Understanding coralline algal responses to ocean acidification: Meta-analysis and synthesis.

Ocean acidification (OA) is a major threat to the persistence of biogenic reefs throughout the world's ocean. Coralline algae are comprised of high magnesium calcite and have long been considered one of the most susceptible taxa to the negative impacts of OA. We summarize these impacts and explore the causes of variability in coralline algal responses using a review/qualitative assessment of all relevant literature, meta-analysis, quantitative assessment of critical responses, and a discussion of physiological mechanisms and directions for future research. We find that most coralline algae experienced reduced abundance, calcification rates, recruitment rates, and declines in pH within the site of calcification in laboratory experiments simulating OA or at naturally elevated CO2 sites. There were no other consistent physiological responses of coralline algae to simulated OA (e.g., photo-physiology, mineralogy, and survival). Calcification/growth was the most frequently measured parameters in coralline algal OA research, and our meta-analyses revealed greater declines in seawater pH were associated with significant decreases in calcification in adults and similar but nonsignificant trends for juveniles. Adults from the family Mesophyllumaceae also tended to be more robust to OA, though there was insufficient data to test similar trends for juveniles. OA was the dominant driver in the majority of laboratory experiments where other local or global drivers were assessed. The interaction between OA and any other single driver was often additive, though factors that changed pH at the surface of coralline algae (light, water motion, epiphytes) acted antagonistically or synergistically with OA more than any other drivers. With advances in experimental design and methodological techniques, we now understand that the physiology of coralline algal calcification largely dictates their responses to OA. However, significant challenges still remain, including improving the geographic and life-history spread of research effort and a need for holistic assessments of physiology.

Decreased Diversity and Abundance of Marine Invertebrates at CO2 Seeps in Warm-Temperate Japan.

Japan has many coastal carbon dioxide seeps as it is one of the most volcanically active parts of the world. These shallow seeps do not have the spectacular aggregations of specialist fauna seen in deep-sea vent systems but they do have gradients in seawater carbonate chemistry that are useful as natural analogues of the effects of ocean acidification on marine biodiversity, ecosystem function and fisheries. Here, we compare macroinvertebrate diversity and abundance on rocky habitats at ambient (mean ≤ 410 µatm) and high (mean 971-1484 µatm) levels of seawater pCO2 in the warm-temperate region of Japan, avoiding areas with toxic sulphur or warm-water conditions. We show that although 70% of intertidal taxa and 40% of shallow subtidal taxa were able to tolerate the high CO2 conditions, there was a marked reduction in the abundance of corals, bivalves and gastropods in acidified conditions. A narrower range of filter feeders, grazers, detritivores, scavengers and carnivores were present at high CO2 resulting in a simplified coastal system that was unable to retain the high standing stocks of marine carbon biomass found in ambient conditions. It is clear that cuts in CO2 emissions would reduce the risks of climate change and ocean acidification impacts on marine biodiversity, shellfish production and biomass in the rocky coastal shores of this region.

Major loss of coralline algal diversity in response to ocean acidification.

Calcified coralline algae are ecologically important in rocky habitats in the marine photic zone worldwide and there is growing concern that ocean acidification will severely impact them. Laboratory studies of these algae in simulated ocean acidification conditions have revealed wide variability in growth, photosynthesis and calcification responses, making it difficult to assess their future biodiversity, abundance and contribution to ecosystem function. Here, we apply molecular systematic tools to assess the impact of natural gradients in seawater carbonate chemistry on the biodiversity of coralline algae in the Mediterranean and the NW Pacific, link this to their evolutionary history and evaluate their potential future biodiversity and abundance. We found a decrease in the taxonomic diversity of coralline algae with increasing acidification with more than half of the species lost in high pCO2 conditions. Sporolithales is the oldest order (Lower Cretaceous) and diversified when ocean chemistry favoured low Mg calcite deposition; it is less diverse today and was the most sensitive to ocean acidification. Corallinales were also reduced in cover and diversity but several species survived at high pCO2 ; it is the most recent order of coralline algae and originated when ocean chemistry favoured aragonite and high Mg calcite deposition. The sharp decline in cover and thickness of coralline algal carbonate deposits at high pCO2 highlighted their lower fitness in response to ocean acidification. Reductions in CO2 emissions are needed to limit the risk of losing coralline algal diversity.

Long-term response of Dictyota dichotoma var. intricata (C. Agardh) Greville (Phaeophyceae) to ocean acidification: Insights from high pCO2 vents.

The ocean acidification may severely affect macroalgal communities of the shallowest coastal habitats where they play relevant structural and functional roles. In this paper were investigated the physiological traits of two populations of Dictyota dichotoma var. intricata, living at two different pH for several generations to assess the reasons of the algae reduced abundance at current (8.1) compared to low pH (6.7). Besides, through transplant experiments, the two populations were analysed for the stress response and reversibility of physiological performance at different pH. The long-term acclimation to high pCO2/low pH favours an ecotype characterised by low energetic costs, higher photochemical efficiency and more resistance to the oxidative stress, compared to individuals living at current pH. These traits promoted the growth and reproduction of the community living at pH 6.7, favouring a lower macroalgal diversity, but a higher ecological success under ocean acidification. The similar behaviour observed between Dictyota living at pH 6.7 and transplanted thalli from pH 6.7 to 8.1, suggested a high tolerance to pH changes in the short-term. On the contrary, adaptive responses may have favoured molecular adjustments on the long-term, as showed by the significant differences between the wild populations at pH 8.1 and 6.7. The overall data indicate that both plasticity and adaptive mechanisms may be the reasons for the success of the brown seaweeds under future high pCO2/low pH. The plasticity due to photochemistry adjustments is likely involved in the early response to environmental changes. Conversely, modifications in the photosynthetic biochemical machinery suggest that more complex adaptive mechanisms occurred in the current population of Dictyota living at pH 6.7. Further studies on population genetics will reveal if any differentiation is taking place at the population level or a local adaptation has already occurred in Dictyota and other brown algae under chronic low pH.

Photosynthesis and mineralogy of Jania rubens at low pH/high pCO2: A future perspective.

Corallinales (Rhodophyta) are high Mg-calcite macroalgae and are considered among the most vulnerable organisms to ocean acidification (OA). These sensitive species play fundamental roles in coastal systems as food source and settlement promoters as well as being involved in reef stabilization, and water carbonate balance. At present only a few studies are focused on erect calcifying macroalgae under low pH/high pCO2 and the contrasting results make difficult to predict the ecological consequences of the OA on the coralline algae. In this paper the physiological reasons behind the resistance of Jania rubens, one of the most common calcareous species, to changing ocean pH are analysed. In particular, we studied the photosynthetic and mineralogical response of J. rubens after a three-week transplant in a natural CO2 vent system. The overall results showed that J. rubens could be able to survive under predicted pH conditions even though with a reduced fitness; nevertheless physiological limits prevent the growth and survival of the species at pH6.7. At low pH (i.e. pH7.5), the maximum and effective PSII efficiency decreased even if the increase of Rubisco expression suggests a compensation effort of the species to cope with the decreased light-driven products. In these circumstances, a pH-driven bleaching phenomenon was also observed. Even though the photosynthesis decreased at low pH, J. rubens maintained unchanged the mineralogical composition and the carbonate content in the cell wall, suggesting that the calcification process may also have a physiological relevance in addition to a structural and/or a protective role. Further studies will confirm the hypotheses on the functional and evolutionary role of the calcification process in coralline algae and on the ecological consequences of the community composition changes under high pCO2 oceans.

Physiological responses of a population of Sargassum vulgare (Phaeophyceae) to high pCO2/low pH: implications for its long-term distribution.

Ocean Acidification (OA) is likely to affect macroalgal diversity in the future with species-specific responses shaping macroalgal communities. In this framework, it is important to focus research on the photosynthetic response of habitat-forming species which have an important structural and functional role in coastal ecosystems. Most of the studies on the impacts of OA involve short-term laboratory or micro/mesocosm experiments. It is more challenging to assess the adaptive responses of macroalgal community to decreasing ocean pH over long-term periods, as they represent the basis of trophic dynamics in marine environments. This work aims to study the physiological traits of a population of Sargassum vulgare that lives naturally in the high pCO2 vents system in Ischia (Italy), in order to predict the species behaviour in a possible OA future scenario. With this purpose, the photosynthetic performance of S. vulgare was studied in a wild, natural population living at low pH (6.7) as well as in a population transplanted from native (6.7) to ambient pH (8.1) for three weeks. The main results show that the photochemical activity and Rubisco expression decreased by 30% after transplanting, whereas the non-photochemical dissipation mechanisms and the photosynthetic pigment content increased by 50% and 40% respectively, in order to compensate for the decrease in photochemical efficiency at low pH. Our data indicated a stress condition for the S. vulgare population induced by pH variation, and therefore a reduced acclimation capability at different pH conditions. The decline of the PSII maximum quantum yield (Fv/Fm) and the increase of PARP enzyme activity in transplanted thalli further supported this hypothesis. The absence of the species at ambient pH conditions close to the vent system, as well as the differences in physiological traits, suggest a local adaptation of S. vulgare at pH6.7, through optimization of photosynthetic performance.