Rubble persistence under ocean acidification threatened by accelerated bioerosion and lower-density coral skeletons.

As the balance between erosional and constructive processes on coral reefs tilts in favor of framework loss under human-induced local and global change, many reef habitats worldwide degrade and flatten. The resultant generation of coral rubble and the beds they form can have lasting effects on reef communities and structural complexity, threatening the continuity of reef ecological functions and the services they provide. To comprehensively capture changing framework processes and predict their evolution in the context of climate change, heavily colonized rubble fragments were exposed to ocean acidification (OA) conditions for 55 days. Controlled diurnal pH oscillations were incorporated in the treatments to account for the known impact of diel carbonate chemistry fluctuations on calcification and dissolution response to OA. Scenarios included contemporary pH (8.05 ± 0.025 diel fluctuation), elevated OA (7.90 ± 0.025), and high OA (7.70 ± 0.025). We used a multifaceted approach, combining chemical flux analyses, mass alteration measurements, and computed tomography scanning images to measure total and chemical bioerosion, as well as chemically driven secondary calcification. Rates of net carbonate loss measured in the contemporary conditions (1.36 kg m-2 year-1) were high compared to literature and increased in OA scenarios (elevated: 1.84 kg m-2 year-1 and high: 1.59 kg m-2 year-1). The acceleration of these rates was driven by enhanced chemical dissolution and reduced secondary calcification. Further analysis revealed that the extent of these changes was contingent on the density of the coral skeleton, in which the micro- and macroborer communities reside. Findings indicated that increased mechanical bioerosion rates occurred in rubble with lower skeletal density, which is of note considering that corals form lower-density skeletons under OA. These direct and indirect effects of OA on chemical and mechanical framework-altering processes will influence the permanence of this crucial habitat, carrying implications for biodiversity and reef ecosystem function.

Impact of dissolved CO2 on calcification in two large, benthic foraminiferal species.

Rising atmospheric CO2 shifts the marine inorganic carbonate system and decreases seawater pH, a process often abbreviated to 'ocean acidification'. Since acidification decreases the saturation state for crystalline calcium carbonate (e.g., calcite and aragonite), rising dissolved CO2 levels will either increase the energy demand for calcification or reduce the total amount of CaCO3 precipitated. Here we report growth of two large benthic photosymbiont-bearing foraminifera, Heterostegina depressa and Amphistegina lessonii, cultured at four different ocean acidification scenarios (400, 700, 1000 and 2200 ppm atmospheric pCO2). Using the alkalinity anomaly technique, we calculated the amount of calcium carbonate precipitated during the incubation and found that both species produced the most carbonate at intermediate CO2 levels. The chamber addition rates for each of the conditions were also determined and matched the changes in alkalinity. These results were complemented by micro-CT scanning of selected specimens to visualize the effect of CO2 on growth. The increased chamber addition rates at elevated CO2 concentrations suggest that both foraminifera species can take advantage of the increased availability of the inorganic carbon, despite a lower saturation state. This adds to the growing number of reports showing the variable response of foraminifera to elevated CO2 concentrations, which is likely a consequence of differences in calcification mechanisms.

Restoration and coral adaptation delay, but do not prevent, climate-driven reef framework erosion of an inshore site in the Florida Keys.

For reef framework to persist, calcium carbonate production by corals and other calcifiers needs to outpace loss due to physical, chemical, and biological erosion. This balance is both delicate and dynamic and is currently threatened by the effects of ocean warming and acidification. Although the protection and recovery of ecosystem functions are at the center of most restoration and conservation programs, decision makers are limited by the lack of predictive tools to forecast habitat persistence under different emission scenarios. To address this, we developed a modelling approach, based on carbonate budgets, that ties species-specific responses to site-specific global change using the latest generation of climate models projections (CMIP6). We applied this model to Cheeca Rocks, an outlier in the Florida Keys in terms of high coral cover, and explored the outcomes of restoration targets scheduled in the coming 20 years at this site by the Mission: Iconic Reefs restoration initiative. Additionally, we examined the potential effects of coral thermal adaptation by increasing the bleaching threshold by 0.25, 0.5, 1 and 2˚C. Regardless of coral adaptative capacity or restoration, net carbonate production at Cheeca Rocks declines heavily once the threshold for the onset of annual severe bleaching is reached. The switch from net accretion to net erosion, however, is significantly delayed by mitigation and adaptation. The maintenance of framework accretion until 2100 and beyond is possible under a decreased emission scenario coupled with thermal adaptation above 0.5˚C. Although restoration initiatives increase reef accretion estimates, Cheeca Rocks will only be able to keep pace with future sea-level rise in a world where anthropogenic CO2 emissions are reduced. Present results, however, attest to the potential of restoration interventions combined with increases in coral thermal tolerance to delay the onset of mass bleaching mortalities, possibly in time for a low-carbon economy to be implemented and complementary mitigation measures to become effective.

pH Regulation and Tissue Coordination Pathways Promote Calcium Carbonate Bioerosion by Excavating Sponges.

Coral reefs are threatened by a multitude of environmental and biotic influences. Among these, excavating sponges raise particular concern since they bore into coral skeleton forming extensive cavities which lead to weakening and loss of reef structures. Sponge bioerosion is achieved by a combination of chemical dissolution and mechanical chip removal and ocean acidification has been shown to accelerate bioerosion rates. However, despite the ecological relevance of sponge bioerosion, the exact chemical conditions in which dissolution takes place and how chips are removed remain elusive. Using fluorescence microscopy, we show that intracellular pH is lower at etching sites compared to ambient seawater and the sponge's tissue. This is realised through the extension of filopodia filled with low intracellular pH vesicles suggesting that protons are actively transported into this microenvironment to promote CaCO3 dissolution. Furthermore, fusiform myocyte-like cells forming reticulated pathways were localised at the interface between calcite and sponge. Such cells may be used by sponges to contract a conductive pathway to remove chips possibly instigated by excess Ca2+ at the boring site. The mechanism underlying CaCO3 dissolution by sponges provides new insight into how environmental conditions can enhance dissolution and improves predictions of future rates of coral dissolution due to sponge activity.

In-situ incubation of a coral patch for community-scale assessment of metabolic and chemical processes on a reef slope.

Anthropogenic pressures threaten the health of coral reefs globally. Some of these pressures directly affect coral functioning, while others are indirect, for example by promoting the capacity of bioeroders to dissolve coral aragonite. To assess the coral reef status, it is necessary to validate community-scale measurements of metabolic and geochemical processes in the field, by determining fluxes from enclosed coral reef patches. Here, we investigate diurnal trends of carbonate chemistry, dissolved organic carbon, oxygen, and nutrients on a 20 m deep coral reef patch offshore from the island of Saba, Dutch Caribbean by means of tent incubations. The obtained trends are related to benthic carbon fluxes by quantifying net community calcification (NCC) and net community production (NCP). The relatively strong currents and swell-induced near-bottom surge at this location caused minor seawater exchange between the incubated reef and ambient water. Employing a compensating interpretive model, the exchange is used to our advantage as it maintains reasonably ventilated conditions, which conceivably prevents metabolic arrest during incubation periods of multiple hours. No diurnal trends in carbonate chemistry were detected and all net diurnal rates of production were strongly skewed towards respiration suggesting net heterotrophy in all incubations. The NCC inferred from our incubations ranges from -0.2 to 1.4 mmol CaCO3 m-2 h-1 (-0.2 to 1.2 kg CaCO3 m-2 year-1) and NCP varies from -9 to -21.7 mmol m-2 h-1 (net respiration). When comparing to the consensus-based ReefBudget approach, the estimated NCC rate for the incubated full planar area (0.36 kg CaCO3 m-2 year-1) was lower, but still within range of the different NCC inferred from our incubations. Field trials indicate that the tent-based incubation as presented here, coupled with an appropriate interpretive model, is an effective tool to investigate, in situ, the state of coral reef patches even when located in a relatively hydrodynamic environment.

Quantification of chemical and mechanical bioerosion rates of six Caribbean excavating sponge species found on the coral reefs of Curaçao.

Excavating sponges are among the most important macro-eroders of carbonate substrates in marine systems. Their capacity to remove substantial amounts of limestone makes these animals significant players that can unbalance the reef carbonate budget of tropical coral reefs. Nevertheless, excavating sponges are currently rarely incorporated in standardized surveys and experimental work is often restricted to a few species. Here were provide chemical and mechanical bioerosion rates for the six excavating sponge species most commonly found on the shallow reef of Curaçao (southern Caribbean): Cliona caribbaea, C. aprica, C. delitrix, C. amplicavata, Siphonodictyon brevitubulatum and Suberea flavolivescens. Chemical, mechanical and total bioerosion rates were estimated based on various experimental approaches applied to sponge infested limestone cores. Conventional standing incubation techniques were shown to strongly influence the chemical dissolution signal. Final rates, based on the change in alkalinity of the incubation water, declined significantly as a function of incubation time. This effect was mitigated by the use of a flow-through incubation system. Additionally, we found that mechanically removed carbonate fragments collected in the flow-through chamber (1 h) as well as a long-term collection method (1 wk) generally yielded comparable estimates for the capacity of these sponges to mechanically remove substratum. Observed interspecific variation could evidently be linked to the adopted boring strategy (i.e. gallery-forming, cavity-forming or network-working) and presence or absence of symbiotic zooxanthellae. Notably, a clear diurnal pattern was found only in species that harbour a dense photosymbiotic community. In these species chemical erosion was substantially higher during the day. Overall, the sum of individually acquired chemical and mechanical erosion using flow-through incubations was comparable to rates obtained gravimetrically. Such consistency is a first in this field of research. These findings support the much needed confirmation that, depending on the scientific demand, the different approaches presented here can be implemented concurrently as standardized methods.