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Microenvironment and Photosynthesis of Zooxanthellae in Scleractinian Corals Studied with Microsensors for 02, Ph and Light

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Microenvironment and Photosynthesis of Zooxanthellae in Scleractinian Corals Studied with Microsensors for 02, Ph and Light MARINE ECOLOGY PROGRESS SERIES Vol. 117: 159-172.1995 Published February 9 Mar. Ecol. Prog. Ser. Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for 02,pH and light Michael ~iihl',Yehuda Cohen2, Tage Dalsgaard3, Bo Barker Jergensenl, Niels Peter Revsbech4 'Max Planck Institute for Marine Microbiology, Fahrenheitstr. 1, D-28359 Bremen, Germany 'Division of Microbial and Molecular Ecology, Life Science Institute, Hebrew University of Jerusalem, Jerusalem 91904, Israel 'National Environmental Research Institute, Department of Freshwater Ecology, PO Box 314, Vejlsevej 25, DK-8600 Silkeborg, Denmark "Department of Microbial Ecology, Institute of Biological Sciences, University of Aarhus, Ny Munkegade Build. 540, DK-8000 Aarhus C, Denmark ABSTRACT- During experimental light-dark cycles, O9 in the tissue of the colonial scleractinian corals Favia sp. and Acropora sp reached >250 % of air saturation after a few minutes in light. Immediately after darkenmg, 0; was depleted rapidly, and within 5 mm the 0; concentration at the tissue surface reached <2 % of air saturation. The pH of the tissue changed within 10 min from about 8.5 in the light to 7.3 m the dark. Oxygen and pH profiles revealed a diffusive boundary layer of flow-dependent thick- ness, which limited coral respiration in the dark. The light field at the tissue surface (measured as scalar irradiance, Eo) differed strongly with respect to light intensity and spectral composition from the inci- dent collimated light (measured as downwelling irradiance, Ed) Scalar irradiance reached up to 180 % of Ed at the coral tissue surface for wavelengths subject to less absorption by the coral tissue (600 to 650 run and >680 nm). The scalar irradiance spectra exhibited bands of chlorophyll a (chl a) (675 run), chl c (630 to 640 nm) and pendinin (540 nm) absorption and a broad absorption band due to chloro- phyll~and carotenoids between 400 and 550 nm. The shape of both action spectra and photosynthesis vs irradiance (Pvs I) curves depended on the choice of the light intensity parameter. Calculations of mi- ha1 slopes and onset of light saturation, Ik, showed that P vs Eo curves exhibit a lower initial slope and a higher 4 than corresponding Pvs Ed curves. Coral respiration in light was calculated as the difference between the measured gross and net photosynthesis, and was found to be >6 times higher at a saturat- ing irradiance of 350 pEm m2s1 than the dark respiration measured under identical hydrodynamic conditions (flow rate of 5 to 6 cm ssl). KEY WORDS: Light-enhanced respiration . 0; and pH dynamics Action spectra P vs I curves . Scalar irradiance INTRODUCTION ers in tropical reef communities, estimated to account for 1 to 10% of total benthic production on a global Symbiotic photosynthetic dinoflagellates (= zooxan- scale (Muscatine 1990). thellae) are common inhabitants of many metazoan Studies of the photophysiology of zooxanthellae and animals in the tropics, e.g. foraminifera, porifera and their interaction with the host coral have inherent cnidarians (Trench 1981). In the polyp tissue of reef methodological problems due to the close interaction corals, high densities of zooxanthellae belonging to the of zooxanthellae and coral metabolism within the <0.5 genus Symbiodinium are found (Porter et al. 1984). to 1 mm thm layer of tissue growing on the calcified These are among the most important primary produc- coral skeleton. Carbon fixed by the zooxanthellae 1Inter-Research 1995 Resale of full article not permitted Mar. Ecol. Prog. Ser 117: 159-172, 1995 might be used for biosynthesis and respiration within up to 200% of incident irradiance at the sediment the symbionts or translocated to the surrounding ani- surface due to intense multiple scattering. The combi- mal tissue, where it is used for respiration and biosyn- nation of the incident collimated light with diffuse scat- thesis (Muscatine et al. 1981, Falkowski et al. 1984). tered light, which was spectrally altered due to absorp- Part of the fixed C is excreted e.g. as mucus, or is mcor- tion by photopigments in the sediments, resulted in a porated into skeletal carbonate. Oxygen produced by strong spectral distortion relative to the incident light. zooxanthellae photosynthesis is used partly for sym- Similar effects of light scattering have been postulated biont respiration and partly for coral respiration. This to occur in corals (Brakel 1979, Falkowski et al. 1990) intimate association between autotrophic and het- but to our knowledge no measurements of the light erotrophic processes in corals (and in many other field at the level of single corals are available. algal-animal symbioses) makes the quantitative and In this study we present direct measurements of 02, spatial separation of respiration and photosynthesis pH, light and photosynthesis in the tissue of scleractm- difficult when 14C isotopes or O2 exchange methods ian corals. The goal was to characterize the chemical are used (Muscatine et al. 1981, Muscatine 1990). Sim- and physical microenvironment of the zooxanthellae ilar methodological problems exist in measurements of and their surrounding coral host. Our results represent the primary production in sediments inhabited by point measurements within single coral polyps and microalgae and in photosynthetic microbial mats demonstrate basic principles of respiration and photo- (Revsbech et al. 1981). A method for measuring gross synthesis regulation in corals. photosynthesis independent of respiration is available based on the use of Oz microelectrodes (Revsbech et al. 1981, Revsbech & Jergensen 1983). MATERIALS AND METHODS The microenvironment of the zooxanthellae is virtu- ally unstudied, although microsensors for pH and 02, Sampling and experimental setup. Small branches and the light-dark shift technique for photosynthesis of Acropora sp. and Favia sp. were sampled by SCUBA measurements, have previously proven useful in the diving from 5 to 10 m depth in the Gulf of Aqaba next study of chemical gradients and transport mechanisms to the H. Steinitz Marine Biological Laboratory, Eilat, within algal-animal symbiosis (Jergensen et al. 1985, Israel. The in situ seawater temperature was 20 to 23OC Revsbech & Jergensen 1986). The few published O2 and maximal light intensities at the sampling depth microelectrode measurements in corals have dealt reached 980 pEin m2s1 downwelling irradiance with the diffusive boundary layer (DBL), which regu- (Shashar et al. 1993). Most specimens had been lates the diffusive exchange between the coral tissue exposed to natural light conditions and exhibited pale and the surrounding seawater (Patterson 1992, Sha- yellow-brownish/green tissue. One colony head of shar et al. 1993). The dynamics of pH and Oz in layers Favia sp. had been exposed for an extended period of endolithic algae in the coral skeleton has also been (>2 yr; Razi Wigo pers. comm.) to very low light condi- studied with O2 microelectrodes and pH minielec- tions in the shade of a larger coral assemblage and had trodes (Shashar & Stambler 1992). dark chocolate-brown tissue. Together with the chemical microenvironment, the After sampling, the corals were transferred directly light field inside the coral tissue is the most important to an aquarium with continuously aerated seawater factor regulating zooxanthellae photosynthesis. The kept at room temperature (21 to 23OC). Water move- optical properties of coral tissue are not known and ment m the aquarium was created by blowing air from only a few studies of the light field near coral reefs an aquarium pump onto the water surface through a have been published [Roos 1967 (cf. Falkowski et al. Pasteur pipette. The approximate flow velocity of the 1990),Jaubert & Vasseur 1974, Brakel 1979, Williams & water over the coral was determined by timing the Carpenter 19901. Recently, fiber-optic microprobes movement of small suspended particles in the water have been developed to measure directional radiant under a dissection microscope. Visible light was inci- fluxes (field radiance) and spherically integrated total dent vertically from above using a tungsten-halogen radiant flux (scalar irradiance) (Jergensen & Des lamp of constant color temperature but variable light Marais 1986, Kuhl & Jergensen 1992, Lassen et al. intensity (Schott KL1500 with neutral density filters) 1992). Microscale light measurements with these and a daylight filter inserted in the light path. The probes in sediments and microbial mats demonstrated lamp was equipped with a fiber-optic cable with a col- that the light field near the sediment surface may be limating lens. Experiments were done within 24 to 42 h very different in spectral composition and intensity after sampling. from the incident radiant flux (irradiance) (Kuhl & Jer- Oxygen and pH measurements. Oxygen concentra- gensen 1992, 1994, Lassen et al. 1992, Kuhl et al. tion was measured with Clark-type Oz microelectrodes 1994a, b). The scalar irradiance in sediments reached (Revsbech & Ward 1983) connected to a custom-built Kuhl et al: Microenvironment of corals 161 picoammeter. In the Favia sp. measurements the O2 interference filter in the holder it was possible to scan microelectrodes were also equipped with a guard through the visible spectrum in 10 nm steps illuminat- cathode (Revsbech 1989).Signals were either recorded ing the coral with monochromatic light. on a strip-chart recorder or collected by a computer via Positioning of microsensors. All microsensors were an A/D card and a custom-made Pascal program. The positioned by either a manually operated or a motor- electrodes had a tip diameter of 6 to 12 pm, a 90% ized micromanipulator (Miirtzhiiuser Germany; L.O.T. response time of ~0.5s, and a stirring sensitivity of 1 to Germany) controlled by a computer and custom-made 2 %. Linear calibration of the O2 microelectrodes was Pascal software. In the Acropora sp. samples, measure- done from readings of the electrode current in air-sat- ments were done with the microelectrodes mounted urated seawater and in nitrogen-flushed seawater. The vertically and the light incident at an angle. In most of O2 concentration in air-saturated seawater was calcu- the Favia sp.
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