Food availability and pCO2 impacts 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 (Ω) of seawater, is projected to have severe consequences for calcifying organisms. Strong evidence suggests that tropical reef-building corals containing algal symbionts (zooxanthellae) will experience dramatic declines in calcification over the next century. The responses of azooxanthellate corals to ocean acidification are less well understood, and because they cannot obtain extra photosynthetic energy from symbionts, they provide a system for studying the direct effects of acidification on the energy available for calcification. The orange cup coral Balanophyllia elegans is a solitary, azooxanthellate scleractinian species common on the California coast where it thrives in the low pH waters of an upwelling regime. During an 8 month study, we addressed the effects of three pCO₂ treatments (410, 770, and 1230 μatm) and two feeding frequencies (High Food and Low Food) on adult Balanophyllia elegans planulation (larval release) rates, and on the survival, growth, and calcification of their juvenile offspring. Planulation rates were affected by food level but not pCO₂, while juvenile survival was highest under 410 μatm and High Food conditions. Our results suggest that feeding rate has a greater impact on calcification of B. elegans than pCO₂. Net calcification was positive even at 1230 μatm (~ 3 times current atmospheric pCO₂), although the increase from 410 to 1230 μatm reduced overall calcification by ~ 25–45%, and reduced skeletal density by ~ 35–45%. Higher pCO₂ also altered aragonite crystal morphology significantly. We discuss how feeding frequency affects azooxanthellate coral calcification, and how B. elegans may respond to ocean acidification in coastal upwelling waters.

Dynamics of seawater carbonate chemistry, production, and calcification of a coral reef flat, Central Great Barrier Reef

Ocean acidification is projected to shift coral reefs from a state of net accretion to one of net dissolution this century. Presently, our ability to predict global-scale changes to coral reef calcification is limited by insufficient data relating seawater carbonate chemistry parameters to in situ rates of reef calcification. Here, we investigate natural trends in carbonate chemistry of the Davies Reef flat in the central Great Barrier Reef on diel and seasonal timescales and relate these trends to benthic carbon fluxes by quantifying net ecosystem calcification (nec) and net community production (ncp). Results show that seawater carbonate chemistry of the Davies Reef flat is highly variable over both diel and seasonal timescales. pH (total scale) ranged from 7.92 to 8.17, pCO₂ ranged from 272 to 542 μatm, and aragonite saturation state (Ω_arag) ranged from 2.9 to 4.1. Diel cycles in carbonate chemistry were primarily driven by ncp, and warming explained 35% and 47% of the seasonal shifts in pCO₂ and pH, respectively. Daytime ncp averaged 36 ± 19 mmol C m⁻² h⁻¹ in summer and 33 ± 13 mmol C m⁻² h⁻¹ in winter; nighttime ncp averaged −22 ± 20 and −7 ± 6 mmol C m⁻² h⁻¹ in summer and winter, respectively. Daytime nec averaged 11 ± 4 mmol CaCO₃ m⁻² h⁻¹ in summer and 8 ± 3 mmol CaCO₃ m⁻² h⁻¹ in winter, whereas nighttime nec averaged 2 ± 4 mmol and −1 ± 3 mmol CaCO₃ m⁻² h⁻¹ in summer and winter, respectively. Net ecosystem calcification was positively correlated with Ω_arag for both seasons. Linear correlations of nec and Ω_arag indicate that the Davies Reef flat may transition from a state of net calcification to net dissolution at Ω_arag values of 3.4 in summer and 3.2 in winter. Diel trends in Ω_arag indicate that the reef flat is currently below this calcification threshold 29.6% of the time in summer and 14.1% of the time in winter.

Respiration of Mediterranean cold-water corals is not affected by ocean acidification as projected for the end of the century

The rise of CO₂ has been identified as a major threat to life in the ocean. About one-third of the anthropogenic CO₂ produced in the last 200 yr has been taken up by the ocean, leading to ocean acidification. Surface seawater pH is projected to decrease by about 0.4 unit between the pre-industrial revolution and 2100. The branching cold-water corals Madrepora oculata and Lophelia pertusa are important, habitat-forming species in the deep Mediterranean Sea. Although previous research has investigated the abundance and distribution of these species, little is known regarding their ecophysiology and potential responses to global environmental change. A previous study indicated that the rate of calcification of these two species remained constant up to 1000 μatm CO₂ a value that is at the upper end of changes projected to occur by 2100. We examined whether the ability to maintain calcification rates in the face of rising pCO₂ affected the energetic requirements of these corals. Over the course of three months, rates of respiration were measured at a pCO₂ ranging between 350 and 1100 μatm to distinguish between short-term response and longer-term acclimation. Respiration rates ranged from 0.074 to 0.266 μmol O₂ (g skeletal dry weight)⁻¹ h⁻¹ and 0.095 to 0.725 μmol O₂ (g skeletal dry weight)⁻¹ h⁻¹ for L. and M. oculata, respectively, and were independent of pCO₂. Respiration increased with time likely due to regular feeding which may have provided an increased energy supply to sustain coral metabolism. Future studies are needed to confirm whether the insensitivity of respiration to increasing pCO₂ is a general feature of deep-sea corals in other regions.

End of the century pCO2 levels do not impact calcification in Mediterranean cold-water corals

Ocean acidification caused by anthropogenic uptake of CO₂ is perceived to be a major threat to calcifying organisms. Cold-water corals were thought to be strongly affected by a decrease in ocean pH due to their abundance in deep and cold waters which, in contrast to tropical coral reef waters, will soon become corrosive to calcium carbonate. Calcification rates of two Mediterranean cold-water coral species, Lophelia pertusa and Madrepora oculata, were measured under variable partial pressure of CO₂ (pCO₂) that ranged between 380 µatm for present-day conditions and 930 µatm for the end of the century. The present study addressed both short- and long-term responses by repeatedly determining calcification rates on the same specimens over a period of 9 months. Besides studying the direct, short-term response to elevated pCO₂ levels, the study aimed to elucidate the potential for acclimation of calcification of cold-water corals to ocean acidification. Net calcification of both species was unaffected by the levels of pCO₂ investigated and revealed no short-term shock and, therefore, no long-term acclimation in calcification to changes in the carbonate chemistry. There was an effect of time during repeated experiments with increasing net calcification rates for both species, however, as this pattern was found in all treatments, there is no indication that acclimation of calcification to ocean acidification occurred. The use of controls (initial and ambient net calcification rates) indicated that this increase was not caused by acclimation in calcification response to higher pCO₂. An extrapolation of these data suggests that calcification of these two cold-water corals will not be affected by the pCO₂ level projected at the end of the century.

A new conceptual model of coral biomineralisation: hypoxia as the physiological driver of skeletal extension (update)

That corals skeletons are built of aragonite crystals with taxonomy-linked ultrastructure has been well understood since the 19th century. Yet, the way by which corals control this crystallization process remains an unsolved question. Here, I outline a new conceptual model of coral biomineralisation that endeavours to relate known skeletal features with homeostatic functions beyond traditional growth (structural) determinants. In particular, I propose that the dominant physiological driver of skeletal extension is night-time hypoxia, which is exacerbated by the respiratory oxygen demands of the coral’s algal symbionts (= zooxanthellae). The model thus provides a new narrative to explain the high growth rate of symbiotic corals, by equating skeletal deposition with the “work-rate” of the coral host needed to maintain a stable and beneficial symbiosis. In this way, coral skeletons are interpreted as a continuous (long-run) recording unit of the stability and functioning of the coral–algae endosymbiosis. After providing supportive evidence for the model across multiple scales of observation, I use coral core data from the Great Barrier Reef (Australia) to highlight the disturbed nature of the symbiosis in recent decades, but suggest that its onset is consistent with a trajectory that has been followed since at least the start of the 1900s. In concluding, I outline how the proposed capacity of cnidarians (which includes modern reef corals) to overcome the metabolic limitation of hypoxia via skeletogenesis also provides a new hypothesis to explain the sudden appearance in the fossil record of calcified skeletons at the Precambrian–Cambrian transition – and the ensuing rapid appearance of most major animal phyla.

The marine carbon system and ocean acidification during Phanerozoic time

The global CO₂-carbonic acid-carbonate system of seawater, although certainly a well-researched topic of interest in the past, has risen to the fore in recent years because of the environmental issue of ocean acidification (often simply termed OA). Despite much previous research, there remain pressing questions about how this most important chemical system of seawater operated at the various time scales of the deep time of the Phanerozoic Eon (the past 545 Ma of Earth’s history), interglacial-glacial time, and the Anthropocene (the time of strong human influence on the behaviour of the system) into the future of the planet. One difficulty in any analysis is that the behaviour of the marine carbon system is not only controlled by internal processes in the ocean, but it is intimately linked to the domains of the atmosphere, continental landscape, and marine carbonate sediments.

For the deep-time behaviour of the system, there exists a strong coupling between the states of various material reservoirs resulting in an homeostatic and self-regulating system. As a working hypothesis, the coupling produces two dominant chemostatic modes: (Mode I), a state of elevated atmospheric CO₂, warm climate, and depressed seawater Mg∕Ca and SO₄∕Ca mol ratios, pH (extended geologic periods of ocean acidification), and carbonate saturation states, and elevated Sr concentrations, with calcite and dolomite as dominant minerals found in marine carbonate sediments (Hothouses, the calcite-dolomite seas), and (Mode II), a state of depressed atmospheric CO₂, cool climate, and elevated seawater Mg∕Ca and SO₄/Ca ratios, pH, and carbonate saturation states, and low Sr concentrations, with aragonite and high magnesian calcites as dominant minerals found in marine carbonate sediments (Icehouses, the aragonite seas).

Investigation of the impacts of deglaciation and anthropogenic inputs on the CO₂–H₂O–CaCO₃ system in global coastal ocean waters from the Last Glacial Maximum (LGM: the last great continental glaciation of the Pleistocene Epoch, 18,000 year BP) to the year 2100 shows that with rising sea level, atmospheric CO₂, and temperature, the carbonate system of coastal ocean water changed and will continue to change significantly. We find that 6,000 Gt of C were emitted as CO₂ to the atmosphere from the growing coastal ocean from the Last Glacial Maximum to late preindustrial time because of net heterotrophy (state of gross respiration exceeding gross photosynthesis) and net calcification processes. Shallow-water carbonate accumulation alone from the Last Glacial Maximum to late preindustrial time could account for ~24 ppmv of the ~100 ppmv rise in atmospheric CO₂, lending some support to the ‘‘coral reef hypothesis’’. In addition, the global coastal ocean is now, or soon will be, a sink of atmospheric CO₂, rather than a source. The pHT (pH values on the total proton scale) of global coastal seawater has decreased from ~8.35 to ~8.18 and the CO₃^2- ion concentration declined by ~19% from the Last Glacial Maximum to late preindustrial time. In comparison, the decrease in coastal water pHT from the year 1900 to 2000 was ~8.18 to ~8.08 and is projected to decrease further from about ~8.08 to ~7.85 between 2000 and 2100. During these 200 years, the CO₃^2- ion concentration will fall by ~ 45%. This decadal rate of decline of the CO₃^2- ion concentration in the Anthropocene is 214 times the average rate of decline for the entire Holocene!

In terms of the modern problem of ocean acidification and its effects, the “other CO₂ problem”, we emphasise that most experimental work on a variety of calcifying organisms has shown that under increased atmospheric CO₂ levels (which attempt to mimic those of the future), and hence decreased seawater CO₃^2- ion concentration and carbonate saturation state, most calcifying organisms will not calcify as rapidly as they do under present-day CO₂ levels. In addition, we conclude that dissolution of the highly reactive carbonate phases, particularly the biogenic and cementing magnesian calcite phases, on reefs will not be sufficient to alter significantly future changes in seawater pH and lead to a buffering of the CO₂-carbonic acid system in waters bathing reefs and other carbonate ecosystems on timescales of decades to centuries. Because of decreased calcification rates and increased dissolution rates in a future higher CO₂, warmer world with seas of lower pH and carbonate saturation state, the rate of accretion of carbonate structures is likely to slow and dissolution may even exceed calcification. The potential of increasing nutrient and organic carbon inputs from land, occurrences of mass bleaching events, and increasing intensity (and perhaps frequency of hurricanes and cyclones as a result of sea surface warming) will only complicate matters more. This composite of stresses will have severe consequences for the ecosystem services that reefs perform, including acting as a fishery, a barrier to storm surges, a source of carbonate sediment to maintain beaches, and an environment of aesthetic appeal to tourist and local populations. It seems obvious that increasing rates of dissolution and bioerosion owing to ocean acidification will result in a progressively increasing calcium carbonate (CaCO₃) deficit in the CaCO₃ budget for many coral reef environments. The major questions that require answers are: will this deficit occur and when and to what extent will the destructive processes exceed the constructive processes?

Interactive effects of ocean acidification and warming on sediment-dwelling marine calcifiers

The increase in human activities, such as the burning of fossil fuels, has elevated the concentration of atmospheric carbon dioxide and warmed the planet through the greenhouse effect. In addition, approximately 30% of the CO2 produced by human activities has dissolved into the oceans, lowering pH and reducing the abundance, and hence the availability, of carbonate ions (CO3 2-), which are essential for calcium carbonate deposition. Of great concern is the impact to photosynthetic marine calcifiers, elevated CO2 and temperature is expected to have a negative impact on the health and survivorship of calcifying marine organisms. This thesis explores the effects of elevated CO2 and temperature on the microenvironment, photosynthetic efficiency, calcification and biomechanical properties in important sediment producers on coral reefs. The reef-building and sedimentdwelling organisms, Halimeda and symbiont-bearing foraminifera are prominent, coexisting taxa in shallow coral reefs and play a vital role in tropical and subtropical ecosystems as producers of sediment and habitats and food sources for other marine organisms. However, there is limited evidence of the effects of ocean warming and acidification in these two keystone species. Irradiance alone was not found to influence photosynthetic efficiency, photoprotective mechanisms and calcification in Halimeda macroloba, Halimeda cylindracea and Halimeda opuntia (Chapter 2). There is also limited knowledge of foraminiferal biology on coral reefs, especially the symbiotic relationship between the protest host and algal symbionts. Marginopora vertebralis, the dominant tropical foraminifera, shows phototactic behavior, which is a unique mechanism for ensuring symbionts experience an ideal light environment. The diurnal photosynthetic responses of in hospite symbiont photosynthesis was linked to host movement and aided in preventing photoinhibition and bleaching by moving away from over-saturating irradiance, to more optimal light fields (Chapter 3). With this greater understanding of Halimeda and foraminiferan biology and photosynthesis, the impacts of ocean warming and acidification on photosynthesis and calcification were then tested (Chapter 4, 5 and 6). Impacts of ocean acidification and warming were investigated through exposure to a combination of four temperature (28, 30, 32, 34°C) and four pCO2 levels (380, 600, 1000, 2000 µatm; equivalent to future climate change scenarios for the current and the years 2065, 2100 and 2200 and simulating the IPCC A1F1 predictions) (Chapter 4). Elevated CO2 and temperature caused a decline in photosynthetic efficiency (FV/FM), calcification and growth in all species. After five weeks at 34°C under all CO2 levels, all species died. The elevated CO2 and temperature greatly affect the CaCO3 crystal formation with reductions in density and width. M. vertebralis experienced the greatest inhibition to crystal formation, suggesting that this high Mg-calcite depositing species is more sensitive to lower pH and higher temperature than aragonite-forming Halimeda species. Exposure to elevated temperature alone or reduced pH alone decreased photosynthesis and calcification in these species. However, there was a strong synergistic effect of elevated temperature and reduced pH, with dramatic reductions in photosynthesis and calcification in all three species. This study suggested that the elevated temperature of 32°C and the pCO2 concentration of 1000 µatm are the upper limit for survival of these species art our site of collection (Heron Island on the Great Barrier Reef, Australia). Microsensors enabled the detection of O2 surrounding specimens at high spatial and temporal resolutions and revealed a 70-80% in decrease in O2 production under elevated CO2 and temperature (1200 µatm 32°C) in Halimeda (Chapter 5) and foraminifera (Chapter 6). The results from O2 microprofiles support the photosynthetic pigment and chlorophyll fluorescence data, showing decreasing O2 production with declining chlorophyll a and b concentrations and a decrease in photosynthetic efficiency under ocean acidification and/or temperature stress. This revealed that photosynthesis and calcification are closely coupled with reductions in photosynthetic efficiency leading to reductions in calcification. Reductions in carbonate availability reduced calcification and that can lead to weakened calcified structures. Elevations in water temperature is expected to augment this weakening, resulting in decreased mechanical integrity and increased susceptibility to storm- and herbivory-induced mortality in Halimeda sp. The morphological and biomechanical properties in H. macroloba and H. cylindracea at different wave exposures were then investigated in their natural reef habitats (Chapter 7). The results showed that both species have morphological (e.g. blade surface area, holdfast volume) and biomechanical (e.g. force required to uproot, force required to break thalli) adaptations to different levels of hydrodynamic exposure. The mechanical integrity and skeletal mineralogy of Halimeda was then investigated in response to future climate change scenarios (Chapter 7). The biomechanical properties (shear strength and punch strength) significantly declined in the more heavily calcified H. cylindracea at 32ºC and 1000 µatm, whereas were variable in less heavily calcified H. macroloba, indicating different responses between Halimeda species. An increase in less-soluble low Mgcalcite was observed under elevated CO2 conditions. Significant changes in Mg:Ca and Sr:Ca ratios under elevated CO2 and temperature conditions suggested that calcification was affected at the ionic level. It is concluded that Halimeda is biomechanically sensitive to elevated temperature and more acidic oceans and may lead to increasing susceptibility to herbivory and higher risk of thallus breakage or removal from the substrate. Experimental results throughout the thesis revealed that ocean acidification and warming have negative impacts on photosynthetic efficiency, productivity, calcification and mechanical integrity, which is likely to lead to increased mortality in these species under a changing climate. A loss of these calcifying keystone species will have a dramatic impact on carbonate accumulation, sediment turnover, and coral reef community and habitat structure.

Symbiosis increases coral tolerance to ocean acidification

Increasing the acidity of ocean waters will directly threaten calcifying marine organisms such as reef-building scleractinian corals, and the myriad of species that rely on corals for protection and sustenance. Ocean pH has already decreased by around 0.1 pH units since the beginning of the industrial revolution, and is expected to decrease by another 0.2–0.4 pH units by 2100. This study mimicked the pre-industrial, present, and near-future levels of pCO² using a precise control system (±5% pCO²), to assess the impact of ocean acidification on the calcification of recently-settled primary polyps of Acropora digitifera, both with and without symbionts, and adult fragments with symbionts. The increase in pCO² of 100 μatm between the pre-industrial period and the present had more effect on the calcification rate of adult A. digitifera than the anticipated future increases of several hundreds of micro-atmospheres of pCO². The primary polyps with symbionts showed higher calcification rates than primary polyps without symbionts, suggesting that (i) primary polyps housing symbionts are more tolerant to near-future ocean acidification than organisms without symbionts, and (ii) corals acquiring symbionts from the environment (i.e. broadcasting species) will be more vulnerable to ocean acidification than corals that maternally acquire symbionts.

Could some coral reefs become sponge reefs as our climate changes?

Coral reefs across the world have been seriously degraded and have a bleak future in response to predicted global warming and ocean acidification (OA). However, this is not the first time that biocalcifying organisms, including corals, have faced the threat of extinction. The end-Triassic mass extinction (200 million years ago) was the most severe biotic crisis experienced by modern marine invertebrates, which selected against biocalcifiers; this was followed by the proliferation of another invertebrate group, sponges. The duration of this sponge-dominated period far surpasses that of alternative stable-ecosystem or phase-shift states reported on modern day coral reefs and, as such, a shift to sponge-dominated reefs warrants serious consideration as one future trajectory of coral reefs. We hypothesise that some coral reefs of today may become sponge reefs in the future, as sponges and corals respond differently to changing ocean chemistry and environmental conditions. To support this hypothesis, we discuss: 1) the presence of sponge reefs in the geological record; 2) reported shifts from coral- to sponge-dominated systems; and 3) direct and indirect responses of the sponge holobiont and its constituent parts (host and symbionts) to changes in temperature and pH. Based on this evidence, we propose that sponges may be one group to benefit from projected climate change and ocean acidification scenarios, and that increased sponge abundance represents a possible future trajectory for some coral reefs, which would have important implications for overall reef functioning.

A coral polyp model of photosynthesis, respiration and calcification incorporating a transcellular ion transport mechanism

A numerical simulation model of coral polyp photosynthesis, respiration and calcification was developed. The model is constructed with three components (ambient seawater, coelenteron and calcifying fluid), and incorporates photosynthesis, respiration and calcification processes with transcellular ion transport by Ca-ATPase activity and passive transmembrane CO₂ transport and diffusion. The model calculates dissolved inorganic carbon and total alkalinity in the ambient seawater, coelenteron and calcifying fluid, dissolved oxygen (DO) in the seawater and coelenteron and stored organic carbon (CH₂O). To reconstruct the drastic variation between light and dark respiration, respiration rate dependency on DO in the coelenteron is incorporated. The calcification rate depends on the aragonite saturation state in the calcifying fluid (Ωa _cal). Our simulation result was a good approximation of “light-enhanced calcification.” In our model, the mechanism is expressed as follows: (1) DO in the coelenteron is increased by photosynthesis, (2) respiration is stimulated by increased DO in the light (or respiration is limited by DO depletion in the dark), then (3) calcification increases due to Ca-ATPase, which is driven by the energy generated by respiration. The model simulation results were effective in reproducing the basic responses of the internal CO₂ system and DO. The daily calcification rate, the gross photosynthetic rate and the respiration rate under a high-flow condition increased compared to those under the zero-flow condition, but the net photosynthetic rate decreased. The calculated calcification rate responses to variations in the ambient aragonite saturation state (Ωa _amb) were nonlinear, and the responses agreed with experimental results of previous studies. Our model predicted that in response to ocean acidification (1) coral calcification will decrease, but will remain at a higher value until Ωa _amb decreases to 1, by maintaining a higher Ωa _cal due to the transcellular ion transport mechanism and (2) the net photosynthetic rate will increase.