Short-term ocean acidification decreases pulsation and growth of the widespread soft coral Xenia umbellata.

Coral reefs may experience lower pH values as a result of ocean acidification (OA), which has negative consequences, particularly for calcifying organisms. Thus far, the effects of this global factor have been mainly investigated on hard corals, while the effects on soft corals remain relatively understudied. We therefore carried out a manipulative aquarium experiment for 21 days to study the response of the widespread pulsating soft coral Xenia umbellata to simulated OA conditions. We gradually decreased the pH from ambient (~8.3) to three consecutive 7-day long pH treatments of 8.0, 7.8, and 7.6, using a CO2 dosing system. Monitored response variables included pulsation rate, specific growth rate, visual coloration, survival, Symbiodiniaceae cell densities and chlorophyll a content, photosynthesis and respiration, and finally stable isotopes of carbon (C) and nitrogen (N) as well as CN content. Pulsation decreased compared to controls with each consecutive lowering of the pH, i.e., 17% at pH 8.0, 26% at pH 7.8 and 32% at pH 7.6, accompanied by an initial decrease in growth rates of ~60% at pH 8.0, not decreasing further at lower pH. An 8.3 ‰ decrease of δ13C confirmed that OA exposed colonies had a higher uptake and availability of atmospheric CO2. Coral productivity, i.e., photosynthesis, was not affected by higher dissolved inorganic C availability and none of the remaining response variables showed any significant differences. Our findings suggest that pulsation is a phenotypically plastic mechanism for X. umbellata to adjust to different pH values, resulting in reduced growth rates only, while maintaining high productivity. Consequently, pulsation may allow X. umbellata to inhabit a broad pH range with minimal effects on its overall health. This resilience may contribute to the competitive advantage that soft corals, particularly X. umbellata, have over hard corals.

The widely distributed soft coral Xenia umbellata exhibits high resistance against phosphate enrichment and temperature increase.

Both global and local factors affect coral reefs worldwide, sometimes simultaneously. An interplay of these factors can lead to phase shifts from hard coral dominance to algae or other invertebrates, particularly soft corals. However, most studies have targeted the effects of single factors, leaving pronounced knowledge gaps regarding the effects of combined factors on soft corals. Here, we investigated the single and combined effects of phosphate enrichment (1, 2, and 8 µM) and seawater temperature increase (26 to 32 °C) on the soft coral Xenia umbellata by quantifying oxygen fluxes, protein content, and stable isotope signatures in a 5-week laboratory experiment. Findings revealed no significant effects of temperature increase, phosphate enrichment, and the combination of both factors on oxygen fluxes. However, regardless of the phosphate treatment, total protein content and carbon stable isotope ratios decreased significantly by 62% and 7% under temperature increase, respectively, suggesting an increased assimilation of their energy reserves. Therefore, we hypothesize that heterotrophic feeding may be important for X. umbellata to sustain their energy reserves under temperature increase, highlighting the advantages of a mixotrophic strategy. Overall, X. umbellata shows a high tolerance towards changes in global and local factors, which may explain their competitive advantage observed at many Indo-Pacific reef locations.

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 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.

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.

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.

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.

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.

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.