Seawater carbonate chemistry, productivity and calcification of Marginopora vertebralis in a laboratory experiment

Changes in the seawater carbonate chemistry (ocean acidification) from increasing atmospheric carbon dioxide (CO2 ) concentrations negatively affect many marine calcifying organisms, but may benefit primary producers under dissolved inorganic carbon (DIC) limitation. To improve predictions of the ecological effects of ocean acidification, the net gains and losses between the processes of photosynthesis and calcification need to be studied jointly on physiological and population levels. We studied productivity, respiration, and abundances of the symbiont-bearing foraminifer species Marginopora vertebralis on natural CO2 seeps in Papua New Guinea and conducted additional studies on production and calcification on the Great Barrier Reef (GBR) using artificially enhanced pCO2 . Net oxygen production increased up to 90% with increasing pCO2 ; temperature, light, and pH together explaining 61% of the variance in production. Production increased with increasing light and increasing pCO2 and declined at higher temperatures. Respiration was also significantly elevated (~25%), whereas calcification was reduced (16-39%) at low pH/high pCO2 compared to present-day conditions. In the field, M. vertebralis was absent at three CO2 seep sites at pHTotal levels below ~7.9 (pCO2 ~700 µatm), but it was found in densities of over 1000 m(-2) at all three control sites. The study showed that endosymbiotic algae in foraminifera benefit from increased DIC availability and may be naturally carbon limited. The observed reduction in calcification may have been caused either by increased energy demands for proton pumping (measured as elevated rates of respiration) or by stronger competition for DIC from the more productive symbionts. The net outcome of these two competing processes is that M. vertebralis cannot maintain populations under pCO2 exceeding 700 µatm, thus are likely to be extinct in the next century.

Seasonality affects macroalgal community response to increases in pCO2

Ocean acidification is expected to alter marine systems, but there is uncertainty about its effects due to the logistical difficulties of testing its large-scale and long-term effects. Responses of biological communities to increases in carbon dioxide can be assessed at CO2 seeps that cause chronic exposure to lower seawater pH over localised areas of seabed. Shifts in macroalgal communities have been described at temperate and tropical pCO2 seeps, but temporal and spatial replication of these observations is needed to strengthen confidence our predictions, especially because very few studies have been replicated between seasons. Here we describe the seawater chemistry and seasonal variability of macroalgal communities at CO2 seeps off Methana (Aegean Sea). Monitoring from 2011 to 2013 showed that seawater pH decreased to levels predicted for the end of this century at the seep site with no confounding gradients in Total Alkalinity, salinity, temperature or wave exposure. Most nutrient levels were similar along the pH gradient; silicate increased significantly with decreasing pH, but it was not limiting for algal growth at all sites. Metal concentrations in seaweed tissues varied between sites but did not consistently increase with pCO2. Our data on the flora are consistent with results from laboratory experiments and observations at Mediterranean CO2 seep sites in that benthic communities decreased in calcifying algal cover and increased in brown algal cover with increasing pCO2. This differs from the typical macroalgal community response to stress, which is a decrease in perennial brown algae and proliferation of opportunistic green algae. Cystoseira corniculata was more abundant in autumn and Sargassum vulgare in spring, whereas the articulated coralline alga Jania rubens was more abundant at reference sites in autumn. Diversity decreased with increasing CO2 regardless of season. Our results show that benthic community responses to ocean acidification are strongly affected by season.

Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica

Rising levels of atmospheric CO2 lead to acidification of the ocean and alter seawater carbonate chemistry, which can negatively impact calcifying organisms, including mollusks. In estuaries, exposure to elevated CO2 levels often co-occurs with other stressors, such as reduced salinity, which enhances the acidification trend, affects ion and acid-base regulation of estuarine calcifiers and modifies their response to ocean acidification. We studied the interactive effects of salinity and partial pressure of CO2 (PCO2) on biomineralization and energy homeostasis in juveniles of the eastern oyster, Crassostrea virginica, a common estuarine bivalve. Juveniles were exposed for 11 weeks to one of two environmentally relevant salinities (30 or 15 PSU) either at current atmospheric PCO2 (400 µatm, normocapnia) or PCO2 projected by moderate IPCC scenarios for the year 2100 (700-800 µatm, hypercapnia). Exposure of the juvenile oysters to elevated PCO2 and/or low salinity led to a significant increase in mortality, reduction of tissue energy stores (glycogen and lipid) and negative soft tissue growth, indicating energy deficiency. Interestingly, tissue ATP levels were not affected by exposure to changing salinity and PCO2, suggesting that juvenile oysters maintain their cellular energy status at the expense of lipid and glycogen stores. At the same time, no compensatory upregulation of carbonic anhydrase activity was found under the conditions of low salinity and high PCO2. Metabolic profiling using magnetic resonance spectroscopy revealed altered metabolite status following low salinity exposure; specifically, acetate levels were lower in hypercapnic than in normocapnic individuals at low salinity. Combined exposure to hypercapnia and low salinity negatively affected mechanical properties of shells of the juveniles, resulting in reduced hardness and fracture resistance. Thus, our data suggest that the combined effects of elevated PCO2 and fluctuating salinity may jeopardize the survival of eastern oysters because of weakening of their shells and increased energy consumption.

Impact of CO2 enrichment on organic matter dynamics during nutrient induced coastal phytoplankton blooms

A mesocosm experiment was conducted to investigate the impact of rising fCO2 on the build-up and decline of organic matter during coastal phytoplankton blooms. Five mesocosms (~38 m³ each) were deployed in the Baltic Sea during spring (2009) and enriched with CO2 to yield a gradient of 355-862 µatm. Mesocosms were nutrient fertilized initially to induce phytoplankton bloom development. Changes in particulate and dissolved organic matter concentrations, including dissolved high-molecular weight (>1 kDa) combined carbohydrates, dissolved free and combined amino acids as well as transparent exopolymer particles (TEP), were monitored over 21 days together with bacterial abundance, and hydrolytic extracellular enzyme activities. Overall, organic matter followed well-known bloom dynamics in all CO2 treatments alike. At high fCO2, higher dPOC:dPON during bloom rise, and higher TEP concentrations during bloom peak, suggested preferential accumulation of carbon-rich components. TEP concentration at bloom peak was significantly related to subsequent sedimentation of particulate organic matter. Bacterial abundance increased during the bloom and was highest at high fCO2. We conclude that increasing fCO2 supports production and exudation of carbon-rich components, enhancing particle aggregation and settling, but also providing substrate and attachment sites for bacteria. More labile organic carbon and higher bacterial abundance can increase rates of oxygen consumption and may intensify the already high risk of oxygen depletion in coastal seas in the future.

Molecular fingerprinting and amplicon sequencing of the bacterial biofilm on settlement tiles deployed along natural pH gradients in Papua New Guinea

Bacterial biofilms provide cues for the settlement of marine invertebrates such as coral larvae, and are therefore important for the resilience and recovery of coral reefs. This study aimed to better understand how ocean acidification may affect the community composition and diversity of bacterial biofilms on surfaces under naturally reduced pH conditions. Settlement tiles were deployed at coral reefs in Papua New Guinea along pH gradients created by two CO2 seeps, and upper and lower tiles surfaces were sampled 5 and 13 months after deployment. Automated Ribosomal Intergenic Spacer Analysis were used to characterize more than 200 separate bacterial communities, complemented by amplicon sequencing of the bacterial 16S rRNA gene of 16 samples. The bacterial biofilm consisted predominantly of Alpha-, Gamma- and Deltaproteobacteria, as well as Cyanobacteria, Flavobacteriia and Cytophaga, whereas putative settlement-inducing taxa only accounted for a small fraction of the community. Bacterial biofilm composition was heterogeneous with approximately 25% shared operational taxonomic units between samples. Among the observed environmental parameters, pH only had a weak effect on community composition (R² ~ 1%) and did not affect community richness and evenness. In contrast, there were strong differences between upper and lower surfaces (contrasting in light exposure and grazing intensity). There also appeared to be a strong interaction between bacterial biofilm composition and the macroscopic components of the tile community. Our results suggest that on mature settlement surfaces in situ, pH does not have a strong impact on the composition of bacterial biofilms. Other abiotic and biotic factors such as light exposure and interactions with other organisms may be more important in shaping bacterial biofilms than changes in seawater pH.

Phytoplankton responses and associated carbon cycling during shipboard carbonate chemistry manipulation experiments conducted around Northwest European shelf seas

The ongoing oceanic uptake of anthropogenic carbon dioxide (CO2) is significantly altering the carbonate chemistry of seawater, a phenomenon referred to as ocean acidification. Experimental manipulations have been increasingly used to gauge how continued ocean acidification will potentially impact marine ecosystems and their associated biogeochemical cycles in the future; however, results amongst studies, particularly when performed on natural communities, are highly variable, which may reflect community/environment-specific responses or inconsistencies in experimental approach. To investigate the potential for identification of more generic responses and greater experimentally reproducibility, we devised and implemented a series (n = 8) of short-term (2-4 days) multi-level (>=4 conditions) carbonate chemistry/nutrient manipulation experiments on a range of natural microbial communities sampled in Northwest European shelf seas. Carbonate chemistry manipulations and resulting biological responses were found to be highly reproducible within individual experiments and to a lesser extent between geographically separated experiments. Statistically robust reproducible physiological responses of phytoplankton to increasing pCO2, characterised by a suppression of net growth for small-sized cells (<10 µm), were observed in the majority of the experiments, irrespective of natural or manipulated nutrient status. Remaining between-experiment variability was potentially linked to initial community structure and/or other site-specific environmental factors. Analysis of carbon cycling within the experiments revealed the expected increased sensitivity of carbonate chemistry to biological processes at higher pCO2 and hence lower buffer capacity. The results thus emphasise how biogeochemical feedbacks may be altered in the future ocean.