Recent research indicates that hard corals in a process that is termed phase shift are often replaced by soft corals in reefs. The simultaneous occurrence of local (i.e. organic eutrophication as highly under-investigated parameter) and global (i.e. ocean warming) factors may facilitate these phase shifts as hard corals are negatively affected by both ocean warming and organic eutrophication. Knowledge about soft coral responses to environmental change remains incomplete, although these organisms are becoming important players in reefs. The present study thus investigated the individual and combined effects of organic eutrophication (as glucose addition) and warming on the ecological data of the pulsating soft coral Xenia umbellata. We assessed health status, growth and pulsation rates of soft corals in a 45 day aquarium experiment, with first manipulation of organic eutrophication (no, low, medium and high glucose addition) over 21 days followed by step-wise increases in water temperature from 26 to 32 °C over 24 days. Findings revealed that glucose addition did not affect health status, growth and pulsation rates of the investigated soft corals. Under simulated ocean warming, soft corals that had experienced organic eutrophication before, maintained significantly higher pulsation rates (averaging 22 beats per minute—bpm) and no mortality compared to the controls that showed a decrease of 56% (averaging 15 bpm) in pulsation rates and mortality of 30% at water temperatures of 32 °C compared to 26 °C. This apparently positive effect of organic eutrophication on the ecological data of soft corals under an ocean warming scenario decreased with increasing water temperature. This study thus indicates that (a) organic eutrophication as additional energy source up to a certain threshold may increase the resistance of soft corals to ocean warming and (b) pulsation rates of soft corals may be used as inexpensive, easily detectable, and non-invasive early warning indicator for ocean warming effects on benthic reef communities. When comparing findings of this study for soft corals with previous results for hard corals, it can be assumed that soft corals under the predicted increases of organic eutrophication and warming gain more and more competitive advantages. This may further facilitate phase shifts from hard to soft corals in warming reefs.

Eutrophication with dissolved organic carbon (DOC) as a far under-investigated stressor, and ocean warming, can strongly affect coral reefs and hard corals as major reefs ecosystem engineers. However, no previous studies have investigated the metabolic responses of soft corals to DOC eutrophication, or its interaction with ocean warming. Thus, we investigated respiration and photosynthesis response of Xenia umbellata, a common mixotrophic soft coral from the Indo-pacific, to (1) three levels of DOC eutrophication simulated by glucose addition over the first 21 days of experiment and (2) ocean warming scenarios where the temperature was gradually increased from 26 °C (control condition) to 32 °C over another 24 days in an aquarium experiment. We found no significant difference in response to DOC treatments and all corals survived regardless of the DOC concentrations, whilst subsequent exposure to simulated ocean warming significantly decreased gross photosynthesis by approximately 50% at 30 °C, and 65% at 32 °C, net photosynthesis by 75% at 30 °C and 79% at 32 °C, and respiration by a maximum of 75% at 30 °C; with a slight increase at 32 °C of 25%. The ratio between gross photosynthesis and respiration decreased by the end of the warming period but remained similar between controls and colonies previously exposed to DOC. Our findings suggest that soft corals may be more resistant than hard corals to DOC eutrophication and in consequence, may potentially experiment in less magnitude the negative effects of increased temperature or subsequently both stressors. The results of this study may contribute to explain the successful role of soft corals in phase shifts as reported from many coral reefs. Where predicted declines in reef ecosystems health due to increased eutrophication levels can be exacerbated by future warming.

Mutualistic nutrient cycling in the coral-algae symbiosis depends on limited nitrogen (N) availability for algal symbionts. Denitrifying prokaryotes capable of reducing nitrate or nitrite to dinitrogen could thus support coral holobiont functioning by limiting N availability. Octocorals show some of the highest denitrification rates among reef organisms, however little is known about the community structures of associated denitrifiers and their response to environmental fluctuations. Combining 16S rRNA gene amplicon sequencing with nirS in-silico PCR and quantitative PCR, we found differences in bacterial community dynamics between two octocorals exposed to excess dissolved organic carbon (DOC) and concomitant warming. While bacterial communities of the gorgonian Pinnigorgia flava remained largely unaffected by DOC and warming, the soft coral Xenia umbellata exhibited a pronounced shift towards Alphaproteobacteria dominance under excess DOC. Likewise, the relative abundance of denitrifiers was not altered in P. flava , but decreased by one order of magnitude in X. umbellata under excess DOC likely due to decreased proportions of Ruegeria spp. Given that holobiont C:N ratios remained stable in P. flava but showed a pronounced increase with excess DOC in X. umbellata host, our results suggest that microbial community dynamics may reflect the nutritional status of the holobiont. Hence, denitrifier abundance may be directly linked to N availability. This suggests a passive regulation of N cycling microbes, which could help stabilize nutrient limitation in the coral-algal symbiosis and thereby support holobiont functioning in a changing environment. Importance Octocorals are important members of reef-associated benthic communities that can rapidly replace scleractinian corals as the dominant ecosystem engineers on degraded reefs. Considering the substantial change in the (a)biotic environment that is commonly driving reef degradation, maintaining a dynamic and metabolically diverse microbial community might contribute to octocoral acclimatization and ecological adaptation. Nitrogen (N) cycling microbes, in particular denitrifying prokaryotes, may support holobiont functioning by limiting internal N availability, but little is known about the identity and (a)biotic drivers of octocoral-associated denitrifiers. Here, we show contrasting dynamics of bacterial communities associated with two common octocoral species, the soft coral Xenia umbellata and the gorgonian Pinnigorgia flava after a six-week exposure to excess dissolved organic carbon (DOC) under concomitant warming conditions. The specific responses of denitrifier communities associated with the two octocoral species aligned with the nutritional status of holobiont members. This suggests a passive regulation of this microbial trait based on N availability in the coral holobiont.

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.