Webb, A.E.

Coral reefs are declining worldwide. The abundance of corals has decreased alongside the rise of filter feeders, turf and algae in response to intensifying human pressures. This shift in prevalence of functional groups alters the biogeochemical processes in tropical water ecosystems, thereby influencing reef biological functions. An urgent challenge is to understand the 15 functional consequences of these shifts in order to develop suitable management strategies that aim at preserving the biological functions of reefs. Here, we quantify biogeochemical processes supporting key reef functions (i.e. net community calcification (NCC) and production (NCP), and nutrient recycling) in situ for five different benthic assemblages currently dominating shallow degraded Caribbean reef habitats. To this end, a custom made tent was placed over communities dominated by either one of five 20 functional groups: coral, turf and macroalgae, bioeroding sponges, cyanobacterial mats or sand, to determine chemical fluxes between these communities and the overlying water, during both day and night. Measured fluxes were then translated into responsible biogeochemical processes by solving a system of differential equations describing the contribution of each process to the measured chemical fluxes. Estimated processes are low compared to those known for reef flats worldwide. No real gain in primary habitat is recorded, with negative or very modest net community calcification rates by all communities. Similarly, 25 net production of biomass through photosynthesis is relatively low during the day and remineralisation of organic matter at night is relatively high in comparison, resulting in net heterotrophy over the survey period by most communities. Estimated recycling through nitrification and denitrification are high but denitrification does not fully counterbalance nutrient release from aerobic mineralisation, rendering all substrates sources of nitrogen. A multivariate pairwise analysis revealed that there is no significant difference between processes occurring on any of the assemblages, suggesting functional homogenisation 30 between distinct substrate types. We infer that the amount and type of organic matter released by abundant algal turfs and cyanobacterial mats on this reef, likely enhances heterotroph activity, and stimulates the proliferation of less diverse copiotrophic microbial populations, rendering the studied reef net heterotrophic and the overall biogeochemical ‘behaviour’ similar regardless of substrate type.

Anthropogenic pressures threaten the health of coral reefs globally. Some of these pressures directly affect coral functioning, while others are indirect, for example by promoting the capacity of bioeroders to dissolve coral aragonite. To assess the coral reef status, it is necessary to validate community-scale measurements of metabolic and geochemical processes in the field, by determining fluxes from enclosed coral reef patches. Here, we investigate diurnal trends of carbonate chemistry, dissolved organic carbon, oxygen, and nutrients on a 20 m deep coral reef patch offshore from the island of Saba, Dutch Caribbean by means of tent incubations. The obtained trends are related to benthic carbon fluxes by quantifying net community calcification (NCC) and net community production (NCP). The relatively strong currents and swell-induced near-bottom surge at this location caused minor seawater exchange between the incubated reef and ambient water. Employing a compensating interpretive model, the exchange is used to our advantage as it maintains reasonably ventilated conditions, which conceivably prevents metabolic arrest during incubation periods of multiple hours. No diurnal trends in carbonate chemistry were detected and all net diurnal rates of production were strongly skewed towards respiration suggesting net heterotrophy in all incubations. The NCC inferred from our incubations ranges from −0.2 to 1.4 mmol CaCO3 m−2 h−1 (−0.2 to 1.2 kg CaCO3 m−2 year−1) and NCP varies from −9 to −21.7 mmol m−2 h−1 (net respiration). When comparing to the consensus-based ReefBudget approach, the estimated NCC rate for the incubated full planar area (0.36 kg CaCO3 m−2 year−1) was lower, but still within range of the different NCC inferred from our incubations. Field trials indicate that the tent-based incubation as presented here, coupled with an appropriate interpretive model, is an effective tool to investigate, in situ, the state of coral reef patches even when located in a relatively hydrodynamic environment.

Embargo until April 04 2020

PhD thesis

For coral reefs to persist, the rate of CaCO3 production must be greater than the rate of erosion to enable positive growth. Negative impacts of global change (ocean acidification and warming) and local stressors (eutrophication, overfishing) on accretion co-occur with positive effects of these changes on bioerosion capacity and chemical dissolution by excavating euendolithic organisms. This is especially relevant for reefs characterised with low calcifying rates as they will tip faster into net loss. The Caribbean reefs suffered from a decrease by up to 80% in scleractinian coral cover in the past 50 years, their configuration bears very little resemblance with reefs pre1980s, in terms of benthic composition, coral cover and structural complexity. Specifically, excavating sponges can contribute up to 90% of the total macroborer activity on coral reefs and their rates of bioerosion are positively affected by pCO2. The overarching aim of this thesis was to quantify and understand the accretion and loss terms of coral reef communities with a focus on the interactions of anthropogenic ocean acidification and eutrophication with bioerosion by coral-excavating sponges.The use of incubations was central in this piece of work. Changes in the chemical composition of the water overlying sponges and reef communities indicate the relative contribution of metabolic processes such as net calcification/dissolution and net respiration/production. However, we first used fluorescence microscopy to investigate the underlying mechanisms of CaCO3 dissolution by excavating sponges. It revealed that they promote CaCO3 dissolution by decreasing pH at the sponge/coral interface. The high [H+] at this site is achieved through delivery of low-pH vesicles by the etching cells. The enzyme carbonic anhydrase, which is responsible for significantly increasing the speed of the reversible reaction H2O+CO2↔H++HCO3−, has been shown to be associated to the sponge’s etching processes and is therefore thought to play a role in the dissolution of CaCO3. By blocking its activity whilst incubating sponges and analysing the rate of dissolution, CA was found to play an important role in speeding up protonation of HCO3− ions at the dissolution site, enabling CO2 to diffuse out of the etching area. When exposed to different ranges of ocean acidification and eutrophication, bioerosion rates increased with both variables but no synergistic relation was revealed. Incubations performed at the community level around Saba and Curacao yielded net community calcification (NCC) rates which were lower than those reported for reef flats worldwide. Still, Saba coral reefs are considered relatively pristine sites compared to the average within the wider Caribbean. Around Curaçao, incubations on reef assemblages dominated by coral yielded even lower NCC rates. Incubations of other benthic assemblages that currently characterized shallow Caribbean reef substrate (such as bioeroding sponges, benthic cyanobacterial mats and sand) all resulted in net dissolution. For both Saba and Curaçao, results suggest that reef calcification on these sites is barely able to compensate the CaCO3 losses due to dissolution from other opportunistic benthic residents. With the ongoing global and local pressures, the delicate balance between CaCO3 accretion and loss is likely to tip.

Health of tropical coral reefs depends largely on the balance between constructive (calcification and cementation) and destructive forces (mechanical-chemical degradation). Gradual increase in dissolved CO2 and the resulting decrease in carbonate ion concentration (“ocean acidification”) in ocean surface water may tip the balance toward net mass loss for many reefs. Enhanced nutrients and organic loading in surface waters (“eutrophication”), may increase the susceptibility of coral reef and near shore environments to ocean acidification. The impacts of these processes on coral calcification have been repeatedly reported, however the synergetic effects on bioerosion rates by sponges are poorly studied. Erosion by excavating sponges is achieved by a combination of chemical dissolution and mechanical chip removal. In this study, Cliona caribbaea, a photosymbiont-bearing excavating sponge widely distributed in Caribbean reef habitats, was exposed to a range of CO2 concentrations, as well as different eutrophication levels. Total bioerosion rates, estimated from changes in buoyant weights over 1 week, increased significantly with pCO2 but not with eutrophication. Observed chemical bioerosion rates were positively affected by both pCO2 and eutrophication but no interaction was revealed. Net photosynthetic activity was enhanced with rising pCO2 but not with increasing eutrophication levels. These results indicate that an increase in organic matter and nutrient renders sponge bioerosion less dependent on autotrophic products. At low and ambient pCO2, day-time chemical rates were ~50% higher than those observed at night-time. A switch was observed in bioerosion under higher pCO2 levels, with night-time chemical bioerosion rates becoming comparable or even higher than day-time rates. We suggest that the difference in rates between day and night at low and ambient pCO2 indicates that the benefit of acquired energy from photosynthetic activity surpasses the positive effect of increased pCO2 levels at night due to holobiont respiration. This implies that excavation must cost cellular energy, by processes, such as ATP usage for active Ca2+ and/or active proton pumping. Additionally, competition for dissolved inorganic carbon species may occur between bioerosion and photosynthetic activity by the symbionts. Either way, the observed changing role of symbionts in bioerosion can be attributed to enhanced photosynthetic activity at high pCO2 levels.