Mar Biol (2007) 151:1287–1298

DOI 10.1007/s00227-006-0589-5

RESEARCH ARTICLE

Adaptation strategies of the corallimorpharian Rhodactis rhodostoma to irradiance and temperature

Baraka Kuguru · Gidon Winters · Sven Beer · Scott R. Santos · Nanette E. Chadwick

Received: 17 February 2006 / Accepted: 9 November 2006 / Published online: 11 January 2007© Springer-Verlag 2007

Abstract Corallimorpharians may dominate some hab-itats on coral reefs and compete with stony corals foraccess to light, yet little is known concerning their photo-synthetic traits. At Eilat in the northern Red Sea, weobserved that the abundance of individuals of the coral-limorpharian Rhodactis rhodostoma decreased signiW-cantly with depth on the reef slope. Field and laboratoryexperiments revealed that they employ several mecha-nisms of photoadaptation to high irradiance on theshallow reef Xat. Their endosymbiotic microalgae (zoo-xanthellae) varied signiWcantly in both abundance andchlorophyll content with level of irradiance. Use of a div-ing pulse amplitude modulated Xuorometer revealedthat the zooxanthellae of R. rhodostoma eVectively dis-perse excess light energy by expressing signiWcantlyhigher values of non-photochemical quenching and

maximum excitation pressure on photosystem II whenexperimentally exposed to high light (HL) versus lowlight (LL). Host corallimorpharian tissues mediated thisresponse by shielding the algal symbionts from high irra-diance. The endoderm of host tentacles thickened signiW-cantly and microalgal cells were located further from themesoglea in HL than in LL. The clades of zooxanthellaehosted by the corallimorpharians also varied with depth.In shallow water, all sampled individuals hosted clade Czooxanthellae, while in deep water the majority hostedclade D. The photosynthetic output of individuals ofR. rhodostoma was less aVected by HL than was that of astony coral examined. When exposed to both high tem-perature (HT) and HL, individuals of R. rhodostomareduced their maximum quantum yield, but not whenexposed to HL at low temperature (LT). In contrast, col-onies of the scleractinian coral Favia favus reduced theirphotosynthetic output when exposed to HL in both tem-perature regimes. After 2 weeks of HT stress, R. rhodos-toma polyps appeared to bleach completely but re-established their zooxanthella populations upon returnto ambient temperature. We conclude that mechanismsof photoadaptation to high irradiance employed by boththe endosymbiotic zooxanthellae and host corallimor-pharians may explain in part the abundance of R. rho-dostoma on some shallow reef Xats. The ability to survivefor weeks at HT while bleached also may allow coralli-morpharians to repopulate shallow reef areas wherescleractinians have been killed by thermal stress.

Introduction

Corallimorpharians occur in a wide range of marinehabitats and may dominate hard substrata in both

Communicated by P.W. Sammarco, Chauvin.

B. Kuguru and G. Winters contributed equally to this work.

S. R. Santos · N. E. Chadwick (&)Department of Biological Sciences, 101 Rouse Life Sciences Building, Auburn University, Auburn, AL 36849, USAe-mail: chadwick@auburn.edu

B. Kuguru · G. WintersInteruniversity Institute for Marine Science, P.O. Box 469, Eilat, Israel

B. Kuguru · N. E. ChadwickFaculty of Life Sciences, Bar Ilan University, Ramat Gan, Israel

G. Winters · S. BeerDepartment of Plant Sciences, Tel Aviv University, Tel Aviv, Israel

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temperate (Chadwick 1991) and tropical regions (denHartog 1980). On coral reefs, they form aggregations atdepths of up to 65 m (S. Einbinder, personal communi-cation) but highest abundances typically occur near thewater surface (<0.5 m depth, den Hartog 1980; Chad-wick-Furman and Spiegel 2000; Muhando et al. 2002).Some corallimorpharians replicate asexually, aggres-sively damage competitors, and withstand physical dis-turbances better than do stony corals (Chadwick 1991;Muhando et al. 2002). Due in part to these traits, theymay rapidly occupy recently opened space followingnatural and anthropogenic disturbances on coral reefs(den Hartog 1977; Langmead and Chadwick-Furman1999; Kuguru et al. 2004). As such, chronically dam-aged coral reefs may become dominated by some oppor-tunistic species of corallimorpharians.

Anatomical and molecular evidence reveals thatmembers of the order Corallimorpharia (Cnidaria:Anthozoa) are closely related to scleractinian corals(Daly et al. 2003) and may have originated due to skel-etal loss by some scleractinians (Medina et al. 2006).However, while numerous studies exist on biochemicaland physiological responses to environmental stressorsin some orders of anthozoans (reviewed in Baker2003), similar responses of corallimorpharians arepoorly understood. Like many marine invertebrates,some corallimorpharians harbor endosymbiotic dino-Xagellate algae (zooxanthellae) (den Hartog 1980;Hamner and Dunn 1980; LaJeunesse 2002). Zooxan-thellae play a vital role in host nourishment via translo-cation of photosynthates (Muscatine et al. 1981).Zooxanthellae comprise many strains or species thatbelong to eight major clades and exhibit a range ofphysiological responses and tolerances (reviewed inCoVroth and Santos 2005). The Symbiodinium clade(s)that an organism harbors may aVect its distribution,reaction to extreme environmental conditions, andability to survive and recover after a disturbance(reviewed in Baker 2003). Only a few species of coralli-morpharians have been examined for associated zoo-xanthella clades and have been found to harbormembers of clade C (LaJeunesse 2002; LaJeunesseet al. 2004).

Irradiance and temperature are major environmen-tal parameters that inXuence the distribution and abun-dance of cnidarians on coral reefs (Falkowski andDubinsky 1981; Fitt et al. 2001). Increases in the levelsof both factors have contributed to frequent bleachingevents on coral reefs during the past two decades(Loya et al. 2001; Muhando et al. 2002). While theeVects of these factors on reef-building corals havebeen well studied, the impacts of thermal and lightstress on other groups of reef cnidarians have been

mostly overlooked. Individuals of Rhodactis rhodos-toma are one of the most common corallimorpharianson coral reef Xats in the Indo-PaciWc region, and maybecome especially abundant following bleaching andother disturbances that kill stony corals (Chadwick-Furman and Spiegel 2000; Kuguru et al. 2004). Weinvestigated responses of individuals of R. rhodostomato variation in irradiance and temperature to betterunderstand the mechanisms that allow members of thisspecies to become abundant on shallow reef Xats. Wehypothesized that individuals of this species (1)decrease signiWcantly in abundance with depth, (2)withstand high irradiance without decreasing theirphotosynthetic output, (3) survive at high temperature(HT) for long periods while bleached, (4) shield theirzooxanthellae from high irradiance, and (5) harbordiVerent clades of zooxanthellae at diVerent depths onthe coral reef.

Methods

Study site and depth distribution

This study was conducted during January 2004 toMarch 2005 on coral reefs adjacent to the Interuniver-sity Institute for Marine Science (IUI) near Eilat at thenorthern tip of the Gulf of Aqaba, Red Sea (29°30�N,34°55�E). To determine the depth distribution of thecorallimorpharian R. rhodostoma, 20 quadrats of 1 m2

each were deployed haphazardly at each of threedepths: reef Xat (0.5 m), shallow slope (3 m), and deepslope (18 m). The number of polyps of this species ineach quadrat was determined while snorkeling orscuba diving.

Photophysiology

Polyps of R. rhodostoma were selected haphazardly at3–20 m depth, collected, and glued to PVC bases usingunderwater epoxy. Selected polyps were each at least10 m apart to avoid collecting individuals that origi-nated asexually from the same aggregation. Followinga 2-week acclimation period in outdoor Xow-through(120 l h¡1) seawater aquaria, the polyps either werereturned to the reef for Weld experiments or trans-ferred to laboratory treatments.

For the Weld experiments, four corallimorpharianswere attached by their PVC bases to underwaterframes and acclimated at each of three depths (5, 10,and 20 m) on the coral reef for 1 month. Followingacclimation, we used an underwater pulse amplitudemodulated (PAM) Xuorometer (the Diving PAM,

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Walz, Germany; Hoegh-Guldberg and Jones 1999;Winters et al. 2003; Iglesias-Prieto et al. 2004) tomeasure photosynthetic parameters in each coral-limorpharian. PAM Xuorometry induces chlorophyllXuorescence in vivo to estimate the potential quantumyield of photosystem II during photosynthesis, aparameter that correlates with more traditional mea-sures of photosynthetic rate such as CO2 uptake andO2 evolution (Beer et al. 1998). At 1 h after sunset, thePAM was used to record the nocturnal maximumquantum yield of photosystem II (Fv/Fm), whereFv = variable Xuorescence and Fm = maximum Xuores-cence for the dark adapted sample. This period ofdarkness is suYcient to maximize the frequency ofopen reaction centers in photosystem II (Winters et al.2003). At noon, the midday eVective quantum yield[(Fm� ¡ F)/Fm� = �F/Fm�] also was measured whereFm� = maximum Xuorescence for the light adapted sam-ple and F = initial Xuorescence for the light adaptedsample (after Genty et al. 1989; Schreiber et al. 1994).Based on these measurements, we calculated for eachpolyp the maximum midday excitation pressure[Qm = 1 ¡ (�F/Fm� at noon)/(Fv/Fm at 1 h after dark-ness), after Maxwell et al. 1994, 1995; Iglesias-Prietoet al. 2004].

A stress experiment on photosynthetic responses tovariation in light and temperature was performed on 16individuals each of the corallimorpharian R. rhodos-toma (3–4 cm diameter each) and for comparison themassive scleractinian coral Favia favus (4–5 cm diame-ter each) in an outdoor running seawater table. Eightindividuals of each species were photoadapted for1 month under each of two treatments created bylayers of plastic netting shades: (1) high light (HL),30% shade with a maximum midday irradiance of1,160 �mol photons m¡2 s¡1 and (2) low light (LL),90% shade with a maximum midday irradiance of350 �mol photons m¡2 s¡1. These treatments mimickedirradiance at 5 and 20 m depth, respectively, whichencompasses most of the depth range of individuals ofR. rhodostoma (Chadwick-Furman and Spiegel 2000)and F. favus (Sheppard and Sheppard 1991). ThediVuse attenuation co-eYcient (Kd), an indicator of thepenetration of solar irradiance in seawater, was 0.0726as measured in situ at the time of the experiment usingan LI-192 underwater quantum sensor lowered from aboat. Irradiances were measured using quantum sen-sors (LI-190SA, LiCor, USA) connected to a data log-ger (LI-1400, LiCor, USA).

Within each of the two light treatments, four indi-viduals of each species were subjected to a gradual risein temperature over 14 days by applying a heater until6°C above mean ambient seawater temperature was

reached (=HT treatment, 31°C), after which polypswere maintained at this temperature for a further18 days. During the entire period, a chiller (TECO,Italy) was used to maintain the remaining animals at25°C, a temperature identical to that of seawater at 4 mdepth on the adjacent coral reef (=low temperature,LT). Submersible temperature loggers (HOBO tem-perature Pro, Onset Computers, USA) monitored thetemperatures in each treatment. The LT treatment of25°C equaled mean summer temperature on the shal-low reef at Eilat (Loya 1985). The HT treatment of31°C was a few degrees above the maximum summertemperature in very shallow water of 28°C, and wasselected to mimic a possible warming event in thisregion.

Four experimental treatments were maintained,each containing four individuals of each species: highlight and high temperature (HLHT), high light andlow temperature (HLLT), low light and high tempera-ture (LLHT), and low light and low temperature(LLLT). The temperature treatment areas were sepa-rated from each other using Styrofoam insulationsheeting, and each was supplied with a separate inXowof running seawater at a rate of 60 l h¡1 (after Zakaiet al. 2006). The water also was well mixed within eachtreatment by a small aquarium pump at a rate of600 l h¡1. Due to the technical constraints of maintain-ing a large number of chambers at diVerent tempera-tures and irradiances, the experimental individualswere grouped within each treatment. This lack of rep-lication of chambers within treatments is standard forlaboratory physiological experiments, and is based onprevious studies which have demonstrated the validityof results for cnidarians using this method (reviewedin Chomski et al. 2004).

During each of 18 days in the stress experimentwhen the HT treatments were maintained at 31°C, Fv/Fm was measured for all individuals using the PAM at1 h after sunset. To assess the photo-protective abilitiesof the corallimorpharian polyps following the abovetreatments, non-photochemical quenching (NPQ)[NPQ = (Fm ¡ Fm�)/Fm�, after Hoegh-Guldberg andJones 1999], also was measured for individuals in alltreatments at the end of the experiment.

Individuals were subjected to the stress experimentfor a total of 32 days (14 days of gradual temperaturerise plus 18 days at HT), during which the corallimor-pharians exposed to the HLHT treatment becamebleached as evidenced by their white appearance. Wethen lowered the temperature back to ambient andmonitored the corallimorpharians for an additionalmonth during which we recorded Fv/Fm at 1 h aftersunset each day. Photographs were taken of each

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individual before, during, and after bleaching whenmicroalgae repopulated the corallimorpharians.

After 32 days in the stress experiment, before recov-ery, and after 30 days in the Weld treatments, 6–8 tenta-cles were removed from each corallimorpharian polypto determine zooxanthella abundance and chlorophyll a(chl a) content. Tentacles were examined because theyare major photosynthetic organs in anthozoans andhave been used widely to assess variation in photosyn-thetic parameters such as zooxanthella abundance andchl a levels (Dunn et al. 2002, 2004). The group of tenta-cles from each polyp was blotted on absorbent tissuepaper to remove all excess water. Then their wet masswas determined accurately using an electronic micro-balance with an error of §0.0002 g (wet mass per groupof 6–8 tentacles = 0.10 § 0.02 g, x § SE). Each group oftentacle tips then was homogenized in 2 ml of Wlteredseawater and the resulting slurry was centrifuged (afterDunn et al. 2002, 2004). In the zooxanthella-containingaliquots we measured (1) chl a content (overnightextraction in 90% acetone, absorbance readings at 664and 630 nm; JeVrey and Humphrey 1975), and (2) zoo-xanthella abundance (cells counted under a light micro-scope using a hemocytometer, modiWed after Warneret al. 2002). Algal pigment and abundance were nor-malized per wet mass of tentacle tissue.

Anatomy

Following 32 days in the stress experiment, 6–8 tenta-cle tips also were removed from each corallimorphar-ian polyp for histological examination. The tentacletips were relaxed in 7% MgCl2 for 3 h, Wxed in 10%formalin for 24 h, washed in 70% ethanol prior to stor-age in a refrigerator at 4°C (after Chadwick-Furmanet al. 2000), and then sent to Tel Aviv University forhistological sectioning. Anatomical parameters (diam-eter of zooxanthella cells, tentacle endoderm thickness,and minimal distances between algal cells and tentaclemesoglea) observed in the histological sections fromeach treatment were quantiWed using image analysis(UTHSCSA Image tool, version 3.0, 2002).

Symbiodinium clades

Tissue samples were obtained from ten polyps ofR. rhodostoma each located at least 10 m apart at eachof two depths on the coral reef slope: shallow (0–4 m)and deep (18–20 m). A few tentacle tips were removedfrom each polyp, preserved in 100% acetone (Fukatsu1999), and shipped to Auburn University, USA. Totalnucleic acids were extracted from the tissues accordingto CoVroth et al. (1992), and Symbiodinium small sub-

unit (18S) ribosomal DNA (rDNA) was ampliWed byPCR using the primers ss5 (5�-GGTTGATCCTGCCAGTAGTCATATGCTTG-3�) and ss3z (5�-AGCACTGCGTCAGTCCGAATAATTCACCGG-3�) accord-ing to Rowan and Powers (1991a). PCR products weredigested with the TaqI restriction enzyme to generaterestriction fragment length polymorphisms (RFLPs) asdescribed in Rowan and Powers (1991a). RFLP analy-sis of 18S-rDNA PCR products separates Symbiodi-nium into several large clades [i.e., Symbiodinium A,B, C (Rowan and Powers 1991a, b), D (Carlos et al.1999), and E (Symbiodinium californium; LaJeunesseand Trench 2000; LaJeunesse 2001)], and allows simpleand rapid identiWcation of the symbiont clade. Diges-tion products were separated on 2% sodium-borateagarose gels and visualized with ethidium bromideunder UV light. RFLP patterns were comparedwith cloned standards or to the literature to assign eachsample to one of the established Symbiodinium 18S-rDNA RFLP clades. Samples of extracted DNA usedin this study are available upon request to the corre-sponding author.

Statistical analyses

Variation in the number of corallimorpharian polyps,and in the zooxanthella abundance, chlorophyll pig-ment concentration, Qm and Fv/Fm of polyps withdepth in the Weld were analyzed using one-way ANO-VAs. The combined eVects of light and temperature onzooxanthella abundance, chlorophyll pigment concen-tration, and NPQ in the stress experiment were ana-lyzed using two-way ANOVAs. EVects of light andtemperature on daily values of Fv/Fm were determinedusing repeated measures two-way ANOVAs, with timeas the repeated measure. EVects of high and low irradi-ance on zooxanthella diameter, endoderm thicknessand distance of zoozanthellae from the mesoglea weredetermined using t-tests. Proportional data were arc-sine transformed prior to statistical analysis. All datamet the parametric test assumptions of homogeneity ofvariances (Leven’s test) and normality (normal proba-bility plots). SigniWcant diVerences among treatmentgroups were determined post-hoc using Student–New-man–Keuls tests.

Results

Abundance of the corallimorpharian R. rhodostomadecreased signiWcantly with depth on the coral reef atEilat (one-way ANOVA, F(2,0.05) = 305.62, P < 0.001,Fig. 1). In contrast, both the abundance of zooxanthellae

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and the concentration of chl a within transplantedcorallimorpharians increased signiWcantly with depth(one-way ANOVAs, F(2,0.05) = ¡19.17, P < 0.001 forzooxanthella abundance and F(2,0.05) = 4.93, P < 0.05 forchl a concentration, Fig. 2a, b, respectively). Excitationpressure on photosystem II (Qm) in transplanted pol-yps was signiWcantly higher in shallow than in deep

water, but did not diVer from either at mid depth (one-way ANOVA, F(2,0.05) = 3.25, P < 0.05, Fig. 2c). Maxi-mum quantum yield (Fv/Fm) did not vary signiWcantlywith depth in the transplanted individuals (one-wayANOVA, F(2,0.05) = 1.28, P = 0.31, Fig. 2d).

In the laboratory experiment, similar results wereobserved as for polyps transplanted in the Weld. Boththe abundance of zooxanthellae and the concentrationof chl a within polyps decreased signiWcantly in HLversus LL, equivalent to light levels at 5 and 20 mdepth on the reef, respectively (Fig. 3a). Both parame-ters also decreased signiWcantly at HT versus LT, andthere was no interaction eVect between light and tem-perature (Table 1). In the HLHT treatment, both zoo-xanthella abundance and chl a concentration decreasedto almost 0 (Fig. 3a), and polyps appeared bleached(Fig. 4a).

The corallimorpharians had signiWcantly higher val-ues of NPQ at HLLT than they did in any of the otherlaboratory treatments (Fig. 3b). NPQ increased signiW-cantly with light level in both temperature treatments(Table 1). Exposure of the polyps to HT depressed theeVect of HL on NPQ (Fig. 3b), possibly due to thealmost complete absence of zooxanthellae in polyps bythe end of the experiment in this treatment (HLHT,Figs. 3a, 4a).

After approximately 1 week in the stress experi-ment, individuals of R. rhodostoma in both HT treat-ments began to decrease their maximum quantum

Fig. 1 Variation in abundance of the corallimorpharian Rhodac-tis rhodostoma with depth on a coral reef at Eilat, northern RedSea. Data are presented as means § SE of polyp abundance in20 1 m2 quadrats examined at each depth. Depths with diVerentsuperscript letters are signiWcantly diVerent at P < 0.05 (Student–Newman–Keuls post-hoc tests following ANOVA analysis, seetext for details)

Depth (m)0.5 18

Num

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of p

olyp

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18a

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Fig. 2 Variation in photosyn-thetic traits of the coral-limorpharian Rhodactis rhodostoma with depth on a coral reef at Eilat, northern Red Sea: a zooxanthella abun-dance, b chlorophyll a concen-tration, c excitation pressure over photosystem II (Qm), and d maximum quantum yield (Fv/Fm). Data are pre-sented as means § SE, n = 5 polyps examined per depth. Depths with diVerent super-script letters are signiWcantly diVerent at P < 0.05 (Student–Newman–Keuls post-hoc tests following ANOVA analysis, see text for details)

Zoo

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yields (Fig. 5a). By the end of the experiment, individu-als in the HLHT treatment had signiWcantly lowermaximum quantum yields than those in all othertreatments (Table 2; Fig. 5a), and became bleached(Fig. 4a). Polyps in the LLHT treatment also signiW-cantly decreased in maximum quantum yield, but notas drastically as those in the HLHT treatment, indicat-ing an added eVect of HL when exposed to HT(Fig. 5a). Polyps in both of the LT treatments did notsigniWcantly decrease their maximum quantum yieldsover the course of the experiment; there was no signiW-cant eVect of light level in the LT treatments (Table 2;Fig. 5a).

In contrast, individuals of the scleractinian coralF. favus signiWcantly reduced their maximum quantumyields at HL in both temperature treatments (Fig. 5b).At LL, the corals did not reduce their maximum quan-tum yields in either of the temperature treatments(Fig. 5b; Table 2). As in the corallimorpharians, thecombination of HLHT created the largest depressionin maximum quantum yield (Fig. 5a, b).

After the temperature decreased, individuals of thecorallimorpharian recovered signiWcantly in terms ofmaximum quantum yield (Fig. 5c; Table 2) and becamepigmented again, indicating repopulation by endosym-biotic zooxanthellae (Fig. 4b).

Under LLLT, the corallimorpharian tentaclescontained histologically discernible layers of ectoderm,mesoglea, and endoderm with zooxanthella cellslocated near the thin mesogleal layer (Fig. 6a). In con-trast, at HLLT, the mesogleal layer was signiWcantlythicker and the zooxanthella cells were signiWcantlylarger and located further distant from the mesogleathan in the LLLT treatment (Fig. 6b; Table 3). In bothHT treatments, the tissue layers became disorganized,the zooxanthellae degenerated, and many empty vacu-oles appeared (Fig. 6c, d). This tissue disintegrationprevented statistical analysis of mesogleal thicknessand zooxanthella size and position in either HT treat-ment.

Individuals of R. rhodostoma on the coral reef atEilat contained algal symbionts belonging to Symbiodi-nium clade C or D (Fig. 7). All polyps (n = 7) sampledfrom shallow water (0–4 m depth) harbored clade C,while in deep water (18–20 m depth) most polyps(73%, n = 11) hosted clade D and a minority (27%)contained clade C. None of the polyps examined fromeither depth contained both clades C and D.

Discussion

We demonstrate here that the corallimorpharianR. rhodostoma employs multiple mechanisms of photo-acclimation, including: (1) variation in both zooxan-thella abundance and chlorophyll concentration withdepth, (2) dispersal of excess light energy via NPQ bythe zooxanthellae at HL, (3) host-mediated shading ofzooxanthellae from HL by thickening of the endoder-mal layer and movement of algal cells away from themesoglea, and (4) variation in the genetic identity ofharbored zooxanthella clades with depth.

The decrease in abundance of this species withdepth observed here is similar to the pattern observedfor these corallimorpharians on other coral reefs in thenorthern Red Sea (Chadwick-Furman and Spiegel

Fig. 3 Variation in a zooxanthella abundance and chlorophyllconcentration and b levels of non-photochemical quenching inpolyps of the corallimorpharian Rhodactis rhodostoma exposedto a stress experiment of four combinations of light and tempera-ture treatments under laboratory conditions: low light and lowtemperature, high light and low temperature, low light and hightemperature, and high light and high temperature. Data are pre-sented as means § SE, n = 4 polyps per treatment after 18 days ofexposure. Treatments with diVerent superscript letters are signiW-cantly diVerent at P < 0.05 (Student–Newman–Keuls post-hoctests following ANOVA analysis, see text for details)

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2000) and Tanzania (Muhando et al. 2002; Kuguruet al. 2004). The high abundance of R. rhodostoma onshallow coral reef Xats indicates an ability to withstandextremely high levels of irradiance. The diverse mecha-nisms of photoacclimation described above may in partexplain this depth distributional pattern.

The increase in chl a concentration and zooxanthellaabundance with depth shown here for polyps of R. rho-dostoma also occurs in some scleractinian corals asphotosynthetic compensation for exposure to LL con-ditions (Falkowski and Dubinsky 1981; Titlyanov et al.2000). Thus at very high levels of irradiance on shallowreef Xats, individuals of this corallimorpharian are ableto reduce both the pigment content per algal cell andthe total number of zooxanthella cells they contain.

Our Xuorescence-based measurements of Fv/Fm, Qm,and NPQ also show that the algal symbionts of this cor-allimorpharian eVectively disperse excess energy in HL

environments. While polyps of R. rhodostoma do notvary signiWcantly in maximum quantum yield Fv/Fmwith depth, some stony corals for example Stylophorapistillata at Eilat decrease Fv/Fm in shallow water, indi-cating chronic photoinhibition in the corals when grow-ing at 2 m as compared to 11 m depth (Winters et al.2003). Values of Qm approach 1.0 in the corallimorpha-rians, indicating that under maximum irradiance manyof the PSII reaction centers in their zooxanthellae areclosed and thus that some photoinhibition occurs atHL (Iglesias-Prieto et al. 2004). Since Fv/Fm does notdecrease in the shallow growing corallimorpharians,these high Qm values could be attributed to a middaydrop in eVective quantum yield due to high levels ofmidday irradiance in shallow water. These corallimor-pharians also exhibit high levels of NPQ at high irradi-ance, another indicator of their ability to disperseexcess light energy.

Table 1 Two-way ANOVAs of photosynthetic parameters with temperature and light treatments in a stress experi-ment on the corallimorphari-an Rhodactis rhodostoma under laboratory conditions at Eilat, northern Red Sea

Photosynthetic parameter

Source of variation df Mean square F P

Chlorophyll a concentration

Temperature 1 179.47 26.98 ***Light 1 62.82 9.44 **Temperature £ light 1 6.86 1.03 nsError 12 6.65

Zooxanthella abundance

Temperature 1 4.44 £ 1014 6.87 *Light 1 2.60 £ 1014 4.01 nsTemperature £ light 1 0.41 £ 1014 0.63 nsError 12 0.65 £ 1014

Non-photochemical quenching

Temperature 1 16.80 4.34 nsLight 1 17.41 4.50 *Temperature £ light 1 4.38 1.13 nsError 12 3.87

ns not signiWcant

*P < 0.05; **P < 0.01; ***P < 0.001

Fig. 4 Photographs of a representative individual of the coral-limorpharian Rhodactis rhodostoma under laboratory conditionsfollowing exposure to a a stress experiment of 18 days of highlight and high temperature, and b a recovery experiment of

14 days after seawater temperature was returned to ambient(25°C). Note bleached appearance in (a) and same polyp withbrown pigmentation in (b) indicating recovery of zooxanthellae

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While individuals of R. rhodostoma appear tophotoadapt to high irradiance, they are sensitive to HTas known for many stony corals (Warner et al. 1999;Fitt et al. 2001; Loya et al. 2001; Bhagooli and Hidaka2003; Rowan 2004). In contrast, the stony coralsF. favus (Fig. 5b), S. pistillata, and Pocillopora dami-cornis (G. Winters, unpublished data) all show loweredphotosynthetic potential (expressed as Fv/Fm) mostlyas a function of irradiance (up to 70% of full sunlight)and less as a function of temperature (up to 31°C). Ourstudy area in the northern Red Sea is exposed to oneof the highest irradiances on earth (e.g., http://www.eosweb.larc.nasa.gov/sse/; Winters et al. 2003).Thus, if photosynthetic sensitivity to light is the normin this area as indicated by the above corals, the coral-limorpharian R. rhodostoma is unusual in showingmore sensitivity to temperature than to light.

The tissue modiWcations observed here in R. rho-dostoma that shade the zooxanthellae from excesslight are similar to those employed by the zoanthidPalythoa caribaeorum, in which a thick epidermisis produced that sunscreens the algal symbionts(LaJeunesse 2002). Similar tissue modiWcations whenexposed to HL have not been observed in the moreclosely related scleractinian corals, but occur in someactinian sea anemones in response to heat stress(Dunn et al. 2002, 2004). At HT, we also observed aloss of functioning zooxanthellae and degeneration ofhost tissue similar that observed in some stony corals,especially in combination with high irradiance (Brownet al. 1995; Warner et al. 1999; Dunn et al. 2002; Bhag-ooli and Hidaka 2003; Rowan 2004). The recoveryof these corallimorpharians from exposure to severalweeks of HT stress contrasts with responses known forsome stony corals which may die from this type ofexposure (Muhando et al. 2002). During extendedperiods of bleaching and while deprived of photosyn-thates from zooxanthellae, the corallimorpharianR. rhodostoma may utilize alternate nutritional strate-gies. In scleractinian corals, endolithic algae can serveas an alternate source of photosynthate and contributeto host survivorship following coral bleaching andprior to repopulation by zooxanthellae (Fine and Loya2002). However, corallimorpharians do not possess acalcareous skeleton so this option is not available tothem. The experimentally bleached corallimorphari-ans in our treatments may have survived by preying onzooplankton (Elliott and Cook 1989), absorbing dis-solved organic material (Schlichter 1982), and/or rely-ing on energy reserves or materials recycled fromdegraded cells (Cikala et al. 1999). Their ability to sur-vive bleaching may contribute to the opportunistic lifehistory strategy exhibited by some members of this

Fig. 5 Variation in maximum quantum yield (Fv/Fm) over timeamong laboratory treatments applied to cnidarians. a The coral-limorpharian Rhodactis rhodostoma in a stress experiment withfour combinations of light and temperature: low light and low tem-perature, high light and low temperature, low light and high tem-perature, and high light and high temperature. b R. rhodostoma ina recovery experiment after temperature in the two HT treatmentswas reduced back to ambient (25°C = LT). c The massive sclerac-tinian coral Favia favus in a stress experiment with the above fourcombinations of light and temperature. N = 4 corallimorphariansand Wve corals per treatment. Data are presented as means § SE

F v/F

m

0.3

0.4

0.5

0.6

0.7

0.8

0.3

0.4

0.5

0.6

0.7

0.8a

Time (days)0 10 12 14 16 18

0.3

0.4

0.5

0.6

0.7

0.8

HL HTHL LTLL HTLL LT

b

c

Rhodactis rhodostoma

Stress experiment

Favia favus

Stress experiment

Rhodactis rhodostoma

Recovery experiment

2 4 6 8

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genus (den Hartog 1977; Langmead and Chadwick-Furman 1999; Kuguru et al. 2004).

This is the Wrst study to document the types of zoo-xanthella clades harbored by corallimorpharians in theRed Sea, and the Wrst to detect clade D zooxanthellaein anthozoans in the northern Red Sea. Our results aresimilar to those of LaJeunesse (2002) and LaJeunesseet al. (2004) in that clade C was associated with some of

the corallimorpharians. However, the Symbiodiniumclades detected here in individuals of R. rhodostomadiVered from those reported for soft and stony corals atEilat, which harbor either clade A or C (Barneah et al.2004; Karako-Lampert et al. 2004). In the southernRed Sea, most stony corals also contain clades A andC, while very few (1.5%) contain clade D (Baker et al.2004). In terms of both the lack of clade A and strong

Table 2 Repeated measures two-way ANOVAs with time as the repeated measure of variation in photosynthetic yield (maximum quantum yield, Fv/Fm) with tempera-ture and light in the coral-limorpharian Rhodactis rhodostoma and the sclerac-tinian coral Favia favus under laboratory conditions at Eilat, northern Red Sea

Species and experiment Source of variation df Mean square F P

R. rhodostoma; stress experiment

Temperature 1 0.070 36.18 ***Light 1 0.008 3.97 nsTemperature £ light 1 0.002 1.02 nsError 12 0.002Time 10 0.006 11.05 ***Time £ temperature 10 0.010 20.10 ***Time £ light 10 0.001 2.23 *Time £ temperature £ light 10 0.001 1.86 nsError 120 0.001

F. favus; stress experiment

Temperature 1 0.008 1.26 nsLight 1 0.068 11.07 **Temperature £ light 1 0.000 0.08 nsError 16 0.006Time 10 0.005 10.33 ***Time £ temperature 10 0.001 1.18 nsTime £ light 10 0.002 4.53 ***Time £ temperature £ light 10 0.001 1.18 nsError 160 0.001

R. rhodostoma; recovery experiment

Temperature 1 0.178 38.04 ***Light 1 0.020 4.36 nsTemperature £ light 1 0.012 2.54 nsError 12 0.005Time 7 0.004 3.27 **Time £ temperature 7 0.001 1.00 nsTime £ light 7 0.002 1.24 nsTime £ temperature £ light 7 0.001 0.43 nsError 84 0.001

In stress experiments, individ-uals were subjected to varia-tion in levels of temperature and light. In the recovery experiment, temperature was returned to ambient. See text for details

ns not signiWcant

*P < 0.05; **P < 0.01; ***P < 0.001

Fig. 6 Photomicrographs of tentacle tissue sections from the corallimorpharian Rho-dactis rhodostoma in a stress experiment after 18 days of exposure to four combina-tions of light and temperature treatments under laboratory conditions: a low light and low temperature, b high light and low temperature, c low light and high temperature, and d high light and high tempera-ture. ZOX zooxanthella, HCN host cell nucleus, DZX degenerated zooxanthella, MES mesoglea, END endo-derm, ECT ectoderm, GVS gastrovascular space. Scale bars are 10 �m each

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presence of clade D, our results are more similar tothose of Toller et al. (2001) for zooxanthellae in stonycorals of the Caribbean Sea, where clade C dominatesat all depths and clade D occurs only in deep water.Most of the scleractinians and alcyonaceans in the RedSea that harbor clade C zooxanthellae transmit themhorizontally, in that the zooxanthellae are acquiredfrom the surrounding environment with each new hostgeneration and not directly from host parents (Barneahet al. 2004; Karako-Lampert et al. 2004). Individuals ofR. rhodostoma also likely acquire their zooxanthellaefrom the environment since they broadcast gametesthat do not contain algal cells (Chadwick-Furman et al.2000).

Variation among clades of zooxanthellae in theirphysiological responses to environmental conditionssuch as irradiance and temperature may result in thedominance of diVerent clades at diVerent depths(reviewed in Baker 2003; Iglesias-Prieto et al. 2004; butsee also CoVroth and Santos 2005; Kinzie et al. 2001;Lajeunesse et al. 2003; Tchernov et al. 2004). Ongoingreciprocal transplantation experiments are aimed atinvestigating the extent to which the zooxanthellaclades associated with in this corallimorpharian aredepth and light dependent (B.L. Kuguru et al., in prep-aration).

We conclude that the corallimorpharian R. rhodos-toma is able to produce large aggregations on someshallow reefs in the highly irradiated northern Red Seapartly due to photoacclimation strategies contributed byboth the host cnidarian and microalgae to the holobiont.Clonal replication of polyps and high sexual reproduc-tive output also likely contribute to the rapid expansionof aggregations on the reef Xat (Chadwick-Furman andSpiegel 2000; Chadwick-Furman et al. 2000). Whilethese corallimorpharians alter their anatomy to screentheir zooxanthellae from excess irradiance, the latterphotoadapt physiologically by dissipating excess lightthrough NPQ and by avoiding chronic photoinhibitionas reXected in maintained high Fv/Fm values. Variationin zooxanthella clades with depth also may contribute tophotoadaptation of the holobiont to variation in irradi-ance levels. Individuals of this corallimorpharian cansurvive extended bleaching and recover fully, likely byaltering their mode of nutrition when aposymbiotic.Thus in comparison with some stony corals, individualsof R. rhodostoma exhibit diverse traits for survival inHL environments. These characteristics may allowmembers of this species to repopulate some shallow reefareas that have been denuded from stony corals follow-ing thermal stress events.

Acknowledgments We thank Tally Levanon, Yonatan Bel-maker, Omer Polak, Barak Guzner, and Karen Tarnaruder of theIUI for assistance during this project. We also thank Itzik Briknerfor the histological preparations. This research was supported byfunds from Bar Ilan University and Auburn University to NEC.This research is submitted in partial fulWllment of the require-ments for the Ph.D. by BK at Bar Ilan University and GW at TelAviv University. Experiments performed in this study complywith the current laws of Israel. This is contribution number 10 ofthe Auburn University Marine Biology Program.

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N = 4 polyps sampled per treatment. Data are presented asmeans § SE. Levels of signiWcance were determined using t-tests.See text for details

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