Declining Coral Skeletal Extension for Forereef Colonies of Siderastrea siderea on the Mesoamerican Barrier Reef System, Southern Belize

BACKGROUND: Natural and anthropogenic stressors are predicted to have increasingly negative impacts on coral reefs. Understanding how these environmental stressors have impacted coral skeletal growth should improve our ability to predict how they may affect coral reefs in the future. We investigated century-scale variations in skeletal extension for the slow-growing massive scleractinian coral Siderastrea siderea inhabiting the forereef, backreef, and nearshore reefs of the Mesoamerican Barrier Reef System (MBRS) in the western Caribbean Sea. METHODOLOGY/PRINCIPAL FINDINGS: Thirteen S. siderea cores were extracted, slabbed, and X-rayed. Annual skeletal extension was estimated from adjacent low- and high-density growth bands. Since the early 1900s, forereef S. siderea colonies have shifted from exhibiting the fastest to the slowest average annual skeletal extension, while values for backreef and nearshore colonies have remained relatively constant. The rates of change in annual skeletal extension were -0.020±0.005, 0.011±0.006, and -0.008±0.006 mm yr⁻¹ per year [mean±SE] for forereef, backreef, and nearshore colonies respectively. These values for forereef and nearshore S. siderea were significantly lower by 0.031±0.008 and by 0.019±0.009 mm yr⁻¹ per year, respectively, than for backreef colonies. However, only forereef S. siderea exhibited a statistically significant decline in annual skeletal extension over the last century. CONCLUSIONS/SIGNIFICANCE: Our results suggest that forereef S. siderea colonies are more susceptible to environmental stress than backreef and nearshore counterparts, which may have historically been exposed to higher natural baseline stressors. Alternatively, sediment plumes, nutrients, and pollution originating from watersheds of Guatemala and Honduras may disproportionately impact the forereef environment of the MBRS. We are presently reconstructing the history of environmental stressors that have impacted the MBRS to constrain the cause(s) of the observed reductions in coral skeletal growth. This should improve our ability to predict and potentially mitigate the effects of future environmental stressors on coral reef ecosystems

Next-century ocean acidification and warming both reduce calcification rate, but only acidification alters skeletal morphology of reef-building coral Siderastrea siderea

Atmospheric pCO2 is predicted to rise from 400 to 900 ppm by year 2100, causing seawater temperature to increase by 1–4 °C and pH to decrease by 0.1–0.3. Sixty-day experiments were conducted to investigate the independent and combined impacts of acidification (pCO2 = 424–426, 888–940 ppm-v) and warming (T = 28, 32 °C) on calcification rate and skeletal morphology of the abundant and widespread Caribbean reef-building scleractinian coral Siderastrea siderea. Hierarchical linear mixed-effects modelling reveals that coral calcification rate was negatively impacted by both warming and acidification, with their combined effects yielding the most deleterious impact. Negative effects of warming (32 °C/424 ppm-v) and high-temperature acidification (32 °C/940 ppm-v) on calcification rate were apparent across both 30-day intervals of the experiment, while effects of low-temperature acidification (28 °C/888 ppm-v) were not apparent until the second 30-day interval—indicating delayed onset of acidification effects at lower temperatures. Notably, two measures of coral skeletal morphology–corallite height and corallite infilling–were negatively impacted by next-century acidification, but not by next-century warming. Therefore, while next-century ocean acidification and warming will reduce the rate at which corals build their skeletons, next-century acidification will also modify the morphology and, potentially, function of coral skeletons

Intrareef variations in Li/Mg and Sr/Ca sea surface temperature proxies in the Caribbean reef‐building coral Siderastrea siderea

Caribbean sea surface temperatures (SSTs) have increased at a rate of 0.2°C per decade since 1971, a rate double that of the mean global change. Recent investigations of the coral Siderastrea siderea on the Belize Mesoamerican Barrier Reef System (MBRS) have demonstrated that warming over the last 30 years has had a detrimental impact on calcification. Instrumental temperature records in this region are sparse, making it necessary to reconstruct longer SST records indirectly through geochemical temperature proxies. Here we investigate the skeletal Sr/Ca and Li/Mg ratios of S. siderea from two distinct reef zones (forereef and backreef) of the MBRS. Our field calibrations of S. siderea show that Li/Mg and Sr/Ca ratios are well correlated with temperature, although both ratios are 3 times more sensitive to temperature change in the forereef than in the backreef. These differences suggest that a secondary parameter also influences these SST proxies, highlighting the importance for site‐ and species‐specific SST calibrations. Application of these paleothermometers to downcore samples reveals highly uncertain reconstructed temperatures in backreef coral, but well‐matched reconstructed temperatures in forereef coral, both between Sr/Ca‐SSTs and Li/Mg‐SSTs, and in comparison to the Hadley Centre Sea Ice and Sea Surface Temperature record. Reconstructions generated from a combined Sr/Ca and Li/Mg multiproxy calibration improve the precision of these SST reconstructions. This result confirms that there are circumstances in which both Li/Mg and Sr/Ca are reliable as stand‐alone and combined proxies of sea surface temperature. However, the results also highlight that high‐precision, site‐specific calibrations remain critical for reconstructing accurate SSTs from coral‐based elemental proxies

Intrareef variations in Li/Mg and Sr/Ca sea surface temperature proxies in the Caribbean reef-building coral Siderastrea siderea

Caribbean sea surface temperatures (SSTs) have increased at a rate of 0.2°C per decade since 1971, a rate double that of the mean global change. Recent investigations of the coral Siderastrea siderea on the Belize Mesoamerican Barrier Reef System (MBRS) have demonstrated that warming over the last 30 years has had a detrimental impact on calcification. Instrumental temperature records in this region are sparse, making it necessary to reconstruct longer SST records indirectly through geochemical temperature proxies. Here we investigate the skeletal Sr/Ca and Li/Mg ratios of S. siderea from two distinct reef zones (forereef and backreef) of the MBRS. Our field calibrations of S. siderea show that Li/Mg and Sr/Ca ratios are well correlated with temperature, although both ratios are 3 times more sensitive to temperature change in the forereef than in the backreef. These differences suggest that a secondary parameter also influences these SST proxies, highlighting the importance for site‐ and species‐specific SST calibrations. Application of these paleothermometers to downcore samples reveals highly uncertain reconstructed temperatures in backreef coral, but well‐matched reconstructed temperatures in forereef coral, both between Sr/Ca‐SSTs and Li/Mg‐SSTs, and in comparison to the Hadley Centre Sea Ice and Sea Surface Temperature record. Reconstructions generated from a combined Sr/Ca and Li/Mg multiproxy calibration improve the precision of these SST reconstructions. This result confirms that there are circumstances in which both Li/Mg and Sr/Ca are reliable as stand‐alone and combined proxies of sea surface temperature. However, the results also highlight that high‐precision, site‐specific calibrations remain critical for reconstructing accurate SSTs from coral‐based elemental proxies

Ocean acidification impairs crab foraging behaviour

Anthropogenic elevation of atmospheric CO2 is driving global-scale ocean acidification, which consequently influences calcification rates of many marine invertebrates and potentially alters their susceptibility to predation. Ocean acidification may also impair an organism's ability to process environmental and biological cues. These counteracting impacts make it challenging to predict how acidification will alter species interactions and community structure. To examine effects of acidification on consumptive and behavioural interactions between mud crabs (Panopeus herbstii) and oysters (Crassostrea virginica), oysters were reared with and without caged crabs for 71 days at three pCO2 levels. During subsequent predation trials, acidification reduced prey consumption, handling time and duration of unsuccessful predation attempt. These negative effects of ocean acidification on crab foraging behaviour more than offset any benefit to crabs resulting from a reduction in the net rate of oyster calcification. These findings reveal that efforts to evaluate how acidification will alter marine food webs should include quantifying impacts on both calcification rates and animal behaviour

Thermal stress reduces pocilloporid coral resilience to ocean acidification by impairing control over calcifying fluid chemistry

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Guillermic, M., Cameron, L. P., De Corte, I., Misra, S., Bijma, J., de Beer, D., Reymond, C. E., Westphal, H., Ries, J. B., & Eagle, R. A. Thermal stress reduces pocilloporid coral resilience to ocean acidification by impairing control over calcifying fluid chemistry. Science Advances, 7(2), (2021): eaba9958, https://doi.org/10.1126/sciadv.aba9958.The combination of thermal stress and ocean acidification (OA) can more negatively affect coral calcification than an individual stressors, but the mechanism behind this interaction is unknown. We used two independent methods (microelectrode and boron geochemistry) to measure calcifying fluid pH (pHcf) and carbonate chemistry of the corals Pocillopora damicornis and Stylophora pistillata grown under various temperature and pCO2 conditions. Although these approaches demonstrate that they record pHcf over different time scales, they reveal that both species can cope with OA under optimal temperatures (28°C) by elevating pHcf and aragonite saturation state (Ωcf) in support of calcification. At 31°C, neither species elevated these parameters as they did at 28°C and, likewise, could not maintain substantially positive calcification rates under any pH treatment. These results reveal a previously uncharacterized influence of temperature on coral pHcf regulation—the apparent mechanism behind the negative interaction between thermal stress and OA on coral calcification.R.A.E. and J.B.R. acknowledge support from National Science Foundation grants OCE-1437166 and OCE-1437371. The work was also supported by the “Laboratoire d’Excellence” LabexMER (ANR-10-LABX-19), cofunded by a grant from the French government under the program “Investissements d’Avenir,” and an IAGC student grant 2017. R.A.E. acknowledges financial and logistical support from the Pritzker Endowment to UCLA IoES, and J.B.R. acknowledges support from the ZMT and the Hanse-Wissenschaftskolleg Fellowship Program and the NSF OCE award #1437371

Boron isotope sensitivity to seawater pH change in a species of Neogoniolithon coralline red alga

The increase in atmospheric carbon dioxide (CO2) observed since the industrial revolution has reduced surface ocean pH by ∼0.1 pH units, with further change in the oceanic system predicted in the coming decades. Calcareous organisms can be negatively affected by extreme changes in seawater pH (pHsw) such as this due to the associated changes in the oceanic carbonate system. The boron isotopic composition (δ11B) of biogenic carbonates has been previously used to monitor pH at the calcification site (pHcf) in scleractinian corals, providing mechanistic insights into coral biomineralisation and the impact of variable pHsw on this process. Motivated by these investigations, this study examines the δ11B of the high-Mg calcite skeleton of the coralline red alga Neogoniolithon sp. to constrain pHcf, and investigates how this taxon’s pHcf is impacted by ocean acidification. δ11B was measured in multiple algal replicates (n = 4–5) cultured at four different pCO2 scenarios – averaging (±1σ) 409 (±6), 606 (±7), 903 (±12) and 2856 (±54) μatm, corresponding to average pHsw (±1σ) of 8.19 (±0.03), 8.05 (±0.06), 7.91 (±0.03) and 7.49 (±0.02) respectively. Results show that skeletal δ11B is elevated relative to the δ11B of seawater borate at all pHsw treatments by up to 18‰. Although substantial variability in δ11B exists between replicate samples cultured at a given pHsw (smallest range = 2.32‰ at pHsw 8.19, largest range = 6.08‰ at pHsw 7.91), strong correlations are identified between δ11B and pHsw (R2 = 0.72, p < 0.0001, n = 16) and between δ11B and B/Ca (R2 = 0.72, p < 0.0001, n = 16). Assuming that skeletal δ11B reflects pHcf as previously observed for scleractinian corals, the average pHcf across all experiments was 1.20 pH units (0.79 to 1.56) higher than pHsw, with the magnitude of this offset varying parabolically with decreasing pHsw, with a maximum difference between pHsw and pHcf at a pHsw of 7.91. Observed relationships between pHsw and calcification rate, and between pHsw and pHcf, suggest that coralline algae exhibit some resilience to moderate ocean acidification via increase of pHcf relative to pHsw in a similar manner to scleractinian corals. However, these results also indicate that pHcf cannot be sufficiently increased by algae exposed to a larger reduction in pHsw, adversely impacting calcification rates of coralline red algae

Exposure duration modulates the response of Caribbean corals to global change stressors

Global change, including rising temperatures and acidification, threatens corals globally. Although bleaching events reveal fine-scale patterns of resilience, traits enabling persistence under global change remain elusive. We conducted a 95-d controlled-laboratory experiment investigating how duration of exposure to warming (~28, 31°C), acidification (pCO2 ~ 343 [present day], ~663 [end of century], ~3109 [extreme] μatm), and their combination influences physiology of reef-building corals (Siderastrea siderea, Pseudodiploria strigosa) from two reef zones on the Belize Mesoamerican Barrier Reef System. Every 30 d, net calcification rate, host protein and carbohydrate, chlorophyll a, and symbiont density were quantified for the same coral individual to characterize acclimation potential under global change. Coral physiologies of the two species were differentially affected by stressors and exposure duration was found to modulate these responses. Siderastrea siderea exhibited resistance to end of century pCO2 and temperature stress, but calcification was negatively affected by extreme pCO2. However, S. siderea calcification rates remained positive after 95 d of extreme pCO2 conditions, suggesting acclimation. In contrast, P. strigosa was more negatively influenced by elevated temperatures, which reduced most physiological parameters. An exception was nearshore P. strigosa, which maintained calcification rates under elevated temperature, suggesting local adaptation to the warmer environment of their natal reef zone. This work highlights how tracking coral physiology across various exposure durations can capture acclimatory responses to global change stressors.First author draf

Physicochemical Control of Caribbean Coral Calcification Linked to Host and Symbiont Responses to Varying pCO2 and Temperature

It is thought that the active physiological regulation of the chemistry of a parent fluid is an important process in the biomineralization of scleractinian corals. Biological regulation of calcification fluid pH (pHCF) and other carbonate chemistry parameters ([CO32−]CF, DICCF, and ΩCF) may be challenged by CO2 driven acidification and temperature. Here, we examine the combined influence of changing temperature and CO2 on calcifying fluid regulation in four common Caribbean coral species—Porites astreoides, Pseudodiploria strigosa, Undaria tenuifolia, and Siderastrea siderea. We utilize skeletal boron geochemistry (B/Ca and δ11B) to probe the pHCF, [CO32−]CF, and DICCF regulation in these corals, and δ13C to track changes in the sources of carbon for calcification. Temperature was found to not influence pHCF regulation across all pCO2 treatments in these corals, in contrast to recent studies on Indo-Pacific pocilloporid corals. We find that [DIC]CF is significantly lower at higher temperatures in all the corals, and that the higher temperature was associated with depletion of host energy reserves, suggesting [DIC]CF reductions may result from reduced input of respired CO2 to the DIC pool for calcification. In addition, δ13C data suggest that under high temperature and CO2 conditions, algal symbiont photosynthesis continues to influence the calcification pool and is associated with low [DIC]CF in P. strigosa and P. astreoides. In P. astreoides this effect is also associated with an increase in chlorophyll a concentration in coral tissues at higher temperatures. These observations collectively support the assertion that physicochemical control over coral calcifying fluid chemistry is coupled to host and symbiont physiological responses to environmental change, and reveals interspecific differences in the extent and nature of this coupling

Impacts of Warming and Acidification on Coral Calcification Linked to Photosymbiont Loss and Deregulation of Calcifying Fluid pH

Corals are globally important calcifiers that exhibit complex responses to anthropogenic warming and acidification. Although coral calcification is supported by high seawater pH, photosynthesis by the algal symbionts of zooxanthellate corals can be promoted by elevated pCO2. To investigate the mechanisms underlying corals’ complex responses to global change, three species of tropical zooxanthellate corals (Stylophora pistillata, Pocillopora damicornis, and Seriatopora hystrix) and one species of asymbiotic cold-water coral (Desmophyllum pertusum, syn. Lophelia pertusa) were cultured under a range of ocean acidification and warming scenarios. Under control temperatures, all tropical species exhibited increased calcification rates in response to increasing pCO2. However, the tropical species’ response to increasing pCO2 flattened when they lost symbionts (i.e., bleached) under the high-temperature treatments—suggesting that the loss of symbionts neutralized the benefit of increased pCO2 on calcification rate. Notably, the cold-water species that lacks symbionts exhibited a negative calcification response to increasing pCO2, although this negative response was partially ameliorated under elevated temperature. All four species elevated their calcifying fluid pH relative to seawater pH under all pCO2 treatments, and the magnitude of this offset (Δ[H+]) increased with increasing pCO2. Furthermore, calcifying fluid pH decreased along with symbiont abundance under thermal stress for the one species in which calcifying fluid pH was measured under both temperature treatments. This observation suggests a mechanistic link between photosymbiont loss (‘bleaching’) and impairment of zooxanthellate corals’ ability to elevate calcifying fluid pH in support of calcification under heat stress. This study supports the assertion that thermally induced loss of photosymbionts impairs tropical zooxanthellate corals’ ability to cope with CO2-induced ocean acidification