Light availability determines susceptibility of reef building corals to ocean acidification

Elevated seawater pCO2, and in turn ocean acidification (OA), is now widely acknowledged to reduce calcification and growth of reef building corals. As with other environmental factors (e.g., temperature and nutrients), light availability fundamentally regulates calcification and is predicted to change for future reef environments alongside elevated pCO2 via altered physical processes (e.g., sea level rise and turbidity); however, any potential role of light in regulating the OA-induced reduction of calcification is still unknown. We employed a multifactorial growth experiment to determine how light intensity and pCO2 together modify calcification for model coral species from two key genera, Acropora horrida and Porites cylindrica, occupying similar ecological niches but with different physiologies. We show that elevated pCO2 (OA)-induced losses of calcification in the light (G L) but not darkness (G D) were greatest under low-light growth conditions, in particular for A. horrida. High-light growth conditions therefore dampened the impact of OA upon G L but not G D. Gross photosynthesis (P G) responded in a reciprocal manner to G L suggesting OA-relieved pCO2 limitation of P G under high-light growth conditions to effectively enhance G L. A multivariate analysis of past OA experiments was used to evaluate whether our test species responses were more widely applicable across their respective genera. Indeed, the light intensity for growth was identified as a significant factor influencing the OA-induced decline of calcification for species of Acropora but not Porites. Whereas low-light conditions can provide a refuge for hard corals from thermal and light stress, our study suggests that lower light availability will potentially increase the susceptibility of key coral species to OA.

Major cellular and physiological impacts of ocean acidification on a reef building coral

As atmospheric levels of CO2 increase, reef-building corals are under greater stress from both increased sea surface temperatures and declining sea water pH. To date, most studies have focused on either coral bleaching due to warming oceans or declining calcification due to decreasing oceanic carbonate ion concentrations. Here, through the use of physiology measurements and cDNA microarrays, we show that changes in pH and ocean chemistry consistent with two scenarios put forward by the Intergovernmental Panel on Climate Change (IPCC) drive major changes in gene expression, respiration, photosynthesis and symbiosis of the coral, Acropora millepora, before affects on biomineralisation are apparent at the phenotype level. Under high CO2 conditions corals at the phenotype level lost over half their Symbiodinium populations, and had a decrease in both photosynthesis and respiration. Changes in gene expression were consistent with metabolic suppression, an increase in oxidative stress, apoptosis and symbiont loss. Other expression patterns demonstrate upregulation of membrane transporters, as well as the regulation of genes involved in membrane cytoskeletal interactions and cytoskeletal remodeling. These widespread changes in gene expression emphasize the need to expand future studies of ocean acidification to include a wider spectrum of cellular processes, many of which may occur before impacts on calcification.

Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions

Coral reefs are globally threatened by climate change-related ocean warming and ocean acidification (OA). To date, slow-response mechanisms such as genetic adaptation have been considered the major determinant of coral reef persistence, with little consideration of rapid-response acclimatization mechanisms. These rapid mechanisms such as parental effects that can contribute to trans-generational acclimatization (e.g. epigenetics) have, however, been identified as important contributors to offspring response in other systems. We present the first evidence of parental effects in a cross-generational exposure to temperature and OA in reef-building corals. Here, we exposed adults to high (28.9°C, 805 µatm PCO2) or ambient (26.5°C, 417 µatm PCO2) temperature and OA treatments during the larval brooding period. Exposure to high treatment negatively affected adult performance, but their larvae exhibited size differences and metabolic acclimation when subsequently re-exposed, unlike larvae from parents exposed to ambient conditions. Understanding the innate capacity corals possess to respond to current and future climatic conditions is essential to reef protection and maintenance. Our results identify that parental effects may have an important role through (1) ameliorating the effects of stress through preconditioning and adaptive plasticity, and/or (2) amplifying the negative parental response through latent effects on future life stages. Whether the consequences of parental effects and the potential for trans-generational acclimatization are beneficial or maladaptive, our work identifies a critical need to expand currently proposed climate change outcomes for corals to further assess rapid response mechanisms that include non-genetic inheritance through parental contributions and classical epigenetic mechanisms.

Diurnal and seasonal measurements of seawater chemistry, temperature and PAR in Hurricane Hole, U.S. Virgin Islands - 2010-2012

Risk analyses indicate that more than 90% of the world's reefs will be threatened by climate change and local anthropogenic impacts by the year 2030 under "business-as-usual" climate scenarios. Increasing temperatures and solar radiation cause coral bleaching that has resulted in extensive coral mortality. Increasing carbon dioxide reduces seawater pH, slows coral growth, and may cause loss of reef structure. Management strategies include establishment of marine protected areas with environmental conditions that promote reef resiliency. However, few resilient reefs have been identified, and resiliency factors are poorly defined. Here we characterize the first natural, non-reef coral refuge from thermal stress and ocean acidification and identify resiliency factors for mangrove-coral habitats. We measured diurnal and seasonal variations in temperature, salinity, photosynthetically active radiation (PAR), and seawater chemistry; characterized substrate parameters; and examined water circulation patterns in mangrove communities where scleractinian corals are growing attached to and under mangrove prop roots in Hurricane Hole, St. John, US Virgin Islands. Additionally, we inventoried the coral species and quantified incidences of coral bleaching, mortality, and recovery for two major reef-building corals, Colpophyllia natans and Diploria labyrinthiformis, growing in mangrove-shaded and exposed (unshaded) areas. Over 30 species of scleractinian corals were growing in association with mangroves. Corals were thriving in low-light (more than 70% attenuation of incident PAR) from mangrove shading and at higher temperatures than nearby reef tract corals. A higher percentage of C. natans colonies were living shaded by mangroves, and no shaded colonies were bleached. Fewer D. labyrinthiformis colonies were shaded by mangroves, however more unshaded colonies were bleached. A combination of substrate and habitat heterogeneity, proximity of different habitat types, hydrographic conditions, and biological influences on seawater chemistry generate chemical conditions that buffer against ocean acidification. This previously undocumented refuge for corals provides evidence for adaptation of coastal organisms and ecosystem transition due to recent climate change. Identifying and protecting other natural, non-reef coral refuges is critical for sustaining corals and other reef species into the future.

Impacts of food availability and pCO2 on planulation, juvenile survival, and calcification of the azooxanthellate scleractinian coral Balanophyllia elegans

Ocean acidification, the assimilation of atmospheric CO2 by the oceans that decreases the pH and CaCO3 saturation state (Omega) of seawater, is projected to have severe adverse consequences for calcifying organisms. While strong evidence suggests calcification by tropical reef-building corals containing algal symbionts (zooxanthellae) will decline over the next century, likely responses of azooxanthellate corals to ocean acidification are less well understood. Because azooxanthellate corals do not obtain photosynthetic energy from symbionts, they provide a system for studying the direct effects of acidification on energy available for calcification. The solitary azooxanthellate orange cup coral Balanophyllia elegans often lives in low-pH, upwelled waters along the California coast. In an 8-month factorial experiment, we measured the effects of three pCO2 treatments (410, 770, and 1220 µatm) and two feeding frequencies (3-day and 21-day intervals) on "planulation" (larval release) by adult B. elegans, and on the survival, skeletal growth, and calcification of newly settled juveniles. Planulation rates were affected by food level but not pCO2. Juvenile mortality was highest under high pCO2 (1220 µatm) and low food (21-day intervals). Feeding rate had a greater impact on calcification of B. elegans than pCO2. While net calcification was positive even at 1220 µatm (~3 times current atmospheric pCO2), overall calcification declined by ~25-45%, and skeletal density declined by ~35-45% as pCO2 increased from 410 to 1220 µatm. Aragonite crystal morphology changed at high pCO2, becoming significantly shorter but not wider at 1220 µatm. We conclude that food abundance is critical for azooxanthellate coral calcification, and that B. elegans may be partially protected from adverse consequences of ocean acidification in habitats with abundant heterotrophic food.

Regulation of intracellular pH in cnidarians: response to acidosis in Anemonia viridis

The regulation of intracellular pH (pHi) is a fundamental aspect of cell physiology that has received little attention in studies of the phylum Cnidaria, which includes ecologically important sea anemones and reef-building corals. Like all organisms, cnidarians must maintain pH homeostasis to counterbalance reductions in pHi, which can arise because of changes in either intrinsic or extrinsic parameters. Corals and sea anemones face natural daily changes in internal fluids, where the extracellular pH can range from 8.9 during the day to 7.4 at night. Furthermore, cnidarians are likely to experience future CO2-driven declines in seawater pH, a process known as ocean acidification. Here, we carried out the first mechanistic investigation to determine how cnidarian pHi regulation responds to decreases in extracellular and intracellular pH. Using the anemone Anemonia viridis, we employed confocal live cell imaging and a pH-sensitive dye to track the dynamics of pHi after intracellular acidosis induced by acute exposure to decreases in seawater pH and NH4Cl prepulses. The investigation was conducted on cells that contained intracellular symbiotic algae (Symbiodinium sp.) and on symbiont-free endoderm cells. Experiments using inhibitors and Na-free seawater indicate a potential role of Na/H plasma membrane exchangers (NHEs) in mediating pHi recovery following intracellular acidosis in both cell types. We also measured the buffering capacity of cells, and obtained values between 20.8 and 43.8 mM per pH unit, which are comparable to those in other invertebrates. Our findings provide the first steps towards a better understanding of acid-base regulation in these basal metazoans, for which information on cell physiology is extremely limited.

Data compilation on the biological response to ocean acidification: environmental and experimental context of data sets and related literature

The exponential growth of studies on the biological response to ocean acidification over the last few decades has generated a large amount of data. To facilitate data comparison, a data compilation hosted at the data publisher PANGAEA was initiated in 2008 and is updated on a regular basis (doi:10.1594/PANGAEA.149999). By January 2015, a total of 581 data sets (over 4 000 000 data points) from 539 papers had been archived. Here we present the developments of this data compilation five years since its first description by Nisumaa et al. (2010). Most of study sites from which data archived are still in the Northern Hemisphere and the number of archived data from studies from the Southern Hemisphere and polar oceans are still relatively low. Data from 60 studies that investigated the response of a mix of organisms or natural communities were all added after 2010, indicating a welcomed shift from the study of individual organisms to communities and ecosystems. The initial imbalance of considerably more data archived on calcification and primary production than on other processes has improved. There is also a clear tendency towards more data archived from multifactorial studies after 2010. For easier and more effective access to ocean acidification data, the ocean acidification community is strongly encouraged to contribute to the data archiving effort, and help develop standard vocabularies describing the variables and define best practices for archiving ocean acidification data.

Colony-specific calcification and mortality under ocean acidification in the branching coral Montipora digitata

Ocean acidification (OA) threatens calcifying marine organisms including reef-building corals. In this study, we examined the OA responses of individual colonies of the branching scleractinian coral Montipora digitata. We exposed nubbins of unique colonies (n = 15) to ambient or elevated pCO2 under natural light and temperature regimes for 110 days. Although elevated pCO2 exposure on average reduced calcification, individual colonies showed unique responses ranging from declines in positive calcification to negative calcification (decalcification) to no change. Similarly, mortality was greater on average in elevated pCO2, but also showed colony-specific patterns. High variation in colony responses suggests the possibility that ongoing OA may lead to natural selection of OA-tolerant colonies within a coral population.

Seawater carbonate chemistry and microbioerosion of coral skeletons

Biological mediation of carbonate dissolution represents a fundamental component of the destructive forces acting on coral reef ecosystems. Whereas ocean acidification can increase dissolution of carbonate substrates, the combined impact of ocean acidification and warming on the microbioerosion of coral skeletons remains unknown. Here, we exposed skeletons of the reef-building corals, Porites cylindrica and Isopora cuneata, to present-day (Control: 400 µatm - 24 °C) and future pCO2-temperature scenarios projected for the end of the century (Medium: +230 µatm - +2 °C; High: +610 µatm - +4 °C). Skeletons were also subjected to permanent darkness with initial sodium hypochlorite incubation, and natural light without sodium hypochlorite incubation to isolate the environmental effect of acidic seawater (i.e., Omega aragonite <1) from the biological effect of photosynthetic microborers. Our results indicated that skeletal dissolution is predominantly driven by photosynthetic microborers, as samples held in the dark did not decalcify. In contrast, dissolution of skeletons exposed to light increased under elevated pCO2-temperature scenarios, with P. cylindrica experiencing higher dissolution rates per month (89%) than I. cuneata (46%) in the high treatment relative to control. The effects of future pCO2-temperature scenarios on the structure of endolithic communities were only identified in P. cylindrica and were mostly associated with a higher abundance of the green algae Ostreobium spp. Enhanced skeletal dissolution was also associated with increased endolithic biomass and respiration under elevated pCO2-temperature scenarios. Our results suggest that future projections of ocean acidification and warming will lead to increased rates of microbioerosion. However, the magnitude of bioerosion responses may depend on the structural properties of coral skeletons, with a range of implications for reef carbonate losses under warmer and more acidic oceans.

Colony-specific investigations reveal highly variable responses among individual corals to ocean acidification and warming

As anthropogenic climate change is an ongoing concern, scientific investigations on its impacts on coral reefs are increasing. Although impacts of combined ocean acidification (OA) and temperature stress (T) on reef-building scleractinian corals have been studied at the genus, species and population levels, there are little data available on how individual corals respond to combined OA and anomalous temperatures. In this study, we exposed individual colonies of Acropora digitifera, Montipora digitata and Porites cylindrica to four pCO2-temperature treatments including 400 µatm-28 °C, 400 µatm-31 °C, 1000 µatm-28 °C and 1000 µatm-31 °C for 26 days. Physiological parameters including calcification, protein content, maximum photosynthetic efficiency, Symbiodinium density, and chlorophyll content along with Symbiodinium type of each colony were examined. Along with intercolonial responses, responses of individual colonies versus pooled data to the treatments were investigated. The main results were: 1) responses to either OA or T or their combination were different between individual colonies when considering physiological functions; 2) tolerance to either OA or T was not synonymous with tolerance to the other parameter; 3) tolerance to both OA and T did not necessarily lead to tolerance of OA and T combined (OAT) at the same time; 4) OAT had negative, positive or no impacts on physiological functions of coral colonies; and 5) pooled data were not representative of responses of all individual colonies. Indeed, the pooled data obscured actual responses of individual colonies or presented a response that was not observed in any individual. From the results of this study we recommend improving experimental designs of studies investigating physiological responses of corals to climate change by complementing them with colony-specific examinations.

Spatial community shift from hard to soft corals in acidified water

Anthropogenic increases in the partial pressure of CO2 (pCO2) cause ocean acidification, declining calcium carbonate saturation states, reduced coral reef calcification and changes in the compositions of marine communities. Most projected community changes due to ocean acidification describe transitions from hard coral to non-calcifying macroalgal communities; other organisms have received less attention, despite the biotic diversity of coral reef communities. We show that the spatial distributions of both hard and soft coral communities in volcanically acidified, semi-enclosed waters off Iwotorishima Island, Japan, are related to pCO2 levels. Hard corals are restricted to non-acidified low- pCO2 (225 µatm) zones, dense populations of the soft coral Sarcophyton elegans dominate medium- pCO2 (831 µatm) zones, and both hard and soft corals are absent from the highest- pCO2 (1,465 µatm) zone. In CO2-enriched culture experiments, high- pCO2 conditions benefited Sarcophyton elegans by enhancing photosynthesis rates and did not affect light calcification, but dark decalcification (negative net calcification) increased with increasing pCO2. These results suggest that reef communities may shift from reef-building hard corals to non-reef-building soft corals under pCO2 levels (550-970 µatm) predicted by the end of this century, and that higher pCO2 levels would challenge the survival of some reef organisms.

Seawater carbonate chemistry and biological processed during experiments with corals Porites sp. & Stylophora pistillata, 2010

Uptake of anthropogenic CO2 by the oceans is altering seawater chemistry with potentially serious consequences for coral reef ecosystems due to the reduction of seawater pH and aragonite saturation state (omega arag). The objectives of this long-term study were to investigate the viability of two ecologically important reef-building coral species, massive Porites sp. and Stylophora pistilata, exposed to high pCO2(or low pH) conditions and to observe possible changes in physiologically related parameters as well as skeletal isotopic composition. Fragments of Porites sp. and S. pistilata were kept for 6-14 months under controlled aquarium conditions characterized by normal and elevated pCO2 conditions, corresponding to pHTvalues of 8.09, 7.49, and 7.19, respectively. In contrast with shorter, and therefore more transient experiments, the long experimental timescale achieved in this study ensures complete equilibration and steady state with the experimental environment and guarantees that the data provide insights into viable and stably growing corals. During the experiments, all coral fragments survived and added new skeleton, even at seawater omega arag <1, implying that the coral skeleton is formed by mechanisms under strong biological control. Measurements of boron (B), carbon (C) and oxygen (O) isotopic composition of skeleton, C isotopic composition of coral tissue and symbiont zooxanthellae, along with physiological data (such as skeletal growth, tissue biomass, zooxanthellae cell density and chlorophyll concentration) allow for a direct comparison with corals living under normal conditions and sampled simultaneously. Skeletal growth and zooxanthellae density were found to decrease, whereas coral tissue biomass (measured as protein concentration) and zooxanthellae chlorophyll concentrations increased under high pCO2 (low pH) conditions. Both species showed similar trends of delta11B depletion and delta18O enrichment under reduced pH, whereas the delta13C results imply species-specific metabolic response to high pCO2 conditions. The skeletal delta11B values plot above seawater delta11B vs. pH borate fractionation curves calculated using either the theoretically derived deltaB value of 1.0194 (Kakihana et al., Bull. Chem. Soc. Jpn. 50(1977), 158) or the empirical deltaB value of 1.0272 (Klochko et al., EPSL 248 (2006), 261). However, the effective deltaB must be greater than 1.0200 in order to yield calculated coral skeletal delta11B values for pH conditions where omega arag >1. The delta11B vs. pH offset from the literature seawater delta11B vs. pH fractionation curves suggests a change in the ratio of skeletal material laid down during dark and light calcification and/or an internal pH regulation, presumably controlled by ion-transport enzymes. Finally, seawater pH significantly influences skeletal delta13C and delta18O. This must be taken into consideration when reconstructing paleo-environmental conditions from coral skeleton

Seawater carbonate chemistry, community calcification and photosynthesis during experiments with coral reefs at Shiraho reef, Ishigaki Island, southwest Japan, 2009

Seven coral reef communities were defined on Shiraho fringing reef, Ishigaki Island, Japan. Net photosynthesis and calcification rates were measured by in situ incubations at 10 sites that included six of the defined communities, and which occupied most of the area on the reef flat and slope. Net photosynthesis on the reef flat was positive overall, but the reef flat acts as a source for atmospheric CO2, because the measured calcification/photosynthesis ratio of 2.5 is greater than the critical ratio of 1.67. Net photosynthesis on the reef slope was negative. Almost all excess organic production from the reef flat is expected to be effused to the outer reef and consumed by the communities there. Therefore, the total net organic production of the whole reef system is probably almost zero and the whole reef system also acts as a source for atmospheric CO2. Net calcification rates of the reef slope corals were much lower than those of the branching corals. The accumulation rate of the former was approximately 0.5 m kyr?1 and of the latter was ~0.7-5 m kyr?1. Consequently, reef slope corals could not grow fast enough to keep up with or catch up to rising sea levels during the Holocene. On the other hand, the branching corals grow fast enough to keep up with this rising sea level. Therefore, a transition between early Holocene and present-day reef communities is expected. Branching coral communities would have dominated while reef growth kept pace with sea level rise, and the reef was constructed with a branching coral framework. Then, the outside of this framework was covered and built up by reef slope corals and present-day reefs were constructed.

Seawater carbonate chemistry and calcification rate of cold-water coral Lophelia pertusa during experiments, 2011

Ocean acidity has increased by 30% since preindustrial times due to the uptake of anthropogenic CO2 and is projected to rise by another 120% before 2100 if CO2 emissions continue at current rates. Ocean acidification is expected to have wide-ranging impacts on marine life, including reduced growth and net erosion of coral reefs. Our present understanding of the impacts of ocean acidification on marine life, however, relies heavily on results from short-term CO2 perturbation studies. Here we present results from the first long-term CO2 perturbation study on the dominant reef-building cold-water coral Lophelia pertusa and relate them to results from a short-term study to compare the effect of exposure time on the coral's responses. Short-term (one week) high CO2 exposure resulted in a decline of calcification by 26-29% for a pH decrease of 0.1 units and net dissolution of calcium carbonate. In contrast, L. pertusa was capable to acclimate to acidified conditions in long-term (six months) incubations, leading to even slightly enhanced rates of calcification. Net growth is sustained even in waters sub-saturated with respect to aragonite. Acclimation to seawater acidification did not cause a measurable increase in metabolic rates. This is the first evidence of successful acclimation in a coral species to ocean acidification, emphasizing the general need for long-term incubations in ocean acidification research. To conclude on the sensitivity of cold-water coral reefs to future ocean acidification further ecophysiological studies are necessary which should also encompass the role of food availability and rising temperatures.

Reduced calcification and lack of acclimatization by coral colonies growing in areas of persistent natural acidification

As the surface ocean equilibrates with rising atmospheric CO2, the pH of surface seawater is decreasing with potentially negative impacts on coral calcification. A critical question is whether corals will be able to adapt or acclimate to these changes in seawater chemistry. We use high precision CT scanning of skeletal cores of Porites astreoides, an important Caribbean reef-building coral, to show that calcification rates decrease significantly along a natural gradient in pH and aragonite saturation (Omega arag). This decrease is accompanied by an increase in skeletal erosion and predation by boring organisms. The degree of sensitivity to reduced ?arag measured on our field corals is consistent with that exhibited by the same species in laboratory CO2 manipulation experiments. We conclude that the Porites corals at our field site were not able to acclimatize enough to prevent the impacts of local ocean acidification on their skeletal growth and development, despite spending their entire lifespan in low pH, low Omega arag seawater.