Ciliary vortex flows and oxygen dynamics in the coral boundary layer

Cesar O Pacherres,Gertraud M Schmidt-Grieb,Claudio Richter,Soeren Ahmerkamp,Moritz Holtappels

doi:10.1038/s41598-020-64420-7

Abstract

The exchange of metabolites between environment and coral tissue depends on the flux across the diffusive boundary layer (DBL) surrounding the tissue. Cilia covering the coral tissue have been shown to create vortices that enhance mixing in the DBL in stagnant water. To study the role of cilia under simulated ambient currents, we designed a new light-sheet microscopy based flow chamber setup. Microparticle velocimetry was combined with high-resolution oxygen profiling in the coral Porites lutea under varying current and light conditions with natural and arrested cilia beating. Cilia-generated vortices in the lower DBL mitigated extreme oxygen concentrations close to the tissue surface. Under light and arrested cilia, oxygen surplus at the tissue surface increased to 350 µM above ambient, in contrast to 25 µM under ciliary beating. Oxygen shortage in darkness decreased from 120 µM (cilia arrested) to 86 µM (cilia active) below ambient. Ciliary redistribution of oxygen had no effect on the photosynthetic efficiency of the photosymbionts and overall oxygen flux across the DBL indicating that oxygen production and consumption was not affected. We found that corals actively change their environment and suggest that ciliary flows serve predominantly as a homeostatic control mechanism which may play a crucial role in coral stress response and resilience.

Highlights

The exchange of metabolites between environment and coral tissue depends on the flux across the diffusive boundary layer (DBL) surrounding the tissue
We evaluated the response of the corals Photosystem II complex (PSII) to the experimental manipulation of flow and light under active and arrested ciliary motion by Pulse Amplitude Modulation (PAM) chlorophyll a fluorometry[35], using a diving PAM fluorometer (Walz, Germany)
The flow and oxygen measurements revealed a clear effect of cilia-induced vortex flow on oxygen concentration in the boundary layer of the coral Porites lutea under natural flow and light conditions

Summary

Introduction

The exchange of metabolites between environment and coral tissue depends on the flux across the diffusive boundary layer (DBL) surrounding the tissue. The photosynthetic algae produce a surplus of oxygen, as a function of light intensity[15,16], zooxanthellae density[17], ambient flow speed[18,19], and dissolved inorganic carbon[20] This excess of oxygen accumulates in the tissue and diffuses across the DBL into the water column aloft[21]. We extend this study to measure the changes in oxygen across the DBL at different flow speeds, light regimes and under active and arrested cilia activity (the latter achieved using sodium orthovanadate4 – see M&M), using the reef-building coral Porites lutea as a model organism. Chlorophyll fluorescence quenching was used to measure the effect of ciliary flows on coral health

Methods

Results

Conclusion