Journal of Experimental Marine Biology and Ecology 263 Ž2001. 211–225 www.elsevier.comrlocaterjembe

Photo-acclimation dynamics of the coral Stylophora pistillata to low and extremely low light E.A. Titlyanov a,b,) , T.V. Titlyanova a , K. Yamazato c , R. van Woesik d a

d

Institute of Marine Biology, Far East Branch of Russian Academy of Sciences, VladiÕostok 690041, Russia b Sesoko Marine Science Center, UniÕersity of the Ryukyus, 3422 Sesoko, Motobu-cho, Okinawa 905-205, Japan c Research Institute for Subtropics, 1 Asahimachi, Naha, Okinawa 9003-0029, Japan Department of Marine Sciences, UniÕersity of the Ryukyus, Senbaru 1, Nishihara, Okinawa 903-0213, Japan Received 22 February 2001; received in revised form 28 April 2001; accepted 10 June 2001

Abstract Photo-acclimation dynamics of the symbiotic coral Stylophora pistillata to lowering light intensities in the range of 95% to 0.8% of incident surface photosynthetic active radiation ŽPAR 0 . was studied. Coral colonies were sampled from 1- to 2-m depths in open and shaded habitats from the fringing reef of Sesoko Island Žnear the Tropical Biosphere Research Center, University of the Ryukyus. Okinawa, Japan. Photo-acclimation of exterior branches of coral colonies were examined in outdoor aquarium, where light regime and feeding were similar to field conditions. Two photo-acclimation reactions were studied: Ž1. changes in chlorophyll concentrations in zooxanthellae; Ž2. changes in zooxanthellar population density in coral branches. In parallel, we measured an average volume of zooxanthellae, proliferating zooxanthellae frequency ŽPZF. and degrading zooxanthellae frequency ŽDZF.. It was shown that the coral S. pistillata can survive and acclimate to a wide range of light intensities from 95% to 0.8% PAR 0 . Acclimation to low light Ž30% and 8% PAR 0 . involves maximizing the light harvesting capacity by increasing photosynthetic pigment concentration in zooxanthellae and zooxanthellar population density in coral branches. Under extremely low light Ž0.8% PAR 0 ., the coral lost zooxanthellae by degradation Žperhaps digestion. and retained zooxanthellae-accumulated high concentrations of chlorophyll. The photoacclimation process is dynamic and immediate. Changes in pigment concentrations in zooxanthellae occurred within 2–4 days and changes in zooxanthellar population densities occurred within

) Corresponding author. Far East Branch of Russian Academy of Sciences, Institute of Marine Biology, Vladivostok-41, Vladivostok 690041, Russia. Tel.: q7-4232-310931; fax: q7-4232-310900. E-mail addresses: [email protected], [email protected] ŽE.A. Titlyanov..

0022-0981r01r$ - see front matter q 2001 Published by Elsevier Science B.V. PII: S 0 0 2 2 - 0 9 8 1 Ž 0 1 . 0 0 3 0 9 - 4

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40 days. Zooxanthellae population densities were regulated by changes in rates of division and degradation of symbiotic cells. q 2001 Published by Elsevier Science B.V. Keywords: Photo-acclimation; Coral; Stylophora pistillata; Chlorophyll concentration; Zooxanthellae population density; Zooxanthellae division; Zooxanthellae degradation

1. Introduction Since light is arguably the most important limiting resource on a coral reef, coral research has focused on photo-acclimation, particularly, aspects involving morphological and physiological changes to corals under different light regimes ŽFalkowski and Dubinsky, 1981; Porter et al., 1984; Titlyanov, 1987; Titlyanov et al., 2000a, 2001; Leletkin et al., 1996.. Adaptation of corals to lowered light intensities at great depths and in shaded sites was studied in detail. The acclimation to low light involves at least three responses that are not mutually exclusive. First, photosynthetic pigments may accumulate in zooxanthellae ŽTitlyanov et al., 1980, 2000a, 2001; Falkowski and Dubinsky, 1981; Dustan, 1982; Porter et al., 1984.. Second, zooxanthellar population densities may increase ŽDrew, 1972; Zvalinsky et al., 1978; Titlyanov et al., 1980; Titlyanov et al., 2000a, 2001.. Third, the morphology of the corals may change ŽKawaguti, 1937; Fricke and Schuhmacher, 1983; Fricke and Meischner, 1985; Titlyanov, 1987.. Moreover, the acclimation response to low light is geared towards increasing the relative quantum yield of photosynthesis by zooxanthellae ŽLeletkin et al., 1980. in order to effectively transform and transport light energy, which, in turn, may involve changes in Photosystems I and II ŽTitlyanov et al., 1980; Zvalinsky et al., 1980.. Corals may also conserve energy budget at low light levels by Ž1. reducing excretion of organic matter ŽCrossland 1987., Ž2. reducing the rate of zooxanthellar respiration ŽLeletkin et al., 1996., Ž3. reducing the rate of coral respiration ŽWethey and Porter, 1976; Chalker et al., 1983; Titlyanov, 1991., and Ž4. increasing the utilization of half-reduced intermediate products of photosynthesis, such as glycerol and amino acids ŽBil’ et al., 1992; Titlyanov et al., 2000a, 2001.. All these responses were discovered and investigated by comparison of physiological state and morphology of coral colonies Žor their exterior branches. from different depths or from open and shaded habitats. In some cases, experiments were conducted on corals maintained under different light conditions in the field during 2–4 weeks ŽTitlyanov et al., 1983. or in experimental aquaria ŽTitlyanov et al., 2000a.. In most cases, morphology and physiological state Žas a result of acclimation. of corals kept in given light conditions Žbut not photo-acclimation dynamics. were studied. So far, it is not clear when the acclimation response occurs after changing light intensity, when the reaction is complete, and how long the process of physiological state of change takes. Undoubtedly, it is methodically impossible to study the process of photo-acclimation in dynamics on all known adaptive reactions in the same experiment. We examined dynamics of two identified responses of acclimation to low light: accumulation of photosynthetic pigments in zooxanthellae, and increase in zooxanthellae density in coral tissue. The light range Ž95–0.8% PAR 0 ., in which adaptive changes were studied, was close to the ecological range of light experienced by

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scleractinian corals Že.g., Falkowski and Dubinsky, 1981; Porter et al., 1984; Titlyanov and Latypov, 1991..

2. Material and methods 2.1. Biological material In September 1997, we collected medium-sized colonies of the coral Stylophora pistillata Esper Ž1797. from 1- to 2-m depth near the Sesoko Tropical Biosphere Research Center, University of the Ryukyus, Okinawa, Japan. Six coral colonies from open shallow sites Ž90% to 70% PAR 0 . and six colonies from shaded Ž40% to 20% PAR 0 . sites. The colonies were placed into plastic bags and transported to a 12-m3 outdoor aquarium that was supplied with running seawater. In general, the aquarium water temperature was 1–2 8C higher than the ocean during daytime, and 1–2 8C lower at night Ži.e., in October 1997, the aquarium temperature was 25–27 8C during daytime, and 23–24 8C at night; in February, the daytime temperature was 22–24 8C and 20–22 8C at night.. Water for the aquarium was derived directly from the adjacent fringing reef, without filtration or settling; therefore, we assume the zooplankton and nutrient supply within the aquarium was the same as the reef. The aquarium water was intensively aerated and the turnover rate was approximately 30% hy1 . The aquarium was partly shaded by black plastic net to reduce light intensity to 30% of the incident surface photosynthetic active radiation ŽPAR 0 .. Samples from open shallow sites were placed into aquaria exposed to full sunlight Ž95% PAR 0 . and corals from shaded shallow sites were placed into aquaria with light of 30% PAR 0 . 2.2. Experimental design Two experiments were undertaken. Five-centimeter branches were broken off coral colonies on the third day of maintenance in aquarium, and fixed with cement onto ceramic tiles in their natural orientation. Each branch was numbered. The coral branches were pretreated with 95% and 30% PAR 0 for 30 days ŽExperiment 1. or for 90 days ŽExperiment 2.. Experiment 1 assessed the zooxanthellae characteristics when coral branches were transferred from 95% to 30% PAR 0 , from 30% to 8% PAR 0 , and from 30% to 0.8% PAR 0 . Twenty branches were placed in each light treatment and maintained for 120 days Žfrom October to February.. On days 1, 10, 20, 40, 60 and 120, three branches from each light treatment were removed and analysed. Means and standard deviations were calculated; n Žbranches. s 3. Experiment 2 assessed daily changes to the physiological state of coral branches during the first week of reacclimation from 95% to 30% PAR 0 , from 30% to 8% PAR 0 and from 30% to 0.8% PAR 0 .Chlorophyll concentration, zooxanthellae numbers and zooxanthellae sizes were measured on days 2, 4 and 8; other characteristics were measured daily Žone branch was used in each analysis.. The experiment was triplicated

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during January–February. Means and standard deviations were calculated; n Žexperiments. s 3. 2.3. Analytical procedures Coral tissue was removed with a Water-Pik ŽJohannes and Wiebe, 1970. and the number of zooxanthellae in each tissue homogenate sample was counted Ž10 fields per count. using a hemocytometer. Zooxanthellae density was expressed as number per polyp. The polyp density on each skeleton was counted with a magnifying glass Ž4 = .. The diameters of 100 zooxanthellae were measured from each branch using a calibrated ocular micrometer at 400 = magnification. Zooxanthellae volume was calculated using the formula of a sphere. Tissue homogenates were observed at 400 = on a hemocytometer grid on which we counted normal, dividing and degrading zooxanthellae. Cells in the process of division were classified as dividing when they showed the initial appearance of a division furrow in the mother cells to the formation of cell envelopes in daughter cells. Colour, size and shape identified degraded or degrading zooxanthellae Žafter Titlyanov et al., 1996.. A total of 500 cells were counted in each sample. The percentage of dividing cells was classified as the proliferating zooxanthellae frequency ŽPZF., and the percentage of degrading cells was classified as the degrading zooxanthellae frequency ŽDZF. in accordance with Titlyanov et al. Ž1996.. PZF and DZF were examined at 0900–1000 h, when number of dividing cells is about 80% of the maximum, and degraded zooxanthellae numbers were highest ŽTitlyanov et al., 1996.. 2.4. Chlorophyll concentrations A known number of zooxanthellae were filtered under vacuum Ž47-mm AP Millipore filters. and placed in a refrigerator for 2 days in an aqueous solution of 90% acetone. The solution with sample was shaken daily. The absorbance of acetone extracts was measured at 630 and 663 nm using a Hitachi U-2000 spectrophotometer, and the concentrations of chlorophyll a and chlorophyll c 2 were determined ŽJeffrey and Humphrey, 1975.. Chlorophyll concentrations were expressed as either mg per 1000 polyps or as mg per mm3 of the zooxanthellae volume. 2.5. Statistical analysis A Student’s t-test ŽBailey, 1981. was used to analyze the data and to evaluate differences between means. Differences between means with a value of p - 0.05 were considered significant.

3. Results Comparison of coral branches before and after pretreatment to the aquarium conditions during 30 days Žfor Experiment 1., and during 90 days Žfor Experiment 2. did not

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show significant differences Ž p ) 0.05. in either chlorophyll concentration in zooxanthellae or zooxanthellae number in polyp tissue. Zooxanthellae sizes, PZF and DZF levels were changed insignificantly. Experiment 1. Transferring the corals from 95% to 30% PAR 0 resulted in an increase in zooxanthellae density by 80% on the 40th day of the experiment with no significant variation thereafter ŽFig. 1a.. The chlorophyll concentration calculated per 10 3 polyps increased significantly to the 40th day of the experiment and then remained unchanged. The chlorophyll concentration calculated per volume of zooxanthellae increased 1.5 times to the 10th day of the experiment. Zooxanthellae volume gradually decreased to

Fig. 1. S. pistillata. Changes in physiological parameters during 120 days of reacclimation Ža. from 95% to 30% PAR 0 ; Žb. from 30% to 8% PAR 0 ; Žc. from 30% to 0.8% PAR 0 ; Žd. control 30% PAR 0 ; Že. control 95% PAR 0 .

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Fig. 1 Ž continued ..

the end of the experiment. The proliferating zooxanthellar frequency ŽPZF. rapidly increased to the 10th day, and then gradually declined. The degrading zooxanthellae frequency ŽDZF. level dropped twofold by the 10th day. Transferring the corals from 30% to 8% PAR 0 resulted in the doubling of zooxanthellae densities by the 40th day of the experiment ŽFig. 1b.. The chlorophyll concentration per zooxanthellae volume increased by 80% by the 10th day of the experiment. The chlorophyll concentration calculated per polyp increased 2.5-fold also by the 10th day of the experiment, and then changed little. The average zooxanthella volume was signifi-

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Fig. 1 Ž continued ..

cantly reduced during the first half of the experiment and increased during the second half. Similarly, the PZF level dropped during the first half of the experiment and increased during the second half, approximating the initial level. The DZF level significantly decreased on the 20th day of the experiment and remained almost unchanged for following days ŽFig. 1b.. Transferring the corals from 30% to 0.8% PAR 0 showed considerably different results ŽFig. 1c. compared with the transfer to 30% and 8% PAR 0 . In low light, the

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zooxanthellae density fell 2.5 times by the 40th day. The zooxanthellae volume significantly declined by the 10th day of the experiment varying on subsequent days and gradually reducing by the end of the experiment. The chlorophyll concentration per polyp showed similar dynamics as the zooxanthellae densities. The chlorophyll concen-

Fig. 2. S. pistillata. Changes in physiological parameters within the first 8 days of reacclimation Ža. from 95% to 30% PAR 0 ; Žb. from 30% to 8% PAR 0 ; Žc. from 95% to 30% PAR 0 ; Žd. control 30% PAR 0 ; Že. control 95% PAR 0 .

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Fig. 2 Ž continued ..

tration in zooxanthellae also increased significantly by the 10th day of the experiment as in previous light treatment. The PZF level significantly decreased by the 20th day, and then remained almost unchanged. At the same time, the DZF level increased seven times by the 20th day and dropped to initial values by the 60th day of the experiment. The control variants Ž95% and 30% PAR 0 . showed fluctuations of measured parameters over time ŽFig. 1d, e.; however, differences were insignificant.

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Fig. 2 Ž continued ..

Experiment 2. Fig. 2a, b shows the results of some physiological changes in branches of S. pistillata during the first 8 days of acclimation to low light Žfrom 95% to 30% PAR 0 and from 30% to 8% PAR 0 .. Changes in these treatments were similar. Zooxanthellae densities significantly increased by the eighth day of the experiment. Pigment concentration in zooxanthellae significantly increased even by the second day and, on the fourth day, it was maximal Žincreased 2–2.5 times compared with initial. and remained almost unchanged for the next 4 days. The average size of zooxanthellae

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sharply reduced on the second day and then varied slightly. PZF level was increased threefold the day after transferring samples to dim light. At the same time, DZF level significantly dropped Žfrom 5.5% to 3.8%., and on the second day of the experiment, the DZF level fell to 0.5%. Further daily changes in the PZF and DZF levels showed a saw-edged curve with marked variability. With lowering light intensity from 30% to 0.8% PAR 0 ŽFig. 2c., the first 8 days of the experiment yielded no significant changes in zooxanthellae density. Dynamics of change in chlorophyll content calculated per polyp or per zooxanthellae volume were similar with that of previous light treatments. Changes in PZF and DZF levels on the first day of the experiment were also similar to those of previous light treatments. During the period from the third to the fifth day, changes in the PZF and DZF levels were insignificant and then, by the end of the experiment Žon the seventh day., the PZF level dropped, while the DZF level increased. The control branches Žunder 95% and 30% PAR 0 . showed slight daily changes, except for PZF and DZF levels, which varied considerably on a daily basis, mainly showing a saw-edged curve of daily changes ŽFig. 2d, e..

4. Discussion S. pistillata is able to acclimate to experimental changes in light intensities from 95% to 0.8% PAR 0 . Field investigations confirm that S. pistillata is able to dwell in both bright and extremely low light ranging from 100% to 0.5% PAR 0 ŽFalkowski and Dubinsky, 1981; Porter et al., 1984; Titlyanov and Latypov, 1991; Titlyanov et al., 1981, 2000a.. Field studies have also shown that acclimation responses to low light intensities include an enhancement of chlorophyll concentrations in zooxanthellae Že.g., Falkowski and Dubinsky, 1981. and an increase in zooxanthellae population densities Že.g., Titlyanov et al., 1981.. Porter et al. Ž1984. analysed a whole coral colonies of S. pistillata Žnot exterior branches as studied by Titlyanov et al., 1981. and concluded that there was no significant change in zooxanthellae density with decrease in light levels, also making the point that previous reports on changes in density were within the error limits of measuring cell density. On the basis of investigations by Porter et al. Ž1984., we can assume that exterior branches of shaded colonies contained higher zooxanthellae density than exterior branches from well-illuminated colonies. At the same time, interior branches of shaded colonies lost zooxanthellae because of extremely low light intensity invoked by self-shading. The latter was shown by analyses on four orders of branches from colonies of Pocillopora damicornis and P. Õerrucosa living in shaded habitats ŽTitlyanov et al., 1988.. In our experimental studies, chlorophyll concentration increased when light intensities were reduced to 0.8% PAR 0 , while zooxanthellae population densities increased when light intensities were reduced only to 8% PAR 0 . Under extremely low light intensities, the corals lost their zooxanthellae Žin spite of an increase in chlorophyll concentration in zooxanthellae., leading to a decrease in chlorophyll concentration calculated per polyp. These limits of reaction in coral adaptation to lowering light intensity were found here for the first time under experimental conditions. The decrease

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in zooxanthellae density under extremely low light intensity was found in the field. Dubinsky and Jokiel Ž1994. examined S. pistillata colonies in the Gulf of Eilat from 66-m depth, and found that zooxanthellae were only present in the upward facing portions of the colonies; there were no zooxanthellae in the downward facing portions. We also studied S. pistillata in the Gulf of Eilat and found that the upward facing portions of the colonies, taken from 2- to 3-m depth, had approximately 12 = 10 3 zooxanthellae per polyp, and about 25 = 10 3 zooxanthellae per polyp in colonies from 40-m depth. However, the downward facing portions of the colonies taken from 40 m supported only 11 = 10 3 zooxanthellae per polyp ŽTitlyanov et al., 2000a.. Corals acclimated to various light intensities contained zooxanthellae that significantly differed in size. Larger zooxanthellae were found in corals acclimated to extremely low light Ž0.8% PAR 0 .. Previously, Titlyanov et al. Ž2000a. showed that colonies S. pistillata from the Gulf of Eilat dwelling at 40-m depth Žlight intensity about 5% PAR 0 . also contained zooxanthellae of larger sizes. We assume two possible reasons of acclimation to large zooxanthellae sizes shaded sites: Ž1. reducing the light intensity to 30–5% PAR 0 led to a significant decrease in the frequency of division and degradation of zooxanthellae, thus increasing the average age of the zooxanthellae population density in the colony and resulting in an accumulation of old large cells; Ž2. if a coral colony contains a mixture of genetically different types of zooxanthellae ŽRowan, 1998. differing in sizes ŽTitlyanov et al., unpublished data., a decrease in light intensity can lead to an increase Žor retention. of one type of zooxanthellae with large cells. Small sizes of zooxanthellae under extremely low light Ž0.8% PAR 0 . probably reflect their slow growth in these conditions. However, we do not exclude possible changes in composition of different types of zooxanthellae. Differences in composition of genetically determined types ŽA, B, C. of zooxanthellae in variously illuminated colonies or in different portions of the corals Montastrea annularis and M. faÕeolata were shown by Rowan et al. Ž1997.. In our experiments on the dynamics of acclimation of the coral S. pistillata, the main changes in chlorophyll concentration of zooxanthellae occurred during the first 4 days under changing light regimes, while changes in zooxanthellae density occurred across 40 days. For these reasons, we presume that in the field the changes in physiological state of zooxanthellae and corals may occur in response to temporary changes in light conditions in the habitat: with the weather changes from dry to rainy season or from changes in water turbidity and coast flow Žsediments. or phytoplankton blooms. The response time for the new physiological state is within 4–6 weeks. Seasonal changes in coral physiology have also been reported ŽHayes and Bush, 1990; Yap et al., 1992; Jones and Yellowless, 1997. and appear highly dependent on light intensities. Our experiments showed that the increase in symbiont population density under shade Ž30% and 8% PAR 0 . was associated with significant increase in PZFrDZF ratio Žfrom 1.02 for initial samples to 1.29 by the 10th day of the experimental condition.. In the case of acclimation of corals to extremely low light intensity when zooxanthellae density significantly declined, the PZFrDZF ratio decreased markedly Žto - 1.0. during acclimation. When zooxanthellae population density was stabilized Ži.e. under complete acclimation., the ratio PZFrDZF approached 1.0. We conclude that with a decline in the light regime in the corals’ habitat, change in symbiont population density is regulated

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mainly by the rates of two processes: division and degradation of symbionts. It is likely that this mechanism of the regulation of zooxanthellae density in corals is universal. In previous studies, the same mechanism of regulation in zooxanthellae density took place during starvation of corals ŽTitlyanov et al., 1996. and under recovery feeding of corals with zooplankton ŽTitlyanov et al., 1999.. Only in shock situations, was the zooxanthellae population density regulated by expulsion of symbionts with endoderm of host cells ŽGates et al., 1992; Titlyanov et al,. 2000b.. The short-term dynamic experiments support this conclusion. Degradation and division rates responded on the first day after transplantation, and changes in pigment content in zooxanthellae, in most cases, were significant on the second day after transplantation. In all treatments with decreasing light intensity, corals responded by increasing cell division intensity, by decreasing intensity of symbiont degradation, reducing zooxanthellae sizes and increasing chlorophyll concentration in zooxanthellae. In corals transferred to dim light, the intensity of zooxanthellae division prevailed over their degradation indicating zooxanthellae accumulation in coral. With transfer to extremely low light, the zooxanthellae division also prevailed over their degradation within the first 5 days, and then the intensity of cell division declined, while zooxanthellar degradation increased and ratio PZFrDZF dropped to - 1.0. We detected sharp and immediate changes after transplanting the branches into different light regimes. Such changes also occur naturally, and daily, on coral reefs, for example, a cloudy day may follow a sunny day. Therefore, acclimation processes are continually adjusting to the external conditions.

5. Conclusion Acclimation of corals to low Ž30% and 8% PAR 0 . and to extremely low Ž0.8% PAR 0 . light began immediately after changing the light regime. Significant changes in Ža. the frequency of cell division and degradation and also in average zooxanthella size were detected the next day, Žb. chlorophyll concentration in zooxanthellae on the second day, and Žc. zooxanthellae population density on the eighth of the experiment. Considerable changes in pigment concentration in zooxanthellae were complete by the fourth day after changing the light regime, similarly for zooxanthellae number by the 40th day of the experiment. Acclimation of corals to low and extremely low light intensity yielded changes in zooxanthellae population density, which was mainly regulated by the differential rates for two processes: division and degradation of zooxanthellae.

Acknowledgements The Russian authors thank the President of the University of the Ryukyus, Professor Keishin Sunagawa, and the Director of the Tropical Biosphere Research Center of the Ryukyu University, Professor Kazunori Takano, for the invitation to work at Sesoko Station as visiting foreign researchers. Special thanks to Professor Minoru Murai, the scientific leader of the Marine Biological Station for care and help in fulfillment of

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experimental work. We are also grateful to all members of the Sesoko Station for use of facilities, technical help, hospitality, and convenience of research work. [SS]

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