High rates of carbon and dinitrogen fixation suggest a critical role of benthic pioneer communities in the energy and nutrient dynamics of coral reefs

Following coral mortality in tropical reefs, pioneer communities dominated by filamentous and crustose algae efficiently colonize substrates previously occupied by coral tissue. This phenomenon is particularly common after mass coral mortality following prolonged bleaching events associated with marine heatwaves. 2. Pioneer communities play an important role for the biological succession and reorganization of reefs after disturbance. However, their significance for critical ecosystem functions previously mediated by corals, such as the efficient cycling of carbon (C) and nitrogen (N) within the reef, remains uncertain. 3. We used 96 carbonate tiles to simulate the occurrence of bare substrates after disturbance in a coral reef of the central Red Sea. We measured rates of C and dinitrogen (N2) fixation of pioneer communities on these tiles monthly over an entire year. Coupled with elemental and stable isotope analyses, these measurements provide insights into macronutrient acquisition, export and the influence of seasonality. 4. Pioneer communities exhibited high rates of C and N2 fixation within 4–8 weeks after the introduction of experimental bare substrates. Ranging from 13 to 25 μmol C cm−2 day−1 and 8 to 54 nmol N cm−2 day−1, respectively, C and N2 fixation rates were comparable to reported values for established Red Sea coral reefs. This similarity indicates that pioneer communities may quickly compensate for the loss of benthic productivity by corals. Notably, between 40% and 85% of fixed organic C was exported into the environment, constituting a vital source of energy for the coral reef food web. 5. Our findings suggest that benthic pioneer communities may play a crucial, yet overlooked role in the C and N dynamics of oligotrophic coral reefs by contributing to the input of new C and N after coral mortality. While not substituting other critical ecosystem functions provided by corals (e.g. structural habitat complexity and coastal protection), pioneer communities likely contribute to maintaining coral reef nutrient cycling through the accumulation of biomass and import of macronutrients following coral loss.

Following coral mortality in tropical reefs, pioneer communities dominated by filamentous and crustose algae efficiently colonize substrates previously occupied by coral tissue. This phenomenon is particularly common after mass coral mortality following prolonged bleaching events associated with marine heatwaves. 2. Pioneer communities play an important role for the biological succession and reorganization of reefs after disturbance. However, their significance for critical ecosystem functions previously mediated by corals, such as the efficient cycling of carbon (C) and nitrogen (N) within the reef, remains uncertain. 3. We used 96 carbonate tiles to simulate the occurrence of bare substrates after disturbance in a coral reef of the central Red Sea. We measured rates of C and dinitrogen (N2) fixation of pioneer communities on these tiles monthly over an entire year. Coupled with elemental and stable isotope analyses, these measurements provide insights into macronutrient acquisition, export and the influence of seasonality. 4. Pioneer communities exhibited high rates of C and N2 fixation within 4–8 weeks after the introduction of experimental bare substrates. Ranging from 13 to 25 μmol C cm−2 day−1 and 8 to 54 nmol N cm−2 day−1, respectively, C and N2 fixation rates were comparable to reported values for established Red Sea coral reefs. This similarity indicates that pioneer communities may quickly compensate for the loss of benthic productivity by corals. Notably, between 40% and 85% of fixed organic C was exported into the environment, constituting a vital source of energy for the coral reef food web. 5. Our findings suggest that benthic pioneer communities may play a crucial, yet overlooked role in the C and N dynamics of oligotrophic coral reefs by contributing to the input of new C and N after coral mortality. While not substituting other critical ecosystem functions provided by corals (e.g. structural habitat complexity and coastal protection), pioneer communities likely contribute to maintaining coral reef nutrient cycling through the accumulation of biomass and import of macronutrients following coral loss.

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 bi‐monthly 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), while carbon losses via respiration and dissolved organic carbon release were 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 phase shifts. Algae‐dominated communities may outcompete coral‐dominated communities due to 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.

2020

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

Anders Meibom, Nils Rädecker

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.

2021

Autotrophic and heterotrophic nutrient fluxes in the dinoflagellate-coral symbiosis – A NanoSIMS perspective

Julia Marie Jeanne Yvonne Bodin, Isabelle Domart-Coulon, Maoz Fine, Thomas Krüger, Anders Meibom

The exchange of metabolites between photosynthetic symbionts and their coral host in shallow-water scleractinians provides the nutritional basis for their successful evolution and the existence of massive coral reefs in oligotrophic tropical waters. Autotrophic nutrition, based on carbon- and nitrogen-rich photosynthetic metabolites, is complemented by heterotrophic uptake and assimilation of organic matter to obtain additional carbon, nitrogen and phosphorus. By combining TEM ultrastructural observations with quantitative NanoSIMS isotopic imaging of tissue sections at sub-cellular resolution, we have compared the exchange of nutrients from the autotrophic assimilation of 15N-nitrate and 13C-bicarbonate with the heterotrophic uptake from 15N- and 13C-labelled brine shrimps in Stylophora pistillata from the Red Sea. Our results confirm that heterotrophy serves as the dominant source of nitrogen for the coral holobiont. On a time scale of 6 hours, heterotrophy provided approximately nine times more nitrogen to the host gastrodermal anabolism than symbiont nitrate fixation and translocation. Heterotrophic nitrogen was also used in anabolic processes in the symbionts, but at a level about 40% lower compared with nitrogen incorporation from nitrate fixation. The role of photosynthesizing symbionts the major contributors of carbon to the coral host was evident from the observation that autotrophic carbon enrichment in the gastrodermal layer was seven times higher in comparison to the heterotrophic carbon acquisition. Our observations directly demonstrate the complementing roles of heterotrophic and autotrophic food acquisition and support the notion that recycling of nutrients in symbiotic coral holobionts is critical to their vitality. The effects of stress from environmental change, including increasing water temperature and ocean acidification, are under investigation.

2015

Autotrophic and heterotrophic nutrient fluxes in the dinoflagellate-coral symbiosis – A NanoSIMS perspective

Julia Marie Jeanne Yvonne Bodin, Isabelle Domart-Coulon, Maoz Fine, Thomas Krüger, Anders Meibom

2015

High summer temperatures amplify functional differences between coral‐ and algae‐dominated reef communities

Nils Rädecker

2020