Malik S. Naumann

Climate change impedes scleractinian corals as primary reef ecosystem engineers.

Coral reefs are among the most diverse and productive ecosystems on our planet. Scleractinian corals function as the primary reef ecosystem engineers, constructing the framework that serves as a habitat for all other coral reef-associated organisms. However, the corals engineering role is particularly susceptible to global climate change. Ocean warming can cause extensive mass coral bleaching, which triggers dysfunction of major engineering processes. Sub-lethal bleaching results in the reduction of both primary productivity and coral calcification. This may lead to changes in the release of organic and inorganic products, thereby altering critical biogeochemical and recycling processes in reef ecosystems. Thermal stress-induced bleaching and subsequent coral mortality, along with ocean acidification, further lead to long-term shifts in benthic community structure, changes in topographic reef complexity, and the modification of reef functioning. Such shifts may cause negative feedback loops and further modification of coral-derived inorganic and organic products. This review emphasises the critical role of scleractinian corals as reef ecosystem engineers and highlights the control of corals over key reef ecosystem goods and services, including high biodiversity, coastal protection, fishing, and tourism. Thus, climate change by impeding coral ecosystem engineers will impair the ecosystem functioning of entire reefs.

Coral surface area quantification–evaluation of established techniques by comparison with computer tomography

The surface area of scleractinian corals represents an important reference parameter required for various aspects of coral reef science. However, with advancements in detection accuracy and novel approaches for coral surface area quantification, evaluation of established techniques in comparison with state-of-the-art technology gains importance to coral researchers. This study presents an evaluation of methodological accuracy for established techniques in comparison to a novel approach composed of computer tomography (CT) and 3-dimensional surface reconstruction. The skeleton surface area of reef corals from six genera representing the most common morphological growth forms was acquired by CT and subsequently measured by computer-aided 3-dimensional surface reconstruction. Surface area estimates for the same corals were also obtained by application of four established techniques: Simple and Advanced Geometry, Wax Coating and Planar Projection Photography. Comparison of the resulting area values revealed significant differences between the majority (82%) of established techniques and the CT reference. Genus-specific analysis assigned the highest accuracy to geometric approximations (Simple or Advanced Geometry) for the majority of assessed coral genera (maximum accuracy: 104%; Simple Geometry with Montipora sp.). The commonly used and invasive Wax Coating technique reached intermediate accuracy (47–74%) for the majority of genera, but performed outstanding in the measurement of branching Acropora spp. corals (maximum accuracy: 101%), while the Planar Projection Photography delivered genera-wide low accuracy (12–36%). Comparison of area values derived from established techniques and CT additionally yielded approximation factors (AFs) applicable as factors in the mathematical improvement of surface area estimates by established techniques in relation to CT reference accuracy.

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

SUMMARY 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.

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.

A precise and non-destructive method to calculate the surface area in living scleractinian corals using X-ray computed tomography and 3D modeling

The surface area of corals represents a major reference parameter for the standardization of flux rates, for coral growth investigations, and for investigations of coral metabolism. The methods currently used to determine the surface area of corals are rather approximate approaches lacking accuracy, or are invasive and often destructive methods that are inapplicable for experiments involving living corals. This study introduces a novel precise and non-destructive technique to quantify surface area in living coral colonies by applying computed tomography (CT) and subsequent 3D reconstruction. Living coral colonies of different taxa were scanned by conventional medical CT either in air or in sea water. Resulting data volumes were processed by 3D modeling software providing realistic 3D coral skeleton surface reconstructions, thus enabling surface area measurements. Comparisons of CT datasets obtained from calibration bodies and coral colonies proved the accuracy of the surface area determination. Surface area quantifications derived from two different surface rendering techniques applied for scanning living coral colonies showed congruent results (mean deviation ranging from 1.32 to 2.03%). The validity of surface area measurement was verified by repeated measurements of the same coral colonies by three test persons. No significant differences between all test persons in all coral genera and in both surface rendering techniques were found (independent sample t-test: all n.s.). Data analysis of a single coral colony required approximately 15 to 30 min for a trained user using the isosurface technique regardless of the complexity and growth form of the latter, rendering the method presented in this study as a time-saving and accurate method to quantify surface areas in both living coral colonies and bare coral skeletons.

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.

Differential recycling of coral and algal dissolved organic matter via the sponge loop

Corals and macroalgae release large quantities of dissolved organic matter (DOM), one of the largest sources of organic matter produced on coral reefs. By rapidly taking up DOM and transforming it into particulate detritus, coral reef sponges are proposed to play a key role in transferring the energy and nutrients in DOM to higher trophic levels via the recently discovered sponge loop. DOM released by corals and algae differs in quality and composition, but the influence of these different DOM sources on recycling by the sponge loop has not been investigated. Here, we used stable isotope pulse-chase experiments to compare the processing of naturally sourced coral- and algal-derived DOM by three Red Sea coral reef sponge species: Chondrilla sacciformis, Hemimycale arabica and Mycale fistulifera. Incubation experiments were conducted to trace 13C- and 15N-enriched coral- and algal-derived DOM into the sponge tissue and detritus. Incorporation of 13C into specific phospholipid-derived fatty acids (PLFAs) was used to differentiate DOM assimilation within the sponge holobiont (i.e. the sponge host vs. its associated bacteria). All sponges assimilated both coral- and algal-derived DOM, but incorporation rates were significantly higher for algal-derived DOM. The two DOM sources were also processed differently by the sponge holobiont. Algal-derived DOM was incorporated into bacteria-specific PLFAs at a higher rate while coral-derived DOM was more readily incorporated into sponge-specific PLFAs. A substantial fraction of the dissolved organic carbon (C) and nitrogen (N) assimilated by the sponges was subsequently converted into and released as particulate detritus (15–24% C and 27–49% N). However, algal-derived DOM was released as detritus at a higher rate. The higher uptake and transformation rates of algal- compared with coral-derived DOM suggest that reef community phase shifts from coral to algal dominance may stimulate DOM cycling through the sponge loop with potential consequences for coral reef biogeochemical cycles and food webs.

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.

Effect of active water movement on energy and nutrient acquisition in coral reef-associated benthic organisms

Most visitors of Indo-Pacific coral reefs observe underwater an unexpected phenomenon on the seafloor. Some colonies of the soft coral family Xeniidae open and close their polyps, some pulsing in synchronized, and others in unsynchronized, motion. This pulsation behavior represents a striking and fascinating feature because, sessile benthic (coral reef-associated) organisms do not usually show any active body movements. Surprisingly, to date, no study has resolved the potential reasons and triggering factors for such an unusual and apparently energy-costly behavior. Intensive literature research results in only two related studies from the 1950s. These early investigations indicate that water temperature and some inorganic ions may affect pulsation rates of xeniid soft corals (1, 2), unfortunately without providing further insights into the potential reasons and/or associated benefits of their pulsation. Now, however, in PNAS, Kremien et al. (3) have succeeded in bringing some light into the darkness. Our colleagues from Israel are able to show, using an interconnected series of in situ observations and laboratory experiments at the Northern Red Sea, that the pulsation movement of the coral reef-associated soft coral species Heteroxenia fuscescens leads to increased water flow and turbulence, thereby generating at least two great benefits: (i) enhancement of photosynthesis via fast removal of excess oxygen; and (ii) prevention of refiltration of surrounding water by neighboring polyps.

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

SUMMARY 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.