Seawater carbonate chemistry and carbon and oxygen isotopes during experiments with planktonic foraminifera Orbulina universa and Globigerina bulloides, 1997

Stable oxygen and carbon isotope measurements on biogenic calcite and aragonite have become standard tools for reconstructing past oceanographic and climatic change. In aquatic organisms, 18O/16O ratios in the shell carbonate are a function of the ratio in the sea water and the calcification temperature (Epstein et al., 1953). In contrast, 13C/12C ratios are controlled by the ratio of dissolved inorganic carbon in sea water and physiological processes such as respiration and symbiont photosynthesis (Spero et al., 1991, doi:10.1029/91PA02022). These geochemical proxies have been used with analyses of foraminifera shells to reconstruct global ice volumes (Shackleton and Opdyke, 1973, doi:10.1016/0033-5894(73)90052-5), surface and deep ocean temperatures (Broecker, 1986, doi:10.1016/0033-5894(86)90087-6; Labeyrie et al., 1987, doi:10.1038/327477a0), ocean circulation changes (Duplessy et al., 1988, doi:10.1029/PA003i003p00343) and glacial-interglacial exchange between the terrestrial and oceanic carbon pools (Sackleton, 1977). Here, we report experimental measurements on living symbiotic and non-symbiotic plankton foraminifera (Orbulina universa and Globigerina bulloides respectively) showing that the 13C/12C and 18O/16O ratios of the calcite shells decrease with increasing seawater [CO3 2-]. Because glacial-period oceans had higher pH and [CO3 2-] than today (Sanyal et al., 1995, doi:10.1038/373234a0), these new relationships confound the standard interpretation of glacial foraminiferal stable-isotope data. In particular, the hypothesis that the glacial-interglacial shift in the 13C/12C ratio was due to a transfer of terrestrial carbon into the ocean(Shackleton ,1977) can be explained alternatively by an increase in ocean alkalinity (Lea et al., 1996). A carbonate-concentration effect could also help explain some of the extreme stable-isotope variations during the Proterozoic and Phanerozoic aeons (Kaufman et al., 1993, doi:10.1016/0012-821X(93)90254-7).

Seawater carbonate chemistry and larval development and settlement of the sea urchin Arbacia lixula in a laboratory experiment

We studied the effects of temperature and pH on larval development, settlement and juvenile survival of a Mediterranean population of the sea urchin Arbacia lixula. Three temperatures (16, 17.5 and 19 °C) were tested at present pH conditions (pHT 8.1). At 19 °C, two pH levels were compared to reflect present average (pHT 8.1) and near-future average conditions (pHT 7.7, expected by 2100). Larvae were reared for 52-days to achieve the full larval development and complete the metamorphosis to the settler stage. We analyzed larval survival, growth, morphology and settlement success. We also tested the carry-over effect of acidification on juvenile survival after 3 days. Our results showed that larval survival and size significantly increased with temperature. Acidification resulted in higher survival rates and developmental delay. Larval morphology was significantly altered by low temperatures, which led to narrower larvae with relatively shorter skeletal rods, but larval morphology was only marginally affected by acidification. No carry-over effects between larvae and juveniles were detected in early settler survival, though settlers from larvae reared at pH 7.7 were significantly smaller than their counterparts developed at pH 8.1. These results suggest an overall positive effect of environmental parameters related to global change on the reproduction of A. lixula, and reinforce the concerns about the increasing negative impact on shallow Mediterranean ecosystems of this post-glacial colonizer.

Seawater carbonate chemistry and resource allocation and extracellular acid-base status in the sea urchin Strongylocentrotus droebachiensis during experiments, 2012

Anthropogenic CO2 emission will lead to an increase in seawater pCO2 of up to 80-100 Pa (800-1000 µatm) within this century and to an acidification of the oceans. Green sea urchins (Strongylocentrotus droebachiensis) occurring in Kattegat experience seasonal hypercapnic and hypoxic conditions already today. Thus, anthropogenic CO2 emissions will add up to existing values and will lead to even higher pCO2 values >200 Pa (>2000 µatm). To estimate the green sea urchins' potential to acclimate to acidified seawater, we calculated an energy budget and determined the extracellular acid base status of adult S. droebachiensis exposed to moderately (102 to 145 Pa, 1007 to 1431 µatm) and highly (284 to 385 Pa, 2800 to 3800 µatm) elevated seawater pCO2 for 10 and 45 days. A 45 - day exposure to elevated pCO2 resulted in a shift in energy budgets, leading to reduced somatic and reproductive growth. Metabolic rates were not significantly affected, but ammonium excretion increased in response to elevated pCO2. This led to decreased O:N ratios. These findings suggest that protein metabolism is possibly enhanced under elevated pCO2 in order to support ion homeostasis by increasing net acid extrusion. The perivisceral coelomic fluid acid-base status revealed that S. droebachiensis is able to fully (intermediate pCO2) or partially (high pCO2) compensate extracellular pH (pHe) changes by accumulation of bicarbonate (maximum increases 2.5 mM), albeit at a slower rate than typically observed in other taxa (10 day duration for full pHe compensation). At intermediate pCO2, sea urchins were able to maintain fully compensated pHe for 45 days. Sea urchins from the higher pCO2 treatment could be divided into two groups following medium-term acclimation: one group of experimental animals (29%) contained remnants of food in their digestive system and maintained partially compensated pHe (+2.3 mM HCO3), while the other group (71%) exhibited an empty digestive system and a severe metabolic acidosis (-0.5 pH units, -2.4 mM HCO3). There was no difference in mortality between the three pCO2 treatments. The results of this study suggest that S. droebachiensis occurring in the Kattegat might be pre-adapted to hypercapnia due to natural variability in pCO2 in its habitat. We show for the first time that some echinoderm species can actively compensate extracellular pH. Seawater pCO2 values of >200 Pa, which will occur in the Kattegat within this century during seasonal hypoxic events, can possibly only be endured for a short time period of a few weeks. Increases in anthropogenic CO2 emissions and leakages from potential sub-seabed CO2 storage (CCS) sites thus impose a threat to the ecologically and economically important species S. droebachiensis.

Seawater carbonate chemistry and copepod Centropages tenuiremis feeding, filtering and respiration rate during experiments, 2012

Climate change mediates marine chemical and physical environments and therefore influences marine organisms. While increasing atmospheric CO2 level and associated ocean acidification has been predicted to stimulate marine primary productivity and may affect community structure, the processes that impact food chain and biological CO2 pump are less documented. We hypothesized that copepods, as the secondary marine producer, may respond to future changes in seawater carbonate chemistry associated with ocean acidification due to increasing atmospheric CO2 concentration. Here, we show that the copepod, Centropages tenuiremis, was able to perceive the chemical changes in seawater induced under elevated CO2 concentration (>1700 µatm, pH < 7.60) with avoidance strategy. The copepod's respiration increased at the elevated CO2 (1000 µatm), associated acidity (pH 7.83) and its feeding rates also increased correspondingly, except for the initial acclimating period, when it fed less. Our results imply that marine secondary producers increase their respiration and feeding rate in response to ocean acidification to balance the energy cost against increased acidity and CO2 concentration.

Seawater carbonate chemistry and combined mechanistic effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101, 2010

The marine diazotrophic cyanobacterium Trichodesmium responds to elevated atmospheric CO2 partial pressure (pCO2) with higher N2 fixation and growth rates. To unveil the underlying mechanisms, we examined the combined influence of pCO2(150 and 900 µatm) and light (50 and 200 µmol photons m-2 s-1) on TrichodesmiumIMS101. We expand on a complementary study that demonstrated that while elevated pCO2 enhanced N2 fixation and growth, oxygen evolution and carbon fixation increased mainly as a response to high light. Here, we investigated changes in the photosynthetic fluorescence parameters of photosystem II, in ratios of the photosynthetic units (photosystem I:photosystem II), and in the pool sizes of key proteins involved in the fixation of carbon and nitrogen as well as their subsequent assimilation. We show that the combined elevation in pCO2 and light controlled the operation of the CO2-concentrating mechanism and enhanced protein activity without increasing their pool size. Moreover, elevated pCO2 and high light decreased the amounts of several key proteins (NifH, PsbA, and PsaC), while amounts of AtpB and RbcL did not significantly change. Reduced investment in protein biosynthesis, without notably changing photosynthetic fluxes, could free up energy that can be reallocated to increase N2 fixation and growth at elevated pCO2 and light. We suggest that changes in the redox state of the photosynthetic electron transportchain and posttranslational regulation of key proteins mediate the high flexibility in resources and energy allocation in Trichodesmium. This strategy should enableTrichodesmium to flourish in future surface oceans characterized by elevated pCO2, higher temperatures, and high light.

Seawater carbonate chemistry, respiration, maximum photochemical efficiency and mortality of brooded larvae of Pocillopora//damicornis in a laboratory experiment

To evaluate the effects of temperature and pCO2 on coral larvae, brooded larvae of Pocillopora damicornis from Nanwan Bay, Taiwan (21°56.179' N, 120°44.85' E), were exposed to ambient (419-470 µatm) and high (604-742 µatm) pCO2 at ~25 and ~29 °C in two experiments conducted in March 2010 and March 2012. Larvae were sampled from four consecutive lunar days (LD) synchronized with spawning following the new moon, incubated in treatments for 24 h, and measured for respiration, maximum photochemical efficiency of PSII (F v/F m), and mortality. The most striking outcome was a strong effect of time (i.e., LD) on larvae performance: respiration was affected by an LD × temperature interaction in 2010 and 2012, as well as an LD × pCO2 × temperature interaction in 2012; F v/F m was affected by LD in 2010 (but not 2012); and mortality was affected by an LD × pCO2 interaction in 2010, and an LD × temperature interaction in 2012. There were no main effects of pCO2 in 2010, but in 2012, high pCO2 depressed metabolic rate and reduced mortality. Therefore, differences in larval performance depended on day of release and resulted in varying susceptibility to future predicted environmental conditions. These results underscore the importance of considering larval brood variation across days when designing experiments. Subtle differences in experimental outcomes between years suggest that transgenerational plasticity in combination with unique histories of exposure to physical conditions can modulate the response of brooded coral larvae to climate change and ocean acidification.

Coccolithophore sensitivities to changing carbonate chemistry - an ecological framework

Coccolithophores are a group of unicellular phytoplankton species whose ability to calcify has a profound influence on biogeochemical element cycling. Calcification rates are controlled by a large variety of biotic and abiotic factors. Among these factors, carbonate chemistry has gained considerable attention during the last years as coccolithophores have been identified to be particularly sensitive to ocean acidification. Despite intense research in this area, a general concept harmonizing the numerous and sometimes (seemingly) contradictory responses of coccolithophores to changing carbonate chemistry is still lacking to date. Here, we present the "substrate-inhibitor concept" which describes the dependence of calcification rates on carbonate chemistry speciation. It is based on observations that calcification rate scales positively with bicarbonate (HCO3-), the primary substrate for calcification, and carbon dioxide (CO2), which can limit cell growth, whereas it is inhibited by protons (H+). This concept was implemented in a model equation, tested against experimental data, and then applied to understand and reconcile the diverging responses of coccolithophorid calcification rates to ocean acidification obtained in culture experiments. Furthermore, we (i) discuss how other important calcification-influencing factors (e.g. temperature and light) could be implemented in our concept and (ii) embed it in Hutchinson's niche theory, thereby providing a framework for how carbonate chemistry-induced changes in calcification rates could be linked with changing coccolithophore abundance in the oceans. Our results suggest that the projected increase of H+ in the near future (next couple of thousand years), paralleled by only a minor increase of inorganic carbon substrate, could impede calcification rates if coccolithophores are unable to fully adapt. However, if calcium carbonate (CaCO3) sediment dissolution and terrestrial weathering begin to increase the oceans' HCO3- and decrease its H+ concentrations in the far future (10 -100 kyears), coccolithophores could find themselves in carbonate chemistry conditions which may be more favorable for calcification than they were before the Anthropocene.

Chemistry and biological processes during experiments with spider crab Hyas araneus

The combined effects of ocean warming and acidification were compared in larvae from two popula- tions of the cold-eurythermal spider crab Hyas araneus, from one of its southernmost populations (around Helgo- land, southern North Sea, 54°N, habitat temperature 3-18°C; collection: January 2008, hatch: January-February 2008) and from one of its northernmost populations (Svalbard, North Atlantic, 79°N, habitat temperature 0-6°C; collection: July 2008, hatch: February-April 2009). Larvae were exposed to temperatures of 3, 9 and 15°C combined with present-day normocapnic (380 ppm CO2) and projected future CO2 concentrations (710 and 3,000 ppm CO2). Calcium content of whole larvae was measured in freshly hatched Zoea I and after 3, 7 and 14 days during the Megalopa stage. Significant differences between Helgoland and Svalbard Megalopae were observed at all investigated temperatures and CO2 condi- tions. Under 380 ppm CO2, the calcium content increased with rising temperature and age of the larvae. At 3 and 9°C, Helgoland Megalopae accumulated more calcium than Svalbard Megalopae. Elevated CO2 levels, especially 3,000 ppm, caused a reduction in larval calcium contents at 3 and 9°C in both populations. This effect set in early, at 710 ppm CO2 only in Svalbard Megalopae at 9°C. Fur- thermore, at 3 and 9°C Megalopae from Helgoland replenished their calcium content to normocapnic levels and more rapidly than Svalbard Megalopae. However, Svalbard Megalopae displayed higher calcium contents under 3,000 ppm CO2 at 15°C. The findings of a lower capacity for calcium incorporation in crab larvae living at the cold end of their distribution range suggests that they might be more sensitive to ocean acidification than those in temperate regions.

Seawater carbonate chemistry and Amphiprion melanopus activity during experiments, 2011

Two of the major threats to coral reefs are increasing sea surface temperature and ocean acidification, both of which result from rising concentrations of atmospheric carbon dioxide (CO2). Recent evidence suggests that both increased water temperature and elevated levels of dissolved CO2 can change the behaviors of fishes in ways that reduce individual fitness, however the interacting effects of these variables are unknown. We used a fully factorial experiment to test the independent and interactive effects of temperature (3 levels: 28.5, 30, and 31.5 °C) and pCO2 (3 levels: averaging 420, 530, and 960 µatm) on food consumption and activity level of juvenile anemonefish Amphiprion melanopus (Bleeker 1852). Experimental levels were consistent with current-day ocean conditions and predictions for mid-century and late-century based on atmospheric CO2 projections. Sibling fish were reared for 21 days from the end of their larval phase in each of the nine treatments, at which time behavioral observations were conducted. Food consumption and foraging activity decreased at the highest temperature. In isolation, CO2 level did not significantly affect behavior; however, there was an interaction with temperature. While rearing at high temperature (31.5 °C) and control (420 µatm) or moderate (530 µatm) CO2 resulted in a reduction of food consumption and foraging activity, rearing at high temperature and high CO2 (960 µatm) resulted in an elevation in these behaviors. Maintaining food consumption and foraging activity in high temperature and CO2 conditions may reduce energy efficiency if the thermal optimum for food assimilation and growth has been exceeded. Maintaining foraging effort might increase predation vulnerability. These results suggest that changes in foraging behaviors caused by the interactive effects of increased SST and CO2 could have significant effects on the growth and survival of juvenile reef fishes by late century.

Seawater carbonate chemistry, calcification and Zn uptake during experiments with coral Stylophora pistillata, 2011

Many studies have investigated the effect of an increase in pCO2 on coral calcification and photosynthesis but the physiological consequences are still relatively speculative. We investigated the effects of ocean acidification on zinc incorporation and gross calcification in the scleractinian coral Stylophora pistillata. Zn is an essential element for health and growth of corals. Colonies were maintained at normal pHT (8.1) and at two low-pH conditions (7.8 and 7.5) during 5 weeks. Corals were exposed to 65Zn dissolved in seawater to assess uptake rates of this element. After 5 weeks, 65Zn activity measured in the whole coral and in the two compartments: tissue and skeleton, differed significantly between pH conditions with concentration factors higher at pHT 8.1, compared to lower pH. Zn is therefore taken less efficiently by corals at reduced pH. Their gross calcification, as measured by 45Ca incorporation, photosynthesis and photosynthetic efficiency did not change with pH even at the lowest level.

Seawater carbonate chemistry and calcification during experiments with coral communities, 2000

Previous studies have demonstrated that coral and algal calcification is tightly regulated by the calcium carbonate saturation state of seawater. This parameter is likely to decrease in response to the increase of dissolved CO2 resulting from the global increase of the partial pressure of atmospheric CO2. We have investigated the response of a coral reef community dominated by scleractinian corals, but also including other calcifying organisms such as calcareous algae, crustaceans, gastropods and echinoderms, and kept in an open-top mesocosm. Seawater pCO2 was modified by manipulating the pCO2 of air used to bubble the mesocosm. The aragonite saturation state (omega arag) of the seawater in the mesocosm varied between 1.3 and 5.4. Community calcification decreased as a function of increasing pCO2 and decreasing omega arag. This result is in agreement with previous data collected on scleractinian corals, coralline algae and in a reef mesocosm, even though some of these studies did not manipulate CO2 directly. Our data suggest that the rate of calcification during the last glacial maximum might have been 114% of the preindustrial rate. Moreover, using the average emission scenario (IS92a) of the Intergovernmental Panel on Climate Change, we predict that the calcification rate of scleractinian-dominated communities may decrease by 21% between the pre-industrial period (year 1880) and the time at which pCO2 will double (year 2065).

Seawater carbonate chemistry, fertilization and early development of the coral eating crown-of-thorns starfish, Acanthaster planci in a laboratory experiment

Outbreaks of crown-of-thorns starfish (COTS), Acanthaster planci, contribute to major declines of coral reef ecosystems throughout the Indo-Pacific. As the oceans warm and decrease in pH due to increased anthropogenic CO2 production, coral reefs are also susceptible to bleaching, disease and reduced calcification. The impacts of ocean acidification and warming may be exacerbated by COTS predation, but it is not known how this major predator will fare in a changing ocean. Because larval success is a key driver of population outbreaks, we investigated the sensitivities of larval A. planci to increased temperature (2-4 °C above ambient) and acidification (0.3-0.5 pH units below ambient) in flow-through cross-factorial experiments (3 temperature × 3 pH/pCO2 levels). There was no effect of increased temperature or acidification on fertilization or very early development. Larvae reared in the optimal temperature (28 °C) were the largest across all pH treatments. Development to advanced larva was negatively affected by the high temperature treatment (30 °C) and by both experimental pH levels (pH 7.6, 7.8). Thus, planktonic life stages of A. planci may be negatively impacted by near-future global change. Increased temperature and reduced pH had an additive negative effect on reducing larval size. The 30 °C treatment exceeded larval tolerance regardless of pH. As 30 °C sea surface temperatures may become the norm in low latitude tropical regions, poleward migration of A. planci may be expected as they follow optimal isotherms. In the absence of acclimation or adaptation, declines in low latitude populations may occur. Poleward migration will be facilitated by strong western boundary currents, with possible negative flow-on effects on high latitude coral reefs. The contrasting responses of the larvae of A. planci and those of its coral prey to ocean acidification and warming are considered in context with potential future change in tropical reef ecosystems.

Incorporation of Mg and Sr in calcite of cultured benthic foraminifera (Heterostegina depressa and Ammonia tepida) and seawater carbonate chemistry, 2010

We investigated the effect of the calcium concentration in seawater and thereby the calcite saturation state (omega) on the magnesium and strontium incorporation into benthic foraminiferal calcite under laboratory conditions. For this purpose individuals of the shallow-water species Heterostegina depressa (precipitating high-Mg calcite, symbiont-bearing) and Ammonia tepida (low-Mg calcite, symbiont-barren) were cultured in media under a range of [Ca2+], but similar Mg/Ca ratios. Trace element/Ca ratios of newly formed calcite were analysed with Laser Ablation Inductively Coupled Plasma Mass Spectrometry (LA-ICP-MS) and normalized to the seawater elemental composition using the equation DTE=(TE/Cacalcite)/(TE/Caseawater). The culturing study shows that DMg of A. tepida significantly decreases with increasing omega at a gradient of -4.3x10-5 per omega unit. The DSr value of A. tepida does not change with omega, suggesting that fossil Sr/Ca in this species may be a potential tool to reconstruct past variations in seawater Sr/Ca. Conversely, DMg of H. depressa shows only a minor decrease with increasing omega, while DSr increases considerably with omega at a gradient of 0.009 per omega unit. The different responses to seawater chemistry of the two species may be explained by a difference in the calcification pathway that is, at the same time, responsible for the variation in the total Mg incorporation between the two species. Since the Mg/Ca ratio in H. depressa is 50-100 times higher than that of A. tepida, it is suggested that the latter exhibits a mechanism that decreases the Mg/Ca ratio of the calcification fluid, while the high-Mg calcite forming species may not have this physiological tool. If the dependency of Mg incorporation on seawater [Ca2+] is also valid for deep-sea benthic foraminifera typically used for paleostudies, the higher Ca concentrations in the past may potentially bias temperature reconstructions to a considerable degree. For instance, 25 Myr ago Mg/Ca ratios in A. tepida would have been 0.2 mmol/mol lower than today, due to the 1.5 times higher [Ca2+] of seawater, which in turn would lead to a temperature underestimation of more than 2 °C.