The role of ciliary vortices on the coral’s oxygen exchange and food capture

Abstract

Tropical shallow corals live in a highly dynamic environment dominated by wave action with water currents ruling over their physiological processes. Due to their relatively small size and lack of mobility, they will interact with the water column via a so called diffusive boundary layer (DBL), a layer of water located at the immediate surface of the coral and where molecular diffusion is the dominant transport mechanism for solutes. All elements needed to ensure the functioning of the coral, and its symbiotic algae, must traverse this layer in order to either reach or leave the coral tissue. Thus, the recent discovery that corals possess the ability to enhance mass transport in the DBL by the generation of vortices caused by the beating of epidermal cilia, opened several questions as of the extent of their effect on the coral’s ecophysiological processes. The aim of this thesis is to better understand the role which ciliary vortices play on the dynamics of the coral boundary layer by studying how these currents intervene in elemental and particle transport processes along the autotrophic and heterotrophic pathways of the coral holobiont. For this purpose, and using a flow-through chamber specifically created for this project (Chapter 2), oxygen (using electrochemical microsensors) and flow dynamics (by Particle image Velocimetry – PIV – and Particle Tracking Velocimetry) were measured at the boundary layer of the massive coral Porites lutea under different flow speeds and light conditions (Chapter 3). Results show that, regardless of the flow speed of the water column, ciliary vortices mitigate extreme oxygen concentrations close to the tissue surface during both oxygen production and consumption. Moreover, the ciliary redistribution of oxygen had no effect on the oxygen flux across the upper DBL further proving that the benefit of vortex mixing is the reduction of oxygen as part of a homeostatic control mechanism, which may play a crucial role in the coral’s relationship with its symbionts and response to environmental stress. However, the ability of ciliary vortices to enhance mass transport was not homogeneous along the coral surface as it depended upon the characteristics of the vortex itself and their location along the coral surface (Chapter 3). In order to better observe and understand these heterogeneities, PIV (using oxygen sensitive nanoparticles –sensPIV Chapter 4), together chlorophyll-sensitive hyperspectral imaging (used to map the μ-metric distribution of chlorophyll inside the coral tissue) were applied for the first time on a coral colony (Chapter 5). Results showed that high chlorophyll areas (septa and coenosarc) were situated outside the vortex structures, while low chlorophyll areas (mouth openings) were situated underneath the vortex suggesting the coupling of ciliary beatings with these areas of high chlorophyll as means to ventilate them and consequently promote the efflux of oxygen out of the tissue (Chapter 5). A mechanism that might be of particular importance in order to mitigate oxygen accumulation inside the tissue containing high chlorophyll concentrations, thus preventing the detrimental consequences of oxygen accumulation (i.e. inhibition of photosynthesis). These small surface currents played important roles not only by boosting chemical mass transport towards and away from the tissue but also by intervening in the coral’s interaction with suspended prey elements. As described in Chapter 6, the vortices generated by the beating of cilia are also key to the coral’s heterotrophic nutrition. These currents enhanced the capture of tiny particles by mucus filaments, providing the first mechanistic explanation for ultraplankton capture in scleractinian corals. Given that heterotrophic feeding provides a safe route in the recovery of corals to bleaching events, their ability to enhance the capture of a highly abundant food source might therefore have important implications when facing climatic stressors. Moreover, the creation of these feeding currents by cilia beating call for a review on the trophic classification of corals – long considered passive suspension feeders – as the results presented here showed they could rather be classified as filter feeders together with mollusks and sponges. Overall, this thesis contributes to the understanding of small-scale variations in the physicochemical and hydrodynamic microenvironment of corals created by the interaction of ciliary vortices and the surrounding water, providing essential mechanistic insights in areas such as symbiotic relationships, micro-heterotrophy and stress response. The complex symbiont-host relationships and the internal and external physicochemical heterogeneities observed here may well represent a source of buffering and acclimation for corals, and thus resilience to environmental stresses. The question that now arises is: how – or rather if –these mechanisms will contribute to the adaptation of coral reefs to an accelerated anthropogenic climate change. The novel tools developed and uniquely combined here proved suitable to address such a question and can, in the future, shed new light on the underlying processes of stress exposure.