by the end of this century, the process known as ocean acidification (OA; Sabine et al., 2004; Doney et al., 2009; Gruber et al., 2012). Seawater pH is suggested to decrease faster in the coastal waters than in the pelagic oceans due to the interactions of hypoxia, respiration, and OA (Cai et al., 2011). Therefore, responses of coastal algae to OA are of general concern, considering the economic and social services provided by the coastal ecosystem that is adjacent to human living areas and that is dependent on coastal primary productivity. On the other hand, dynamic environmental changes in the coastal waters can interact with OA (Beardall et al., 2009).

Seawater carbonate chemistry, physiology and skeletal mineralogy of coralline alga Corallina elongata in a laboratory experiment

Marine organisms inhabiting environments where pCO2/pH varies naturally are suggested to be relatively resilient to future ocean acidification. To test this hypothesis, the effect of elevated pCO2 was investigated in the articulated coralline red alga Corallina elongata from an intertidal rock pool on the north coast of Brittany (France), where pCO2 naturally varied daily between 70 and 1000 µatm. Metabolism was measured on algae in the laboratory after they had been grown for 3 weeks at pCO2 concentrations of 380, 550, 750 and 1000 µatm. Net and gross primary production, respiration and calcification rates were assessed by measurements of oxygen and total alkalinity fluxes using incubation chambers in the light and dark. Calcite mol % Mg/Ca (mMg/Ca) was analysed in the tips, branches and basal parts of the fronds, as well as in new skeletal structures produced by the algae in the different pCO2 treatments. Respiration, gross primary production and calcification in light and dark were not significantly affected by increased pCO2. Algae grown under elevated pCO2 (550, 750 and 1000 µatm) formed fewer new structures and produced calcite with a lower mMg/Ca ratio relative to those grown under 380 µatm. This study supports the assumption that C. elongata from a tidal pool, where pCO2 fluctuates over diel and seasonal cycles, is relatively robust to elevated pCO2 compared to other recently investigated coralline algae.

Seawater carbonate chemistry and microbioerosion of coral skeletons

Biological mediation of carbonate dissolution represents a fundamental component of the destructive forces acting on coral reef ecosystems. Whereas ocean acidification can increase dissolution of carbonate substrates, the combined impact of ocean acidification and warming on the microbioerosion of coral skeletons remains unknown. Here, we exposed skeletons of the reef-building corals, Porites cylindrica and Isopora cuneata, to present-day (Control: 400 µatm - 24 °C) and future pCO2-temperature scenarios projected for the end of the century (Medium: +230 µatm - +2 °C; High: +610 µatm - +4 °C). Skeletons were also subjected to permanent darkness with initial sodium hypochlorite incubation, and natural light without sodium hypochlorite incubation to isolate the environmental effect of acidic seawater (i.e., Omega aragonite <1) from the biological effect of photosynthetic microborers. Our results indicated that skeletal dissolution is predominantly driven by photosynthetic microborers, as samples held in the dark did not decalcify. In contrast, dissolution of skeletons exposed to light increased under elevated pCO2-temperature scenarios, with P. cylindrica experiencing higher dissolution rates per month (89%) than I. cuneata (46%) in the high treatment relative to control. The effects of future pCO2-temperature scenarios on the structure of endolithic communities were only identified in P. cylindrica and were mostly associated with a higher abundance of the green algae Ostreobium spp. Enhanced skeletal dissolution was also associated with increased endolithic biomass and respiration under elevated pCO2-temperature scenarios. Our results suggest that future projections of ocean acidification and warming will lead to increased rates of microbioerosion. However, the magnitude of bioerosion responses may depend on the structural properties of coral skeletons, with a range of implications for reef carbonate losses under warmer and more acidic oceans.

Seawater carbonate chemistry and egg production, hatching and metabolic rates of a Mediterranean copepod species (Acartia clausi) in a laboratory experiment

This study includes the first information on the combined effect of low pH and raised temperature on egg production rate (EP), hatching success (HS), excretion and respiration of the Mediterranean copepod Acartia clausi. Adult individuals of A. clausi and fresh surface seawater were collected at a coastal station in Saronikos Gulf during April 2012. Four different conditions were applied: two different pH levels (present: 8.09 and future: 7.83) at two temperature values (present: 16°C and present+4 °C= 20°C). EP and HS success decreased significantly over the duration of exposure at future pH at both temperature conditions. However, the analysis of the combined effect of pH, T, chlorophyll a and the duration of the experiments on EP and HS revealed that ocean acidification had no discernible effect, whereas warming; food and the duration of exposure were more significant for the reproductive output of A. clausi. Temperature appeared to have a positive effect on respiration and excretion. Acidification had no clear effect on respiration, but a negative effect on the A. clausi excretion was observed. Acidification and warming resulted in the increase of the excretion rate and the increase was higher than that observed by warming only. Our findings showed that a direct effect of ocean acidification on copepod's vital rates was not obvious, except maybe in the case of excretion. Therefore, the combination of acidification with the ambient oligotrophic conditions and the warming could result in species being less able to allocate resources for coping with multiple stressors.

Impact of ocean acidification in the metabolism and swimming behavior of the dolphinfish (Coryphaena hippurus) early larvae

Since the industrial revolution, [CO2]atm has increased from 280 µatm to levels now exceeding 380 µatm and is expected to rise to 730-1,020 µatm by the end of this century. The consequent changes in the ocean's chemistry (e.g., lower pH and availability of the carbonate ions) are expected to pose particular problems for marine organisms, especially in the more vulnerable early life stages. The aim of this study was to investigate how the future predictions of ocean acidification may compromise the metabolism and swimming capabilities of the recently hatched larvae of the tropical dolphinfish (Coryphaena hippurus). Here, we show that the future environmental hypercapnia (delta pH 0.5; 0.16 % CO2, ~1,600 µatm) significantly (p < 0.05) reduced oxygen consumption rate up to 17 %. Moreover, the swimming duration and orientation frequency also decreased with increasing pCO2 (50 and 62.5 %, respectively). We argue that these hypercapnia-driven metabolic and locomotory challenges may potentially influence recruitment, dispersal success, and the population dynamics of this circumtropical oceanic top predator.

The larvae of congeneric gastropods showed differential responses to the combined effects of ocean acidification, temperature and salinity

The tolerance and physiological responses of the larvae of two congeneric gastropods, the intertidal Nassarius festivus and subtidal Nassarius conoidalis, to the combined effects of ocean acidification (PCO2 at 380, 950, 1250 ppm), temperature (15, 30 degrees C) and salinity (10, 30 psu) were compared. Results of three-way ANOVA on cumulative mortality after 72-h exposure showed significant interactive effects in which mortality increased with pCO(2) and temperature, but reduced at higher salinity for both species, with higher mortality being obtained for N. conoidalis. Similarly, respiration rate of the larvae increased with temperature and pCO(2) level for both species, with a larger percentage increase for N. conoidalis. Larval swimming speed increased with temperature and salinity for both species whereas higher pCO(2) reduced swimming speed in N. conoidalis but not N. festivus. The present findings indicated that subtidal congeneric species are more sensitive than their intertidal counterparts to the combined effects of these stressors. (c) 2014 Elsevier Ltd. All rights reserved.

Seawater carbonate chemistry and community metabolism during an experiment with a coral reef, 2003

The effect of elevated pCO2 on the metabolism of a coral reef community dominated by macroalgae has been investigated utilizing the large 2650 m3 coral reef mesocosm at the Biosphere-2 facility near Tucson, Arizona. The carbonate chemistry of the water was manipulated to simulate present-day and a doubled CO2 future condition. Each experiment consisted of a 1-2 month preconditioning period followed by a 7-9 day observational period. The pCO2 was 404 ± 63 ?atm during the present-day pCO2 experiment and 658 ± 59 ?atm during the elevated pCO2 experiment. Nutrient levels were low and typical of natural reefs waters (NO3? 0.5-0.9 ?M, NH4+ 0.4 ?M, PO43? 0.07-0.09 ?M). The temperature and salinity of the water were held constant at 26.5 ± 0.2°C and 34.4 ± 0.2 ppt. Photosynthetically available irradiance was 10 ± 2 during the present-day experiment and 7.4 ± 0.5 mol photons m?2 d?1 during the elevated pCO2 experiment. The primary producer biomass in the mesocosm was dominated by four species of macroalgae; Haptilon cubense, Amphiroa fragillisima, Gelidiopsis intricata and Chondria dasyphylla. Algal biomass was 10.4 mol C m?2 during the present-day and 8.7 mol C m?2 and during the elevated pCO2 experiments. As previously observed, the increase in pCO2 resulted in a decrease in calcification from 0.041 ± 0.007 to 0.006 ± 0.003 mol CaCO3 m?2 d?1. Net community production (NCP) and dark respiration did not change in response to elevated pCO2. Light respiration measured by a new radiocarbon isotope dilution method exceeded dark respiration by a factor of 1.2 ± 0.3 to 2.1 ± 0.4 on a daily basis and by 2.2 ± 0.6 to 3.9 ± 0.8 on an hourly basis. The 1.8-fold increase with increasing pCO2 indicates that the enhanced respiration in the light was not due to photorespiration. Gross production (GPP) computed as the sum of NCP plus daily respiration (light + dark) increased significantly (0.24 ± 0.03 vs. 0.32 ± 0.04 mol C m?2 d?1). However, the conventional calculation of GPP based on the assumption that respiration in the light proceeds at the same rate as the dark underestimated the true rate of GPP by 41-100% and completely missed the increased rate of carbon cycling due to elevated pCO2. We conclude that under natural, undisturbed, nutrient-limited conditions elevated CO2 depresses calcification, stimulates the rate of turnover of organic carbon, particularly in the light, but has no effect on net organic production. The hypothesis that an increase pCO2 would produce an increase in net production that would counterbalance the effect of decreasing saturation state on calcification is not supported by these data.

Calcification repsonse of m,arione bivalves to changed carbonate chemistry

Bivalve calcification, particularly of the early larval stages, is highly sensitive to the change in ocean carbonate chemistry resulting from atmospheric CO2 uptake. Earlier studies suggested that declining seawater [CO32-] and thereby lowered carbonate saturation affect shell production. However, disturbances of physiological processes such as acid-base regulation by adverse seawater pCO2 and pH can affect calcification in a secondary fashion. In order to determine the exact carbonate system component by which growth and calcification are affected it is necessary to utilize more complex carbonate chemistry manipulations. As single factors, pCO2 had no effects and [HCO3-] and pH had only limited effects on shell growth, while lowered [CO32-] strongly impacted calcification. Dissolved inorganic carbon (CT) limiting conditions led to strong reductions in calcification, despite high [CO32-], indicating that [HCO3-] rather than [CO32-] is the inorganic carbon source utilized for calcification by mytilid mussels. However, as the ratio [HCO3-] / [H+] is linearly correlated with [CO32-] it is not possible to differentiate between these under natural seawater conditions. An equivalent of about 80 µmol kg-1 [CO32-] is required to saturate inorganic carbon supply for calcification in bivalves. Below this threshold biomineralization rates rapidly decline. A comparison of literature data available for larvae and juvenile mussels and oysters originating from habitats differing substantially with respect to prevailing carbonate chemistry conditions revealed similar response curves. This suggests that the mechanisms which determine sensitivity of calcification in this group are highly conserved. The higher sensitivity of larval calcification seems to primarily result from the much higher relative calcification rates in early life stages. In order to reveal and understand the mechanisms that limit or facilitate adaptation to future ocean acidification, it is necessary to better understand the physiological processes and their underlying genetics that govern inorganic carbon assimilation for calcification.