Eutrophication and Deoxygenation Drive High Methane Emissions from a Brackish Coastal System.

Coastal environments are a major source of marine methane in the atmosphere. Eutrophication and deoxygenation have the potential to amplify the coastal methane emissions. Here, we investigate methane dynamics in the eutrophic Stockholm Archipelago. We cover a range of sites with contrasting water column redox conditions and rates of organic matter degradation, with the latter reflected by the depth of the sulfate-methane transition zone (SMTZ) in the sediment. We find the highest benthic release of methane (2.2-8.6 mmol m-2 d-1) at sites where the SMTZ is located close to the sediment-water interface (2-10 cm). A large proportion of methane is removed in the water column via aerobic or anaerobic microbial pathways. At many locations, water column methane is highly depleted in 13C, pointing toward substantial bubble dissolution. Calculated and measured rates of methane release to the atmosphere range from 0.03 to 0.4 mmol m-2 d-1 and from 0.1 to 1.7 mmol m-2 d-1, respectively, with the highest fluxes at locations with a shallow SMTZ and anoxic and sulfidic bottom waters. Taken together, our results show that sites suffering most from both eutrophication and deoxygenation are hotspots of coastal marine methane emissions.

Ebullition dominates methane emissions in stratified coastal waters.

Coastal areas are an important source of methane (CH4). However, the exact origins of CH4 in the surface waters of coastal regions, which in turn drive sea-air emissions, remain uncertain. To gain a comprehensive understanding of the current and future climate change feedbacks, it is crucial to identify these CH4 sources and processes that regulate its formation and oxidation. This study investigated coastal CH4 dynamics by comparing water column data from six stations located in the brackish Tvärminne Archipelago, Baltic Sea. The sediment biogeochemistry and microbiology were further investigated at two stations (i.e., nearshore and offshore). These stations differed in terms of stratification, bottom water redox conditions, and organic matter loading. At the nearshore station, CH4 diffusion from the sediment into the water column was negligible, because nearly all CH4 was oxidized within the upper sediment column before reaching the sediment surface. On the other hand, at the offshore station, there was significant benthic diffusion of CH4, albeit the majority underwent oxidation before reaching the sediment-water interface, due to shoaling of the sulfate methane transition zone (SMTZ). The potential contribution of CH4 production in the water column was evaluated and was found to be negligible. After examining the isotopic signatures of δ13C-CH4 across the sediment and water column, it became apparent that the surface water δ13C-CH4 values observed in areas with thermal stratification could not be explained by diffusion, advective fluxes, nor production in the water column. In fact, these values bore a remarkable resemblance to those detected below the SMTZ. This supports the hypothesis that the source of CH4 in surface waters is more likely to originate from ebullition than diffusion in stratified brackish coastal systems.

Responses of the coral reef cryptobiome to environmental gradients in the Red Sea.

An essential component of the coral reef animal diversity is the species hidden in crevices within the reef matrix, referred to as the cryptobiome. These organisms play an important role in nutrient cycling and provide an abundant food source for higher trophic levels, yet they have been largely overlooked. Here, we analyzed the distribution patterns of the mobile cryptobiome (>2000 µm) along the latitudinal gradient of the Saudi Arabian coast of the Red Sea. Analysis was conducted based on 54 Autonomous Reef Monitoring Structures. We retrieved a total of 5273 organisms, from which 2583 DNA sequences from the mitochondrially encoded cytochrome c oxidase I were generated through sanger sequencing. We found that the cryptobiome community is variable over short geographical distances within the basin. Regression tree models identified sea surface temperature (SST), percentage cover of hard coral and turf algae as determinant for the number of operational taxonomic units present per Autonomous Reef Monitoring Structures (ARMS). Our results also show that the community structure of the cryptobiome is associated with the energy available (measured as photosynthetic active radiation), sea surface temperature, and nearby reef habitat characteristics (namely hard corals, turf and macroalgae). Given that temperature and reef benthic characteristics affect the cryptobiome, current scenarios of intensive climate change are likely to modify this fundamental biological component of coral reef functioning. However, the trajectory of change is unknow and can be site specific, as for example, diversity is expected to increase above SST of 28.5°C, and with decreasing hard coral and turf cover. This study provides a baseline of the cryptobenthic community prior to major coastal developments in the Red Sea to be used for future biodiversity studies and monitoring projects. It can also contribute to better understand patterns of reef biodiversity in a period where Marine Protected Areas are being discussed in the region.

Methane emissions offset atmospheric carbon dioxide uptake in coastal macroalgae, mixed vegetation and sediment ecosystems.

Coastal ecosystems can efficiently remove carbon dioxide (CO2) from the atmosphere and are thus promoted for nature-based climate change mitigation. Natural methane (CH4) emissions from these ecosystems may counterbalance atmospheric CO2 uptake. Still, knowledge of mechanisms sustaining such CH4 emissions and their contribution to net radiative forcing remains scarce for globally prevalent macroalgae, mixed vegetation, and surrounding depositional sediment habitats. Here we show that these habitats emit CH4 in the range of 0.1 - 2.9 mg CH4 m-2 d-1 to the atmosphere, revealing in situ CH4 emissions from macroalgae that were sustained by divergent methanogenic archaea in anoxic microsites. Over an annual cycle, CO2-equivalent CH4 emissions offset 28 and 35% of the carbon sink capacity attributed to atmospheric CO2 uptake in the macroalgae and mixed vegetation habitats, respectively, and augment net CO2 release of unvegetated sediments by 57%. Accounting for CH4 alongside CO2 sea-air fluxes and identifying the mechanisms controlling these emissions is crucial to constrain the potential of coastal ecosystems as net atmospheric carbon sinks and develop informed climate mitigation strategies.

Interaction effects of crude oil and nutrient exposure on settlement of coral reef benthos.

Anthropogenic stressors increasingly cause ecosystem-level changes to sensitive marine habitats such as coral reefs. Intensification of coastal development and shipping traffic can increase nutrient and oil pollution on coral reefs, yet these two stressors have not been studied in conjunction. Here, we simulate a disturbance scenario exposing carbonate settlement tiles to nutrient and oil pollution in a full-factorial design with four treatments: control, nutrients, oil, and combination to examine community structure and net primary productivity (NPP) of pioneer communities throughout 28 weeks. Compared to the control treatment oil pollution decreased overall settlement and NPP, while nutrients increased turf algae and NPP. However, the combination of these two stressors resulted in similar community composition and NPP as the control. These results indicate that pioneer communities may experience shifts due to nutrient enrichment, and/or oil pollution. However, the timing and duration of an event will influence recovery trajectories requiring further study.

Fleshy red algae mats act as temporary reservoirs for sessile invertebrate biodiversity.

Many coastal ecosystems, such as coral reefs and seagrass meadows, currently experience overgrowth by fleshy algae due to the interplay of local and global stressors. This is usually accompanied by strong decreases in habitat complexity and biodiversity. Recently, persistent, mat-forming fleshy red algae, previously described for the Black Sea and several Atlantic locations, have also been observed in the Mediterranean. These several centimetre high mats may displace seagrass meadows and invertebrate communities, potentially causing a substantial loss of associated biodiversity. We show that the sessile invertebrate biodiversity in these red algae mats is high and exceeds that of neighbouring seagrass meadows. Comparative biodiversity indices were similar to or higher than those recently described for calcifying green algae habitats and biodiversity hotspots like coral reefs or mangrove forests. Our findings suggest that fleshy red algae mats can act as alternative habitats and temporary sessile invertebrate biodiversity reservoirs in times of environmental change.

High spatiotemporal variability of methane concentrations challenges estimates of emissions across vegetated coastal ecosystems.

Coastal methane (CH4 ) emissions dominate the global ocean CH4 budget and can offset the "blue carbon" storage capacity of vegetated coastal ecosystems. However, current estimates lack systematic, high-resolution, and long-term data from these intrinsically heterogeneous environments, making coastal budgets sensitive to statistical assumptions and uncertainties. Using continuous CH4 concentrations, δ13 C-CH4  values, and CH4  sea-air fluxes across four seasons in three globally pervasive coastal habitats, we show that the CH4 distribution is spatially patchy over meter-scales and highly variable in time. Areas with mixed vegetation, macroalgae, and their surrounding sediments exhibited a spatiotemporal variability of surface water CH4 concentrations ranging two orders of magnitude (i.e., 6-460 nM CH4 ) with habitat-specific seasonal and diurnal patterns. We observed (1) δ13 C-CH4  signatures that revealed habitat-specific CH4 production and consumption pathways, (2) daily peak concentration events that could change >100% within hours across all habitats, and (3) a high thermal sensitivity of the CH4 distribution signified by apparent activation energies of ~1 eV that drove seasonal changes. Bootstrapping simulations show that scaling the CH4 distribution from few samples involves large errors, and that ~50 concentration samples per day are needed to resolve the scale and drivers of the natural variability and improve the certainty of flux calculations by up to 70%. Finally, we identify northern temperate coastal habitats with mixed vegetation and macroalgae as understudied but seasonally relevant atmospheric CH4  sources (i.e., releasing ≥ 100 µmol CH4  m-2  day-1 in summer). Due to the large spatial and temporal heterogeneity of coastal environments, high-resolution measurements will improve the reliability of CH4 estimates and confine the habitat-specific contribution to regional and global CH4 budgets.

Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling.

Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions.

Nitrogen fixation and denitrification activity differ between coral- and algae-dominated Red Sea reefs.

Coral reefs experience phase shifts from coral- to algae-dominated benthic communities, which could affect the interplay between processes introducing and removing bioavailable nitrogen. However, the magnitude of such processes, i.e., dinitrogen (N2) fixation and denitrification levels, and their responses to phase shifts remain unknown in coral reefs. We assessed both processes for the dominant species of six benthic categories (hard corals, soft corals, turf algae, coral rubble, biogenic rock, and reef sands) accounting for > 98% of the benthic cover of a central Red Sea coral reef. Rates were extrapolated to the relative benthic cover of the studied organisms in co-occurring coral- and algae-dominated areas of the same reef. In general, benthic categories with high N2 fixation exhibited low denitrification activity. Extrapolated to the respective reef area, turf algae and coral rubble accounted for > 90% of overall N2 fixation, whereas corals contributed to more than half of reef denitrification. Total N2 fixation was twice as high in algae- compared to coral-dominated areas, whereas denitrification levels were similar. We conclude that algae-dominated reefs promote new nitrogen input through enhanced N2 fixation and comparatively low denitrification. The subsequent increased nitrogen availability could support net productivity, resulting in a positive feedback loop that increases the competitive advantage of algae over corals in reefs that experienced a phase shift.

Relative abundance of nitrogen cycling microbes in coral holobionts reflects environmental nitrate availability.

Recent research suggests that nitrogen (N) cycling microbes are important for coral holobiont functioning. In particular, coral holobionts may acquire bioavailable N via prokaryotic dinitrogen (N2) fixation or remove excess N via denitrification activity. However, our understanding of environmental drivers on these processes in hospite remains limited. Employing the strong seasonality of the central Red Sea, this study assessed the effects of environmental parameters on the proportional abundances of N cycling microbes associated with the hard corals Acropora hemprichii and Stylophora pistillata. Specifically, we quantified changes in the relative ratio between nirS and nifH gene copy numbers, as a proxy for seasonal shifts in denitrification and N2 fixation potential in corals, respectively. In addition, we assessed coral tissue-associated Symbiodiniaceae cell densities and monitored environmental parameters to provide a holobiont and environmental context, respectively. While ratios of nirS to nifH gene copy numbers varied between seasons, they revealed similar seasonal patterns in both coral species, with ratios closely following patterns in environmental nitrate availability. Symbiodiniaceae cell densities aligned with environmental nitrate availability, suggesting that the seasonal shifts in nirS to nifH gene abundance ratios were probably driven by nitrate availability in the coral holobiont. Thereby, our results suggest that N cycling in coral holobionts probably adjusts to environmental conditions by increasing and/or decreasing denitrification and N2 fixation potential according to environmental nitrate availability. Microbial N cycling may, thus, extenuate the effects of changes in environmental nitrate availability on coral holobionts to support the maintenance of the coral-Symbiodiniaceae symbiosis.

Nutrient pollution enhances productivity and framework dissolution in algae- but not in coral-dominated reef communities.

Ecosystem services provided by coral reefs may be susceptible to the combined effects of benthic species shifts and anthropogenic nutrient pollution, but related field studies are scarce. We thus investigated in situ how dissolved inorganic nutrient enrichment, maintained for two months, affected community-wide biogeochemical functions of intact coral- and degraded algae-dominated reef patches in the central Red Sea. Results from benthic chamber incubations revealed 87% increased gross productivity and a shift from net calcification to dissolution in algae-dominated communities after nutrient enrichment, but the same processes were unaffected by nutrients in neighboring coral communities. Both community types changed from net dissolved organic nitrogen sinks to sources, but the increase in net release was 56% higher in algae-dominated communities. Nutrient pollution may, thus, amplify the effects of community shifts on key ecosystem services of coral reefs, possibly leading to a loss of structurally complex habitats with carbonate dissolution and altered nutrient recycling.

High plasticity of nitrogen fixation and denitrification of common coral reef substrates in response to nitrate availability.

Nitrogen cycling in coral reefs may be affected by nutrient availability, but knowledge about concentration-dependent thresholds that modulate dinitrogen fixation and denitrification is missing. We determined the effects of different nitrate concentrations (ambient, 1, 5, 10 µM nitrate addition) on both processes under two light scenarios (i.e., light and dark) using a combined acetylene assay for two common benthic reef substrates, i.e., turf algae and coral rubble. For both substrates, dinitrogen fixation rates peaked at 5 µM nitrate addition in light, whereas denitrification was highest at 10 µM nitrate addition in the dark. At 10 µm nitrate addition in the dark, a near-complete collapse of dinitrogen fixation concurrent with a 76-fold increase in denitrification observed for coral rubble, suggesting potential threshold responses linked to the nutritional state of the community. We conclude that dynamic nitrogen cycling activity may help stabilise nitrogen availability in microbial communities associated with coral reef substrates.

Heat stress destabilizes symbiotic nutrient cycling in corals.

Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral-algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral-algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral-algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.

Heterotrophic bacterioplankton responses in coral- and algae-dominated Red Sea reefs show they might benefit from future regime shift.

In coral reefs, dissolved organic matter (DOM) cycling is a critical process for sustaining ecosystem functioning. However, global and local stressors have caused persistent shifts from coral- to algae-dominated benthic communities. The influence of such phase shifts on DOM nature and its utilization by heterotrophic bacterioplankton remains poorly studied. Every second month for one year, we retrieved seawater samples enriched in DOM produced by coral- and algae-dominated benthic communities in a central Red Sea reef during a full annual cycle. Seawater incubations were conducted in the laboratory under in situ temperature and light conditions by inoculating enriched DOM samples with bacterial assemblages collected in the surrounding waters. Dissolved organic carbon (DOC) concentrations were higher in the warmer months (May-September) in both communities, resulting in higher specific growth rates and bacterial growth efficiencies (BGE). However, these high summer values were significantly enhanced in algal-DOM relative to coral-DOM, suggesting the potential for bacterioplankton biomass increase in reefs with algae replacing healthy coral cover under warmer conditions. The potential exacerbation of heterotrophic bacterial activity in the ongoing widespread regime shift from coral- to algae-dominated communities may have detrimental consequences for the overall health of tropical coral reefs.

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.

Rethinking the interplay between affluence and vulnerability to aid climate change adaptive capacity.

Affluence and vulnerability are often seen as opposite sides of a coin-with affluence generally understood as reducing forms of vulnerability through increased resilience and adaptive capacity. However, in the context of climate change and an increase in associated hazards and disasters, we suggest the need to re-examine this dynamic relationship-a complex association we define here as the Affluence-Vulnerability Interface (AVI). We review research in different national contexts to show how a more nuanced understanding of the AVI can (a) problematize the notion that increasing material affluence necessarily has a mitigating influence on social vulnerability, (b) extend our analysis of social vulnerability beyond low-income regions to include affluent contexts and (c) improve our understanding of how psychosocial characteristics influence people's vulnerability. Finally, we briefly outline three methodological approaches that we believe will assist future engagement with the AVI.

Nitrogen eutrophication particularly promotes turf algae in coral reefs of the central Red Sea.

While various sources increasingly release nutrients to the Red Sea, knowledge about their effects on benthic coral reef communities is scarce. Here, we provide the first comparative assessment of the response of all major benthic groups (hard and soft corals, turf algae and reef sands-together accounting for 80% of the benthic reef community) to in-situ eutrophication in a central Red Sea coral reef. For 8 weeks, dissolved inorganic nitrogen (DIN) concentrations were experimentally increased 3-fold above environmental background concentrations around natural benthic reef communities using a slow release fertilizer with 15% total nitrogen (N) content. We investigated which major functional groups took up the available N, and how this changed organic carbon (Corg) and N contents using elemental and stable isotope measurements. Findings revealed that hard corals (in their tissue), soft corals and turf algae incorporated fertilizer N as indicated by significant increases in δ15N by 8%, 27% and 28%, respectively. Among the investigated groups, Corg content significantly increased in sediments (+24%) and in turf algae (+33%). Altogether, this suggests that among the benthic organisms only turf algae were limited by N availability and thus benefited most from N addition. Thereby, based on higher Corg content, turf algae potentially gained competitive advantage over, for example, hard corals. Local management should, thus, particularly address DIN eutrophication by coastal development and consider the role of turf algae as potential bioindicator for eutrophication.

Publisher Correction: Denitrification Aligns with N2 Fixation in Red Sea Corals.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Denitrification Aligns with N2 Fixation in Red Sea Corals.

Denitrification may potentially alleviate excess nitrogen (N) availability in coral holobionts to maintain a favourable N to phosphorous ratio in the coral tissue. However, little is known about the abundance and activity of denitrifiers in the coral holobiont. The present study used the nirS marker gene as a proxy for denitrification potential along with measurements of denitrification rates in a comparative coral taxonomic framework from the Red Sea: Acropora hemprichii, Millepora dichotoma, and Pleuractis granulosa. Relative nirS gene copy numbers associated with the tissues of these common corals were assessed and compared with denitrification rates on the holobiont level. In addition, dinitrogen (N2) fixation rates, Symbiodiniaceae cell density, and oxygen evolution were assessed to provide an environmental context for denitrification. We found that relative abundances of the nirS gene were 16- and 17-fold higher in A. hemprichii compared to M. dichotoma and P. granulosa, respectively. In concordance, highest denitrification rates were measured in A. hemprichii, followed by M. dichotoma and P. granulosa. Denitrification rates were positively correlated with N2 fixation rates and Symbiodiniaceae cell densities. Our results suggest that denitrification may counterbalance the N input from N2 fixation in the coral holobiont, and we hypothesize that these processes may be limited by photosynthates released by the Symbiodiniaceae.

Multiple stressor effects on coral reef ecosystems.

Global climate change has profound implications on species distributions and ecosystem functioning. In the coastal zone, ecological responses may be driven by various biogeochemical and physical environmental factors. Synergistic interactions can occur when the combined effects of stressors exceed their individual effects. The Red Sea, characterized by strong gradients in temperature, salinity, and nutrients along the latitudinal axis provides a unique opportunity to study ecological responses over a range of these environmental variables. Using multiple linear regression models integrating in situ, satellite and oceanographic data, we investigated the response of coral reef taxa to local stressors and recent climate variability. Taxa and functional groups responded to a combination of climate (temperature, salinity, air-sea heat fluxes, irradiance, wind speed), fishing pressure and biogeochemical (chlorophyll a and nutrients - phosphate, nitrate, nitrite) factors. The regression model for each species showed interactive effects of climate, fishing pressure and nutrient variables. The nature of the effects (antagonistic or synergistic) was dependent on the species and stressor pair. Variables consistently associated with the highest number of synergistic interactions included heat flux terms, temperature, and wind speed followed by fishing pressure. Hard corals and coralline algae abundance were sensitive to changing environmental conditions where synergistic interactions decreased their percentage cover. These synergistic interactions suggest that the negative effects of fishing pressure and eutrophication may exacerbate the impact of climate change on corals. A high number of interactions were also recorded for algae, however for this group, synergistic interactions increased algal abundance. This study is unique in applying regression analysis to multiple environmental variables simultaneously to understand stressor interactions in the field. The observed responses have important implications for understanding climate change impacts on marine ecosystems and whether managing local stressors, such as nutrient enrichment and fishing activities, may help mitigate global drivers of change.