Reef accumulation is decoupled from recent degradation in the central and southern Red Sea.

Reefs are biogenic structures that result in three-dimensional accumulations of calcium carbonate. Over geological timescales, a positive balance between the production and accumulation of calcium carbonate versus erosional and off-reef transport processes maintains positive net accretion on reefs. Yet, how ecological processes occurring over decadal timescales translate to the accumulation of geological structures is poorly understood, in part due to a lack of studies with detailed time-constrained chronologies of reef accretion over decades to centuries. Here, we combined ecological surveys of living reefs with palaeoecological reconstructions and high-precision radiometric (U-Th) age-dating of fossil reefs represented in both reef sediment cores and surficial dead in situ corals, to reconstruct the history of community composition and carbonate accumulation across the central and southern Saudi Arabian Red Sea throughout the late Holocene. We found that reefs were primarily comprised of thermally tolerant massive Porites colonies, creating a consolidated coral framework, with unconsolidated branching coral rubble accumulating among massive corals on shallow (5-8 m depth) exposed (windward), and gently sloping reef slopes. These unconsolidated reef rubble fields were formed primarily from ex situ Acropora and Pocillopora coral fragments, infilled post deposition within a sedimentary matrix. Bayesian age-depth models revealed a process of punctuated deposition of post-mortem coral fragments transported from adjacent reef environments. That a large portion of Saudi Arabian Red Sea reef slopes is driven by allochthonous deposition (transportation) has important implications for modeling carbonate budgets and reef growth. In addition, a multi-decadal lag exists between the time of death for branching in situ coral and incorporation into the unconsolidated reef rubble. This indicates that recent climate related degradation in the 21st century has not had an immediately negative effect on reef building processes affecting a large portion of the reef area in the Saudi Arabian Red Sea.

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.

A portfolio of climate-tailored approaches to advance the design of marine protected areas in the Red Sea.

Intensified coastal development is compromising the health and functioning of marine ecosystems. A key example of this is the Red Sea, a biodiversity hotspot subjected to increasing local human pressures. While some marine-protected areas (MPAs) were placed to alleviate these stressors, it is unclear whether these MPAs are managed or enforced, thus providing limited protection. Yet, most importantly, MPAs in the Red Sea were not designed using climate considerations, likely diminishing their effectiveness against global stressors. Here, we propose to tailor the design of MPAs in the Red Sea by integrating approaches to enhance climate change mitigation and adaptation. First, including coral bleaching susceptibility could produce a more resilient network of MPAs by safeguarding reefs from different thermal regions that vary in spatiotemporal bleaching responses, reducing the risk that all protected reefs will bleach simultaneously. Second, preserving the basin-wide genetic connectivity patterns that are assisted by mesoscale eddies could further ensure recovery of sensitive populations and maintain species potential to adapt to environmental changes. Finally, protecting mangrove forests in the northern and southern Red Sea that act as major carbon sinks could help offset greenhouse gas emissions. If implemented with multinational cooperation and concerted effort among stakeholders, our portfolio of climate-tailored approaches may help build a network of MPAs in the Red Sea that protects more effectively its coastal resources against escalating coastal development and climate instability. Beyond the Red Sea, we anticipate this study to serve as an example of how to improve the utility of tropical MPAs as climate-informed conservation tools.

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°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.

Anthropogenic-induced acceleration of elemental burial rates in blue carbon repositories of the Arabian Gulf.

Along the past century, the Arabian Gulf has experienced a continuous and fast coastal development leading to increase the human pressures on the marine environment. The present study attempts to describe the historical changes of trace elements in the sediments of vegetated coastal habitats in the western Arabian Gulf. 210Pb-dated sediment cores collected from seagrass, mangrove and saltmarsh habitats were analyzed to evaluate historical variations in concentrations and burial rates of 20 trace elements (Al, As, Ba, Ca, Co, Cr, Cu, Fe, Hg, K, Mg, Mn, Na, Ni, P, Pb, S, Sr, V and Zn). The highest correlations (Spearman correlation coefficients ≥0.51) were found between crustal elements (Al, Fe, Co, Cr, K, Na, Mg, Mn, Ni, V, and P), suggesting a common crustal source in the Gulf. The increased concentrations of these crustal elements in modern marine sediments of the Arabian Gulf seem to be linked to increased mineral dust deposition in the area. Over the last century, both elemental concentrations and burial rates increased by factors of 1-9 and 1-15, respectively, with a remarkably fast increase occurring in the past six decades (~1960 - early 2000). This is most likely due to an increase in anthropogenic pressures along the Gulf coast. Our study demonstrates that sediments in vegetated coastal habitats provide long-term archives of trace elements concentrations and burial rates reflecting human activities in the Arabian Gulf.

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.

Accelerated burial of petroleum hydrocarbons in Arabian Gulf blue carbon repositories.

Massive consumption of petroleum since the past century has led to considerable emissions into marine ecosystems. Marine sediments may accumulate substantial quantities of petroleum and associated contaminants in oil-producing areas. Here, we report accelerated accumulation of total petroleum hydrocarbons (TPH) in 'blue carbon' vegetated ecosystems of the Arabian Gulf - the world's most important region for oil production. In addition to increased accumulation with the onset of oil exploitation, sediment records reflect a large depositional event associated with the 1991 Gulf War, with the magnitude of these maxima varying across habitats, depending on their elevation along the shoreline. Blue carbon ecosystems of the Arabian Gulf currently bury about 2300 megagrams (Mg) of TPHs annually and have accumulated TPH stocks of 59,799 Mg over the past 25 years alone. Massive burial and sequestration of TPH by blue carbon ecosystems is an important, but thus far unrecognized, removal mechanism in the Arabian Gulf. Conserving these ecosystems is important to avoid possible remobilization of sequestered TPH into the surrounding environment.

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.

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 pH(tot) in August were 239±20 µatm and 8.22±0.1, respectively. The mean (± SD) pCO2 and pH(tot) 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.