Seawater carbonate chemistry and sperm swimming speed of the polychaete Galeolaria caespitosa in lab experiment

The rapidity of ocean acidification intensifies selection pressure for resilient phenotypes, particularly during sensitive early life stages. The scope for selection is greater in species with greater within-species variation in responses to changing environments, thus enhancing the potential for adaptation. We investigated among-male variation in sperm swimming responses (percent motility and swimming speeds) of the serpulid polychaete Galeolaria caespitosa to near- (delta pH 0.3) and far-future ocean acidification (delta pH 0.5). Responses of sperm swimming to acidification varied significantly among males and were overall negative. Robust sperm swimming behavior under near-future ocean acidification in some males may ameliorate climate change impacts, if traits associated with robustness are heritable, and thereby enhance the potential for adaptation to far-future conditions. Reduced sperm swimming in the majority of male G. caespitosa may decrease their fertilization success in a high CO2 future ocean. Resultant changes in offspring production could affect recruitment success and population fitness downstream.

Seawater carbonate chemistry and sperm swimming speed, fertilization success of the Australasian sea urchin Heliocidaris erythrogramma in lab experiment

Background: Climate change will lead to intense selection on many organisms, particularly during susceptible early life stages. To date, most studies on the likely biotic effects of climate change have focused on the mean responses of pooled groups of animals. Consequently, the extent to which inter-individual variation mediates different selection responses has not been tested. Investigating this variation is important, since some individuals may be preadapted to future climate scenarios. Methodology/Principal Findings: We examined the effect of CO2-induced pH changes ("ocean acidification") in sperm swimming behaviour on the fertilization success of the Australasian sea urchin Heliocidaris erythrogramma, focusing on the responses of separate individuals and pairs. Acidification significantly decreased the proportion of motile sperm but had no effect on sperm swimming speed. Subsequent fertilization experiments showed strong inter-individual variation in responses to ocean acidification, ranging from a 44% decrease to a 14% increase in fertilization success. This was partly explained by the significant relationship between decreases in percent sperm motility and fertilization success at delta pH = 0.3, but not at delta pH = 0.5. Conclusions and Significance: The effects of ocean acidification on reproductive success varied markedly between individuals. Our results suggest that some individuals will exhibit enhanced fertilization success in acidified oceans, supporting the concept of 'winners' and 'losers' of climate change at an individual level. If these differences are heritable it is likely that ocean acidification will lead to selection against susceptible phenotypes as well as to rapid fixation of alleles that allow reproduction under more acidic conditions. This selection may ameliorate the biotic effects of climate change if taxa have sufficient extant genetic variation upon which selection can act.

Seawater carbonate chemistry, and Lithophyllum sp. and Feldmannia spp. coverage and dry weight during experiments, 2009

Climate-driven change represents the cumulative effect of global through local-scale conditions, and understanding their manifestation at local scales can empower local management. Change in the dominance of habitats is often the product of local nutrient pollution that occurs at relatively local scales (i.e. catchment scale), a critical scale of management at which global impacts will manifest. We tested whether forecasted global-scale change [elevated carbon dioxide (CO2) and subsequent ocean acidification] and local stressors (elevated nutrients) can combine to accelerate the expansion of filamentous turfs at the expense of calcifying algae (kelp understorey). Our results not only support this model of future change, but also highlight the synergistic effects of future CO2 and nutrient concentrations on the abundance of turfs. These results suggest that global and local stressors need to be assessed in meaningful combinations so that the anticipated effects of climate change do not create the false impression that, however complex, climate change will produce smaller effects than reality. These findings empower local managers because they show that policies of reducing local stressors (e.g. nutrient pollution) can reduce the effects of global stressors not under their governance (e.g. ocean acidification). The connection between research and government policy provides an example whereby knowledge (and decision making) across local through global scales provides solutions to some of the most vexing challenges for attaining social goals of sustainability, biological conservation and economic development.

Seawater carbonate chemistry, larval settlement and growth rate during experiments with coral Porites astreoides, 2008

In response to the increases in pCO2 projected in the 21st century, adult coral growth and calcification are expected to decrease significantly. However, no published studies have investigated the effect of elevated pCO2 on earlier life history stages of corals. Porites astreoides larvae were collected from reefs in Key Largo, Florida, USA, settled and reared in controlled saturation state seawater. Three saturation states were obtained, using 1 M HCl additions, corresponding to present (380 ppm) and projected pCO2 scenarios for the years 2065 (560 ppm) and 2100 (720 ppm). The effect of saturation state on settlement and post-settlement growth was evaluated. Saturation state had no significant effect on percent settlement; however, skeletal extension rate was positively correlated with saturation state, with ~50% and 78% reductions in growth at the mid and high pCO2 treatments compared to controls, respectively.

Seawater carbonate chemistry and processes during experiments with coral Acropora eurystoma, 2006

The rise in atmospheric CO2 has caused significant decrease in sea surface pH and carbonate ion (CO3-2) concentration. This decrease has a negative effect on calcification in hermatypic corals and other calcifying organisms. We report the results of three laboratory experiments designed specifically to separate the effects of the different carbonate chemistry parameters (pH, CO3-2, CO2 [aq], total alkalinity [AT], and total inorganic carbon [CT]) on the calcification, photosynthesis, and respiration of the hermatypic coral Acropora eurystoma. The carbonate system was varied to change pH (7.9-8.5), without changing CT; CT was changed keeping the pH constant, and CT was changed keeping the pCO2 constant. In all of these experiments, calcification (both light and dark) was positively correlated with CO3-2 concentration, suggesting that the corals are not sensitive to pH or CT but to the CO3-2 concentration. A decrease of ~30% in the CO3-2 concentration (which is equivalent to a decrease of about 0.2 pH units in seawater) caused a calcification decrease of about 50%. These results suggest that calcification in today's ocean (pCO2 = 370 ppm) is lower by ~20% compared with preindustrial time (pCO2 = 280 ppm). An additional decrease of ~35% is expected if atmospheric CO2 concentration doubles (pCO2 = 560 ppm). In all of these experiments, photosynthesis and respiration did not show any significant response to changes in the carbonate chemistry of seawater. Based on this observation, we propose a mechanism by which the photosynthesis of symbionts is enhanced by coral calcification at high pH when CO2(aq) is low. Overall it seems that photosynthesis and calcification support each other mainly through internal pH regulation, which provides CO3-2 ions for calcification and CO2(aq) for photosynthesis.

Seawater carbonate chemistry and morphometric coordinates and morphology of the control 8-arm pluteus of brittlestar Ophiothrix fragilis, 2008

The world's oceans are slowly becoming more acidic. In the last 150 yr, the pH of the oceans has dropped by ~0.1 units, which is equivalent to a 25% increase in acidity. Modelling predicts the pH of the oceans to fall by 0.2 to 0.4 units by the year 2100. These changes will have significant effects on marine organisms, especially those with calcareous skeletons such as echinoderms. Little is known about the possible long-term impact of predicted pH changes on marine invertebrate larval development. Here we predict the consequences of increased CO2 (corresponding to pH drops of 0.2 and 0.4 units) on the larval development of the brittlestar Ophiothrix fragilis, which is a keystone species occurring in high densities and stable populations throughout the shelf seas of northwestern Europe (eastern Atlantic). Acidification by 0.2 units induced 100% larval mortality within 8 d while control larvae showed 70% survival over the same period. Exposure to low pH also resulted in a temporal decrease in larval size as well as abnormal development and skeletogenesis (abnormalities, asymmetry, altered skeletal proportions). If oceans continue to acidify as expected, ecosystems of the Atlantic dominated by this keystone species will be seriously threatened with major changes in many key benthic and pelagic ecosystems. Thus, it may be useful to monitor O. fragilis populations and initiate conservation if needed.

Seawater carbonate chemistry and biological processes during experiments with postlarvae of barnacle of Semibalanus balanoides and Elminius modestus, 2010

Ocean acidification and global warming are occurring concomitantly, yet few studies have investigated how organisms will respond to increases in both temperature and CO2. Intertidal microcosms were used to examine growth, shell mineralogy and survival of two intertidal barnacle post-larvae, Semibalanus balanoides and Elminius modestus, at two temperatures (14 and 19°C) and two CO2 concentrations (380 and 1,000 ppm), fed with a mixed diatom-flagellate diet at 15,000 cells ml-1 with flow rate of 10 ml-1 min-1. Control growth rates, using operculum diameter, were 14 ± 8 µm day-1 and 6 ± 2 µm day-1 for S. balanoides and E. modestus, respectively. Subtle, but significant decreases in E. modestus growth rate were observed in high CO2 but there were no impacts on shell calcium content and survival by either elevated temperature or CO2. S. balanoides exhibited no clear alterations in growth rate but did show a large reduction in shell calcium content and survival under elevated temperature and CO2. These results suggest that a decrease by 0.4 pH(NBS) units alone would not be sufficient to directly impact the survival of barnacles during the first month post-settlement. However, in conjunction with a 4-5°C increase in temperature, it appears that significant changes to the biology of these organisms will ensue.

Seawater carbonate chemistry, pigments and biological processes during experiments with coralline alga Corallina sessilis

Previous studies have shown that increasing atmospheric CO2 concentrations affect calcification in some planktonic and macroalgal calcifiers due to the changed carbonate chemistry of seawater. However, little is known regarding how calcifying algae respond to solar UV radiation (UVR, UVA+UVB, 280-400 nm). UVR may act synergistically, antagonistically or independently with ocean acidification (high CO2/low pH of seawater) to affect their calcification processes. We cultured the articulated coralline alga Corallina sessilis Yendo at 380 ppmv (low) and 1000 ppmv (high) CO2 levels while exposing the alga to solar radiation treatments with or without UVR. The presence of UVR inhibited the growth, photosynthetic O2evolution and calcification rates by13%, 6% and 3% in the low and by 47%, 20% and 8% in the high CO2 concentrations, respectively, reflecting a synergistic effect of CO2 enrichment with UVR. UVR induced significant decline of pH in the CO2-enriched cultures. The contents of key photosynthetic pigments, chlorophyll a and phycobiliproteins decreased, while UV-absorptivity increased under the highpCO2/low pH condition. Nevertheless, UV-induced inhibition of photosynthesis increased when the ratio of particulate inorganic carbon/particulate organic carbon decreased under the influence of CO2-acidified seawater, suggesting that the calcified layer played a UV-protective role. Both UVA and UVB negatively impacted photosynthesis and calcification, but the inhibition caused by UVB was about 2.5-2.6 times that caused by UVA. The results imply that coralline algae suffer from more damage caused by UVB as they calcify less and less with progressing ocean acidification.

Seawater carbonate chemistry and Gadus morhua length, weight and sperm biological processes, 2010

Ocean acidification, as a consequence of increasing marine pCO2, may have severe effects on the physiology of marine organisms. However, experimental studies remain scarce, in particular concerning fish. While adults will most likely remain relatively unaffected by changes in seawater pH, early life-history stages are potentially more sensitive - particularly the critical stage of fertilization, in which sperm motility plays a central role. In this study, the effects of ocean acidification (decrease of pHT to 7.55) on sperm motility of Baltic cod, Gadus morhua, were assessed. We found no significant effect of decreased pH on sperm speed, rate of change of direction or percent motility for the population of cod analyzed. We predict that future ocean acidification will probably not pose a problem for sperm behavior, and hence fertilization success, of Baltic cod.

Seawater carbonate chemistry and biological processes of Amphisorus hemprichii, Amphisorus kudakajimensis and Calcarina gaudichaudii during experiments, 2011

Ocean acidification, which like global warming is an outcome of anthropogenic CO2emissions, 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 ofAmphisorus 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.

Seawater carbonate chemistry and protein sports of barnicle Balanus amphitrite during experiments, 2011

The majority of benthic marine invertebrates have a complex life cycle, during which the pelagic larvae select a suitable substrate, attach to it, and then metamorphose into benthic adults. Anthropogenic ocean acidification (OA) is postulated to affect larval metamorphic success through an altered protein expression pattern (proteome structure) and post-translational modifications. To test this hypothesis, larvae of an economically and ecologically important barnacle species Balanus amphitrite, were cultured from nauplius to the cyprid stage in the present (control) and in the projected elevated concentrations of CO2 for the year 2100 (the OA treatment). Cyprid response to OA was analyzed at the total proteome level as well as two protein post-translational modification (phosphorylation and glycosylation) levels using a 2-DE based proteomic approach. The cyprid proteome showed OA-driven changes. Proteins that were differentially up or down regulated by OA come from three major groups, namely those related to energy-metabolism, respiration, and molecular chaperones, illustrating a potential strategy that the barnacle larvae may employ to tolerate OA stress. The differentially expressed proteins were tentatively identified as OA-responsive, effectively creating unique protein expression signatures for OA scenario of 2100. This study showed the promise of using a sentinel and non-model species to examine the impact of OA at the proteome level.

Seawater carbonate chemistry and brown dottyback (Pseudochromis fuscus) movement and feeding behaviour during experiments, 2011

Changes in olfactory-mediated behaviour caused by elevated CO2 levels in the ocean could affect recruitment to reef fish populations because larval fish become more vulnerable to predation. However, it is currently unclear how elevated CO2 will impact the other key part of the predator-prey interaction - the predators. We investigated the effects of elevated CO2 and reduced pH on olfactory preferences, activity levels and feeding behaviour of a common coral reef meso-predator, the brown dottyback (Pseudochromis fuscus). Predators were exposed to either current-day CO2 levels or one of two elevated CO2 levels (~600 µatm or ~950 µatm) that may occur by 2100 according to climate change predictions. Exposure to elevated CO2 and reduced pH caused a shift from preference to avoidance of the smell of injured prey, with CO2treated predators spending approximately 20% less time in a water stream containing prey odour compared with controls. Furthermore, activity levels of fish was higher in the high CO2 treatment and feeding activity was lower for fish in the mid CO2treatment; indicating that future conditions may potentially reduce the ability of the fish to respond rapidly to fluctuations in food availability. Elevated activity levels of predators in the high CO2 treatment, however, may compensate for reduced olfactory ability, as greater movement facilitated visual detection of food. Our findings show that, at least for the species tested to date, both parties in the predator-prey relationship may be affected by ocean acidification. Although impairment of olfactory-mediated behaviour of predators might reduce the risk of predation for larval fishes, the magnitude of the observed effects of elevated CO2 acidification appear to be more dramatic for prey compared to predators. Thus, it is unlikely that the altered behaviour of predators is sufficient to fully compensate for the effects of ocean acidification on prey mortality.

Seawater carbonate chemistry and processes during experiments with a coral community, 2008

Ocean acidification represents a key threat to coral reefs by reducing the calcification rate of framework builders. In addition, acidification is likely to affect the relationship between corals and their symbiotic dinoflagellates and the productivity of this association. However, little is known about how acidification impacts on the physiology of reef builders and how acidification interacts with warming. Here, we report on an 8-week study that compared bleaching, productivity, and calcification responses of crustose coralline algae (CCA) and branching (Acropora) and massive (Porites) coral species in response to acidification and warming. Using a 30-tank experimental system, we manipulated CO2 levels to simulate doubling and three- to fourfold increases [Intergovernmental Panel on Climate Change (IPCC) projection categories IV and VI] relative to present-day levels under cool and warm scenarios. Results indicated that high CO2 is a bleaching agent for corals and CCA under high irradiance, acting synergistically with warming to lower thermal bleaching thresholds. We propose that CO2 induces bleaching via its impact on photoprotective mechanisms of the photosystems. Overall, acidification impacted more strongly on bleaching and productivity than on calcification. Interestingly, the intermediate, warm CO2 scenario led to a 30% increase in productivity in Acropora, whereas high CO2 lead to zero productivity in both corals. CCA were most sensitive to acidification, with high CO2 leading to negative productivity and high rates of net dissolution. Our findings suggest that sensitive reef-building species such as CCA may be pushed beyond their thresholds for growth and survival within the next few decades whereas corals will show delayed and mixed responses.

Seawater carbonate chemistry and impacts of calcium and carbonate ion concentration on Mg and Sr incorporation in cultured benthic foraminifera (Ammonia tepida and Heterostegina depressa), 2011

Laboratory culture experiments were conducted to determine effects of seawater carbonate ion concentration ([CO32-]), and thereby calcite saturation state, 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 [CO32-] and thereby higher calcite saturation state, is absent in either species. Comparison to results from a similar culturing experiment, in which calcite saturation state 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.

Nutrient availability affects the response of the calcifying chlorophyte Halimeda opuntia (L.) J.V. Lamouroux to low pH

Atmospheric carbon dioxide emissions cause a decrease in the pH and aragonite saturation state of surface ocean water. As a result, calcifying organisms are expected to suffer under future ocean conditions, but their physiological responses may depend on their nutrient status. Because many coral reefs experience high inorganic nutrient loads or seasonal changes in nutrient availability, reef organisms in localized areas will have to cope with elevated carbon dioxide and changes in inorganic nutrients. Halimeda opuntia is a dominant calcifying primary producer on coral reefs that contributes to coral reef accretion. Therefore, we investigated the carbon and nutrient balance of H. opuntia exposed to elevated carbon dioxide and inorganic nutrients. We measured tissue nitrogen, phosphorus and carbon content as well as the activity of enzymes involved in inorganic carbon uptake and nitrogen assimilation (external carbonic anhydrase and nitrate reductase, respectively). Inorganic carbon content was lower in algae exposed to high CO2, but calcification rates were not significantly affected by CO2 or inorganic nutrients. Organic carbon was positively correlated to external carbonic anhydrase activity, while inorganic carbon showed the opposite correlation. Carbon dioxide had a significant effect on tissue nitrogen and organic carbon content, while inorganic nutrients affected tissue phosphorus and N:P ratios. Nitrate reductase activity was highest in algae grown under elevated CO2 and inorganic nutrient conditions and lowest when phosphate was limiting. In general, we found that enzymatic responses were strongly influenced by nutrient availability, indicating its important role in dictating the local responses of the calcifying primary producer H. opuntia to ocean acidification.