Nutrient availability affects the response of juvenile corals and the endosymbionts to ocean acidification

The interactive effects of nutrient availability and ocean acidification on coral calcification were investigated using post-settlement juvenile corals of Acropora digitifera cultured in nutrient-sufficient or nutrient-depleted seawater for 4 d and then exposed to seawater with different partial pressure of carbon dioxide () conditions (38.8 or 92.5 Pa) for 10 d. After the nutrient pretreatment, corals in the high nutrient condition (HN corals) had a significantly higher abundance of endosymbiotic algae than did those in the low nutrient condition (LN corals). The high abundance of endosymbionts in HN corals was reduced as a result of subsequent seawater acidification, and the chlorophyll a per algal cell increased. The photosynthetic oxygen production rate by endosymbionts was enhanced by the acidified seawater regardless of the nutrient treatment, indicating that the reduction in endosymbiont density in HN corals due to acidification was compensated for by the increase in chlorophyll a per cell. Though the photosynthetic rate increased in the acidified conditions for both LN and HN corals, the calcification rate significantly decreased for LN corals but not for HN corals. The acquisition of nutrients from seawater, rather than the increase in alkalinity caused by photosynthesis, might effectively alleviate the negative response of coral calcification to seawater acidification, suggesting that the response of corals and their endosymbionts to ocean acidification can be influenced by nutrient conditions.

Seawater carbonate chemistry and processes during experiments with Emiliania huxleyi (PML B93/11A)

The formation of calcareous skeletons by marine planktonic organisms and their subsequent sinking to depth generates a continuous rain of calcium carbonate to the deep ocean and underlying sediments. This is important in regulating marine carbon cycling and ocean-atmosphere CO2 exchange. The present rise in atmospheric CO2 levels causes significant changes in surface ocean pH and carbonate chemistry. Such changes have been shown to slow down calcification in corals and coralline macroalgae, but the majority of marine calcification occurs in planktonic organisms. Here we report reduced calcite production at increased CO2 concentrations in monospecific cultures of two dominant marine calcifying phytoplankton species, the coccolithophorids Emiliania huxleyi and Gephyrocapsa oceanica . This was accompanied by an increased proportion of malformed coccoliths and incomplete coccospheres. Diminished calcification led to a reduction in the ratio of calcite precipitation to organic matter production. Similar results were obtained in incubations of natural plankton assemblages from the north Pacific ocean when exposed to experimentally elevated CO2 levels. We suggest that the progressive increase in atmospheric CO2 concentrations may therefore slow down the production of calcium carbonate in the surface ocean. As the process of calcification releases CO2 to the atmosphere, the response observed here could potentially act as a negative feedback on atmospheric CO2 levels.

Seawater carbonate chemistry during experiments with Stylophora pistillata, 2008

The decrease in the saturation state of seawater, following seawater acidification, is believed to be the main factor leading to a decrease in the calcification of marine organisms. To provide a physiological explanation for this phenomenon, the effect of seawater acidification was studied on the calcification and photosynthesis of the scleractinian tropical coral Stylophora pistillata. Coral nubbins were incubated for 8 days at three different pH (7.6, 8.0, and 8.2). To differentiate between the effects of the various components of the carbonate chemistry (pH, CO32, HCO3, CO2), tanks were also maintained under similar pH, but with 2-mM HCO3 added to the seawater. The addition of 2-mM bicarbonate significantly increased the photosynthesis in S. pistillata, suggesting carbon-limited conditions. Conversely, photosynthesis was insensitive to changes in pH and pCO2. Seawater acidification decreased coral calcification by ca. 0.1-mg CaCO3 g-1 d-1 for a decrease of 0.1 pH units. This correlation suggested that seawater acidification affected coral calcification by decreasing the availability of the CO32 substrate for calcification. However, the decrease in coral calcification could also be attributed either to a decrease in extra- or intracellular pH or to a change in the buffering capacity of the medium, impairing supply of CO32 from HCO3.

Seawater carbonate chemistry and biological processes of Mytilus edulis during experiments, 2011

Progressive ocean acidification due to anthropogenic CO2 emissions will alter marine ecosytem processes. Calcifying organisms might be particularly vulnerable to these alterations in the speciation of the marine carbonate system. While previous research efforts have mainly focused on external dissolution of shells in seawater under saturated with respect to calcium carbonate, the internal shell interface might be more vulnerable to acidification. In the case of the blue mussel Mytilus edulis, high body fluid pCO2 causes low pH and low carbonate concentrations in the extrapallial fluid, which is in direct contact with the inner shell surface. In order to test whether elevated seawater pCO2 impacts calcification and inner shell surface integrity we exposed Baltic M. edulis to four different seawater pCO2 (39, 142, 240, 405 Pa) and two food algae (310-350 cells mL-1 vs. 1600-2000 cells mL-1) concentrations for a period of seven weeks during winter (5°C). We found that low food algae concentrations and high pCO2 values each significantly decreased shell length growth. Internal shell surface corrosion of nacreous ( = aragonite) layers was documented via stereomicroscopy and SEM at the two highest pCO2 treatments in the high food group, while it was found in all treatments in the low food group. Both factors, food and pCO2, significantly influenced the magnitude of inner shell surface dissolution. Our findings illustrate for the first time that integrity of inner shell surfaces is tightly coupled to the animals' energy budget under conditions of CO2 stress. It is likely that under food limited conditions, energy is allocated to more vital processes (e.g. somatic mass maintenance) instead of shell conservation. It is evident from our results that mussels exert significant biological control over the structural integrity of their inner shell surfaces.

Seawater carbonate chemistry and Astrangia poculata mass and zooxanthellate during experiments, 2012

The effects of nutrients and pCO2 on zooxanthellate and azooxanthellate colonies of the temperate scleractinian coral Astrangia poculata (Ellis and Solander, 1786) were investigated at two different temperatures (16 °C and 24 °C). Corals exposed to elevated pCO2 tended to have lower relative calcification rates, as estimated from changes in buoyant weights. Experimental nutrient enrichments had no significant effect nor did there appear to be any interaction between pCO2 and nutrients. Elevated pCO2 appeared to have a similar effect on coral calcification whether zooxanthellae were present or absent at 16 °C. However, at 24 °C, the interpretation of the results is complicated by a significant interaction between gender and pCO2 for spawning corals. At 16 °C, gamete release was not observed, and no gender differences in calcification rates were observed - female and male corals showed similar reductions in calcification rates in response to elevated CO2 (15% and 19% respectively). Corals grown at 24 °C spawned repeatedly and male and female corals exhibited two different growth rate patterns - female corals grown at 24 °C and exposed to CO2 had calcification rates 39% lower than females grown at ambient CO2, while males showed a non-significant decline of 5% under elevated CO2. The increased sensitivity of females to elevated pCO2 may reflect a greater investment of energy in reproduction (egg production) relative to males (sperm production). These results suggest that both gender and spawning are important factors in determining the sensitivity of corals to ocean acidification, and considering these factors in future research may be critical to predicting how the population structures of marine calcifiers will change in response to ocean acidification.

Seawater carbonate chemistry, nutrients and growth rate during experiments with coral Astrangia poculata and field observations, 2010

Zooxanthellate colonies of the scleractinian coral Astrangia poculata were grown under combinations of ambient and elevated nutrients (5 µM NO, 0.3 µM PO4, and 2nM Fe) and CO2 (780 ppmv) treatments for a period of 6 months. Coral calcification rates, estimated from buoyant weights, were not significantly affected by moderately elevated nutrients at ambient CO2 and were negatively affected by elevated CO2 at ambient nutrient levels. However, calcification by corals reared under elevated nutrients combined with elevated CO2 was not significantly different from that of corals reared under ambient conditions, suggesting that CO2 enrichment can lead to nutrient limitation in zooxanthellate corals. A conceptual model is proposed to explain how nutrients and CO2 interact to control zooxanthellate coral calcification. Nutrient limited corals are unable to utilize an increase in dissolved inorganic carbon (DIC) as nutrients are already limiting growth, thus the effect of elevated CO2 on saturation state drives the calcification response. Under nutrient replete conditions, corals may have the ability to utilize more DIC, thus the calcification response to CO2 becomes the product of a negative effect on saturation state and a positive effect on gross carbon fixation, depending upon which dominates, the calcification response can be either positive or negative. This may help explain how the range of coral responses found in different studies of ocean acidification can be obtained.

Effects of ocean acidification on population dynamics and community structure of crustose coralline algae

Calcification and growth of crustose coralline algae (CCA) are affected by elevated seawater pCO2 and associated changes in carbonate chemistry. However, the effects of ocean acidification (OA) on population and community-level responses of CCA have barely been investigated. We explored changes in community structure and population dynamics (size structure and reproduction) of CCA in response to OA. Recruited from an experimental flow-through system, CCA settled onto the walls of plastic aquaria and developed under exposure to one of three pCO2 treatments (control [present day, 389±6 ppm CO2], medium [753±11 ppm], and high [1267±19 ppm]). Elevated pCO2 reduced total CCA abundance and affected community structure, in particular the density of the dominant species Pneophyllum sp. and Porolithon onkodes. Meanwhile, the relative abundance of P. onkodes declined from 24% under control CO2 to 8.3% in high CO2 (65% change), while the relative abundance of Pneophyllum sp. remained constant. Population size structure of P. onkodes differed significantly across treatments, with fewer larger individuals under high CO2. In contrast, the population size structure and number of reproductive structures (conceptacles) per crust of Pneophyllum sp. was similar across treatments. The difference in the magnitude of the response of species abundance and population size structure between species may have the potential to induce species composition changes in the future. These results demonstrate that the impacts of OA on key coral reef builders go beyond declines in calcification and growth, and suggest important changes to aspects of population dynamics and community ecology.

Experiment: Competition between calcifying and noncalcifying temperate marine macroalgae under elevated CO2 levels

Since pre-industrial times, uptake of anthropogenic CO2 by surface ocean waters has caused a documented change of 0.1 pH units. Calcifying organisms are sensitive to elevated CO2 concentrations due to their calcium carbonate skeletons. In temperate rocky intertidal environments, calcifying and noncalcifying macroalgae make up diverse benthic photoautotrophic communities. These communities may change as calcifiers and noncalcifiers respond differently to rising CO2 concentrations. In order to test this hypothesis, we conducted an 86?d mesocosm experiment to investigate the physiological and competitive responses of calcifying and noncalcifying temperate marine macroalgae to 385, 665, and 1486 µatm CO2. We focused on comparing 2 abundant red algae in the Northeast Atlantic: Corallina officinalis (calcifying) and Chondrus crispus (noncalcifying). We found an interactive effect of CO2 concentration and exposure time on growth rates of C. officinalis, and total protein and carbohydrate concentrations in both species. Photosynthetic rates did not show a strong response. Calcification in C. officinalis showed a parabolic response, while skeletal inorganic carbon decreased with increasing CO2. Community structure changed, as Chondrus crispus cover increased in all treatments, while C. officinalis cover decreased in both elevated-CO2 treatments. Photochemical parameters of other species are also presented. Our results suggest that CO2 will alter the competitive strengths of calcifying and noncalcifying temperate benthic macroalgae, resulting in different community structures, unless these species are able to adapt at a rate similar to or faster than the current rate of increasing sea-surface CO2 concentrations.

Effect of increased pCO2 level on early shell development in great scallop (Pecten maximus Lamarck) larvae

As a result of high anthropogenic CO2 emissions, the concentration of CO2 in the oceans has increased, causing a decrease in pH, known as ocean acidification (OA). Numerous studies have shown negative effects on marine invertebrates, and also that the early life stages are the most sensitive to OA. We studied the effects of OA on embryos and unfed larvae of the great scallop (Pecten maximus Lamarck), at pCO(2) levels of 469 (ambient), 807, 1164, and 1599 µatm until seven days after fertilization. To our knowledge, this is the first study on OA effects on larvae of this species. A drop in pCO(2) level the first 12 h was observed in the elevated pCO(2) groups due to a discontinuation in water flow to avoid escape of embryos. When the flow was restarted, pCO(2) level stabilized and was significantly different between all groups. OA affected both survival and shell growth negatively after seven days. Survival was reduced from 45% in the ambient group to 12% in the highest pCO(2) group. Shell length and height were reduced by 8 and 15 %, respectively, when pCO(2) increased from ambient to 1599 µatm. Development of normal hinges was negatively affected by elevated pCO(2) levels in both trochophore larvae after two days and veliger larvae after seven days. After seven days, deformities in the shell hinge were more connected to elevated pCO(2) levels than deformities in the shell edge. Embryos stained with calcein showed fluorescence in the newly formed shell area, indicating calcification of the shell at the early trochophore stage between one and two days after fertilization. Our results show that P. maximus embryos and early larvae may be negatively affected by elevated pCO(2) levels within the range of what is projected towards year 2250, although the initial drop in pCO(2) level may have overestimated the effect of the highest pCO(2) levels. Future work should focus on long-term effects on this species from hatching, throughout the larval stages, and further into the juvenile and adult stages.

Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory incubations

To identify the properties of taxa sensitive and resistant to ocean acidification (OA), we tested the hypothesis that coral reef calcifiers differ in their sensitivity to OA as predictable outcomes of functional group alliances determined by conspicuous traits. We contrasted functional groups of eight corals and eight calcifying algae defined by morphology in corals and algae, skeletal structure in corals, spatial location of calcification in algae, and growth rate in corals and algae. The responses of calcification to OA were unrelated to morphology and skeletal structure in corals; they were, however, affected by growth rate in corals and algae (fast calcifiers were more sensitive than slow calcifiers), and by the site of calcification and morphology in algae. Species assemblages characterized by fast growth, and for algae, also cell-wall calcification, are likely to be ecological losers in the future ocean. This shift in relative success will affect the relative and absolute species abundances as well as the goods and services provided by coral reefs.

Interactions among chronic and acute impacts on coral recruits: the importance of size-escape thresholds

Newly settled recruits typically suffer high mortality from disturbances, but rapid growth reduces their mortality once size-escape thresholds are attained. Ocean acidification (OA) reduces the growth of recruiting benthic invertebrates, yet no direct effects on survivorship have been demonstrated. We tested whether the reduced growth of coral recruits caused by OA would increase their mortality by prolonging their vulnerability to an acute disturbance: fish herbivory on surrounding algal turf. After two months' growth in ambient or elevated CO2 levels, the linear extension and calcification of coral (Acropora millepora) recruits decreased as CO2 partial pressure (pCO2) increased. When recruits were subjected to incidental fish grazing, their mortality was inversely size dependent. However, we also found an additive effect of pCO2 such that recruit mortality was higher under elevated pCO2 irrespective of size. Compared to ambient conditions, coral recruits needed to double their size at the highest pCO2 to escape incidental grazing mortality. This general trend was observed with three groups of predators (blenny, surgeonfish, and parrotfish), although the magnitude of the fish treatment varied among species. Our study demonstrates the importance of size-escape thresholds in early recruit survival and how OA can shift these thresholds, potentially intensifying population bottlenecks in benthic invertebrate recruitment.

Seawater carbonate chemistry and biological processes during experiments with four strains of Emiliania huxleyi

Four strains of the coccolithophore E. huxleyi (RCC1212, RCC1216, RCC1238, RCC1256) were grown in dilute batch culture at four CO2 levels ranging from ~200 µatm to ~1200 µatm. Growth rate, particulate organic carbon content, and particulate inorganic carbon content were measured, and organic and inorganic carbon production calculated. The four strains did not show a uniform response to carbonate chemistry changes in any of the analysed parameters and none of the four strains displayed a response pattern previously described for this species. We conclude that the sensitivity of different strains of E. huxleyi to acidification differs substantially and that this likely has a genetic basis. We propose that this can explain apparently contradictory results reported in the literature.

Seawater carbonate chemistry and biological processes during experiments with calcifiing organisms, 2009

Anthropogenic elevation of atmospheric carbon dioxide (pCO2) is making the oceans more acidic, thereby reducing their degree of saturation with respect to calcium carbonate (CaCO3). There is mounting concern over the impact that future CO2-induced reductions in the CaCO3 saturation state of seawater will have on marine organisms that construct their shells and skeletons from this mineral. Here, we present the results of 60 d laboratory experiments in which we investigated the effects of CO2-induced ocean acidification on calcification in 18 benthic marine organisms. Species were selected to span a broad taxonomic range (crustacea, cnidaria, echinoidea, rhodophyta, chlorophyta, gastropoda, bivalvia, annelida) and included organisms producing aragonite, low-Mg calcite, and high-Mg calcite forms of CaCO3. We show that 10 of the 18 species studied exhibited reduced rates of net calcification and, in some cases, net dissolution under elevated pCO2. However, in seven species, net calcification increased under the intermediate and/or highest levels of pCO2, and one species showed no response at all. These varied responses may reflect differences amongst organisms in their ability to regulate pH at the site of calcification, in the extent to which their outer shell layer is protected by an organic covering, in the solubility of their shell or skeletal mineral, and whether they utilize photosynthesis. Whatever the specific mechanism(s) involved, our results suggest that the impact of elevated atmospheric pCO2 on marine calcification is more varied than previously thought.