Seawater carbonate chemistry and maximum growth rates of Skeletonema marinoi and Alexandrium ostenfeldii, toxin composition of Alexandrium ostenfeldii in a laboratory experiment

Phytoplankton populations can display high levels of genetic diversity that, when reflected by phenotypic variability, may stabilize a species response to environmental changes. We studied the effects of increased temperature and CO2 availability as predicted consequences of global change, on 16 genetically different isolates of the diatom Skeletonema marinoi from the Adriatic Sea and the Skagerrak (North Sea), and on eight strains of the PST (paralytic shellfish toxin)-producing dinoflagellate Alexandrium ostenfeldii from the Baltic Sea. Maximum growth rates were estimated in batch cultures of acclimated isolates grown for five to 10 generations in a factorial design at 20 and 24 °C, and present day and next century applied atmospheric pCO2, respectively. In both species, individual strains were affected in different ways by increased temperature and pCO2. The strongest response variability, buffering overall effects, was detected among Adriatic S. marinoi strains. Skagerrak strains showed a more uniform response, particularly to increased temperature, with an overall positive effect on growth. Increased temperature also caused a general growth stimulation in A. ostenfeldii, despite notable variability in strain-specific response patterns. Our data revealed a significant relationship between strain-specific growth rates and the impact of pCO2 on growth-slow growing cultures were generally positively affected, while fast growing cultures showed no or negative responses to increased pCO2. Toxin composition of A. ostenfeldii was consistently altered by elevated temperature and increased CO2 supply in the tested strains, resulting in overall promotion of saxitoxin production by both treatments. Our findings suggest that phenotypic variability within populations plays an important role in the adaptation of phytoplankton to changing environments, potentially attenuating short-term effects and forming the basis for selection. In particular, A. ostenfeldii blooms may expand and increase in toxicity under increased water temperature and atmospheric pCO2 conditions, with potentially severe consequences for the coastal ecosystem.

Seawater carbonate chemistry, nutrients and growth rate of coral (Acropora intermedia) and coral-reef seaweed (Lobophora papenfussii) during experiments, 2011

Space competition between corals and seaweeds is an important ecological process underlying coral-reef dynamics. Processes promoting seaweed growth and survival, such as herbivore overfishing and eutrophication, can lead to local reef degradation. Here, we present the case that increasing concentrations of atmospheric CO2 may be an additional process driving a shift from corals to seaweeds on reefs. Coral (Acropora intermedia) mortality in contact with a common coral-reef seaweed (Lobophora papenfussii) increased two- to threefold between background CO2 (400 ppm) and highest level projected for late 21st century (1140 ppm). The strong interaction between CO2 and seaweeds on coral mortality was most likely attributable to a chemical competitive mechanism, as control corals with algal mimics showed no mortality. Our results suggest that coral (Acropora) reefs may become increasingly susceptible to seaweed proliferation under ocean acidification, and processes regulating algal abundance (e.g. herbivory) will play an increasingly important role in maintaining coral abundance.

Seawater carbonate chemistry, survival rate, shell mass growth, shell dissolution and locomotory speed of Limacina retroversa in a laboratory experiment

Anthropogenic carbon dioxide emissions induce ocean acidification, thereby reducing carbonate ion concentration, which may affect the ability of calcifying organisms to build shells. Pteropods, the main planktonic producers of aragonite in the worlds' oceans, may be particularly vulnerable to changes in sea water chemistry. The negative effects are expected to be most severe at high-latitudes, where natural carbonate ion concentrations are low. In this study we investigated the combined effects of ocean acidification and freshening on Limacina retroversa, the dominant pteropod in sub polar areas. Living L. retroversa, collected in Northern Norwegian Sea, were exposed to four different pH values ranging from the pre-industrial level to the forecasted end of century ocean acidification scenario. Since over the past half-century the Norwegian Sea has experienced a progressive freshening with time, each pH level was combined with a salinity gradient in two factorial, randomized experiments investigating shell degradation, swimming behavior and survival. In addition, to investigate shell degradation without any physiologic influence, one perturbation experiments using only shells of dead pteropods was performed. Lower pH reduced shell mass whereas shell dissolution increased with pCO2. Interestingly, shells of dead organisms had a higher degree of dissolution than shells of living individuals. Mortality of Limacina retroversa was strongly affected only when both pH and salinity reduced simultaneously. The combined effects of lower salinity and lower pH also affected negatively the ability of pteropods to swim upwards. Results suggest that the energy cost of maintaining ion balance and avoiding sinking (in low salinity scenario) combined with the extra energy cost necessary to counteract shell dissolution (in high pCO2 scenario), exceed the available energy budget of this organism causing the pteropods to change swimming behavior and begin to collapse. Since L. retroversa play an important role in the transport of carbonates to the deep oceans these findings have significant implications for the mechanisms influencing the inorganic carbon cycle in the sub-polar area.

Effects of CO2 enrichment on photosynthesis, growth, and nitrogen metabolism of the seagrass Zostera noltii

Seagrass ecosystems are expected to benefit from the global increase in CO2 in the ocean because the photosynthetic rate of these plants may be Ci-limited at the current CO2 level. As well, it is expected that lower external pH will facilitate the nitrate uptake of seagrasses if nitrate is cotransported with H+ across the membrane as in terrestrial plants. Here, we investigate the effects of CO2 enrichment on both carbon and nitrogen metabolism of the seagrass Zostera noltii in a mesocosm experiment where plants were exposed for 5 months to two experimental CO2 concentrations (360 and 700 ppm). Both the maximum photosynthetic rate (Pm) and photosynthetic efficiency (a) were higher (1.3- and 4.1-fold, respectively) in plants exposed to CO2-enriched conditions. On the other hand, no significant effects of CO2 enrichment on leaf growth rates were observed, probably due to nitrogen limitation as revealed by the low nitrogen content of leaves. The leaf ammonium uptake rate and glutamine synthetase activity were not significantly affected by increased CO2 concentrations. On the other hand, the leaf nitrate uptake rate of plants exposed to CO2-enriched conditions was fourfold lower than the uptake of plants exposed to current CO2 level, suggesting that in the seagrass Z. noltii nitrate is not cotransported with H+ as in terrestrial plants. In contrast, the activity of nitrate reductase was threefold higher in plant leaves grown at high-CO2 concentrations. Our results suggest that the global effects of CO2 on seagrass production may be spatially heterogeneous and depend on the specific nitrogen availability of each system. Under a CO2 increase scenario, the natural levels of nutrients will probably become limiting for Z. noltii. This potential limitation becomes more relevant because the expected positive effect of CO2 increase on nitrate uptake rate was not confirmed.

Seawater carbonate chemistry and carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi (calcifying strain CCMP 371) during experiments, 2011

Coccolithophores are unicellular phytoplankton that produce calcium carbonate coccoliths as an exoskeleton. Emiliania huxleyi, the most abundant coccolithophore in the world's ocean, plays a major role in the global carbon cycle by regulating the exchange of CO2 across the ocean-atmosphere interface through photosynthesis and calcium carbonate precipitation. As CO2 concentration is rising in the atmosphere, the ocean is acidifying and ammonium (NH4) concentration of future ocean water is expected to rise. The latter is attributed to increasing anthropogenic nitrogen (N) deposition, increasing rates of cyanobacterial N2 fixation due to warmer and more stratified oceans, and decreased rates of nitrification due to ocean acidification. Thus future global climate change will cause oceanic phytoplankton to experience changes in multiple environmental parameters including CO2, pH, temperature and nitrogen source. This study reports on the combined effect of elevated pCO2 and increased NH4 to nitrate (NO3) ratio (NH4/NO3) on E. huxleyi, maintained in continuous cultures for more than 200 generations under two pCO2 levels and two different N sources. Here we show that NH4 assimilation under N-replete conditions depresses calcification at both low and high pCO2, alters coccolith morphology, and increases primary production. We observed that N source and pCO2 synergistically drive growth rates, cell size and the ratio of inorganic to organic carbon. These responses to N source suggest that, compared to increasing CO2 alone, a greater disruption of the organic carbon pump could be expected in response to the combined effect of increased NH4/NO3 ratio and CO2 level in the future acidified ocean. Additional experiments conducted under lower nutrient conditions are needed prior to extrapolating our findings to the global oceans. Nonetheless, our results emphasize the need to assess combined effects of multiple environmental parameters on phytoplankton biology in order to develop accurate predictions of phytoplankton responses to ocean acidification.

Growth response of an early successional assemblage of coralline algae and benthic diatoms to ocean acidification

The sustained absorption of anthropogenically released atmospheric CO2 by the oceans is modifying seawater carbonate chemistry, a process termed ocean acidification (OA). By the year 2100, the worst case scenario is a decline in the average oceanic surface seawater pH by 0.3 units to 7.75. The changing seawater carbonate chemistry is predicted to negatively affect many marine species, particularly calcifying organisms such as coralline algae, while species such as diatoms and fleshy seaweed are predicted to be little affected or may even benefit from OA. It has been hypothesized in previous work that the direct negative effects imposed on coralline algae, and the direct positive effects on fleshy seaweeds and diatoms under a future high CO2 ocean could result in a reduced ability of corallines to compete with diatoms and fleshy seaweed for space in the future. In a 6-week laboratory experiment, we examined the effect of pH 7.60 (pH predicted to occur due to ocean acidification just beyond the year 2100) compared to pH 8.05 (present day) on the lateral growth rates of an early successional, cold-temperate species assemblage dominated by crustose coralline algae and benthic diatoms. Crustose coralline algae and benthic diatoms maintained positive growth rates in both pH treatments. The growth rates of coralline algae were three times lower at pH 7.60, and a non-significant decline in diatom growth meant that proportions of the two functional groups remained similar over the course of the experiment. Our results do not support our hypothesis that benthic diatoms will outcompete crustose coralline algae under future pH conditions. However, while crustose coralline algae were able to maintain their presence in this benthic rocky reef species assemblage, the reduced growth rates suggest that they will be less capable of recolonizing after disturbance events, which could result in reduced coralline cover under OA conditions.

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.

Seawater carbonate chemistry and hatching rate, malformation rate, metamorphosis rate and shell growth of the Pacific abalone in a laboratory experiment

The hatching process of the Pacific abalone Haliotis discus hannai was prolonged at a pH of 7.6 and pH 7.3, and the embryonic developmental success was reduced. The hatching rate at pH 7.3 was significantly (10.8%) lower than that of the control (pH 8.2). The malformation rates at pH 7.9 and pH 8.2 were less than 20% but were 53.8% and 77.3% at pH 7.6 and pH 7.3, respectively. When newly hatched larvae were incubated for 48 h at pH 7.3, only 2.7% of the larvae settled, while more than 70% of the larvae completed settlement in the other three pH treatments. However, most 24 h old larvae could complete metamorphosis in all four pH treatments. Overall, a 0.3-unit reduction in water pH will produce no negative effect on the early development of the Pacific abalone, but further reduction in pH to the values predicted for seawater by the end of this century will have strong detrimental effects.

Effects of light and elevated pCO2 on the growth and photochemical efficiency of Acropora cervicornis

The effects of light and elevated pCO2 on the growth and photochemical efficiency of the critically endangered staghorn coral, Acropora cervicornis, were examined experimentally. Corals were subjected to high and low treatments of CO2 and light in a fully crossed design and monitored using 3D scanning and buoyant weight methodologies. Calcification rates, linear extension, as well as colony surface area and volume of A. cervicornis were highly dependent on light intensity. At pCO2 levels projected to occur by the end of the century from ocean acidification (OA), A. cervicornis exhibited depressed calcification, but no change in linear extension. Photochemical efficiency (F v /F m ) was higher at low light, but unaffected by CO2. Amelioration of OA-depressed calcification under high-light treatments was not observed, and we suggest that the high-light intensity necessary to reach saturation of photosynthesis and calcification in A. cervicornis may limit the effectiveness of this potentially protective mechanism in this species. High CO2 causes depressed skeletal density, but not linear extension, illustrating that the measurement of extension by itself is inadequate to detect CO2 impacts. The skeletal integrity of A. cervicornis will be impaired by OA, which may further reduce the resilience of the already diminished populations of this endangered species.

Effect of ocean acidification on growth and otolith condition of juvenile scup, Stenotomus chrysops

Increasing amounts of atmospheric carbon dioxide (CO2) from human industrial activities are causing changes in global ocean carbonate chemistry, resulting in a reduction in pH, a process termed "ocean acidification." It is important to determine which species are sensitive to elevated levels of CO2 because of potential impacts to ecosystems, marine resources, biodiversity, food webs, populations, and effects on economies. Previous studies with marine fish have documented that exposure to elevated levels of CO2 caused increased growth and larger otoliths in some species. This study was conducted to determine whether the elevated partial pressure of CO2 (pCO2) would have an effect on growth, otolith (ear bone) condition, survival, or the skeleton of juvenile scup, Stenotomus chrysops, a species that supports both important commercial and recreational fisheries. Elevated levels of pCO2 (1200-2600 µatm) had no statistically significant effect on growth, survival, or otolith condition after 8 weeks of rearing. Field data show that in Long Island Sound, where scup spawn, in situ levels of pCO2 are already at levels ranging from 689 to 1828 µatm due to primary productivity, microbial activity, and anthropogenic inputs. These results demonstrate that ocean acidification is not likely to cause adverse effects on the growth and survivability of every species of marine fish. X-ray analysis of the fish revealed a slightly higher incidence of hyperossification in the vertebrae of a few scup from the highest treatments compared to fish from the control treatments. Our results show that juvenile scup are tolerant to increases in seawater pCO2, possibly due to conditions this species encounters in their naturally variable environment and their well-developed pH control mechanisms.

Juvenile sea stars exposed to acidification decrease feeding and growth with no acclimation potential

Ocean acidification has the potential to affect growth and calcification of benthic marine invertebrates, particularly during their early life history. We exposed field-collected juveniles of Asterias rubens from Kiel Fjord (western Baltic Sea) to 3 seawater CO2 partial pressure (pCO2) levels (ranging from around 650 to 3500 µatm) in a long-term (39 wk) and a short-term (6 wk) experiment. In both experiments, survival and calcification were not affected by elevated pCO2. However, feeding rates decreased strongly with increasing pCO2, while aerobic metabolism and NH4+ excretion were not significantly affected by CO2 exposure. Consequently, high pCO2 reduced the scope for growth in A. rubens. Growth rates decreased substantially with increasing pCO2 and were reduced even at pCO2 levels occurring in the habitat today (e.g. during upwelling events). Sea stars were not able to acclimate to higher pCO2, and growth performance did not recover during the long-term experiment. Therefore, the top-down control exerted by this keystone species may be diminished during periods of high environmental pCO2 that already occur occasionally and will be even higher in the future. However, some individuals were able to grow at high rates even at high pCO2, indicating potential for rapid adaption. The selection of adapted specimens of A. rubens in this seasonally acidified habitat may lead to higher CO2 tolerance in adult sea stars of this population compared to the juvenile stage. Future studies need to address the synergistic effects of multiple stressors such as acidification, warming and reduced salinity, which will simultaneously impact the performance of sea stars in this habitat.