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Al-Horani Et Al. (2007) Coral Reefs (2007) 26:531–538 DOI 10.1007/s00338-007-0250-x REPORT Dark calciWcation and the daily rhythm of calciWcation in the scleractinian coral, Galaxea fascicularis F. A. Al-Horani · É. Tambutté · D. Allemand Received: 30 January 2007 / Accepted: 8 May 2007 / Published online: 7 June 2007 © Springer-Verlag 2007 Abstract The rate of calciWcation in the scleractinian Keywords Corals · Galaxea fascicularis · CalciWcation coral Galaxea fascicularis was followed during the day- rhythm · Dark calciWcation time using 45Ca tracer. The coral began the day with a low calciWcation rate, which increased over time to a maximum in the afternoon. Since the experiments were carried out Introduction under a Wxed light intensity, these results suggest that an intrinsic rhythm exists in the coral such that the calciWca- There have been extensive studies during the last two tion rate is regulated during the daytime. When corals were decades on coral calciWcation and its interactions at many incubated for an extended period in the dark, the calciWca- levels. CalciWcation is important for reef building and plays tion rate was constant for the Wrst 4 h of incubation and a role in seawater carbonate chemistry, which is inXuenced then declined, until after one day of dark incubation, calci- by the atmospheric CO2 levels (Barnes and Chalker 1990; Wcation ceased, possibly as a result of the depletion of Frankignoulle et al. 1994; Gattuso et al. 1998; Kleypas et al. coral energy reserves. The addition of glucose and Artemia 1999; Gattuso and Buddemeier 2000; Langdon et al. 2000; reduced the dark calciWcation rate for the short duration of Marubini et al. 2001, 2002; Leclercq et al. 2002; Reynaud the experiment, indicating an expenditure of oxygen in res- et al. 2003; Langdon and Atkinson 2005). Most of the infor- piration. ArtiWcial hypoxia reduced the rate of dark calciW- mation gained on coral calciWcation has focused on light cation to about 25% compared to aerated coral samples. It calciWcation while little attention has been given to dark cal- is suggested that G. fascicularis obtains its oxygen needs ciWcation. CalciWcation requires energy and involves vari- from the surrounding seawater during the nighttime, ous enzymes and carriers (Barnes and Taylor 1973; Chalker whereas during the day time the coral exports oxygen to and Taylor 1975; Ip et al. 1991; Goiran et al. 1996; Al- the seawater. Moghrabi et al. 1996; Allemand et al. 1998; Furla et al. 1998; Al-Horani et al. 2003a). It is accepted that corals cal- cify at a faster rate in the light compared with the dark, through a phenomenon usually termed light-enhanced calci- Communicated by Biology Editor M.P. Lesser. Wcation. In the light, photosynthetically produced reduced F. A. Al-Horani (&) carbon compounds are transported to the growing parts of Marine Science Station, PO Box 195, the coral to be used as energy resources and building blocks, Aqaba 77110, Jordan while O2 produced during photosynthesis supports meta- e-mail: [email protected] bolic respiration (Patton et al. 1977; Rinkevich and Loya É. Tambutté · D. Allemand 1983; Falkowski et al. 1984; Fang et al. 1989; Al-Horani Centre ScientiWque de Monaco, et al. 2003b). Carbon dioxide Wxation by photosynthesis av. St Martin, MC 98000, Monaco removes this respiratory product and controls the pH in the coral tissues (Furla et al. 1998; Al-Horani et al. 2003a). This D. Allemand UMR 1112 UNSA-INRA, Parc Valrose, led to the belief that photosynthesis was the driving force BP 71, 06108 Nice Cedex 2, France behind the higher rate of calciWcation in the coral during the 123 532 Coral Reefs (2007) 26:531–538 daytime (Goreau 1959; Pearse and Muscatine 1971; Chalker of the Centre ScientiWque de Monaco using nylon threads and Taylor 1975). In the dark, photosynthesis ceases com- as described by Al-Moghrabi et al. (1993). After about pletely and the coral depends on a self-service mode of 3 months, the polyps developed into small microcolonies, action to sustain growth and calciWcation (Muscatine 1990). which were used in the experiments described in this study. To date, calciWcation in the dark has received little attention The aquarium was supplied with Mediterranean seawater with in coral research. Previous studies of dark calciWcation did low nutrient and chlorophyll a concentrations (Ferrier-Pagès not go beyond an estimation of the ratio between light and et al. 1998) and illuminated with metal halide lamps (HQI, dark calciWcation rates (reviewed by Gattuso et al. 1999). 400 W) at a constant irradiance of 200-mol photons m¡2 s¡1 As a result, there is currently a need for further information (12 h:12 h light:dark cycles). Water temperature in the aquar- about the process of dark calciWcation in corals. ium was 27°C while the seawater pH was between 8.1 and Various methods have been employed to study calciWca- 8.2. The seawater had an aragonite saturation state of 3.1–3.7. tion, with the use of radioisotopes being one of the main techniques for work involving both corals and other marine- EZux experiments calcifying organisms. However, measuring 45Ca exchange with 40Ca produces errors because this exchange gives appar- In order to test the eZux of 45Ca from the coral coelenteron, ent calciWcation in the absence of real precipitation (Goreau three microcolonies were incubated in small plastic vials with 1959). The processing of samples also produces additional 25 ml of seawater at 27°C for one hour. The speciWc activity errors. In some cases, dark calciWcation has been confused of the water at the beginning was ca. 23,000 dpm. A 100-l with isotopic exchange (Chalker and Taylor 1975). In other volume of the labeled seawater was used to count the activity cases, coral researchers have assumed that isotopic exchange (mixed with 4 ml scintillation Xuid). Counting was carried out is small compared to true calciWcation occurring in the light for 5 min in a scintillation counter. After the end of the incu- and have used dark calciWcation as a control for experiments bation period, the microcolonies were dipped in nonlabeled involving light calciWcation (reviewed by Barnes and Chal- seawater ten times to remove nonspeciWc bound 45Ca. The ker 1990). Using cultured microcolonies with no skeletons microcolonies were then transferred to 100 ml nonlabeled exposed to the radioisotope-labeled incubation medium, seawater and incubated under the same conditions used in the Tambutté et al. (1995, 1996) reduced the errors associated experiment to determine the eZux rate. A 100-l water sam- with isotopic exchange. Further improvements were made by ple was taken for counting at 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 12, 14, including dead colonies in the incubation experiments to esti- 16, 18, 20, 25, 30, 40, 50, 60, 70, 80, 100 and 120 min. mate the rate of isotopic exchange (Al-Horani et al. 2005). These results showed that dark calciWcation does occur in Processing of coral skeleton corals and that rates were always higher compared with those obtained using isotopic exchange methods. But the question At the end of the incubation period, the microcolonies were of what drives calciWcation in the dark remains. The use of then blotted dry on tissue paper and boiled with ca. 10 ml Ca2+ microsensors has proved to be a valuable tool for study- 2 N NaOH solution for 30 min to hydrolyze the tissue ing the dynamics and Xuxes of Ca2+ at a microscale level in layer. After the tissue hydrolysis was complete, the hydro- corals (De Beer et al. 2000; Al-Horani et al. 2003a). The lysate was decanted and the skeleton was washed with 2+ V application of Ca and pH microsensors in di erent com- 10 ml distilled H2O. The skeleton was then blotted dry on partments of the coral, including the calcifying Xuid between tissue paper and dried overnight at 70°C in oven. The next the skeleton and the tissue layer, has provided many details day, the dried skeletons were weighed and hydrolyzed com- about the mechanism of light calciWcation (Al-Horani et al. pletely by concentrated HCl solution and 250 l of the 2003a). hydrolysate was mixed with 4-ml scintillation Xuid and The present study was carried out to develop our under- counted for 5 min in the scintillation counter. standing of dark calciWcation in the coral Galaxea fascicu- laris, daytime calciWcation, and the driving forces of dark Daytime calciWcation rates calciWcation in this species. In order to measure changes in the rate of coral calciWcation during the day, the calciWcation rate was measured at 09:00, Materials and methods 12:00, 15:00, 18:00 and 20:00 h. Biological samples Dark incubations and measurement of calciWcation rates Single polyps of G. fascicularis from colonies from the Gulf CalciWcation in the dark was measured in triplicate for the of Aqaba (Jordan), were suspended in seawater in the aquaria coral microcolonies after incubating in the dark for 1, 2, 4, 123 Coral Reefs (2007) 26:531–538 533 12, 24, 48 and 72 h. After dark incubation, the corals were Results incubated with 45Ca at 27°C in stirred seawater for 1 h each. The Wrst four measurements were made during the EZux experiments showed that radioactive tracers were night so that the normal light dark cycle of the coral was not washed out after about 10 min of stirring in clean seawater; disturbed. as a result, this time was used in treatment of samples after incubation in radioactive tracers. EVects of addition of external energy sources The calciWcation rate measured in the light was about twice that in the dark (4.07 § 0.15 mol Ca2+/g wt/h Replicates of G.
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