Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions.

Functional traits define species by their ecological role in the ecosystem. Animals themselves are host-microbe ecosystems (holobionts), and the application of ecophysiological approaches can help to understand their functioning. In hard coral holobionts, communities of dinitrogen (N2)-fixing prokaryotes (diazotrophs) may contribute a functional trait by providing bioavailable nitrogen (N) that could sustain coral productivity under oligotrophic conditions. This study quantified N2 fixation by diazotrophs associated with four genera of hermatypic corals on a northern Red Sea fringing reef exposed to high seasonality. We found N2 fixation activity to be 5- to 10-fold higher in summer, when inorganic nutrient concentrations were lowest and water temperature and light availability highest. Concurrently, coral gross primary productivity remained stable despite lower Symbiodinium densities and tissue chlorophyll a contents. In contrast, chlorophyll a content per Symbiodinium cell increased from spring to summer, suggesting that algal cells overcame limitation of N, an essential element for chlorophyll synthesis. In fact, N2 fixation was positively correlated with coral productivity in summer, when its contribution was estimated to meet 11% of the Symbiodinium N requirements. These results provide evidence of an important functional role of diazotrophs in sustaining coral productivity when alternative external N sources are scarce.

Monitoring of coastal coral reefs near Dahab (Gulf of Aqaba, Red Sea) indicates local eutrophication as potential cause for change in benthic communities.

Coral reef ecosystems fringing the coastline of Dahab (South Sinai, Egypt) have experienced increasing anthropogenic disturbance as an emergent international tourism destination. Previous reports covering tourism-related impacts on coastal environments, particularly mechanical damage and destructive fishing, have highlighted the vital necessity for regular ecosystem monitoring of coral reefs near Dahab. However, a continuous scientific monitoring programme of permanent survey sites has not been established to date. Thus, this study conducted in situ monitoring surveys to investigate spatio-temporal variability of benthic reef communities and selected reef-associated herbivores along with reef health indicator organisms by revisiting three of the locally most frequented dive sites during expeditions in March 2010, September 2011 and February 2013. In addition, inorganic nutrient concentrations in reef-surrounding waters were determined to evaluate bottom-up effects of key environmental parameters on benthic reef community shifts in relation to grazer-induced top-down control. Findings revealed that from 2010 to 2013, live hard coral cover declined significantly by 12 % at the current-sheltered site Three Pools (TP), while showing negative trends for the Blue Hole (BH) and Lighthouse (LH) sites. Hard coral cover decline was significantly and highly correlated to a substantial increase in turf algae cover (up to 57 % at TP) at all sites, replacing hard corals as dominant benthic space occupiers in 2013. These changes were correlated to ambient phosphate and ammonium concentrations that exhibited highest values (0.64 ± 0.07 µmol PO4 (3-) l(-1), 1.05 ± 0.07 µmol NH4 (+) l(-1)) at the degraded site TP. While macroalgae appeared to respond to both bottom-up and top-down factors, change in turf algae was consistent with expected indications for bottom-up control. Temporal variability measured in herbivorous reef fish stocks reflected seasonal impacts by local fisheries, with concomitant changes in macroalgal cover. These findings represent the first record of rapid, localised change in benthic reef communities near Dahab, consistent with indications for bottom-up controlled early-stage phase shifts, underlining the necessity for efficient regional wastewater management for coastal facilities.

Inorganic nutrient availability affects organic matter fluxes and metabolic activity in the soft coral genus Xenia.

The release of organic matter (OM) by scleractinian corals represents a key physiological process that importantly contributes to coral reef ecosystem functioning, and is affected by inorganic nutrient availability. Although OM fluxes have been studied for several dominant reef taxa, no information is available for soft corals, one of the major benthic groups in tropical reef environments. Thus, this study investigates OM fluxes along with other key physiological parameters (i.e. photosynthesis, respiration and chlorophyll a tissue content) in the common soft coral genus Xenia after a 4-week exposure period to elevated ammonium (N; 20.0 µmol l(-1)), phosphate (P; 2.0 µmol l(-1)) and combined inorganic nutrient enrichment treatment (N+P). Corals maintained without nutrient enrichment served as non-treated controls and revealed constant uptake rates for particulate organic carbon (POC) (-0.315±0.161 mg POC m(-2) coral surface area h(-1)), particulate nitrogen (PN) (-0.053±0.018 mg PN m(-2) h(-1)) and dissolved organic carbon (DOC) (-4.8±2.1 mg DOC m(-2) h(-1)). Although DOC uptake significantly increased in the N treatment, POC flux was not affected. The P treatment significantly enhanced PN release as well as photosynthesis and respiration rates, suggesting that autotrophic carbon acquisition of zooxanthellae endosymbionts influences OM fluxes by the coral host. Our physiological findings confirm the significant effect of inorganic nutrient availability on OM fluxes and key metabolic processes for the soft coral Xenia, and provide the first clues on OM cycles initiated by soft corals in reef environments exposed to ambient and elevated inorganic nutrient concentrations.

First evidence for zooplankton feeding sustaining key physiological processes in a scleractinian cold-water coral.

Scleractinian cold-water corals (CWC) represent key taxa controlling deep-sea reef ecosystem functioning by providing structurally complex habitats to a high associated biodiversity, and by fuelling biogeochemical cycles via the release of organic matter. Nevertheless, our current knowledge on basic CWC properties, such as feeding ecology and key physiological processes (i.e. respiration, calcification and organic matter release), is still very limited. Here, we show evidence for the trophic significance of zooplankton, essentially sustaining levels of the investigated key physiological processes in the cosmopolitan CWC Desmophyllum dianthus (Esper 1794). Our results from laboratory studies reveal that withdrawal (for up to 3 weeks) of zooplankton food (i.e. Artemia salina) caused a significant decline in respiration (51%) and calcification (69%) rates compared with zooplankton-fed specimens. Likewise, organic matter release, in terms of total organic carbon (TOC), decreased significantly and eventually indicated TOC net uptake after prolonged zooplankton exclusion. In fed corals, zooplankton provided 1.6 times the daily metabolic C demand, while TOC release represented 7% of zooplankton-derived organic C. These findings highlight zooplankton as a nutritional source for D. dianthus, importantly sustaining respiratory metabolism, growth and organic matter release, with further implications for the role of CWC as deep-sea reef ecosystem engineers.

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.

Contrasting seasonal responses in dinitrogen fixation between shallow and deep-water colonies of the model coral Stylophora pistillata in the northern Red Sea.

Tropical corals are often associated with dinitrogen (N2)-fixing bacteria (diazotrophs), and seasonal changes in key environmental parameters, such as dissolved inorganic nitrogen (DIN) availability and seawater temperature, are known to affect N2 fixation in coral-microbial holobionts. Despite, then, such potential for seasonal and depth-related changes in N2 fixation in reef corals, such variation has not yet been investigated. Therefore, this study quantified seasonal (winter vs. summer) N2 fixation rates associated with the reef-building coral Stylophora pistillata collected from depths of 5, 10 and 20 m in the northern Gulf of Aqaba (Red Sea). Findings revealed that corals from all depths exhibited the highest N2 fixation rates during the oligotrophic summer season, when up to 11% of their photo-metabolic nitrogen demand (CPND) could be met by N2 fixation. While N2 fixation remained seasonally stable for deep corals (20 m), it significantly decreased for the shallow corals (5 and 10 m) during the DIN-enriched winter season, accounting for less than 2% of the corals' CPND. This contrasting seasonal response in N2 fixation across corals of different depths could be driven by 1) release rates of coral-derived organic matter, 2) the community composition of the associated diazotrophs, and/or 3) nutrient acquisition by the Symbiodinium community.

Coral mucus fuels the sponge loop in warm- and cold-water coral reef ecosystems.

Shallow warm-water and deep-sea cold-water corals engineer the coral reef framework and fertilize reef communities by releasing coral mucus, a source of reef dissolved organic matter (DOM). By transforming DOM into particulate detritus, sponges play a key role in transferring the energy and nutrients in DOM to higher trophic levels on Caribbean reefs via the so-called sponge loop. Coral mucus may be a major DOM source for the sponge loop, but mucus uptake by sponges has not been demonstrated. Here we used laboratory stable isotope tracer experiments to show the transfer of coral mucus into the bulk tissue and phospholipid fatty acids of the warm-water sponge Mycale fistulifera and cold-water sponge Hymedesmia coriacea, demonstrating a direct trophic link between corals and reef sponges. Furthermore, 21-40% of the mucus carbon and 32-39% of the nitrogen assimilated by the sponges was subsequently released as detritus, confirming a sponge loop on Red Sea warm-water and north Atlantic cold-water coral reefs. The presence of a sponge loop in two vastly different reef environments suggests it is a ubiquitous feature of reef ecosystems contributing to the high biogeochemical cycling that may enable coral reefs to thrive in nutrient-limited (warm-water) and energy-limited (cold-water) environments.

The "Flexi-Chamber": A Novel Cost-Effective In Situ Respirometry Chamber for Coral Physiological Measurements.

Coral reefs are threatened worldwide, with environmental stressors increasingly affecting the ability of reef-building corals to sustain growth from calcification (G), photosynthesis (P) and respiration (R). These processes support the foundation of coral reefs by directly influencing biogeochemical nutrient cycles and complex ecological interactions and therefore represent key knowledge required for effective reef management. However, metabolic rates are not trivial to quantify and typically rely on the use of cumbersome in situ respirometry chambers and/or the need to remove material and examine ex situ, thereby fundamentally limiting the scale, resolution and possibly the accuracy of the rate data. Here we describe a novel low-cost in situ respirometry bag that mitigates many constraints of traditional glass and plexi-glass incubation chambers. We subsequently demonstrate the effectiveness of our novel "Flexi-Chamber" approach via two case studies: 1) the Flexi-Chamber provides values of P, R and G for the reef-building coral Siderastrea cf. stellata collected from reefs close to Salvador, Brazil, which were statistically similar to values collected from a traditional glass respirometry vessel; and 2) wide-scale application of obtaining P, R and G rates for different species across different habitats to obtain inter- and intra-species differences. Our novel cost-effective design allows us to increase sampling scale of metabolic rate measurements in situ without the need for destructive sampling and thus significantly expands on existing research potential, not only for corals as we have demonstrated here, but also other important benthic groups.

Benthic primary production budget of a Caribbean reef lagoon (Puerto Morelos, Mexico).

High photosynthetic benthic primary production (P) represents a key ecosystem service provided by tropical coral reef systems. However, benthic P budgets of specific ecosystem compartments such as macrophyte-dominated reef lagoons are still scarce. To address this, we quantified individual and lagoon-wide net (Pn) and gross (Pg) primary production by all dominant functional groups of benthic primary producers in a typical macrophyte-dominated Caribbean reef lagoon near Puerto Morelos (Mexico) via measurement of O2 fluxes in incubation experiments. The photosynthetically active 3D lagoon surface area was quantified using conversion factors to allow extrapolation to lagoon-wide P budgets. Findings revealed that lagoon 2D benthic cover was primarily composed of sand-associated microphytobenthos (40%), seagrasses (29%) and macroalgae (27%), while seagrasses dominated the lagoon 3D surface area (84%). Individual Pg was highest for macroalgae and scleractinian corals (87 and 86 mmol O2 m(-2) specimen area d(-1), respectively), however seagrasses contributed highest (59%) to the lagoon-wide Pg. Macroalgae exhibited highest individual Pn rates, but seagrasses generated the largest fraction (51%) of lagoon-wide Pn. Individual R was highest for scleractinian corals and macroalgae, whereas seagrasses again provided the major lagoon-wide share (68%). These findings characterise the investigated lagoon as a net autotrophic coral reef ecosystem compartment revealing similar P compared to other macrophyte-dominated coastal environments such as seagrass meadows and macroalgae beds. Further, high lagoon-wide P (Pg: 488 and Pn: 181 mmol O2 m(-2) lagoon area d(-1)) and overall Pg:R (1.6) indicate substantial benthic excess production within the Puerto Morelos reef lagoon and suggest the export of newly synthesised organic matter to surrounding ecosystems.