Prolonged exposure to elevated CO2 promotes growth of the algal symbiont Symbiodinium muscatinei in the intertidal sea anemone Anthopleura elegantissima

Some photosynthetic organisms benefit from elevated levels of carbon dioxide, but studies on the effects of elevated PCO₂ on the algal symbionts of animals are very few. This study investigated the impact of hypercapnia on a photosynthetic symbiosis between the anemone Anthopleura elegantissima and its zooxanthella Symbiodinium muscatinei. Anemones were maintained in the laboratory for 1 week at 37 Pa PCO₂ and pH 8.1. Clonal pairs were then divided into two groups and maintained for 6 weeks under conditions naturally experienced in their intertidal environment, 45 Pa PCO₂, pH 8.1 and 231 Pa PCO₂, pH 7.3. Respiration and photosynthesis were measured after the 1-week acclimation period and after 6 weeks in experimental conditions. Density of zooxanthellal cells, zooxanthellal cell size, mitotic index and chlorophyll content were compared between non-clonemate anemones after the 1-week acclimation period and clonal anemones at the end of the experiment. Anemones thrived in hypercapnia. After 6 weeks, A. elegantissima exhibited higher rates of photosynthesis at 45 Pa (4.2 µmol O₂ g⁻¹ h⁻¹) and 231 Pa (3.30 µmol O₂ g⁻¹ h⁻¹) than at the initial 37 Pa (1.53 µmol O₂ g⁻¹ h⁻¹). Likewise, anemones at 231 Pa received more of their respiratory carbon from zooxanthellae (CZAR  = 78.2%) than those at 37 Pa (CZAR  = 66.6%) but less than anemones at 45 Pa (CZAR  = 137.3%). The mitotic index of zooxanthellae was significantly greater in the hypercapnic anemones than in anemones at lower PCO₂. Excess zooxanthellae were expelled by their hosts, and cell densities, cell diameters and chlorophyll contents were not significantly different between the groups. The response of A. elegantissima to hypercapnic acidification reveals the potential adaptation of an intertidal, photosynthetic symbiosis for high PCO₂.

Productivity gains do not compensate for reduced calcification under near-future ocean acidification in the photosynthetic benthic foraminifera Marginopora vertebralis

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 foraminifera 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, with 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%), while 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 pH_Total 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.

Threshold of carbonate saturation state determined by CO2 control experiment (update)

Acidification of the oceans by increasing anthropogenic CO₂ emissions will cause a decrease in biogenic calcification and an increase in carbonate dissolution. Previous studies have suggested that carbonate dissolution will occur in polar regions and in the deep sea where saturation state with respect to carbonate minerals (Ω) will be <1 by 2100. Recent reports demonstrate nocturnal carbonate dissolution of reefs, despite a Ω_a (aragonite saturation state) value of >1. This is probably related to the dissolution of reef carbonate (Mg-calcite), which is more soluble than aragonite. However, the threshold of Ω for the dissolution of natural sediments has not been clearly determined. We designed an experimental dissolution system with conditions mimicking those of a natural coral reef, and measured the dissolution rates of aragonite in corals, and of Mg-calcite excreted by other marine organisms, under conditions of Ω_a > 1, with controlled seawater pCO₂. The experimental data show that dissolution of bulk carbonate sediments sampled from a coral reef occurs at Ω_a values of 3.7 to 3.8. Mg-calcite derived from foraminifera and coralline algae dissolves at Ω_a values between 3.0 and 3.2, and coralline aragonite starts to dissolve when Ω_a = 1.0. We show that nocturnal carbonate dissolution of coral reefs occurs mainly by the dissolution of foraminiferans and coralline algae in reef sediments.

Effect of ocean acidification and temperature increase on the planktonic foraminifer Neogloboquadrina pachyderma (sinistral)

The present study investigated the effects of ocean acidification and temperature increase on Neogloboquadrina pachyderma (sinistral), the dominant planktonic foraminifer in the Arctic Ocean. Due to the naturally low concentration of CO32− in the Arctic, this foraminifer could be particularly sensitive to the forecast changes in seawater carbonate chemistry. To assess potential responses to ocean acidification and climate change, perturbation experiments were performed on juvenile and adult specimens by manipulating seawater to mimic the present-day carbon dioxide level and a future ocean acidification scenario (end of the century) under controlled (in situ) and elevated temperatures (1 and 4 °C, respectively). Foraminifera mortality was unaffected under all the different experiment treatments. Under low pH, N. pachyderma (s) shell net calcification rates decreased. This decrease was higher (30 %) in the juvenile specimens than decrease observed in the adults (21 %) ones. However, decrease in net calcification was moderated when both, pH decreased and temperature increased simultaneously. When only temperature increased, a net calcification rate for both life stages was not affected. These results show that forecast changes in seawater chemistry would impact calcite production in N. pachyderma (s), possibly leading to a reduction of calcite flux contribution and consequently a decrease in biologic pump efficiency.

Does carbonate ion control planktonic foraminifera shell calcification in upwelling regions?

Planktonic foraminifera shell weights have been recognized as possible proxy for surface water carbonate ion concentration CO₃ and atmospheric CO₂. However, to utilize this proxy, it is important to understand whether shell weights truly reflect surface water CO₃. We utilize shell weights of Globigerina bulloides and Globigerinoides ruber in the size range of 300 to 355 µm from a sediment core recovered from above the lysocline in the upwelling region of western Arabian Sea. Shell weights of G. ruber and G. bulloides show significant correlation with their shell size from recent to 16 kyr, which suggests that shell calcification was controlled by optimum growth conditions. On the other hand, during 16 to 22 kyr, there is no correlation between shell weights and shell size. However, shell weights of G. bulloides exhibit significant negative correlation with annual sea surface temperature which suggests that G. bulloides calcification might have been controlled by surface water CO₃. Therefore it is suggested here that shell weights of G. ruber and G. bulloides cannot be utilized to reconstruct surface water CO₃ in this region.

Independent impacts of calcium and carbonate ion concentration on Mg and Sr incorporation in cultured benthic foraminifera

Laboratory culture experiments were conducted to determine effects of seawater carbonate ion concentration ([CO₃^2-]), and thereby calcite saturation state (Ω), on Mg and Sr incorporation into calcite of two species of shallow-water benthic foraminifera: Ammonia tepida and Heterostegina depressa. Impact on Mg and Sr incorporation by increased seawater [CO₃^2-] and thereby higher Ω, is absent in either species. Comparison to results from a similar culturing experiment, in which Ω was varied as a function of [Ca²⁺], reveals that saturation state affects incorporation of Mg and Sr through calcium- rather than carbonate availability. The similarity in response by both species is surprising since the average Mg/Ca ratio is ~ 70 times higher in H. depressa than in A. tepida. Furthermore, these results suggest that the ions involved in biomineralization (i.e. Ca²⁺ and DIC) are processed by separate cellular transport mechanisms. The similar response of Mg and Sr incorporation in this study suggests that only differences in the Ca²⁺ transport mechanism affect divalent cation partitioning.

Non-lethal effects of ocean acidification on two symbiont-bearing benthic foraminiferal species

We conducted experiments to assess the effect of elevated atmospheric carbon dioxide concentrations on survival, fitness, shell microfabric and growth of two species of symbiont-bearing coral-reef benthic foraminifera, using pCO₂ Ievels similar to those likely to occur in shallow marine pore waters in the decades ahead. Foraminifera were cultured at constant temperature and controlled pCO₂ (385 ppmv, 1000 ppmv, and 2000 ppmv) for six weeks, and total alkalinity and dissolved inorganic carbon were measured to characterize the carbonate chemistry of the incubations. Foraminiferal survival and cellular energy levels were assessed using Adenosine Triphosphate (ATP) analyses, and test microstructure and growth were evaluated using high resolution SEM and image analysis. Fitness and survival of Amphistegina (A.) gibbosa and Archaias (A.) angulatus were not directly affected by elevated pCO₂ and the concomitant decrease in pH and calcite saturation states (Ω_c values) of the seawater (pH and Ω_c values of 8.12, 7.86, and 7.50, and 5.4, 3.4, and 1.5, for control, 1000 ppmv, and 2000 ppmv, respectively). In A. gibbosa, a species precipitating low-Mg calcite, test growth was not affected by elevated pCO₂, but areas of dissolved calcium carbonate were observed even though Ω_c was >1 in all treatments; the fraction of test area dissolved increased with decreasing Ω_c. Similar dissolution was observed in offspring produced in the 2000 ppmv pCO₂ treatments. In A. angulatus, whose tests are more-solubile high-Mg calcite, growth was greatly diminished in the 2000 ppmv pCO₂ treatment compared to the control. These non-lethal effects of ocean acidification – reduced growth in A. angulatus, and enhanced dissolution in A. gibbosa – may reflect differences in test mineralogy for the two species; the long-term ecological consequences of these effects are not yet known.

Contrasting calcification responses to ocean acidification between two reef foraminifers harboring different algal symbionts

Ocean acidification, which like global warming is an outcome of anthropogenic CO₂ emissions, severely impacts marine calcifying organisms, especially those living in coral reef ecosystems. However, knowledge about the responses of reef calcifiers to ocean acidification is quite limited, although coral responses are known to be generally negative. In a culture experiment with two algal symbiont-bearing, reef-dwelling foraminifers, Amphisorus kudakajimensis and Calcarina gaudichaudii, in seawater under five different pCO₂ conditions, 245, 375, 588, 763 and 907 μatm, maintained with a precise pCO₂-controlling technique, net calcification of A. kudakajimensis was reduced under higher pCO₂, whereas calcification of C. gaudichaudii generally increased with increased pCO₂. In another culture experiment conducted in seawater in which bicarbonate ion concentrations were varied under a constant carbonate ion concentration, calcification was not significantly different between treatments in Amphisorus hemprichii, a species closely related to A. kudakajimensis, or in C. gaudichaudii. From these results, we concluded that carbonate ion and CO₂ were the carbonate species that most affected growth of Amphisorus and Calcarina, respectively. The opposite responses of these two foraminifer genera probably reflect different sensitivities to these carbonate species, which may be due to their different symbiotic algae.

Threshold of carbonate saturation state determined by a CO2 control experiment

Acidification of the oceans by increasing anthropogenic CO₂ emissions will cause a decrease in biogenic calcification and an increase in carbonate dissolution. Previous studies suggest that carbonate dissolution will occur in polar regions and in the deep-sea oceans where saturation state with respect to carbonate minerals (Ω) will be <1 by 2100. However, carbonate in coral reefs distributed in tropical zones will not dissolve because the major carbonate in such reefs is aragonite, and the saturation state with respect to aragonite (Ω_a) is >1. Recent reports demonstrated nocturnal carbonate dissolution reefs, despite Ω_a > 1, probably relate to the dissolution of the minor reef carbonate (Mg-calcite), which is more soluble than aragonite. However, the threshold of Ω for the dissolution of natural sediments has not been clearly determined, and it is unknown whether these dissolution processes actually occur under natural conditions. This work describes the measurement of the dissolution rates of coral aragonite and Mg calcite excreted by marine organisms under conditions of Ω_a > 1 with controlled seawater pCO₂. Laboratory experimental data of the present study show that bulk carbonate sediments sampled from a coral reef start to dissolve when Ω_a = 3.7, and dissolution rates increase with falling Ω_a. Mg-calcite derived from foraminifera and coralline algae dissolved when Ω_a reached 3.4, whereas coralline aragonite started to dissolve when Ω_a was almost 1.0. We show that nocturnal carbonate dissolution of coral reefs occurs mainly by the dissolution of foraminifera and coralline algae in reef sediment.

Effect of salinity induced pH changes on benthic foraminifera: a laboratory culture experiment

The coastal water pH varies with salinity. Therefore, to study the effect of salinity induced pH variations on benthic foraminifera, live specimens of Rosalina globularis were subjected to different salinities (10, 15, 20, 25, 30, 35 and 40 ‰) with pH varying from 7.2 to 8.2. A total of 210 specimens were used and the experiment was conducted in replicates. It was observed that the salinity induced pH changes affect the calcification of foraminifera. However the response is not linear. The maximum growth is reported in the specimens kept at 35 ‰ salinity (pH 8.0) while the rest of the specimens maintained at salinity higher or lower than 35 ‰, showed comparatively lesser growth. A significant drop in pH severely hampers the calcification capability of benthic foraminifera. Specimens kept at 10 and 15 ‰ (pH 7.2 and 7.5, respectively) became opaque within two days of lowering the salinity and later on their tests dissolved within 24 and 43 days, respectively. Besides calcification capability, pH also affects reproduction. No specimen reproduced at 10 and 15 ‰ salinity while only a few specimens (3 %) reproduced at 20 ‰. As compared to 10–20 ‰ salinity, ∼60 % reproduction was observed in specimens subjected to 25–40 ‰ salinity. The drop in pH also decreased the calcification rate as specimens at 20 ‰ salinity took twice the time to reach maturity than normal range (25–40 ‰). We conclude that salinity induced drop in pH adversely affects the calcification capability and reproduction in benthic foraminifera. It is inferred that the time required to reach reproductive maturity increases at the extreme salinity tolerance limits. However, beyond a certain limit, a further increase in pH does not affect benthic foraminifera; rather they respond to salinity as per their salinity tolerance range.