Zvy Dubinsky Editors the World of Medusa and Her Sisters

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The Cnidaria, Past, Present and Future The world of Medusa and her sisters Corals and Light: From Energy Source to Deadly Threat 29

Zvy Dubinsky and David Iluz

Abstract The bathymetric distribution of reef-building, zooxanthellate corals is constrained by the attenuation of underwater light. The products of algal symbiont photosynthesis provide a major share of the energy, supporting the metabolic needs of the animal host. The two orders of magnitude in the underwater light field spanned by corals are overcome by photoacclimative responses of both the algae and the animal host. The corals decrease the photosynthetic fraction of their energy budget as light dims with depth, increasing their heterotrophic dependence on predation. In shallow water, corals are exposed to photodynamic dangers to which both host and symbiont are susceptible. These effects are mitigated by an array of antioxidative mechanisms that wax and wane in a diel periodicity to meet the concomitant fluctuation in oxygen evolution. The nocturnal tentacular extension seen in many corals is terminated at dawn by light, probably mediated by the photosynthesis of the zooxanthellae. The Goreau paradigm of “light-enhanced calcification” is summarized while recently documented exceptions are discussed. The role of light as an information source, besides its acknowledged role as an energy source, is evident in the poorly understood role of lunar periodicity in triggering the spectacular mass-spawning episodes of pacific corals. The characteristics of the underwater light field, its intensity and directionality, control the architecture of zooxanthellate coral colonies, favoring the optimization of the light exposure of the zooxanthellae. This rejview summarizes the main gaps in our understanding of the interaction of corals and light, thereby suggesting promising future research directions.

Keywords 0HOTOACCLIMATION s 56 s ,IGHT ENHANCED CALCIlCATION s 0HOTODYNAMIC DAMAGE s -OONLIGHT s 4ENTACLE EXTENSION s -ASS SPAWNING s :OOXANTHELLAE

29.1 The Bathymetric Distribution of Coral : $UBINSKY *) Reefs and Underwater Light 4HE -INA AND %VERARD 'OODMAN &ACULTY OF ,IFE 3CIENCES "AR )LAN 5NIVERSITY 2AMAT 'AN )SRAEL The relationship of coral reefs to depth and light has been e-mail: [email protected] suggested and documented as early as 1825 by Quoy and $ )LUZ *) Gaimard (1825), and there is a ﬁgure showing the parallel 4HE -INA AND %VERARD 'OODMAN &ACULTY OF ,IFE 3CIENCES course of light and reef development in a paper by Wells "AR )LAN 5NIVERSITY 2AMAT 'AN )SRAEL (1957) (Fig. 29.1). In general, in most locations, reefs decline 3CHOOL OF !GRICULTURE AND %NVIRONMENTAL 3TUDIES "EIT "ERL at depths close to the euphotic depth (z ), where the light #OLLEGE +FAR 3ABA )SRAEL eu e-mail: [email protected] intensity is down to 1 % of its subsurface values. However,

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Percentage of light from the surface 0 25 50 75 100

0 255075100 Light energy, g cal cm-2 h-1 Number of hermatypic coral species 0 15 30 45 60 75 90 105 120

75 Depth, m 90

105

120 Fig. 29.2 4HE ATTENUATION OF LIGHT IN THE WATERS OF THE 'ULF OF !QABA %ILAT .ORTHERN 2ED 3EA 4HE EUPHOTIC DEPTH OF SUBSURFACE IRRADIANCE 135 RANGES FROM A WINTER MINIMUM OF ^n M IN SUMMER

14 16 18 20 22 24 26 28 30 (Fricke et al. 1987 ABOUND AS DEEP AS M &IG 29.3). Temperature, ( °C) -OST OF THAT LIGHT LIMITED DISTRIBUTION IS ATTRIBUTABLE TO THE dependence of the coral animal host on the photosynthate 30 35 40 45 50 produced by the algal symbionts that decreases with depth, Oxygen, ml l-1 as is discussed in the following sections. This notion is in Fig. 29.1 The generalized bathymetric distribution of coral species AGREEMENT WITH -ORSE ET AL 1988 AND "ABCOCK AND -UNDY and of the environmental parameters temperature, oxygen, and irradi- (1996), who provided evidence of the ability of at least some ance. The numbers of coral species decrease concomitantly with light coral planulae to detect light directionality and intensity and ENERGY !FTER 7ELLS 1957)) settle accordingly, optimizing the underwater distribution of the light ﬁeld for symbiont photosynthesis. that cannot be translated into depth, since, depending on In a global survey of reefs, Bigot et al. () summa- water transparency, it may be anywhere from a few meters to rized as follows: “The number of coral species, their produc- WELL OVER M &OR INSTANCE IN THE WELL DEVELOPED REEFS OF tion, and growth rates decrease with depth, due to the THE 2ED 3EA THE EUPHOTIC DEPTH RANGES FROM A WINTER MINI- decreasing light levels. Therefore, coral species continue to MUM OF ^n M IN SUMMER &IG 29.2). This ﬂuctuation THRIVE UP TO IRRADIANCE LEVELS OF n REACHING A MAXI- is caused by the combination of reduced solar irradiance in MUM JUST BELOW THE SURFACE OF THE WATER !T LOWER IRRADIANCE winter and a seasonal increase in cloud cover, with nutrient- levels, some species such as with only 1 % of the surface driven proliferation of light-absorbing phytoplankton assem- light; but in this case, only small colonies develop and coral blages (Iluz et al. )N THE PAPER BY ,OYA AND 3LOBODKIN reefs are never formed.” In general, an array of photoaccli- (1971 DESCRIBING THE REEFS OF THE 'ULF OF !QABA %ILAT mative mechanisms, discussed below, enables zooxanthel- .ORTHERN 2ED 3EA REEF MORPHOLOGY AND DISTRIBUTION CHANGE late corals to exceed their respiration needs for substrate by WITH DEPTH BETWEEN ITS PEAK DISTRIBUTION AT n M PETERING products of photosynthesis at irradiances even below the OUT TOWARDS M ,OYA AND 3LOBODKIN 1971). Nevertheless, EUPHOTIC DEPTH $UBINSKY ET AL 3TAMBLER AND $UBINSKY isolated colonies and stands of Leptoseris hawaiiensis ).

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Fig. 29.3 Leptoseris hawaiiensis IN %ILAT 2ED 3EA ABOUNDS AS DEEP AS M 4HE PLANAR HORIZONTAL MORPHOLOGY IS CHARACTERISTIC OF DEEP WATER low-light corals

29.2 Zooxanthellae: Providers of Energy 29.3 Photoacclimation of the Zooxanthellae The term zooxanthellae for algal symbionts living within AQUATIC INVERTEBRATES WAS COINED BY "RANDT 1881), who docu- The capability of zooxanthellate corals to thrive over a bathy- MENTED THEIR PRESENCE IN SEVERAL AQUATIC INVERTEBRATE TAXA METRIC RANGE OF n M REQUIRES THEM TO BE ABLE TO COPE WITH (Fig. )N SUBSEQUENT EXPERIMENTS WITH STARVED ANEMONES an irradiance range from the intense sunshine at the reef table Brandt reached the conclusion that the animals obtained nutri- DOWN TO ^ OF THAT OR FOR EXAMPLE FROM TO μmole ment from the zooxanthellae when deprived of animal food QUANTA M−2.s−1. This is accomplished by a series of phenotypic, (Brandt 1881). The widespread distribution and role of the zoo- photoacclimative adjustments of the zooxanthellae, including xanthellae in corals were discussed in reviews by Yonge optical, photobiological, ultrastructural, biochemical, and (1931 $ROOP 1963 AND MORE RECENTLY BY 3TAMBLER A). physiological changes, similar to those reported for free-living These symbionts were isolated and cultured [e.g., for methods, PHYTOPLANKTON $UBINSKY ET AL 1986). These strategies and SEE -C,AUGHLIN AND :AHL 1959), and their taxonomy was MECHANISMS MITIGATE THE FOLD REDUCTION IN AVAILABLE SOLAR defined (e.g., Trench 1987 3UBSEQUENTLY IT WAS DISCOVERED energy, while preventing photodynamic damage to zooxan- THAT ZOOXANTHELLAE WERE AN ARRAY OF EIGHT CLADES ! ( DIFFER- thellae exposed to the full, near-surface intense insolation. The ing in their affinity to host species and their geographic and lRST IN THE SEQUENCE OF PHOTOACCLIMATIVE RESPONSES IS THE bathymetric distribution (for a detailed discussion, see, e.g., change in cellular pigment content, which ranged from 2 pg Baker (), Chen et al. (), Berkelmans and van Oppen CHLOROPHYLL IN SHALLOW WATER COLONIES OF THE COMMON 2ED 3EA ( ,AMPERT +ARAKO ET AL AND 3TAMBLER B)). coral Stylophora pistillata to 8 pg chlorophyll in dim-light Brandt’s suggestions regarding the role of zooxanthellae colonies Table 29.1 &ALKOWSKI AND $UBINSKY 1981). This AS A SOURCE OF FOOD FOR THEIR HOSTS WERE SUBSEQUENTLY CON- fourfold increase in pigmentation is accompanied by a confirmed in several studies [to mention just a few: Yonge COMITANT EXPANSION OF THE THYLAKOID SURFACE AREA REQUIRED FOR (1931), Odum and Odum (1955 AND -USCATINE ET AL 1983, accommodating the light-harvesting antennae and associated )]. In these studies, it was shown that high-energy prod- STRUCTURES $UBINSKY ET AL 1983) (Fig. 29.5). This phenotypic ucts of the photosynthesis of the zooxanthellae, including ACCLIMATION TOOK PLACE WITHIN WEEK WHEN HIGH LIGHTnACCLI- sugars, lipids, and amino acids, were “translocated” to their mated colonies were transplanted to low light. Interestingly, animal host (Pearse 1971 %DEN ET AL 1996; Titlyanov et al. THE CONVERSE TRANSPLANTATION n LOW TO HIGH LIGHT n FAILED AND $EPENDING ON CORAL SPECIES AND AS DISCUSSED BELOW resulted in colony mortality, until Cohen et al. () suc- also ambient light, the zooxanthellae may provide as much ceeded in such transplants, allowing a few weeks of acclima- AS OF THE RESPIRATORY REQUIREMENTS OF THE CORAL HOST tion at intermediate depths and irradiance levels. These studies (Falkowski et al. ). underscore the dangers facing corals that are acclimated to a

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Fig. 29.4 "RANDTS ORIGINAL PLATE SHOWING ALGAE SYMBIOTIC WITH DIVERSE AQUATIC INVERTEBRATES 4HE TERM ZOOXANTHELLAE APPEARED IN THAT PAPER (From Brandt 1881)

Table 29.1 High- and low-light acclimation in Stylophora pistillata OF SURFACE INTENSITY :OOXANTHELLAE HARVESTED FROM MEASURED CORAL SUR- ZOOXANTHELLAE !FTER &ALKOWSKI AND $UBINSKY 1981 3HALLOW WATER face were counted microscopically, to determine areal cell densities. HIGH LIGHT GROWING COLONIES (, OF S. pistillata compared to colonies From extracted chlorophyll and cell counts from the same colony sur- FROM DEEPLY SHADED CREVICES ,, WHERE IRRADIANCE AMOUNTED TO ^ faces, the cellular chlorophyll concentration was calculated Treatment μg chl a cm−2 6 cells cm−2 pg chl a cell−1 (, 3.6 ± 1.1 ,, ,,(, 3.9 1.1 3.7 low-light environment, poised to harvest as much light as pos- favus, Plerogyra sinuosa, and Goniopora lobata, it was evi- sible, when experimentally transplanted to high light. When dent that the levels of both enzymes closely followed the diel that happens, rates of photon harvesting vastly exceed those of light pattern in response to that of the photosynthetic activity their utilization, which is impeded by the relatively slow of the zooxanthellae (Fig. 29.6). The location of the zooxan- THROUGHPUT RATES VIA THE QUINONE POOL 5NDER SUCH A COMBINA- thellae inside the symbiosome organelle in the host tissue TION FREE RADICALS ARE GENERATED WITH DEADLY CONSEQUENCES 4O necessitated, in addition to the response of the algae, a host COUNTER THE DANGERS IMPOSED BY HIGH LIGHTnTRIGGERED FREE RADI- mechanism in order to avoid potential photodynamic damage. cals, both the zooxanthellae and the host corals developed an The results of photoacclimation include major differences in array of defenses, of which several have been described. These ϕ THE QUANTUM YIELD OF PHOTOSYNTHESIS RANGING FROM THE include the antioxidant enzymes catalase and superoxide dis- highest possible one mole of oxygen evolved (or CO2 assimi- MUTASE ,EVY ET AL ). In these studies of the corals Favia lated) for 8 mol of photons absorbed (ϕ = 1/8) in corals grow-

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Fig. 29.5 (a) Transmission electron micrograph of zooxanthellae from cell is occupied by thylakoid membranes, intercepting virtually every high-light Stylophora pistillata. Note the photoprotective carotenoid PHOTON $UBINSKY ET AL 1983). Corals as in Table 29.1. The diameter of globules and the paucity of thylakoids. (b %LECTRON MICROGRAPH OF ZOO- THE ZOOXANTHELLAE IS ^ μm xanthellae from low-light S. pistillata. The entire cross-section of the

ING AT DIM μMOLES QUANTA M−2s−1 to ϕ ^ IN SHALLOW WATER ). This results in a significant shift from near-energy HIGH LIGHT COLONIES $UBINSKY ET AL ). The change in pig- autotrophy in the high-light colonies to predominant depen- mentation resulted in the corresponding four to fivefold differ- dence on heterotrophic zooplankton predation for most of ences in areal chlorophyll concentrations (Table 29.1) and in their energy budget (Fig. 29.9). However, surprisingly, the COLONY ABSORPTIVITY RANGING FROM TO IN HIGH LIGHT high-light colonies of virtually all zooxanthellate corals ivory-colored colonies to ~95 % in nearly black-shaded ones invest structures and energy, a costly effort to capture zoo- (Fig. 29.7 )T IS NOTEWORTHY THAT 2ED 3EA ZOOXANTHELLATE CORALS plankton, as can be seen in their abundant tentacles armed display a strong hysteresis pattern (Fig. 29.8), whereby after- with stinging cells, extended at sunset for the ensuing night- noon values were significantly higher than morning ones for time emergence of the vertically migrating zooplankton THE SAME IRRADIANCE LEVELS ,EVY ET AL ). This phenome- (Lobophyllia, Favia). Thus, under low light, corals depend NON EVEN THOUGH UBIQUITOUS DOES NOT YET HAVE A SATISFACTORY on capturing zooplankton as a source of energy to supple- explanation. ment the meager trickle provided by the light-limited 7HILE THE MULTIPLE EFFECTS OF 56 RADIATION ARE OUTSIDE THE ZOOXANTHELLAE 5NDER HIGH LIGHT THE SITUATION IS REVERSED scope of the present review, Cohen et al. () found that there, corals rely on zooplankton as a source of nutrients, 56 ACCELERATES PHOTOACCLIMATION PROCESSES IN CORALS IN WAYS such as nitrogen, to match the abundant flux of otherwise similar to those of the effects of light. “empty” carbon, of “junk food” provided by the photosynthetic activity of the algal symbionts, and to satisfy the uni- VERSAL 2EDlELD RATIOS ALLOWING GROWTH &ALKOWSKI ET AL 29.4 Light and Trophic Status of Corals , 1993). Indeed, the light-dependent difference in trophic status between corals living under high light, that are The abundant light available to the high-light colonies of S. predominantly autotrophic, and low light colonies, which pistillata AND THE HIGH CONCENTRATIONS OF 2U"IS#O &ISHER depend on, predation on zooplankton, was demonstrated by et al. 1989 MORE THAN COMPENSATE FOR THEIR LOW QUANTUM -USCATINE AND +APLAN ). These authors demonstrated YIELD AND FOR USING LIGHT hWASTEFULLYv (ENCE THE HIGH LIGHTn that difference between dependence on photosynthesis and acclimated colonies of that coral provide translocated photo- on predation, using ratios of stable isotopes of nitrogen. That SYNTHATES AMOUNTING TO ^ OF THE METABOLIC REQUIREMENTS difference between predominantly autotrophic shallow- of the coral holobiont (host and symbionts) against only water corals and deep-water ones feeding on zooplankton, SOME IN THE MESOPHOTIC COLONIES &ALKOWSKI ET AL was confirmed (based on C chromatography) by Titlyanov

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Fig. 29.6 4HE DIEL LEVELS OF THE ANTIOXIDANT ENZYME 3/$ IN THE CORALS lowed the diel light pattern, in response to that of the photosynthetic Favia favus, Plerogyra sinuosa, and Goniopora lobata, in both host and ACTIVITY OF THE ZOOXANTHELLAE !FTER ,EVY ET AL ) zooxanthellae. It is evident that the levels of the enzyme closely fol-

et al. (). This divergence was also evident in the high 29.5 Colony Morphology C:N ratios of high-light corals compared to lower ones in DEEP WATER COLONIES 2AHAV ET AL 1989). It is noteworthy that Coral colonies are known for their plasticity, which posed dif- THE RESIDENCE TIME OF CARBON ACQUIRED BY THE ZOOXANTHELLAE ficulties in their taxonomy, as was already pointed out by and translocated to animal hosts is significantly shorter than Bernard ( AND DISCUSSED IN DETAIL BY 6ERON 1995). This that stemming from predation on zooplankton. The photo- phenotypic variability is controlled by the following environ- synthetically derived carbon is readily and primarily used by mental forces: light, current (Chindapol et al. ), and grav- the animal host as a substrate for respiration, while that ITY -EROZ ET AL ), with light playing the main role (Graus obtained from prey digestion is incorporated in cellular AND -AC)NTYRE 1976). The effect of light is a dramatic flatten- structures (Bachar et al. ). ing of subspherical colonies (Fig. ) and a horizontal fan-

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Fig. 29.7 High- and low-light colonies of Stylophora pistillata WITH ABSORPTIVITY RANGING FROM TO IN THE HIGH LIGHT IVORY COLORED COLONIES to ~95 % in the nearly black-shaded ones

Fig. 29.8 2ED 3EA 0.12 zooxanthellate corals morning display a strong hysteresis pattern, 0.1 after noon whereby for the same irradiance levels, afternoon values were 0.08 -1 signiﬁcantly higher g than the morning ones -1 !FTER ,EVY ET AL ) 0.06 hour 2

mg o 0.04

0.02

0 -100 100 200 300 400 500

-0.02

-0.04 mmol photonsI m-2sec-1 ning of rounded, branching species (Fig. 29.11). This change average light intensity than that impinging on a ﬂat area, in colony architecture results in a dramatic reduction in the thereby avoiding potential high-light damage. The horizon- ratio between live tissue and harvested light, expressed as tally ﬂattened architecture characteristic to low-light colonies reduction in the height-to-diameter ratio of S. pistillata colo- ascertain the opposite, i.e., the live-tissue area is similar to the NIES [-ASS ET AL %INBINDER ET AL ). The amount of optical cross section of the colony, namely, the shadow cast by light available for the photosynthetic activity of a zooxanthel- it, maximizing access of the algal symbiont to much of the dim late, shallow water colony is ‘diluted’ over a large branched or light reaching the colonies. The response of corals to trans- spherical tissue area, exposing the zooxanthellae to a far lower plantation between light extremes results in dramatic reorgani-

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Fig. 29.9 -ODEL OF CARBON ENERGY mOW AND BUDGET IN CORALS synthesis, Tc = carbon translocated from zooxanthellae to animal, Δz = expressed in mg carbon per cm−2 PER DAY (, CORALS SHOULD HAVE NO GROWTH OF ZOOX BIOMASS 2Z RESPIRATION OF ZOOX Δs = skeletal Δ need for predation (left IN CONTRAST TO ,, CORALS right), which have to growth, ! GROWTH OF ANIMAL 2! RESPIRATION OF ANIMAL 0$ $# CAPTURE ZOOPLANKTON ://0 AS A SOURCE OF ENERGY :B = biomass of PARTICULATE AND DISSOLVED ORGANIC CARBON 2C RESPIRATION OF CORAL HOLO- zooxanthellae (zoox), B! = biomass of animal host, PG = gross photo- BIONT !FTER &ALKOWSKI ET AL ))

Fig. 29.10 The effect of low light is a dramatic ﬂattening of subspherical colonies. $EEP Platygyra colony from the submarine 9AGO AT ^ M DEPTH

zation of the growth patterns, as shown in the reciprocal bottom, they were a clone, with the same genetic constitution transplantation experiments on Montipora verrucosa in showing the large range of phenotypic plasticity. Hawaii (Fig. 29.12), where, within 3 months, the low-light, ! PARALLEL mATTENING RESPONSE IS EVIDENT IN 2ED 3EA S. pis- horizontal, flat colony transferred to high light ‘sprouted’ an tillata COLONIES ALONG A DEPTH GRADIENT -ASS ET AL ) as UPRIGHT BRANCHING GROWTH !N OPPOSITE RESPONSE WAS SEEN IN they flatten in response to the decrease in irradiance (Fig. the high-light colony that developed a horizontal, flat ‘shelf’ colonies (29.13). In experiments where both water flow and FOLLOWING ITS TRANSPLANTATION TO LOW LIGHT 3INCE BOTH COLONIES irradiance were manipulated experimentally, the dominance were originally taken from a massive colony spread out verti- of light was evident in controlling colony modifications cally from a high-light upper part to a dim-light region at its 3HWARTSBERG ET AL ).

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avoid diurnal ﬁshes that prey on coral tissue and tentacles. Besides these goals, the extension of tentacles vastly increases the exposed surface of the corals and allows tissue oxygen- ation at night, while controlling algal exposure to light and, by THAT REGULATING OXYGEN EVOLUTION RATES !NY ILLUMINATION OF A coral at night, while its tentacles are extended, causes a tentacle contraction response. If a single polyp is illuminated, it contracts, and the contraction spreads within minutes through- OUT THE COLONY 5SING MONOCHROMATIC LIGHT ,EVY ET AL ) illuminated single polyps of Favia favus at night, when the tentacles of the entire colony were extended, and documented the spectrum of the tentacles’ withdrawal (Fig. 29.17). It turned out that the response was similar to the spectral response of photosynthesis, leading the authors to suggest that the response of the host was mediated by the photosynthesis of the zooxanthellae that oxygenated the animal tissues or changed their pH. This view is supported by the lack of response to illumination of the azooxanthellate coral Cladopsammia sp. (Fig. 29.18), whose tentacles remain constantly extended and Fig. 29.11 Stylophora pistillata AT M COLLECTED BY THE SUBMARINE Yago. The fan-shaped, horizontally ﬂattened colony architecture is it does not respond to light induced tentacle closure. typical of low-light environments

29.8 Light Enhanced Calcification (LEC) 29.6 Host Factor and Light Based on the convincing evidence of stimulation of calcifica- There is ample proof that in the cells of the coral animal, there tion by light, Yonge (1931 AND +AWAGUTI AND 3AKUMOTU are compounds that accelerate, facilitate, or stimulate the secre- () already suggested a causative relationship between tion, excretion, or leakage of photosynthate from the zooxan- the photosynthetic activity of the zooxanthellae and coral thellae to the host. These were termed collectively “host factor” growth. This relationship is clearly evident whenever the diel (& OR hHOST RELEASE FACTORv (2& -ALKIN ET AL 1996; course of both processes is examined (Barnes and Chalker -USCATINE 1967; Grant et al. ; Biel et al. ). They dif- -ASS ET AL ), with a diurnal peak of calcification fer in composition, show species-specificity, and vary in the around noon and its cessation at night, occasionally even translocated compounds. However, it turns out that the light accompanied by some skeletal dissolution tracking night- history of the zooxanthellae determines the sensitivity or time respiration (Fig. 29.19). When Goreau (1959) and responsiveness of zooxanthellae to HF presence. In S. pistil- Goreau and Goreau (1959), using Ca and C radioisotopes, lata, nutrient-limited, high-light zooxanthellae readily showed the correlation between the diel patterns of the pho- responded to the host homogenate by releasing ~2.5 times tosynthetic activity of the zooxanthellae and that of the light- more C-labeled photosynthate than the controls kept in sea- enhanced calcification of the coral, it became a nearly water (Fig. ). However, zooxanthellae freshly isolated UNIVERSALLY ACCEPTED PARADIGM %XPLANATIONS OF THAT PHE- FROM MnDEEP SHADE ACCLIMATED COLONIES WHICH WERE RELA- NOMENON WERE SUMMARIZED BY 0EARSE AND -USCATINE 1971). tively nutrient-replete due to the limited light-driven carbon 5SING C-labeling, these authors demonstrated the contribu- influx, showed no response to the host homogenate (Fig. 29.15). tion of photosynthates such as glycerol, lipids, and various amino acids ‘translocated’ to the host, to the calcification PROCESS !DDITIONAL SUPPORT FOR THE IMPORTANCE OF PRODUCTS OF 29.7 Tentacle Expansion algal photosynthesis was offered by Crossland and Barnes (), who claimed that algal photosynthesis provides -ANY CORALS EXPAND THEIR TENTACLES AT DUSK AND THESE REMAIN ENERGY THAT IS !40 GENERATED ACCORDING TO A SCHEME THEY extended until sunrise (Fig. 29.16 of Plerogyra sinuosa, Favia suggested, through the citrulline-ornithine pathway. Pearse favus, and Lobophyllia corymbosa). However that behavior AND -USCATINE 1971) also acknowledged the effect of sym- weakens under dim light, and deep-water corals may remain biont photosynthesis, namely, that the removal of CO2 raises with partially extended tentacles at all times. It seems that the the pH, thereby facilitating calcification according to the daytime extension serves a few purposes: it aims to capture EQUATIONS PROPOSED BY 'OREAU 1959) and reevaluated by demersal zooplankton during their nocturnal raise, and to Gattuso et al. (1999 AND !LLEMAND ET AL ). This aspect

[email protected] Fig. 29.12 High-light (a) profusely branched, upper part of a following 3 months after transplantation to high light. Note the vertical Montipora verrucosa colony in Hawaii; (b) lower part, ﬂat, horizontal, branch; (d) High-light colony of the same species after 3 months at low shaded part of the same colony; (c $EEP WATER M. verrucosa colony light, showing the development of a ﬂat, horizontal growth

Fig. 29.13 !S irradiance decreases OPEN SQUARES n 0!2 THE COLONIES OF the coral S. pistillata became progressively flattened with the diameter/height ratio (filled circles) changes from ~1 in the high light subspherical colonies to ~5 in flatttened, fan-shaped low-light, deep-water COLONIES !FTER -ASS et al. )

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Fig. 29.14 The test for the “host factor”. The coral tissue is removed from the skeleton, the homogenate is centrifuged, and the algae are separated from the host homogenate. The zooxanthellae are incubated in the light with C, and SUBSEQUENTLY INCUBATED in the dark with the animal homogenate, and with seawater as a control. The percentage of C excreted in the dark is determined

Fig. 29.15 The host-factor effect on excretion of C-labeled photosynthate. Blue (, zooxanthellae from M μMOLE Q M−2 s−1. Red ,, zooxanthellae from M μMOLE Q M−2 s−1 %XCRETION IN seawater is taken as !FTER $UBINSKY et al. 1986). Only the zooxanthellae from the high-light coral responded to the host homogenate by increased excretion

2++ has been studied in great detail by several researchers and Calcification Ca+−>+ CO23 CaCO2 H reviewed by Barnes and Chalker ( AND %REZ ET AL () in relation to seawater chemistry, and it is continu- Or, conversely, that calcification actually lends support to ously being reexamined and refined (Jokiel ). However, photosynthesis by releasing CO2 by a process called THE EQUATIONS OF CALCIlCATION AND PHOTOSYNTHESIS CAN BE “transcalcification”: interpreted as indication that the two processes compete for 2+ Ca+−>++2 HCO33 CaCO CO22 H O, CO2: PROPOSED BY -C#ONNAUGHEY AND 7HELAN 1997). This hypoth-

Photosynthesis CO22+−>+ H O CH 2 O O 2 ESIS HAS SINCE BEEN REJECTED BY MOST WORKERS !LLEMAND ET AL

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Fig. 29.16 ,IGHT CONTROL OF TENTACLE EXPANSION IN THE 2ED 3EA CORALS Favia favus (a, b), Pleurogyra sinuosa (c, d), and Lobophylia corymbosa (e, f IN THE 2ED 3EA Left, daytime, tentacles retracted; Right, at night, tentacles expanded

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30 0.20 25 0.15 20 15 0.10 10 0.05 5

0 0 Algae absorbance Response time (min) 350 400 450 500 550 600 650 700 750 Wavelength (nm)

Fig. 29.17 4HE TIME REQUIRED FOR TENTACLE WITHDRAWAL IN Favia favus Comparison of the action spectrum of F. favus tentacle contraction to (ﬁlled circles) following illumination of a spot, as a function of the light the light spectrum absorbed by the zooxanthellae at an irradiance level wavelength. That action spectrum closely resembles the absorptance of OF μMOL QUANTA M S ,EVY ET AL ) the zooxanthellae (open squares 6ALUES ARE MEANS 3$ .

enhancement of calcification rates is, paradoxically, greatest in the algae- poor tips of branches.” This dilemma is evident in most fast- growing, branched corals as well as in the zooxanthellate hydrocoral Millepora dichotoma (Fig. ). Based ON THEIR DOUBLE LABEL EXPERIMENTS WITH #ALCIUM AND #ARBON THEY SUGGESTED n AS A SOLUTION TO THAT DILEMMA n that light enhancement of calcification in the algae-poor tip results from photosynthesis by zooxanthellae further down the branch. Fang et al. (1989) also raise the same issue, suggesting that the support of calcification by symbiont photosynthesis is based on spatial separation between the sites where photosynthesis and calcification take place and the products of photosynthesis reach the calcification sites. Further difficulties emerged upon examination of cases where no clear support of Fig. 29.18 4HE AZOOXANTHELLATE 2ED 3EA CORAL Cladopsammia sp. does not respond to light stimulation calcification by photosynthesis could be detected, for instance, under dim light, as light does stimulate calcification but with NO QUANTITATIVE CORRELATION -ASS ET AL , Fig. 29.21). 3CHNEIDER AND %REZ ) report yet another difficulty 4HE CURRENT SITUATION REGARDING ,%# IS SUCCINCTLY SUMMA- IN THE ,%# PARADIGM THEY WERE ABLE TO INCREASE CORAL CALCIl- RIZED BY !LLEMAND ET AL ): “…at the macroscale level, it cation rates by manipulating water chemistry but failed to see is most probable that zooxanthellae enhance calcification any concomitant increase in zooxanthellate photosynthesis. under light conditions, at the microscale level many studies !N INTERESTING ASPECT OF THE LINK BETWEEN PHOTOSYNTHESIS AND have to be performed in order to understand how zooxanthel- calcification got support from the results of Goffredo et al. LAE PLAY A ROLE IN ,%#xv 4HEY CONTINUE TO JUSTIFY THEIR CON-

(), working on the Panarea CO2 vent. They showed that clusion: “calcification itself is still a black box” and “we have the zooxanthellate coral Balanophyllia pruvoti is more toler- to admit that the major steps of coral calcification remain to ant of ocean acidification than the azooxanthellate species be discovered”. Obviously the relationship of light and coral Astroides calycularis and Leptopsammia pruvoti. species calcification still remains a main challenge for future research. Astroides calycularis and Leptopsammia pruvoti !N ADDI- tional proposed contribution of algal metabolism to calcification is the removal of phosphate that interferes with the 29.9 Internal Light Gradients Within FORMATION OF THE SKELETAL ARAGONITE CRYSTALS 3IMKISS ). Coral Colonies 3EVERAL STUDIES HAVE BEEN EXAMINING VARIOUS FACETS OF THE relationship between symbiont photosynthesis and coral calci- !LREADY 3HIBATA AND (AXO 1969) examined the millimeter lCATION PROGRESSIVELY ADDING TO THE CELLULAR 3CHNEIDER AND scale of light penetration into the massive coral Favia, and %REZ ; Holcomb et al. ); and chemical (Jokiel described the resulting layering of the algal symbionts ) aspects of the relationship between the two concomi- (Fig. 29.22), as well as the underlying stratum of the boring tant processes. Nevertheless, the theory is not without theo- Chlorophyte Astreobium. With the advent of spectral micro- RETICAL DIFlCULTIES 0EARSE AND -USCATINE 1971 STATE h,IGHT sensors such analyses became far more rigorous and detailed

[email protected] 482 Z. Dubinsky and D. Iluz

Fig. 29.19 $IEL COURSE OF CALCIlCATION VS LIGHT AND PHOTOSYNTHESIS enhanced calcification paradigm. Both calcification and photosynthesis (PN NET PHOTOSYNTHESIS 0!2 PHOTOSYNTHETIC AVAILABLE RADIATION FOLLOW THE PATTERN OF LIGHT BUT WITH A DELAY $URING THE NIGHT BOTH !FTER -ASS ET AL ). Both photosynthesis and calcification follow respiration and some skeletal dissolution are evident the diel pattern of irradiance intensity, clearly supporting the light

(Kuhl et al. 1995). Furthermore, these tools allowed relating the depth profiles of light intensity and its spectral distribution to the concomitant photosynthesis profile (Fig. 29.23). 4HAT STUDY AND SUBSEQUENT WORKS 7ANGPRASEURT ET AL ; 2OTH ; Fig. -ARCELINO ET AL ) underscore the limitations and over simplification inherent in the stan- dard practice of studying coral photobiology nearly exclu- sively in relation to the light impinging on the coral surface )LUZ AND $UBINSKY ! FURTHER ATTEMPT TOWARDS A microscale charting of the internal light fields within coral skeletons was accomplished by applying fractals to the task -ARCELINO ET AL ). However, the interesting realization that skeletal elements function as light guides has yet to be linked to the concomitant, detailed spatial resolution of the photosynthesis of zooxanthellae.

29.10 Light and Reproduction

The reproductive activities of several corals, including both Fig. 29.20 The hydrocoral Millepora dichotoma shows the pattern broadcasting and brooding species, are synchronized with typical to corals, where the fastest growing tips lack zooxanthellae lunar phases (Fig. 29.25a !TODA ) timed the spawning of Pocillopora damicornis TO NIGHTS n OF THE LUNAR MONTH This author listed additional species that correspond to that PEAKING ON THE EIGHTH EVENING AFTER THE !UGUST FULL MOON pattern, which also coincides with the spectacular mass This event occurs with extraordinary consistency and is pre- SPAWNING OF MOST CORAL SPECIES ON THE !USTRALIAN 'REAT "ARRIER dictable to within a few minutes from year to year”. Based 2EEF '"2 (OWEVER SOME '"2 SPECIES AS WELL AS 2ED 3EA on currently available information, we may summarize that CORALS SPAWN AT NEW MOON :AKAI ET AL ; Fig. 29.25b). the timing of coral spawning during the year, in terms of Harrison and Wallace ) review the above patterns, as well months, is determined by seasonal patterns such as tempera- as such differing from the seemingly predominant one. ture and food availability, on which gonad maturation 6IZE ET AL REPORT THAT h)N THE 'ULF OF -EXICO CORALS depends. However the remarkably precise timing within the undergo mass spawning on just one or two nights per year, month, even though variable among species and localities, is

[email protected] 29 Corals and Light: From Energy Source to Deadly Threat 483

Fig. 29.21 The .6 relation between calciﬁcation and

PHOTOSYNTHESIS AT M )

(green) and at 65 m -2 (pink IN THE 2ED 3EA cm coral S. pistillata. 7HILE AT M THERE IS A -1 .4 clear stoichiometric I h 3 relationship between the two processes, no such correlation is evident under dim light

!FTER -ASS ET AL ) mol CaCo

μ .2

Calcification ( 0.0 10m Feb Rsqr = 0.97, a =0.88 65m Feb Rsqr = 0.03, a =0.11

0.0 .2 .4 .6 μ -2 -1 Photosynthesis ( mole o2 cm h )

Fig. 29.22 ! SECTION through the coral Favia pallida &ROM 3HIBATA and Haxo 1969). (B The tissue layer containing the zooxanthellae; W white skeletal zone; G green layer of the boring ﬁlamentous alga Ostreobium reineckei layer)

correlated to the lunar phases, probably mediated by crypto- by discrete optical components of early nocturnal illumina- CHROMES ,EVY ET AL ), in ways yet to be elucidated. tion”. Nevertheless, the widely accepted lunar control dogma While the date of spawning is set by the lunar cycle, the is far from universally accepted. Brady et al. (), work- HOURMIN OF SPAWNING IS SET BY THE SPECTRAL QUALITY OF LIGHT ing in the laboratory with Montastrea franksi indicate that around sunset. Boch et al. ( AND 3WEENEY ET AL ) spawn timing is not controlled by a circadian rhythm and show that shifts in twilight color and intensity on nights both that it is directly controlled by local solar light cycle. within and between evenings, immediately before and after !LTERNATIVE EXPLANATIONS BASED ON REGIONAL DIFFERENCES IN the full moon, are correlated with the observed times of syn- wind patterns were also suggested (van Woesik ). chronized mass spawning, and that these optical phenomena The notion that the lunar control of coral reproduction are a biologically plausible cue for the synchronization of is somehow synchronized by light is supported by the these mass spawning events. That view is supported by Boch documented interference of coastal “light pollution” with et al. () who conclude that “spawning synchrony on a the patterns of coral reproduction (Jokiel et al. 1985). particular lunar night and speciﬁc time of night is a threshold In summary, the cellular mechanisms responsible for the response to differential periods of darkness after twilight that lunar light triggering and timing of coral reproduction still is primarily inﬂuenced by lunar photoperiod and secondarily await further research and elucidation.

[email protected] 484 Z. Dubinsky and D. Iluz

Fig. 29.23 Photosynthesis Photosynthesis (nmol O2 cm-3 s-1) (bars), O2 and pH in the TISSUE OF !CROPORA SP FROM 0 20406080100 5 to 6 m water depth. Incident photon irradiance n NM WAS -0.5 O pH 535 μMOLE QUANTA M S 2 (From Kuhl et al. 1995) 0.0

0.5 Depth (mm)

1.0

0 100 200 300 400 500 600

O2 (μM)

7.6 7.8 8.0 8.2 8.4 pH

Fig. 29.24 ,IGHT dynamics in the CORALnALGAL SYMBIOSIS (1 $OWNWELLING SUNLIGHT ,IGHT NOT absorbed by the coral or Symbiodinium is (2) reflected by the coral skeleton, and (3) enters the porous skeleton, re-emerging as diffuse reflectance. The multiple scattering by the skeleton amplifies the light Symbiodinium is exposed to (From 2OTH )

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Fig. 29.25 a &ROM :AKAI ,UNAR PERIODICITY OF PLANULAE RELEASE BY :AKAI ET AL ). (a) Boch et al. () show corals spawning, based Stylophora pistillata COLONIES MAINTAINED IN THE LABORATORY IN %ILAT ON DATA POOLED FROM SEVERAL CORAL SPECIES PEAKING ON NIGHTS n AFTER .ORTHERN 2ED 3EA PEAKING ON NIGHT AFTER FULL MOON .UMBERS ON THE the full moon. That pattern is similar to the planulae released by S. y axis representing the total number of planulae released each lunar pistillata in relation to the lunar cycle (b) NIGHT $ATA WERE POOLED FROM THREE LUNAR CYCLES DURING !FTER

"ERKELMANS 2 VAN /PPEN -*( 4HE ROLE OF ZOOXANTHELLAE IN THE 29.11 Conclusions thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an ERA OF CLIMATE CHANGE 0ROC 2OYAL 3OC "IOL 3CI n The main foci for future research in the vast ﬁeld of coral "ERNARD (- 4HE SPECIES PROBLEM IN CORALS .ATURE photobiology are likely to be the following: "IEL +9 'ATES 2$ -USCATINE , %6ECTS OF FREE AMINO ACIDS ON the photosynthetic carbon metabolism of symbiotic dinoXagellates. 2USS * 0LANT 0HYSIOL n 1. Furthering the molecular, chemical and cellular mecha- "IGOT , #HABANET 0 #HARPY , #ONAND # 1UOD * 0 4ESSIER % NISMS UNDERLYING ,%# #$2/- h3UIVI DES 2ÏCIFS #ORALLIENSv 02% #/)5% %LUCIDATING THE PATHWAY LINKING THE LIGHT REGIME TO CORAL "OCH #! !NANTHASUBRAMANIAM " 3WEENEY !- $OYLE &* RD -ORSE $% %FFECTS OF LIGHT DYNAMICS ON CORAL SPAWNING SYNCHRONY colony architecture. "IOL "ULL n 5NDERSTANDING THE MODE OF ACTION OF LUNAR LIGHT ON CORAL "RADY !+ (ILTON *$ 6IZE 0$ #ORAL SPAWN TIMING IS A DIRECT reproductive temporal patterns. response to solar light cycles and is not an entrained circadian -APPING THE INTERNAL LIGHT lELDS WITHIN CORAL SKELETONS RESPONSE #ORAL 2EEFS n "RANDT + ÃBER DAS :USAMMENLEBEN VON 4HIEREN UND !LGEN and their physiological effects 6ERH 0HYSIOLOGISCHER 'ES nn #HEN #! 9ANG 97 7EI .6 4SAI 73 &ANG ,3 3YMBIONT diversity in scleractinian corals from tropical reefs and subtropical NON REEF COMMUNITIES IN 4AIWAN #ORAL 2EEFS n #HINDAPOL . +AANDORP *! #RONEMBERGER # -ASS 4 'ENIN ! References -ODELLING GROWTH AND FORM OF THE SCLERACTINIAN CORAL POCILLOPORA VERRUCOSA AND THE INmUENCE OF HYDRODYNAMICS 0,O3 #OMPUT "IOL !LLEMAND $ 4AMBUTTE % :OCCOLA $ 4AMBUTTE 3 #ORAL CALCIl- E CATION CELLS TO REEFS )N $UBINSKY : 3TAMBLER . EDS #ORAL REEFS #OHEN ) $ISHON ' )LUZ $ $UBINSKY : 56 " AS A PHOTOACCLI- AN ECOSYSTEM IN TRANSITION 3PRINGER 3CIENCE .EW 9ORK matory enhancer of the hermatypic coral Stylophora pistillata. PP n /PEN * -AR 3CI n !TODA + 4HE LARVA AND POSTLARVAL DEVELOPMENT OF SOME REEF #ROSSLAND #* "ARNES $* 4HE ROLE OF METABOLIC NITROGEN IN CORAL BUILDING CORALS ) 0OCILLOPORA DAMICORNIS CESPITOSA $ANA 3CI 2EP CALCIlCATION -AR "IOL n 4OHOKU 5NIV 3ER n $ROOP -2 !LGAE AND INVERTEBRATES IN SYMBIOSIS )N .UTMAN "ABCOCK 2# -UNDY #. #ORAL RECRUITMENT CONSEQUENCES OF 03 -OSSE " EDS 3YMBIOTIC ASSOCIATIONS SYMPOSIUM SOCIETY GEN- settlement choice for early growth and survivorship in two sclerac- ERAL MICROBIOLOGY VOL #AMBRIDGE 5NIVERSITY 0RESS ,ONDON TINIANS * %XP -AR "IOL %COL n PP n "ACHAR ! !CHITUV 9 0ASTEMAK : $UBINSKY : !UTOTROPHY VER- $UBINSKY : &ALKOWSKI 0' 3CHARF $ !SPECTS OF ADAPTATION OF sus heterotrophy: the origin of carbon determines its fate in a sym- hermatypic corals and their endosymbiontic zooxanthellae to light. BIOTIC SEA ANEMONE * %XP -AR "IOL %COL n "ULL )NST /CEANOGR &ISH n "AKER !# &LEXIBILITY AND SPECIlCITY IN CORALnALGAL SYMBIOSIS $UBINSKY : &ALKOWSKI 0' 0ORTER *7 -USCATINE , !BSORPTION DIVERSITY ECOLOGY AND BIOGEOGRAPHY OF 3YMBIODINIUM !NNU 2EV and utilization of radiant energy by light-and shade-adapted colo- %COL 3YST n nies of the hermatypic coral Stylophora pistillata 0ROC 2 3OC "ARNES $* #HALKER "% #ALCIlCATION AND PHOTOSYNTHESIS IN REEF ,ONDON "n BUILDING CORALS AND ALGAE )N $UBINSKY : ED #ORAL REEF ECOSYS- $UBINSKY : &ALKOWSKI 0' 7YMAN + ,IGHT HARVESTING AND UTI- TEMS ECOSYSTEMS OF THE WORLD VOL PP n LIZATION IN PHYTOPLANKTON 0LANT #ELL 0HYSIOL n

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%DEN .) "IL &+ 4ITLYANOV % $UBINSKY : 0HOTOSYNTHETIC +AWAGUTI 3 3AKUMOTO $ 4HE EFFECT OF LIGHT ON TI ME CALCIUM CAPACITY AND COMPOSITION OF # lXATION PRODUCTS IN SYMBIOTIC DEPOSITION OF CORALS "ULL /CEANOGR )NST 4AIWAN n ZOOXANTHELLAE OF 3TYLOPHORA PISTILLATA IN VIVO UNDER DIFFERENT LIGHT +UHL - #OHEN 9 $ALSGAARD 4 *ORGENSEN "" 2EVSBECH .0 AND NUTRIENT CONDITIONS )N 3TEINBERGER 9 ED 0RESERVATION OF OUR -ICROENVIRONMENT AND PHOTOSYNTHESIS OF ZOOXANTHELLAE IN SCLERAC- WORLD IN THE WAKE OF CHANGE VOL !" )3%%13 0UBLICATION tinian corals studied with microsensors for O2 P( AND LIGHT -AR *ERUSALEM PP n %COL 0ROG 3ER n %INBINDER 3 -ASS 4 "ROKOVICH % $UBINSKY : %REZ * 4CHERNOV $ ,AMPERT +ARAKO 3 .OGA 3TAMBLER . +ATCOF $* !CHITUV 9 $UBINSKY #HANGES IN MORPHOLOGY AND DIET OF THE CORAL 3TYLOPHORA PIS- : 3IMON "LECHER . !QUATIC #ONSERV -AR &RESHW %COSYST TILLATA ALONG A DEPTH GRADIENT -AR %COL 0ROG 3ER n 0UBLISHED ONLINE IN 7ILEY )NTER3CIENCE www.interscience.wiley. %REZ * 2EYNAUD 3 3ILVERMAN * 3CHNEIDER + !LLEMAND $ #ORAL com). doi: AQC %FFECTS OF DEPTH AND EUTROPHICATION ON calcification under ocean acidification and global change. In: THE ZOOXANTHELLA CLADES OF 3TYLOPHORA PISTILLATA FROM THE 'ULF OF $UBINSKY : 3TAMBLER . EDS #ORAL REEFS AN ECOSYSTEM IN TRANSI- %ILAT 2ED 3EA TION 3PRINGER .ETHERLANDS PP n ,EVY / $UBINSKY : !CHITUV 9 0HOTOBEHAVIOR OF STONY CORALS &ALKOWSKI 0' $UBINSKY : ,IGHT SHADE ADAPTATION OF Stylophora RESPONSES TO LIGHT SPECTRA AND INTENSITY * %XP "IOL n pistillata A HERMATYPIC CORAL FROM THE 'ULF OF %ILAT .ATURE ,EVY / $UBINSKY : 3CHNEIDER + !CHITUV 9 :AKAI $ 'ORBUNOV -9 n $IURNAL HYSTERESIS IN CORAL PHOTOSYNTHESIS -AR %COL 0ROG &ALKOWSKI 0' $UBINSKY : -USCATINE , 0ORTER * ,IGHT AND THE 3ER n BIOENERGETICS OF A SYMBIOTIC CORAL "IO3CIENCE n ,EVY / !CHITUV 9 9ACOBI 9: 3TAMBLER . $UBINSKY : 4HE &ALKOWSKI 0' -C#LOSKY , -USCATINE , $UBINSKY : impact of spectral composition and light periodicity on the activity 0OPULATION CONTROL IN SYMBIOTIC CORALS "IO3CIENCE n OF TWO ANTIOXIDANT ENZYMES 3/$ AND #!4 IN THE CORAL Favia &ANG , 3 #HEN 9 7* #HEN # 3 7HY DOES THE WHITE TIP OF favus * %XP -AR "IOL %COL n STONY CORAL GROW SO FAST WITHOUT ZOOXANTHELLAE -AR "IOL ,EVY / !PPELBAUM , ,EGGAT 7 'OTHLIF 9 (AYWARD $# -ILLER $ n (OEGH 'ULDBRG / ,IGHT RESPONSIVE CRYPTOCHROMES FROM THE &ISHER 4 3CHURTZ 3WIRSKI 2 'EPSTEIN 3 $UBINSKY : #HANGES SIMPLEST MARINE EUMETAZOAN ANIMALS 3CIENCE n IN THE LEVELS OF 2IBULOSE BISPHOSPHATE CARBOXYLASEOXYGENASE ,OYA 9 3LOBODKIN ," 4HE CORAL REEFS OF %ILAT 'ULF OF %ILAT 2UBISCO IN 4ETRAEDRON MINIMUM #HLOROPHYTA DURING LIGHT AND 2ED 3EA 0ROC :OOL 3OC ,ONDON n SHADE ADAPTATION 0LANT #ELL 0HYSIOL n -ALKIN ! $UBINSKY : &OMINA ) "IL + #OMPOSITION AND TRANS- &RICKE (7 6ARESCHI % 3CHLICHTER $ 0HOTOECOLOGY OF SYMBIOTIC location of symbiotic algae photosynthates at different nutritions in CORAL ,EPTOSERIS FRAGILIS IN THE 2ED 3EA -AR %COL 0ROG 3ER PRESENCE OF HOST FACTOR )N 3TEINBERGER 9 ED 0RESERVATION OF OUR n WORLD IN THE WAKE OF CHANGE VOL !" )3%%13 0UBLICATION 'ATTUSO *0 !LLEMAND $ &RANKIGNOULLE - 0HOTOSYNTHESIS AND *ERUSALEM PP n calcification at cellular, organismal and community levels in coral -ARCELINO ,! 7ESTNEAT -7 3TOYNEVA 6 (ENSS * 2OGERS *$ ET AL reefs: a review of interactions and control by carbonate chemistry. -ODULATION OF LIGHT ENHANCEMENT TO SYMBIOTIC ALGAE BY !M :OOL n LIGHT SCATTERING IN CORALS AND EVOLUTIONARY TRENDS IN BLEACHING 0,O3 'OFFREDO 3 #AROSELLI % -EZZO & ET AL 4HE PUZZLING PRESENCE OF /NE E DOIJOURNALPONE CALCITE IN SKELETONS OF MODERN SOLITARY CORALS FROM THE -EDITERRANEAN -ASS 4 %INBINDER 3 "ROKOVICH % 3HASHAR . 6AGO 2 %REZ * $UBINSKY 3EA 'EOCHIM #OSMOCHIM !CTA n : 0HOTOACCLIMATION OF Stylophora pistillata to light extremes: 'OREAU 4& 4HE PHYSIOLOGY OF SKELETON FORMATION IN CORALS ) ! METABOLISM AND CALCIlCATION -AR %COL 0ROG 3ER n method for measuring the rate of calcium deposition by corals under -C#ONNAUGHEY 4 7HELAN *& #ALCIlCATION GENERATES PROTONS DIFFERENT CONDITIONS "IOL "ULL n FOR NUTRIENT AND BICARBONATE UPTAKE %ARTH 3CI 2EV n Goreau TF, Goreau NI (1959) The physiology of skeleton formation in -C,AUGHLIN **! :AHL 0! !XENIC ZOOXANTHELLAE FROM VARIOUS corals. II. Calcium deposition by hermatypic corals under various INVERTEBRATE HOSTS !NN . 9 !CAD 3CI n CONDITIONS IN THE REEF "IOL "ULL n -EROZ % "RICKNER ) ,OYA 9 0ERETZMAN 3HEMER ! )LAN - 4HE 'RANT 32 &ISHER %* #HANG *( -OLE "- $ANGL *, 3UBTERFUGE EFFECT OF GRAVITY ON CORAL MORPHOLOGY 0ROC 2 3OC " "IOL 3CI and manipulation: type III effector proteins of phytopathogenic bac- n TERIA !NNU 2EV -ICROBIOL n -ORSE $% (OOKER . -ORSE !.# *ENSEN 2! #ONTROL OF LARVAL 'RAUS 22 -AC)NTYRE )' ,IGHT CONTROL OF GROWTH FORM IN COLO- METAMORPHOSIS AND RECRUITMENT IN SYMPATRIC !GANCIID CORALS * %XP NIAL REEF CORALS COMPUTER SIMULATION 3CIENCE n -AR "IOL %COL n (ARRISON 0, 7ALLACE ## 2EPRODUCTION DISPERSAL AND RECRUIT- -USCATINE , 'LYCEROL EXCRETION BY SYMBIOTIC ALGAE FROM CORALS MENT OF SCLERACTINIAN CORALS )N $UBINSKY : ED #ORAL REEF ECOSYS- AND 4RIDACNA AND ITS CONTROL BY THE HOST 3CIENCE TEMS ECOSYSTEMS OF THE WORLD VOL %LSEVIER 3CIENCE 0UBLISHERS -USCATINE , +APLAN )2 2ESOURCE PARTITIONING BY REEF CORALS AS !MSTERDAM PP n )3". determined from stable isotope composition II. 15N of zooxanthel- (OLCOMB - 4AMBUTTÏ % !LLEMAND $ 4AMBUTTÏ 3 ,IGHT LAE AND ANIMAL TISSUE VERSUS DEPTH 0AC 3CI n enhanced calcification in: effects of glucose, glycerol and oxygen -USCATINE , &ALKOWSKI 0' $UBINSKY : #ARBON BUDGETS IN Stylophora pistillata. PeerJ 2:e375 SYMBIOTIC ASSOCIATIONS %NDOCYTOBIOLOGY n )LUZ $ $UBINSKY : #ORAL PHOTOBIOLOGY NEW LIGHT ON OLD VIEWS -USCATINE , &ALKOWSKI 0' 0ORTER * $UBINSKY : &ATE OF PHO- :OOLOGY n tosynthetically fixed carbon in light and shade-adapted corals. Proc )LUZ $ 9EHOSHUA 9 $UBINSKY : 4HE QUANTUM YIELDS OF PHYTO- 2 3OC ,ONDON "n PLANKTON PHOTOSYNTHESIS IN THE 'ULF OF !QABA %ILAT .ORTHERN 2ED /DUM (4 /DUM %0 4ROPHIC STRUCTURE AND PRODUCTIVITY OF A 3EA )SRAEL * 0LANT 3CI n WINDWARD CORAL REEF COMMUNITY ON %NIWETOK ATOLL %COLOG -ONOGR *OKIEL 0, 4HE REEF CORAL TWO COMPARTMENT PROTON mUX MODEL A n new approach relating tissue-level physiological processes to gross 0EARSE 6" -USCATINE , 2OLE OF SYMBIOTIC ALGAE ZOOXANTHEL- CORALLUM MORPHOLOGY * %XP -AR "IOL %COL n LAE IN CORAL CALCIlCATION "IOL "ULL n *OKIEL 0, )TO 29 ,IU 0- .IGHT IRRADIANCE AND SYNCHRONIZATION 1UOY *2 'AIMARD *0 -ÏMOIRE SUR LACCROISSEMENT DES of lunar spawning of larvae in the reef coral Pocillopora damicornis POLYPES LITHOPHYTES CONSIDÏRÏ GÏOLOGIQUEMENT !NN 3CI .AT ,INNAEUS -AR "IOL n n

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2AHAV / $UBINSKY : !CHITUV 9 &ALKOWSKI 0' !MMONIUM 3WEENEY !- "OCH #! *OHNSEN 3 -ORSE $% 4WILIGHT SPECTRAL METABOLISM IN THE ZOOXANTHELLATE CORAL 3TYLOPHORA PISTILLATA 0ROC DYNAMICS AND THE CORAL REEF INVERTEBRATE SPAWNING RESPONSE * %XP 2OY 3OC ,ONDON "n "IOL n 2OTH -3 4HE ENGINE OF THE REEF PHOTOBIOLOGY OF THE CORALnALGAL 4ITLYANOV % ,ELETKIN 6 $UBINSKY : !UTOTROPHY AND PREDATION SYMBIOSIS &RONT -ICROBIOL IN THE HERMATYPIC CORAL 3TYLOPHORA PISTILLATA IN DIFFERENT LIGHT HABI- 3CHNEIDER + %REZ * 4HE EFFECT OF CARBONATE CHEMISTRY ON CALCI- TATS 3YMBIOSIS n lCATION AND PHOTOSYNTHESIS IN THE HERMATYPIC CORAL !CROPORA EURYS- 4RENCH 2+ $INOmAGELLATES IN NON PARASITIC SYMBIOSES )N TOMA ,IMNOL /CEANOGR n 4AYLOR &*2 ED 4HE BIOLOGY OF DINOmAGELLATES "LACKWELL 3CIENTIlC 3HIBATA !+ (AXO &4 ,IGHT TRANSMISSION AND SPECTRAL DISTRIBU- /XFORD PP n tion through epiand endozoic algal layers in the brain coral Favia. VAN 7OESIK 2 #ALM BEFORE THE SPAWN GLOBAL CORAL SPAWNING "IO) "ULL 7OODS (OLE n PATTERNS ARE EXPLAINED BY REGIONAL WIND lELDS 0ROC 2 3OC " 3HWARTSBERG - +IZNER : $UBINSKY : "ACHAR ! -ORPHOLOGICAL n DOIRSPB GROWTH RESPONSE OF 3TYLOPHORA PISTILLATA TO IN SITU MANIPULATIONS OF 6ERON *%. #ORALS IN SPACE AND TIME BIOGEOGRAPHY AND EVOLU- LIGHT INTENSITY AND WATER mOW REGIME )SRAEL * %COL %VOL n TION OF THE 3CLERACTINIA #OMSTOCK#ORNELL )THACA PP 3IMKISS + 0OSSIBLE EFFECTS OF ZOOXANTHELLAE ON CORAL GROWTH 6IZE 0$ (ILTON *$ "RADY !+ $AVIES 37 ,IGHT SENSING AND %XPERIENTIA the coordination of coral broadcast spawning behavior. In: 3TAMBLER . A -ARINE MICRORALGAECYANOBACTERIA INVERTEBRATE Proceedings of the 11th international coral reef symposium, Ft. SYMBIOSIS TRADING ENERGY FOR STRATEGIC MATERIAL )N 3ECKBACH * ,AUDERDALE PP n $UBINSKY : EDS !LL mESH IS GRASS PLANT ANIMAL INTERACTIONS 7ANGPRASEURT $ ,ARKUM !7 2ALPH 0* +àHL - B ,IGHT GRADI- $ORDRECHT 4HE .ETHERLANDS 3PRINGER 3CIENCE VOL PP n ENTS AND OPTICAL MICRONICHES IN CORAL TISSUES &RONT -ICROBIOL 3TAMBLER . B :OOXANTHELLAE THE YELLOW SYMBIONTS INSIDE ANI- doi:FMICB E#OLLECTION MALS )N $UBINSKY : 3TAMBLER . EDS #ORAL REEFS AN ECOSYSTEM IN Wells JW (1957). Coral reefs. In: Hedgpeth, JW (ed) Treatise on marine TRANSITION $ORDRECHT 4HE .ETHERLANDS 3PRINGER 3CIENCE ECOLOGY AND PALEOECOLOGY ) %COLOGY 'EOL 3OC !M -EM VOL PP n PP n 3TAMBLER . $UBINSKY : 0HOTOTROPHS IN THE TWILIGHT ZONE )N 9ONGE #- 4HE SIGNIlCANCE OF THE RELATIONSHIP BETWEEN CORALS 3ECKBACH * ED !LGAE AND CYANOBACTERIA IN EXTREME ENVIRON- AND ZOOXANTHELL .ATURE n MENTS VOL #ELLULAR /RIGIN ,IFE IN %XTREME (ABITATS AND :AKAI $ $UBINSKY : !VISHAI ! #AARAS 4 #HADWICK .% ,UNAR !STROBIOLOGY $ORDRECHT 4HE .ETHERLANDS 3PRINGER 3CIENCE periodicity of planula release in the reef-building coral Stylophora PP n pistillata -AR %COL 0ROG 3ER n

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