Anomalies in the carbonate system of Red Sea coastal habitats

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Baldry, K., Saderne, V., McCorkle, D. C., Churchill, J. H., Agust, S., & Duarte, C. M. Anomalies in the carbonate system of Red Sea coastal habitats. Biogeosciences, 17(2), (2020): 423-439, doi:10.5194/bg-17-423-2020.We use observations of dissolved inorganic carbon (DIC) and total alkalinity (TA) to assess the impact of ecosystem metabolic processes on coastal waters of the eastern Red Sea. A simple, single-end-member mixing model is used to account for the influence of mixing with offshore waters and evaporation–precipitation and to model ecosystem-driven perturbations on the carbonate system chemistry of coral reefs, seagrass meadows and mangrove forests. We find that (1) along-shelf changes in TA and DIC exhibit strong linear relationships that are consistent with basin-scale net calcium carbonate precipitation; (2) ecosystem-driven changes in TA and DIC are larger than offshore variations in >70 % of sampled seagrass meadows and mangrove forests, changes which are influenced by a combination of longer water residence times and community metabolic rates; and (3) the sampled mangrove forests show strong and consistent contributions from both organic respiration and other sedimentary processes (carbonate dissolution and secondary redox processes), while seagrass meadows display more variability in the relative contributions of photosynthesis and other sedimentary processes (carbonate precipitation and oxidative processes). The results of this study highlight the importance of resolving the influences of water residence times, mixing and upstream habitats on mediating the carbonate system and coastal air–sea carbon dioxide fluxes over coastal habitats in the Red Sea.This research has been supported by the King Abdullah University of Science and Technology (KAUST) (grant nos. BAS/1/1071-01-01 and BAS/1/1072-01-01) and the Investment in Science fund at WHOI

Seagrass beds as ocean acidification refuges for mussels? High resolution measurements of pCO2 and O2 in a Zostera marina and Mytilus edulis mosaic habitat

It has been speculated that macrophytes beds might act as a refuge for calcifiers from ocean acidification. In the shallow nearshores of the western Kiel Bay (Baltic Sea), mussel and seagrass beds are interlacing, forming a mosaic habitat. Naturally, the diverse physiological activities of seagrasses and mussels are affected by seawater carbonate chemistry and they locally modify it in return. Calcification by shellfishes is sensitive to seawater acidity; therefore the photosynthetic activity of seagrasses in confined shallow waters creates favorable chemical conditions to calcification at daytime but turn the habitat less favorable or even corrosive to shells at night. In contrast, mussel respiration releases CO2, turning the environment more favorable for photosynthesis by adjacent seagrasses. At the end of summer, these dynamics are altered by the invasion of high pCO2/low O2 coming from the deep water of the Bay. However, it is in summer that mussel spats settle on the leaves of seagrasses until migrating to the permanent habitat where they will grow adult. These early life phases (larvae/spats) are considered as most sensitive with regard to seawater acidity. So far, the dynamics of CO2 have never been continuously measured during this key period of the year, mostly due to the technological limitations. In this project we used a combination of state-of-the-art technologies and discrete sampling to obtain high-resolution time-series of pCO2 and O2 at the interface between a seagrass and a mussel patch in Kiel Bay in August and September 2013. From these, we derive the entire carbonate chemistry using statistical models. We found the monthly average pCO2 more than 50 % (approx. 640 μatm for August and September) above atmospheric equilibrium right above the mussel patch together with large diel variations of pCO2 within 24 h: 887 ± 331 μatm in August and 742 ± 281 μatm in September (mean ± SD). We observed important daily corrosiveness for calcium carbonates (Ωarag and Ωcalc < 1) centered on sunrise. On the positive side, the investigated habitat never suffered from hypoxia during the study period. We emphasize the need for more experiments on the impact of these acidic conditions on (juvenile) mussels with a focus on the distinct day-night variations observed

Intense pCO2 and [O2] Oscillations in a Mussel-Seagrass Habitat: Implications for Calcification

Numerous studies have been conducted on the effect of ocean acidification on calcifiers inhabiting nearshore benthic habitats, such as the blue mussel Mytilus edulis. The majority of these experiments was performed under stable CO2 partial pressure (pCO2), carbonate chemistry and oxygen (O2) levels, reflecting present or expected future open ocean conditions. Consequently, levels and variations occurring in coastal habitats, due to biotic and abiotic processes, were mostly neglected, even though these variations largely override global long-term trends. To highlight this hiatus and guide future research, state-of-the-art technologies were deployed to obtain high-resolution time series of pCO2 and [O2] on a mussel patch within a Zostera marina seagrass bed, in Kiel Bay (western Baltic Sea) in August and September 2013. Combining the in situ data with results of discrete sample measurements, a full seawater carbonate chemistry was derived using statistical models. An average pCO2 more than 50 % (~ 640 µatm) higher than current atmospheric levels was found right above the mussel patch. Diel amplitudes of pCO2 were large: 765 ± 310 (mean ± SD). Corrosive conditions for calcium carbonates (Ωarag and Ωcalc < 1) centered on sunrise were found, but the investigated habitat never experienced hypoxia throughout the study period. It is estimated that mussels experience conditions limiting calcification for 12–15 h per day, based on a regional calcium carbonate concentration physiological threshold. Our findings call for more extensive experiments on the impact of fluctuating corrosive conditions on mussels. We also stress the complexity of the interpretation of carbonate chemistry time series data in such dynamic coastal environments

Macroalgae may mitigate ocean acidification effects on mussel calcification by increasing pH and its fluctuations

Ocean acidification (OA) is generally assumed to negatively impact calcification rates of marine organisms. At a local scale however, biological activity of macrophytes may generate pH fluctuations with rates of change that are orders of magnitude larger than the long-term trend predicted for the open ocean. These fluctuations may in turn impact benthic calcifiers in the vicinity. Combining laboratory, mesocosm and field studies, such interactions between OA, the brown alga Fucus vesiculosus, the sea grass Zostera marina and the blue mussel Mytilus edulis were investigated at spatial scales from decimetres to 100s of meters in the western Baltic. Macrophytes increased the overall mean pH of the habitat by up to 0.3 units relative to macrophyte-free, but otherwise similar, habitats and imposed diurnal pH fluctuations with amplitudes ranging from 0.3 to more than 1 pH unit. These amplitudes and their impact on mussel calcification tended to increase with increasing macrophyte biomass to bulk water ratio. At the laboratory and mesocosm scales, biogenic pH fluctuations allowed mussels to maintain calcification even under acidified conditions by shifting most of their calcification activity into the daytime when biogenic fluctuations caused by macrophyte activity offered temporal refuge from OA stress. In natural habitats with a low biomass to water body ratio, the impact of biogenic pH fluctuations on mean calcification rates of M. edulis was less pronounced. Thus, in dense algae or seagrass habitats, macrophytes may mitigate OA impact on mussel calcification by raising mean pH and providing temporal refuge from acidification stress

Total alkalinity production in a mangrove ecosystem reveals an overlooked Blue Carbon component

Mangroves have the capacity to sequester organic carbon (C-org) in their sediments permanently. However, the carbon budget of mangroves is also affected by the total alkalinity (TA) budget. Principally, TA emitted from carbonate sediment dissolution is a perennial sink of atmospheric CO2. The assessment of the TA budget of mangrove carbonate sediments in the Red Sea revealed a large TA emission of 403 +/- 17 mmol m(-2)d(-1), independent of light, seasons, or the presence of pneumatophores, compared to -36 +/- 10 mmol m(-2)d(-1)in lagoon sediment. We estimate the TA emission from carbonate dissolution in Red Sea mangroves supported a CO2 uptake of 345 +/- 15 gC m(-2)yr(-1), 23-fold the C-org burial rate of 15 gC m(-2)yr(-1). The focus on C-org burial in sediments may substantially underestimate the role of mangroves in CO(2)removal. Quantifying the role of mangroves in climate change mitigation requires carbonate dissolution to be included in assessments.Peer reviewe

High summer temperatures amplify functional differences between coral- and algae-dominated reef communities

Shifts from coral to algal dominance are expected to increase in tropical coral reefs as a result of anthropogenic disturbances. The consequences for key ecosystem functions such as primary productivity, calcification, and nutrient recycling are poorly understood, particularly under changing environmental conditions. We used a novel in situ incubation approach to compare functions of coral- and algae-dominated communities in the central Red Sea bimonthly over an entire year. In situ gross and net community primary productivity, calcification, dissolved organic carbon fluxes, dissolved inorganic nitrogen fluxes, and their respective activation energies were quantified to describe the effects of seasonal changes. Overall, coral-dominated communities exhibited 30% lower net productivity and 10 times higher calcification than algae-dominated communities. Estimated activation energies indicated a higher thermal sensitivity of coral-dominated communities. In these communities, net productivity and calcification were negatively correlated with temperature (>40% and >65% reduction, respectively, with +5 degrees C increase from winter to summer), whereas carbon losses via respiration and dissolved organic carbon release more than doubled at higher temperatures. In contrast, algae-dominated communities doubled net productivity in summer, while calcification and dissolved organic carbon fluxes were unaffected. These results suggest pronounced changes in community functioning associated with coral-algal phase shifts. Algae-dominated communities may outcompete coral-dominated communities because of their higher productivity and carbon retention to support fast biomass accumulation while compromising the formation of important reef framework structures. Higher temperatures likely amplify these functional differences, indicating a high vulnerability of ecosystem functions of coral-dominated communities to temperatures even below coral bleaching thresholds. Our results suggest that ocean warming may not only cause but also amplify coral-algal phase shifts in coral reefs.Peer reviewe

Oxygen supersaturation protects coastal marine fauna from ocean warming

Ocean warming affects the life history and fitness of marine organisms by, among others, increasing animal metabolism and reducing oxygen availability. In coastal habitats, animals live in close association with photosynthetic organisms whose oxygen supply supports metabolic demands and may compensate for acute warming. Using a unique high-frequency monitoring dataset, we show that oxygen supersaturation resulting from photosynthesis closely parallels sea temperature rise during diel cycles in Red Sea coastal habitats. We experimentally demonstrate that oxygen supersaturation extends the survival to more extreme temperatures of six species from four phyla. We clarify the mechanistic basis of the extended thermal tolerance by showing that hyperoxia fulfills the increased metabolic demand at high temperatures. By modeling 1 year of water temperatures and oxygen concentrations, we predict that oxygen supersaturation from photosynthetic activity invariably fuels peak animal metabolic demand, representing an underestimated factor of resistance and resilience to ocean warming in ectotherms

Integrating environmental variability to broaden the research on coral responses to future ocean conditions

Our understanding of the response of reef-building corals to changes in their physical environment is largely based on laboratory experiments, analysis of long-term field data, and model projections. Experimental data provide unique insights into how organisms respond to variation of environmental drivers. However, an assessment of how well experimental conditions cover the breadth of environmental conditions and variability where corals live successfully is missing. Here, we compiled and analyzed a globally distributed dataset of in-situ seasonal and diurnal variability of key environmental drivers (temperature, pCO2, and O2) critical for the growth and livelihood of reef-building corals. Using a meta-analysis approach, we compared the variability of environmental conditions assayed in coral experimental studies to current and projected conditions in their natural habitats. We found that annual temperature profiles projected for the end of the 21st century were characterized by distributional shifts in temperatures with warmer winters and longer warm periods in the summer, not just peak temperatures. Furthermore, short-term hourly fluctuations of temperature and pCO2 may regularly expose corals to conditions beyond the projected average increases for the end of the 21st century. Coral reef sites varied in the degree of coupling between temperature, pCO2, and dissolved O2, which warrants site-specific, differentiated experimental approaches depending on the local hydrography and influence of biological processes on the carbonate system and O2 availability. Our analysis highlights that a large portion of the natural environmental variability at short and long timescales is underexplored in experimental designs, which may provide a path to extend our understanding on the response of corals to global climate change

Extreme variations of pCO2 and pH in a macrophyte meadow of the Baltic Sea in summer: evidence of the effect of photosynthesis and local upwelling

The impact of ocean acidification on benthic habitats is a major preoccupation of the scientific community. However, the natural variability of pCO2 and pH in those habitats remains understudied, especially in temperate areas. In this study we investigated temporal variations of the carbonate system in nearshore macrophyte meadows of the western Baltic Sea. These are key benthic ecosystems, providing spawning and nursery areas as well as food to numerous commercially important species. In situ pCO2, pH (total scale), salinity and PAR irradiance were measured with a continuous recording sensor package dropped in a shallow macrophyte meadow (Eckernförde bay, western Baltic Sea) during three different weeks in July (pCO2 and PAR only), August and September 2011.The mean (± SD) pCO2 in July was 383±117 µatm. The mean (± SD) pCO2 and pHtot in August were 239±20 µatm and 8.22±0.1, respectively. The mean (± SD) pCO2 and pHtot in September were 1082±711 µatm and 7.83±0.40, respectively. Daily variations of pCO2 due to photosynthesis and respiration (difference between daily maximum and minimum) were of the same order of magnitude: 281±88 µatm, 219±89 μatm and 1488±574 µatm in July, August and September respectively. The observed variations of pCO2 were explained through a statistical model considering wind direction and speed together with PAR irradiance. At a time scale of days to weeks, local upwelling of elevated pCO2 water masses with offshore winds drives the variation. Within days, primary production is responsible. The results demonstrate the high variability of the carbonate system in nearshore macrophyte meadows depending on meteorology and biological activities. We highlight the need to incorporate these variations in future pCO2 scenarios and experimental designs for nearshore habitats

Differential Responses of Calcifying and Non-Calcifying Epibionts of a Brown Macroalga to Present-Day and Future Upwelling pCO2

Seaweeds are key species of the Baltic Sea benthic ecosystems. They are the substratum of numerous fouling epibionts like bryozoans and tubeworms. Several of these epibionts bear calcified structures and could be impacted by the high pCO2 events of the late summer upwellings in the Baltic nearshores. Those events are expected to increase in strength and duration with global change and ocean acidification. If calcifying epibionts are impacted by transient acidification as driven by upwelling events, their increasing prevalence could cause a shift of the fouling communities toward fleshy species. The aim of the present study was to test the sensitivity of selected seaweed macrofoulers to transient elevation of pCO2 in their natural microenvironment, i.e. the boundary layer covering the thallus surface of brown seaweeds. Fragments of the macroalga Fucus serratus bearing an epibiotic community composed of the calcifiers Spirorbis spirorbis (Annelida) and Electra pilosa (Bryozoa) and the non-calcifier Alcyonidium hirsutum (Bryozoa) were maintained for 30 days under three pCO2 conditions: natural 460±59 µatm, present-day upwelling1193±166 µatm and future upwelling 3150±446 µatm. Only the highest pCO2 caused a significant reduction of growth rates and settlement of S. spirorbis individuals. Additionally, S. spirorbis settled juveniles exhibited enhanced calcification of 40% during daylight hours compared to dark hours, possibly reflecting a day-night alternation of an acidification-modulating effect by algal photosynthesis as opposed to an acidification-enhancing effect of algal respiration. E. pilosa colonies showed significantly increased growth rates at intermediate pCO2 (1193 µatm) but no response to higher pCO2. No effect of acidification on A. hirsutum colonies growth rates was observed. The results suggest a remarkable resistance of the algal macro-epibionts to levels of acidification occurring at present day upwellings in the Baltic. Only extreme future upwelling conditions impacted the tubeworm S. spirorbis, but not the bryozoans