Assessing the physiological responses of the gastropod Crepidula fornicata to predicted ocean acidification and warming

Organisms inhabiting coastal waters naturally experience diel and seasonal physico-chemical variations. According to various assumptions, coastal species are either considered to be highly tolerant to environmental changes or, conversely, living at the thresholds of their physiological performance. Therefore, these species are either more resistant or more sensitive, respectively, to ocean acidification and warming. Here, we focused on Crepidula fornicata, an invasive gastropod that colonized bays and estuaries on northwestern European coasts during the 20th century. Small (<3 cm in length) and large (>4.5 cm in length), sexually mature individuals of C. fornicata were raised for 6 months in three different pCO2 conditions (390 µatm, 750 µatm, and 1400 µatm) at four successive temperature levels (10°C, 13°C, 16°C, and 19°C). At each temperature level and in each pCO2 condition, we assessed the physiological rates of respiration, ammonia excretion, filtration and calcification on small and large individuals. Results show that, in general, temperature positively influenced respiration, excretion and filtration rates in both small and large individuals. Conversely, increasing pCO2 negatively affected calcification rates, leading to net dissolution in the most drastic pCO2 condition (1400 µatm) but did not affect the other physiological rates. Overall, our results indicate that C. fornicata can tolerate ocean acidification, particularly in the intermediate pCO2 scenario. Moreover, in this eurythermal species, moderate warming may play a buffering role in the future responses of organisms to ocean acidification.

Performance data of the coral Pocillopora verrucosa and environmental conditions along the Saudi Arabian Red Sea coast as assessed during 3 expeditions in the years 2011 and 2012

Large scale patterns of ecologically relevant traits may help identify drivers of their variability and conditions beneficial or adverse to the expression of these traits. Antimicrofouling defenses in scleractinian corals regulate the establishment of the associated biofilm as well as the risks of infection. The Saudi Arabian Red Sea coast features a pronounced thermal and nutritional gradient including regions and seasons with potentially stressful conditions to corals. Assessing the patterns of antimicrofouling defenses across the Red Sea may hint at the susceptibility of corals to global change. We investigated microfouling pressure as well as the relative strength of 2 alternative antimicrofouling defenses (chemical antisettlement activity, mucus release) along the pronounced environmental gradient along the Saudi Arabian Red Sea coast in 2 successive years. Microfouling pressure was exceptionally low along most of the coast but sharply increased at the southernmost sites. Mucus release correlated with temperature. Chemical defense tended to anti-correlate with mucus release. As a result, the combined action of mucus release and chemical antimicrofouling defense seemed to warrant sufficient defense against microbes along the entire coast. In the future, however, we expect enhanced energetic strain on corals when warming and/or eutrophication lead to higher bacterial fouling pressure and a shift towards putatively more costly defense by mucus release.

Effects of ocean acidification on Posidonia oceanica epiphytic community and shoot productivity

1. Biological interactions can alter predictions that are based on single-species physiological response. It is known that leaf segments of the seagrass Posidonia oceanica will increase photosynthesis with lowered pH, but it is not clear whether the outcome will be altered when the whole plant and its epiphyte community, with different respiratory and photosynthetic demands, are included. In addition, the effects on the Posidonia epiphyte community have rarely been tested under controlled conditions, at near-future pH levels. 2. In order to better evaluate the effects of pH levels as projected for the upcoming decades on seagrass meadows, shoots of P. oceanica with their associated epiphytes were exposed in the laboratory to three pH levels (ambient: 8.1, 7.7 and 7.3, on the total scale) for 4 weeks. Net productivity, respiration, net calcification and leaf fluorescence were measured on several occasions. At the end of the study, epiphyte community abundance and composition, calcareous mass and crustose coralline algae growth were determined. Finally, photosynthesis vs. irradiance curves (PE) was produced from segments of secondary leaves cleaned of epiphytes and pigments extracted. 3. Posidonia leaf fluorescence and chlorophyll concentrations did not differ between pH treatments. Net productivity of entire shoots and epiphyte-free secondary leaves increased significantly at the lowest pH level yet limited or no stimulation in productivity was observed at the intermediate pH treatment. Under both pH treatments, significant decreases in epiphytic cover were observed, mostly due to the reduction of crustose coralline algae. The loss of the dominant epiphyte producer yet similar photosynthetic response for epiphyte-free secondary leaves and shoots suggests a minimal contribution of epiphytes to shoot productivity under experimental conditions. 4. Synthesis. Observed responses indicate that under future ocean acidification conditions foreseen in the next century an increase in Posidonia productivity is not likely despite the partial loss of epiphytic coralline algae which are competitors for light. A decline in epiphytic cover could, however, reduce the feeding capacity of the meadow for invertebrates. In situ long-term experiments that consider both acidification and warming scenarios are needed to improve ecosystem-level predictions.

Impact of medium-term exposure to elevated pCO2 levels on the physiological energetics of the mussel Mytilus chilensis

This study evaluated the impact of medium-term exposure to elevated pCO2 levels (750-1200 ppm) on the physiological processes of juvenile Mytilus chilensis mussels over a period of 70 d in a mesocosm system. Three equilibration tanks filled with filtered seawater were adjusted to three pCO2 levels: 380 (control), 750 and 1200 ppm by bubbling air or an air-CO2 mixture through the water. For the control, atmospheric air (with aprox. 380 ppm CO2) was bubbled into the tank; for the 750 and 1200 ppm treatments, dry air and pure CO2 were blended to each target concentration using mass flow controllers for air and CO2. No impact on feeding activity was observed at the beginning of the experiment, but a significant reduction in clearance rate was observed after 35 d of exposure to highly acidified seawater. Absorption rate and absorption efficiency were reduced at high pCO2 levels. In addition, oxygen uptake fell significantly under these conditions, indicating a metabolic depression. These physiological responses of the mussels resulted in a significant reduction of energy available for growth (scope for growth) with important consequences for the aquaculture of this species during medium-term exposure to acid conditions. The results of this study clearly indicate that high pCO2 levels in the seawater have a negative effect on the health of M. chilensis. Therefore, the predicted acidification of seawater associated with global climate change could be harmful to this ecologically and commercially important mussel.

Acclimatization to high-variance habitats does not enhance physiological tolerance of two key Caribbean corals to future temperature and pH

Corals are acclimatized to populate dynamic habitats that neighbour coral reefs. Habitats such as seagrass beds exhibit broad diel changes in temperature and pH that routinely expose corals to conditions predicted for reefs over the next 50-100 years. However, whether such acclimatization effectively enhances physiological tolerance to, and hence provides refuge against, future climate scenarios remains unknown. Also, whether corals living in low-variance habitats can tolerate present-day high-variance conditions remains untested. We experimentally examined how pH and temperature predicted for the year 2100 affects the growth and physiology of two dominant Caribbean corals (Acropora palmata and Porites astreoides) native to habitats with intrinsically low (outer-reef terrace, LV) and/or high (neighbouring seagrass, HV) environmental variance. Under present-day temperature and pH, growth and metabolic rates (calcification, respiration and photosynthesis) were unchanged for HV versus LV populations. Superimposing future climate scenarios onto the HV and LV conditions did not result in any enhanced tolerance to colonies native to HV. Calcification rates were always lower for elevated temperature and/or reduced pH. Together, these results suggest that seagrass habitats may not serve as refugia against climate change if the magnitude of future temperature and pH changes is equivalent to neighbouring reef habitats.

Temperature and acidification variability reduce physiological performance in the intertidal zone porcelain crab Petrolisthes//cinctipes

We show here that increased variability of temperature and pH synergistically negatively affects the energetics of intertidal zone crabs. Under future climate scenarios, coastal ecosystems are projected to have increased extremes of low tide-associated thermal stress and ocean acidification-associated low pH, the individual or interactive effects of which have yet to be determined. To characterize energetic consequences of exposure to increased variability of pH and temperature, we exposed porcelain crabs, Petrolisthes cinctipes, to conditions that simulated current and future intertidal zone thermal and pH environments. During the daily low tide, specimens were exposed to no, moderate or extreme heating, and during the daily high tide experienced no, moderate or extreme acidification. Respiration rate and cardiac thermal limits were assessed following 2.5 weeks of acclimation. Thermal variation had a larger overall effect than pH variation, though there was an interactive effect between the two environmental drivers. Under the most extreme temperature and pH combination, respiration rate decreased while heat tolerance increased, indicating a smaller overall aerobic energy budget (i.e. a reduced O2 consumption rate) of which a larger portion is devoted to basal maintenance (i.e. greater thermal tolerance indicating induction of the cellular stress response). These results suggest the potential for negative long-term ecological consequences for intertidal ectotherms exposed to increased extremes in pH and temperature due to reduced energy for behavior and reproduction.

Seawater carbonate chemistry and physiological response of the Mediterranean crustose coralline alga Lithophyllum cabiochae to elevated pCO2 and temperature

The response of respiration, photosynthesis, and calcification to elevated pCO2 and temperature was investigated in isolation and in combination in the Mediterranean crustose coralline alga Lithophyllum cabiochae. Algae were maintained in aquaria during 1 year at near-ambient conditions of irradiance, at ambient or elevated temperature (+3 °C), and at ambient (ca. 400 µatm) or elevated pCO2 (ca. 700 µatm). Respiration, photosynthesis, and net calcification showed a strong seasonal pattern following the seasonal variations of temperature and irradiance, with higher rates in summer than in winter. Respiration was unaffected by pCO2 but showed a general trend of increase at elevated temperature at all seasons, except in summer under elevated pCO2. Conversely, photosynthesis was strongly affected by pCO2 with a decline under elevated pCO2 in summer, autumn, and winter. In particular, photosynthetic efficiency was reduced under elevated pCO2. Net calcification showed different responses depending on the season. In summer, net calcification increased with rising temperature under ambient pCO2 but decreased with rising temperature under elevated pCO2. Surprisingly, the highest rates in summer were found under elevated pCO2 and ambient temperature. In autumn, winter, and spring, net calcification exhibited a positive or no response at elevated temperature but was unaffected by pCO2. The rate of calcification of L. cabiochae was thus maintained or even enhanced under increased pCO2. However, there is likely a trade-off with other physiological processes. For example, photosynthesis declines in response to increased pCO2 under ambient irradiance. The present study reports only on the physiological response of healthy specimens to ocean warming and acidification, however, these environmental changes may affect the vulnerability of coralline algae to other stresses such as pathogens and necroses that can cause major dissolution, which would have critical consequence for the sustainability of coralligenous habitats and the budgets of carbon and calcium carbonate in coastal Mediterranean ecosystems.

Ocean acidification increases the accumulation of toxic phenolic compounds across trophic levels

Increasing atmospheric CO2 concentrations are causing ocean acidification (OA), altering carbonate chemistry with consequences for marine organisms. Here we show that OA increases by 46-212% the production of phenolic compounds in phytoplankton grown under the elevated CO2 concentrations projected for the end of this century, compared with the ambient CO2 level. At the same time, mitochondrial respiration rate is enhanced under elevated CO2 concentrations by 130-160% in a single species or mixed phytoplankton assemblage. When fed with phytoplankton cells grown under OA, zooplankton assemblages have significantly higher phenolic compound content, by about 28-48%. The functional consequences of the increased accumulation of toxic phenolic compounds in primary and secondary producers have the potential to have profound consequences for marine ecosystem and seafood quality, with the possibility that fishery industries could be influenced as a result of progressive ocean changes.

Decline in growth of foraminifer Marginopora rossi under eutrophication and ocean acidification scenarios

The combination of global and local stressors is leading to a decline in coral reef health globally. In the case of eutrophication, increased concentrations of dissolved inorganic nitrogen (DIN) and phosphorus (DIP) are largely attributed to local land use changes. From the global perspective, increased atmospheric CO2 levels are not only contributing to global warming but also ocean acidification (OA). Both eutrophication and OA have serious implications for calcium carbonate production and dissolution among calcifying organisms. In particular, benthic foraminifera precipitate the most soluble form of mineral calcium carbonate (high-Mg calcite), potentially making them more sensitive to dissolution. In this study, a manipulative orthogonal two-factor experiment was conducted to test the effects of dissolved inorganic nutrients and OA on the growth, respiration and photophysiology of the large photosymbiont-bearing benthic foraminifer, Marginopora rossi. This study found the growth rate of M. rossi was inhibited by the interaction of eutrophication and acidification. The relationship between M. rossi and its photosymbionts became destabilized due to the photosymbiont's release from nutrient limitation in the nitrate-enriched treatment, as shown by an increase in zooxanthellae cells per host surface area. Foraminifers from the OA treatments had an increased amount of Chl a per cell, suggesting a greater potential to harvest light energy, however, there was no net benefit to the foraminifer growth. Overall, this study demonstrates that the impacts of OA and eutrophication are dose dependent and interactive. This research indicates an OA threshold at pH 7.6, alone or in combination with eutrophication, will lead to a decline in M. rossi calcification. The decline in foraminifera calcification associated with pollution and OA will have broad ecological implications across their ubiquitous range and suggests that without mitigation it could have serious implications for the future of coral reefs.

Individual and population-level responses to ocean acidification

Ocean acidification is predicted to have detrimental effects on many marine organisms and ecological processes. Despite growing evidence for direct impacts on specific species, few studies have simultaneously considered the effects of ocean acidification on individuals (e.g. consequences for energy budgets and resource partitioning) and population level demographic processes. Here we show that ocean acidification increases energetic demands on gastropods resulting in altered energy allocation, i.e. reduced shell size but increased body mass. When scaled up to the population level, long-term exposure to ocean acidification altered population demography, with evidence of a reduction in the proportion of females in the population and genetic signatures of increased variance in reproductive success among individuals. Such increased variance enhances levels of short-term genetic drift which is predicted to inhibit adaptation. Our study indicates that even against a background of high gene flow, ocean acidification is driving individual- and population-level changes that will impact eco-evolutionary trajectories.

Calcification is not the Achilles'heel of cold-water corals in an acidifying ocean

Ocean acidification is thought to be a major threat to coral reefs: laboratory evidence and CO2 seep research has shown adverse effects on many coral species, although a few are resilient. There are concerns that cold-water corals are even more vulnerable as they live in areas where aragonite saturation (Omega ara) is lower than in the tropics and is falling rapidly due to CO2 emissions. Here, we provide laboratory evidence that net (gross calcification minus dissolution) and gross calcification rates of three common cold-water corals, Caryophyllia smithii, Dendrophyllia cornigera, and Desmophyllum dianthus, are not affected by pCO2 levels expected for 2100 (pCO2 1058 µatm, Omega ara 1.29), and nor are the rates of skeletal dissolution in D. dianthus. We transplanted D. dianthus to 350 m depth (pHT 8.02; pCO2 448 µatm, Omega ara 2.58) and to a 3 m depth CO2 seep in oligotrophic waters (pHT 7.35; pCO2 2879 µatm, Omega ara 0.76) and found that the transplants calcified at the same rates regardless of the pCO2 confirming their resilience to acidification, but at significantly lower rates than corals that were fed in aquaria. Our combination of field and laboratory evidence suggests that ocean acidification will not disrupt cold-water coral calcification although falling aragonite levels may affect other organismal physiological and/or reef community processes.