Mucus carbohydrate composition correlates with scleractinian coral phylogeny.

The mucus surface layer serves vital functions for scleractinian corals and consists mainly of carbohydrates. Its carbohydrate composition has been suggested to be influenced by environmental conditions (e.g., temperature, nutrients) and microbial pressures (e.g., microbial degradation, microbial coral symbionts), yet to what extend the coral mucus composition is determined by phylogeny remains to be tested. To investigate the variation of mucus carbohydrate compositions among coral species, we analyzed the composition of mucosal carbohydrate building blocks (i.e., monosaccharides) for five species of scleractinian corals, supplemented with previously reported data, to discern overall patterns using cluster analysis. Monosaccharide composition from a total of 23 species (belonging to 14 genera and 11 families) revealed significant differences between two phylogenetic clades that diverged early in the evolutionary history of scleractinian corals (i.e., complex and robust; p = 0.001, R2 = 0.20), mainly driven by the absence of arabinose in the robust clade. Despite considerable differences in environmental conditions and sample analysis protocols applied, coral phylogeny significantly correlated with monosaccharide composition (Mantel test: p < 0.001, R2 = 0.70). These results suggest that coral mucus carbohydrates display phylogenetic dependence and support their essential role in the functioning of corals.

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.

Individual and combined effect of organic eutrophication (DOC) and ocean warming on the ecophysiology of the Octocoral Pinnigorgia flava.

Dissolved organic carbon (DOC) enrichment and ocean warming both negatively affect hard corals, but studies on their combined effects on other reef organisms are scarce. Octocorals are likely to become key players in future reef communities, but they are still highly under-investigated with regard to their responses to global and local environmental changes. Thus, we evaluated the individual and combined effects of DOC enrichment (10, 20 and 40 mg L-1 DOC, added as glucose) and warming (stepwise from 26 to 32 °C) on the widespread Indo-Pacific gorgonian Pinnigorgia flava in a 45-day laboratory experiment. Oxygen fluxes (net photosynthesis and respiration), as well as Symbiodiniaceae cell density and coral growth were assessed. Our results highlight a differential ecophysiological response to DOC enrichment and warming as well as their combination. Individual DOC addition did not significantly affect oxygen fluxes nor Symbiodiniaceae cell density and growth, while warming significantly decreased photosynthesis rates and Symbiodiniaceae cell density. When DOC enrichment and warming were combined, no effect on P. flava oxygen fluxes was observed while growth responded to certain DOC conditions depending on the temperature. Our findings indicate that P. flava is insensitive to the individual effect of DOC enrichment, but not to warming and the two stressors combined. This suggests that, if temperature remains below certain thresholds, this gorgonian species may gain a competitive advantage over coral species that are reportedly more affected by DOC eutrophication. However, under the expected increasing temperature scenarios, it is also likely that this octocoral species will be negatively affected, with potential consequences on community structure. This study contributes to our understanding of the conditions that drive phase shift dynamics in coastal coral reef ecosystemds.

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.

The pulsating soft coral Xenia umbellata shows high resistance to warming when nitrate concentrations are low.

The resistance of hard corals to warming can be negatively affected by nitrate eutrophication, but related knowledge for soft corals is scarce. We thus investigated the ecophysiological response of the pulsating soft coral Xenia umbellata to different levels of nitrate eutrophication (control = 0.6, medium = 6, high = 37 µM nitrate) in a laboratory experiment, with additional warming (27.7 to 32.8 °C) from days 17 to 37. High nitrate eutrophication enhanced cellular chlorophyll a content of Symbiodiniaceae by 168%, while it reduced gross photosynthesis by 56%. After additional warming, polyp pulsation rate was reduced by 100% in both nitrate eutrophication treatments, and additional polyp loss of 7% d-1 and total fragment mortality of 26% was observed in the high nitrate eutrophication treatment. Warming alone did not affect any of the investigated response parameters. These results suggest that X. umbellata exhibits resistance to warming, which may facilitate ecological dominance over some hard corals as ocean temperatures warm, though a clear negative physiological response occurs when combined with nitrate eutrophication. This study thus confirms the importance of investigating combinations of global and local factors to understand and manage changing coral reefs.

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.

Effective asexual reproduction of a widespread soft coral: comparative assessment of four different fragmentation methods.

BACKGROUND: Many coral reefs worldwide are experiencing declines in hard corals, resulting in other benthic organisms, e.g., soft corals, becoming more dominant. As such, more studies on the ecophysiology of soft corals are needed. Despite many methods for asexual reproduction of hard corals, effective methods for soft corals, i.e., without a hard skeleton, are scarce. This study, thus, assessed four fragmentation methods, the glue, rubber band, tunnel mesh, and plug mesh method for the pulsating soft coral Xenia umbellata that is widely distributed in the tropical Indo-Pacific. METHODS: Methods were comparatively assessed by determining the required time and labor for the fragmentation plus the health status of the fragmented corals by measuring their oxygen fluxes and pulsation rates, i.e., a special feature of this soft coral that can be used as a proxy for its health. RESULTS: There were no significant health status differences between methods. This was indicated by similar gross photosynthesis (between 7.4 to 9.7 µg O2 polyp-1 h-1) and pulsating rates (between 35 and 44 pulses min-1) among methods. In terms of time/labor intensity and success rates, i.e., the percentage of fragments attached to the desired surface, the plug mesh method was the most efficient method with a significantly higher success rate (95 ± 5%), while the others had a success rate between 5 ± 5 and 45 ± 15%. The time needed for fragmentation, though not significant, was also the shortest (78 ± 11 s fragment-1), while other methods required between 84 ± 14 and 126 ± 8 s frag-1. The plug mesh method may thus be a valuable tool related to the reproduction of soft corals for use in subsequent experimental work.

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.

A meta-analysis to assess long-term spatiotemporal changes of benthic coral and macroalgae cover in the Mexican Caribbean.

Coral reefs in the wider Caribbean declined in hard coral cover by ~80% since the 1970s, but spatiotemporal analyses for sub-regions are lacking. Here, we explored benthic change patterns in the Mexican Caribbean reefs through meta-analysis between 1978 and 2016 including 125 coral reef sites. Findings revealed that hard coral cover decreased from ~26% in the 1970s to 16% in 2016, whereas macroalgae cover increased to ~30% in 2016. Both groups showed high spatiotemporal variability. Hard coral cover declined in total by 12% from 1978 to 2004 but increased again by 5% between 2005 and 2016 indicating some coral recovery after the 2005 mass bleaching event and hurricane impacts. In 2016, more than 80% of studied reefs were dominated by macroalgae, while only 15% were dominated by hard corals. This stands in contrast to 1978 when all reef sites surveyed were dominated by hard corals. This study is among the first within the Caribbean region that reports local recovery in coral cover in the Caribbean, while other Caribbean reefs have failed to recover. Most Mexican Caribbean coral reefs are now no longer dominated by hard corals. In order to prevent further reef degradation, viable and reliable conservation alternatives are required.

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.

Effects of Water Column Mixing and Stratification on Planktonic Primary Production and Dinitrogen Fixation on a Northern Red Sea Coral Reef.

The northern Red Sea experiences strong annual differences in environmental conditions due to its relative high-latitude location for coral reefs. This allows the study of regulatory effects by key environmental parameters (i.e., temperature, inorganic nutrient, and organic matter concentrations) on reef primary production and dinitrogen (N2) fixation, but related knowledge is scarce. Therefore, this study measured environmental parameters, primary production and N2 fixation of phytoplankton groups in the water overlying a coral reef in the Gulf of Aqaba. To this end, we used a comparative approach between mixed and stratified water column scenarios in a full year of seasonal observations. Findings revealed that inorganic nutrient concentrations were significantly higher in the mixed compared to the stratified period. While gross photosynthesis and N2 fixation rates remained similar, net photosynthesis decreased from mixed to stratified period. Net heterotrophic activity of the planktonic community increased significantly during the stratified compared to the mixed period. While inorganic nitrogen (N) availability was correlated with net photosynthesis over the year, N2 fixation only correlated with N availability during the mixed period. This emphasizes the complexity of planktonic trophodynamics in northern Red Sea coral reefs. Comparing mixed and stratified planktonic N2 fixation rates with those of benthic organisms and substrates revealed a close seasonal activity similarity between free-living pelagic and benthic diazotrophs. During the mixed period, N2 fixation potentially contributed up to 3% of planktonic primary production N demand. This contribution increased by ca. one order of magnitude to 21% during the stratified period. Planktonic N2 fixation is likely a significant N source for phytoplankton to maintain high photosynthesis under oligotrophic conditions in coral reefs, especially during stratified conditions.

Light induced intraspecific variability in response to thermal stress in the hard coral Stylophora pistillata.

Recent research suggests that prior exposure of several months to elevated irradiance induces enhanced thermal tolerance in scleractinian corals. While this tolerance has been reported at the species level, individual coral colonies may react differently due to individual variability in thermal tolerance. As thermal anomalies are predicted to become common in the upcoming future, intraspecific variation may be key to the survival of coral populations. In order to study light-history based thermal stress responses on individual colonies, we developed a preliminary microcosm experiment where three randomly chosen, aquacultured colonies of the model coral Stylophora pistillata were exposed to two irradiance treatments (200 and 400 µmol photons m-2 s-1) for 31 days, followed by artificially induced heat stress (∼33.4 °C). We found different responses to occur at both the intraspecific and the intracolonial levels, as indicated by either equal, less severe, delayed, and/or even non-necrotic responses of corals previously exposed to the irradiance of 400 compared to 200 µmol photons m-2 s-1. In addition, all individual colonies revealed light-enhanced calcification. Finally, elevated irradiance resulted in a lower chlorophyll a concentration in one colony compared to the control treatment, and the same colony displayed more rapid bleaching compared to the other ones. Taken together, this study highlights the potential importance of intra-individual variability in physiological responses of scleractinian corals and provides recommendations for improving methodological designs for future studies.