Abundance and Clonal Replication in the Tropical Corallimorpharian Rhodactis Rhodostoma

Invertebrate Biology 119(4): 351-360. 0 2000 American Microscopical Society, Inc.

Abundance and clonal replication in the tropical corallimorpharian Rhodactis rhodostoma

Nanette E. Chadwick-Furmana and Michael Spiegel

Interuniversity Institute for Marine Science, PO. Box 469, Eilat, Israel, and Faculty of Life Sciences, Bar Ilan University, Ramat Gan, Israel

Abstract. The corallimorpharian Rhodactis rhodostoma appears to be an opportunistic species capable of rapidly monopolizing patches of unoccupied shallow substrate on tropical reefs. On a fringing coral reef at Eilat, Israel, northern Red Sea, we examined patterns of abundance and clonal replication in R. rhodostoma in order to understand the modes and rates of spread of polyps across the reef flat. Polyps were abundant on the inner reef flat (maximum 1510 polyps m-* and 69% cover), rare on the outer reef flat, and completely absent on the outer reef slope at >3 m depth. Individuals cloned throughout the year via 3 distinct modes: longitudinal fission, inverse budding, and marginal budding. Marginal budding is a replicative mode not previously described. Cloning mode varied significantly with polyp size. Approximately 9% of polyps cloned each month, leading to a clonal doubling time of about 1 year. The rate of cloning varied seasonally and depended on day length and seawater temperature, except for a brief reduction in cloning during midsummer when polyps spawned gametes. Polyps of R. rhodostoma appear to have replicated extensively following a catastrophic low-tide disturbance in 1970, and have become an alternate dominant to stony corals on parts of the reef flat.

Additional key words: Cnidaria, coral reef, sea anemone, asexual reproduction, Red Sea

Soft-bodied benthic cnidarians such as sea anemo- & Chadwick-Furman 1999a). Replication rate has nes and soft corals may form aggregations or colonies been shown to vary >10-fold between clones of the that occupy large areas of hard substrate and thus com- temperate corallimorpharian Corynactis californica pete for space with stony corals on tropical reefs (Se- (Chadwick & Adams 1991). In the tropical coralli- bens 1976; Benayahu & Loya 1977; Langmead & morpharian Rhodactis indosinensis, replication rate Chadwick-Furman 1999a,b). Sea anemones occurring also varies between clones, and depends on seasonal on hard substrates on coral reefs include two distinct changes in seawater temperature (Chen et al. 1995b). types of organisms, the actiniarians (or true sea anem- Polyps of R. indosinensis vary their size and sex de- ones) and the corallimorpharians. The latter differ pending on whether they occur on the edge or in the from true sea anemones in that they lack muscles on center of clonal aggregations (Chen et al. 1995~).Pat- the pedal disk, and their internal morphology and nem- terns of clonal replication have been quantified in only atocysts are more similar to those of scleractinian cor- these 2 species of corallimorpharians, despite the eco- als (Carlgren 1949; den Hartog 1980). In molecular logical importance of this group in some mat-ine hab- phylogenetic analyses, corallimorpharians appear to itats. fall either within the Scleractinia (Fautin & Lowen- Clonal replication in corallimorpharians involves stein 1992) or within a separate group that includes several distinct modes per species, including pedal lac- the Actiniaria (Chen et al. 1995a). eration, fission (den Hartog 1980), and budding (Chen Some corallimorpharians undergo clonal replication et al. 1995b). In contrast, any one species of actinian to form large aggregations on hard marine substrates sea anemone generally uses only one of these clonal in temperate kelp forests (Chadwick 1991) and on modes (Chia 1976). In pedal laceration, the margin of tropical coral reefs (den Hartog 1980, 1994; Langmead the pedal disk constricts into small pieces that separate from the disk (Chia 1976). These small lacerated piec-

a Author for correspondence: Interuniversity Institute for es eventually regenerate a mouth and tentacles, thus Marine Science, PO. Box 469, Eilat, Israel. E-mail: forming new polyps. In longitudinal fission, the entire [email protected] polyp elongates longitudinally, the mouth splits and 352 Chadwick-Furman & Spiegel the column pinches in along the plane of fission. The Gardens fringing reef at Eilat, northern Red Sea polyp then divides in the center to form 2 or more (29’30’3 1”N, 35’55’22”E). This site contains large ag- equal-sized daughter polyps (Chadwick & Adams gregations of polyps of Rhodactis rhodostoma (Fig. l), 1991; Chen et al. 1995b). Although several types of and the benthic community structure and recent history budding occur in cnidarians (Chia 1976), only one of this reef have been well documented (Fishelson type, inverse budding, has been described for coralli- 1970; Loya 1990 and references therein). morpharians. In inverse budding, part of the margin of The flat, wide polyps of R. rhodostoma are up to 8 the pedal disk separates from the substrate, rises up, cm in diameter at this site. The oral disk is covered and becomes folded over the oral disk of the polyp with short, curly discal tentacles, surrounded by thick- (Chen et al. 1995b). Then the area connecting the bud er marginal tentacles that may be induced to form bul- to the maternal polyp constricts, and the bud separates bous white acrospheres upon contact with certain cni- and floats away as a detached propagule (Chen et al. darian competitors (Langmead & Chadwick-Furman 1995b). Little is known about the relative importance 1999b). The species identification of polyps was con- of each of these modes of cloning in corallimorphar- firmed by taxonomic experts (D.G. Fautin and J.C. den ians. Hartog). Several of the estimated 18 species in the tropical Preliminary observations on reefs at Eilat indicated corallimorpharian genus Rhodactis ( = Discosoma) that members of this species were patchy in occurrence (MILNEEDWARDS & HAIME1851) are known to repli- and limited to areas <3 m deep. We studied a reef site cate clonally (Carlgren 1949; den Hartog 1980). All with dense aggregations of R. rhodostoma (Fig. l), so members of this genus possess endosymbiotic zooxan- reported values probably represent maximal abundanc- thellae, and are limited to shallow marine substrates, es for this species at Eilat. Within the study site, a reef usually associated with coral reefs (den Hartog 1980). flat area with high abundance of polyps of R. rhodos- Individuals of R. indosinensis form small to large ag- toma was selected for placement of sampling transects. gregations via clonal replication on intertidal coral All transects were placed parallel to shore, along the reefs in Taiwan (Chen et al. 1995b). Polyps of a con- same area of shoreline. One 10x2 meter belt transect gener, R. rhodostoma (EHRENBERG1934), form patchy was deployed in each of 5 shallow reef zones: reef aggregations on shallow reef flats in the Indian Ocean patches in the lagoon, inner reef flat, middle reef flat, and Red Sea (Langmead & Chadwick-Furman 1999a outer reef flat, and shallow reef slope at 2.5 m depth. and references therein). In R. rhodostoma, polyps Within each of the 20 square meters of each transect, along the edges of the aggregations kill the tissues of all polyps of R. rhodostoma were counted and their some neighboring stony corals, and then overgrow percent cover estimated. their exposed skeletons by moving onto them and rep- We then randomly selected 3 aggregations, one each licating (Langmead & Chadwick-Furman 1999b). Pol- on the inner, middle, and outer reef flat. Within these yps of R. rhodostoma thus potentially compete with aggregations, we assessed variation in polyp size and reef-building corals and may replicate clonally to over- cloning rate with 3 factors: (1) aggregation (located on grow them. inner, middle, or outer reef flat), (2) position within Understanding clonal processes in R. rhodostoma is aggregation (center or edge), and (3) orientation within important in estimating potential rates of spread of this aggregation (horizontal or vertical) (modified after species across the reef. We describe here the abun- Chen et al. 199%). We defined as central those polyps dance and replicative patterns of polyps of R. rhodo- that were completely surrounded by conspecifics, and stoma on a reef flat at Eilat, Israel, northern Red Sea. as edge the polyps that were only partly surrounded We describe a unique mode of clonal replication in by other polyps, or were isolated from conspecific con- this species, estimate the doubling time for polyps, and tact. Horizontal polyps were defined as those attached discuss their current abundance in relation to recent to horizontal substrate, with their oral disks facing up- changes in the community structure of this reef. In a wards. Vertical polyps were defined as those on ver- companion paper, we show that sexual reproduction in tical walls of substrate, with their oral disks facing this corallimorpharian involves the annual spawning of sideways (modified after Chadwick-Furman & Loya large planktonic eggs that allow dispersal to distant 1992). reef habitats (Chadwick-Furman et al. 2000). Each month, we examined 25 polyps in each of 4 categories within each of the 3 aggregations: horizon- Methods tal central, horizontal edge, vertical central, and vertical edge (N = 100 polyps per month per aggrega- This project was conducted from September 1996 tion). All polyps were measured within a randomly to July 1998, on the shallow reef flat of the Japanese selected area of each category, until 25 polyps had Cloning in a corallimorpharian 353

Fig. 1. An aggregation of the corallimorpharian Rhodactis rhodostoma on the inner reef flat at the Japanese Gardens fringing reef, Eilat, northern Red Sea. Other organisms visible are macroalgae and a giant clam. Scale bar, 50 cm.

been sampled for each category each month. For each aggregations at the study site, and few observed at polyp examined, we measured the longest and shortest other reef areas in Eilat. Within the study site, the pol- oral disk diameter and calculated a mean diameter (af- yps occurred at low percent cover on reef patches in ter Lin et al. 1992; Chen et al. 1995b). We also the lagoon (Fig. 2A). They attained a maximal abun- checked the polyp for evidence of fission or budding, dance of 678 ? 561 polyps m-* (29 ? 23% cover) on such as elongation or constriction of the polyp margin, the inner reef flat, decreased in abundance toward the and described and photographed replicating polyps in outer reef flat, and were absent on the outer reef slope the field. In total, 6900 polyps were examined over (Fig. 2A). They formed small to large aggregations almost 2 years of field observations (300 polyps that were distributed patchily on the substrate, as dem- month-' X 23 months). onstrated by their large variation in percent cover and We calculated the doubling time for R. rhodostoma abundance between each square meter along the inner as the time to double the number of polyps in a clone flat transect (Fig. 2B). They occurred at amaximum of this species, from field observations of clonal rep- density of 69% cover and 1510 polyps m-2 (Figs. 1, lication (after Chadwick & Adams 1991). Statistical 2B). analyses were performed using the SAS program, ver- sion 6. Before application of parametric tests, data Modes of cloning were examined for normality and homogeneity of variances. Unless otherwise indicated, data are presented During monthly surveys, 625 polyps were observed as means 2 1 standard deviation. to replicate clonally (9.1% of all polyps, N = 6900). They used 3 distinct modes of cloning: longitudinal Results fission and inverse budding, which have been described previously (see above and Chen et al. 1995b), Distribution and abundance and marginal budding, which is described here for the On a large scale, polyps of Rhodactis rhodostoma first time. were patchy in occurrence, in that there were many Longitudinal fission was the most common mode of 354 Chadwick-Furman & Spiegel

1600 A Abundance Marginal budding occurred in 25.6% of replicating ,400 E3 Percent cover polyps. In this mode of cloning, which has never be- n 1 fore been described, a small area along the margin of the polyp, including part of the pedal disk, column, and oral disk, constricted into one or more buds that eventually separated from the parent polyp (Fig. 3E,F). Mouths, initially lacking in the buds, developed after separation from the parent polyp. Marginal budding led to the production of 2 or more unequal-sized pol- YPS. Inverse budding occurred in only 1.1% of replicat- " " ing polyps. Initially, part of the pedal disk detached Lagoon Inner Middle Outer Shallow from the substrate, rose up, and hung free in the water flat flat flat slope (Fig. 3G). Then the tissue constricted between this Reef habitat raised area and the rest of the polyp, resulting in a bud attached to the polyp by a narrow region of tissue (Fig. 3H). The upper part of the column connecting the bud to the parent polyp then contracted, so that the bud 1400 70 - v) hung upside down over the oral disk of the parent. N 1200 60 The bud finally separated completely from the parent E 0 a polyp and floated away. This type of cloning produced g 1000 50 % small polyp buds that were not initially attached to the 40 substrate. 0 Y 30 3 Seasonality of cloning 400 20 a The frequency of clonal replication in R. rhodosto- 200 10 ma, by all 3 modes together, varied widely between n n months (Fig. 4A). However, it did not vary signifi- 5 10 15 20 " cantly between the 2 years examined (t-test, t = 0.139, Distance along inner flat transect (m) p = 31). During the first year (Sept.1996-Aug.1997), 9.0 2 3.2% (N = 12 months) of polyps replicated each Fig. 2. Variation in the abundance and percent cover of pol- month, and during the second year (Sept.1997-July yps of the corallimorpharian Rhoductis rhodostornu. (A) A 1998), 9.1 ? 2.9% (N = 11 months) of polyps repli- series of 5 transects parallel to shore, from the inner lagoon cated each month. to the shallow outer reef slope (N = 20 1-m2quadrats ex- During both years, replication was maximal during amined per zone). (B) The inner reef flat transect with 20 1- m2 quadrats, showing the patchy distribution in a high-den- late spring (16.7% of polyps in May 1997 and 11.3% sity area. in April 1998) and early fall (10.7% in October 1996 and 14.0% in September 1997) (Fig. 4A). The lowest frequencies of replication were during winter (4.0% of replication, accounting for 73.3% of replicating pol- polyps in February 1997 and 6.3% of polyps in Jan- yps. To initiate fission, polyps elongated longitudinal- uary 1998) and mid-summer (7.3% of polyps in July ly, stretching the oral disk (Fig. 3A). Then the mouth 1997 and 5.3% in July 1998). Taken overall, the mean split, and the 2 new mouths separated from each other monthly values for replication rate did not correlate on the oral disk (Fig. 3B). The column and oral disk significantly with those for either day length or sea- constricted between the mouths, with the pedal disk water temperature (Fig. 4B) (Pearson's correlation test: areas separating last, and the polyp split into 2 ap- r = .24 and p = .26, r = .25 and p = .24, respectively). proximately equal daughter polyps. Separation of the However, the decline in cloning during mid-summer daughter polyps resulted in a tearing of the column coincided with the annual spawning of gametes, and wall and exposure of the mesenteries and gastrovas- when the months immediately before and after the an- cular cavity (Fig. 3C). Finally, the torn sides of the nual spawning event (Fig. 4A) were excluded from column rolled inward and fused. Longitudinal fission analysis, cloning rate correlated significantly with both occasionally resulted in the formation of 3 or 4 daugh- day length and seawater temperature (Pearson's cor- ter polyps (Fig. 3D). relation test: r = .49 and p<.05; r = .68 and p<.Ol, Cloning in a corallimorpharian 355

Fig. 3. Modes of cloning in the corallimorpharian Rhodactis rhodostoma. Diameter of each polyp, 4-6 cm. (A) Polyp elongation at the staft of longitudinal fission. (B) Separation of 2 mouths on the elongated oral disk during fission. (Cj Constriction of the column and oral disk to complete separation of daughter polyps during fission. Note exposed mesenteries at center. (D) Three-mouth fission, resulting in 3 daughter polyps of about equal size. Mouth (mj. (E,F) Marginal budding: areas of constriction (b) along the polyp margin lead to the formation of new polyps. (G) Inverse budding: bud formation after detachment of part of the pedal disk from the substrate. (Hj Inverse budding: bud raised up over the oral disk of a parent polyp. respectively). Day length explained more of the vari- did not differ significantly in size from non-cloning ation in replication rate than did seawater temperature polyps (35.1 -C 9.4 mm), but budding polyps (44.3 5 (multiple regression test, partial r2 = -46 and .21 re- 7.0 mm) were significantly larger than those in the spectively). The annual cycle for fission was similar other 2 categories (multiple comparisons t-test, t = to that for total replication, with maxima in both April/ 1.86, LSD = 4.53, Fig. 5). Polyps initiated fission only May and September. The frequency of marginal bud- if >16 mm diameter (N = 32), and budded only if ding peaked only in AprilJMay each year, and no sea- they were >30 mm diameter (N = 17, Fig. 5). sonal frequency peaks were observed for the rare Polyp size varied significantly with 2 other factors mode of inverse budding. examined (Table 1, model I1 3-way ANOVA test). Ver- tical polyps were significantly larger than horizontal Polyp size polyps, and central polyps were larger than edge pol- The mode of cloning varied significantly with polyp yps (Fig. 6A, Table l). Polyp size did not vary signif- size (model I1 one-way ANOVA, df = 2, 297, F = icantly among the 3 aggregations examined (Fig. 6A, 8.05, p<.OOl), as measured during May 1997 when Table 1). Cloning frequency also did not vary signif- cloning frequency was maximal (Figs. 4A, 5). Polyps icantly with any of the 3 factors examined (aggrega- that underwent fission (diameter = 34.9 ? 8.8 mm) tion, position, or orientation within aggregations) (Chi- 356 Chadwick-Furman & Spiegel

25jA reef flat was 27,480 polyps in 80 m2 of substrate area, 4 or 343 polyps m-*. This number of polyps could have been produced from 10 initial recruits within 7 to 14 years, depending on the duration of each replication event.

Discussion Distribution and abundance We demonstrate here that polyps of the corallimorpharian Rhodactis rhodostoma occur at high abun- 0 ASON D 1 F MAMJ I ASOND I F MAMl J A dance on a reef flat at Eilat, northern Red Sea. We also 1996 1997 1998 reveal a strong cross-reef zonation pattern for members of this species. Polyps occurred at high densities on - .o- . day length the inner reef flat, decreased toward the outer reef flat, 30 l5 1 B +water temperature r and were absent on the reef slope (Figs. 1, 2). The P. ,' 9 0 '0 higher abundance of polyps on the inner vs. outer reef ,,Is 0' no flat (Fig. 2A) leads us to propose that conditions are more favorable for members of this species on the inner reef flat, possibly due to relatively low levels of water motion. Corallimorpharians in the genus Rhodactis form aggregations of varying size on shallow reefs throughout the tropics (den Hartog 1980, 1994), and deserve fur- 1 ther study of their spatial extent and ecological im- 18 portance. Large aggregations of Rhodactis ( = Dis- ASONL) 1 I MAMl IASOND 1 FMAMI IA 1996 1997 1998 cosoma) polyps have been reported on coral reefs in the Caribbean (den Hartog 1980; Elliot & Cook 1989), Fig. 4. Seasonal variation in physical factors and in cloning rate of the corallimo@arian Rhodactis rhodostoma. (A) Seychelles (den Hartog 1994), Malaysia (Ridzwan Proportion of cloning polyps as measured for 3 aggregations 1993), and Taiwan (Chen et al. 1995b). In a previous (N = 100 polyps per aggregation). Arrows indicate the tim- study at Eilat, we also documented dense aggregations ing of annual broadcast spawning of gametes (Chadwick- of polyps of R. rhodostoma on the reef flat (Langmead Furman et al. 2000). (B) Day length and seawater tempera- & Chadwick-Furman 1999a). At nearby Ras Abu Gal- ture at 3 m depth, from daily measurements at Eilat (source: um, south of Eilat in the Egyptian Red Sea, individuals Israeli Meteorological Service, Beit Dagan). of R. rhodostoma similarly dominate the substrate on the protected inner reef flat, forming an almost contin- squared 4-way frequency test, p>.05 for all variables, uous carpet of polyps over >lo0 m2 of reef area (N.E. Fig. 6B). Chadwick-Furman, unpubl. obs.).

Doubling time of polyps Modes of cloning To estimate the doubling time for polyps of R. rho- The use of longitudinal fission as the main mode of dostoma, we assumed an initial aggregation size of cloning in R. rhodostoma is similar to the pattern 100 polyps. We then used the mean percent of polyps known for several other corallimorpharians (reviewed that replicated each month during the first year, since in Chen et al. 1995b). Longitudinal fission occurs in there was no significant between-year variation (see an almost identical proportion of polyps in R. rhodo- above). We assumed that each replication event re- stoma (73% of dividing polyps) and R. indosinensis quired 1-2 months for completion (after Chen et al. (74% of dividing polyps, Chen et al. 1995b). 1995b). If each replication event required one month Inverse budding (Fig. 3G,H) is relatively rare in R. or less, and 9.0% of the polyps replicated each month rhodostoma, and has been reported previously only in (see above), the aggregation became 2.8X larger each R. indosinensis (Chen et al. 1995b). This unusual type year, and if each division event required 2 months, the of cloning apparently produces detached polyps that aggregation became 1.7X larger each year. The total float away to colonize other locations. It would be in- number of polyps counted within transects on the Eilat teresting to know if this mode of cloning occurs in any Cloning in a corallimorpharian 357

0Not replicating (N=25 1) had been produced by pedal laceration (reviewed in El Fissioning (N=32) Chen et al. 1995b).

120 1 H Budding (N= 17) Seasonality of cloning The polyps of many tropical zooxanthellate anthozoans appear to grow and replicate fastest when light and/or temperature levels are highest, thus facilitating 80 8a maximal photosynthetic energy production by their zo- cci oxanthellae (reviewed by Highsmith 1979; Lin et al. 0 n L 1992; Chen et al. 1995b). Because zooxanthellae often supply 100% or more of the carbon needs of tropical anthozoan species (Tsuchida & Potts 1994 and references therein), seasonal variation in planktonic food availability may be a less important factor than it is for temperate zone anthozoans. Plankton abundance varies seasonally at Eilat, reaching a maximum during 10 20 30 40 50 60 70 the spring each year (March to May, Genin et al. 1995). Both maximal plankton abundance and rising Oral disk diameter (mm) levels of day length and temperature may contribute to high cloning rates in R. rhodostornu during the late Fig. 5. Size-frequency distribution for polyps of the coral- spring at Eilat (Fig. 4A). limorpharian Rhodactis rhodostoma, showing variation in We observed cloning rates drop in midsummer size with mode of cloning. Data are from May 1997, when when the polyps spawned gametes (Fig. 4A). Imme- cloning was most common. diately before spawning, female polyps of R. rhodostoma are full of eggs, which represent up to 30% of of the other 18 known Rhodactis ( = Discosoma) spe- their body mass (Chadwick-Furman et al. 2000). Thus, cies (Carlgren 1949; den Hartog 1980), and also polyps devote a large proportion of their energy and whether it is limited only to members of this tropical body space to the production of gametes during the corallimorpharian genus. month or two immediately before spawning. The third mode of replication described here, mar- We propose that the observed drop in cloning in this ginal budding, has never been reported previously, ei- species during mid-summer, when physical conditions ther for corallimorpharians (Chen et al. 1995b) or for appear to be best for photosynthesis and growth (Fig. actinian sea anemones (Chia 1976). While similar to 4B), is due to a temporary diversion of energy to sex- pedal laceration, which likewise involves separation of ual reproduction. Division may remain low for a part of the pedal disk from the parent polyp (reviewed month or two after spawning because of tissue repair in Chia 1976), marginal budding differs in that it also and reorganization processes following the release of incorporates part of the column and oral disk in each large volumes of gametes from the polyps’ mesenter- bud (Fig. 3E,F). Marginal budding may occur in other ies. Similarly, with the exception of juveniles, colonies common corallimorpharians, since it would be rela- of the stony coral Stylophora pistilluta also decrease tively easy to mistakenly suppose these marginal buds their rate of colony growth during mid-summer at Ei-

Table 1. Model I1 3-way analysis of variance of polyp size with 3 factors in the tropical corallimorpharian Rhodactis rhodostoma at Eilat, northern Red Sea.

Source of variation df ss F-value P Aggregation 2 290.81 2.47 .0865 Central vs. edge position 1 2,560.84 43.48 .0001 Horizontal vs. vertical orientation 1 6,659.94 113.07 .0001 Aggregation X position 2 186.66 1.58 .2068 Aggregation X orientation 2 227.27 1.93 .4171 Position X orientation 1 5.74 0.10 .7551 Aggregation X position X orientation 2 999.80 8.49 .0003 Error 288 16,963.92 358 Chadwick-Furman & Spiegel

Position: Polyp size Ul Vertical center Vertical edge Orientation: Variation in the mode of replication with polyp size Horizontal center R Horizontal edge (Fig. 5) has been observed in other corallimorpharians A (Chen et al. 1995b) and actinian sea anemones (Sebens 6o 1 I 1982; Lin et al. 1992). Only budding polyps were larger than average in R. rhodostoma (Fig. 5). Thus, large size does not appear to be a necessary prerequisite for fission in R. rhodostoma. Our field observations also showed that the relatively large polyps in the center of aggregations and on vertical surfaces did not clone more frequently than those in other positions (compare Fig. 6A and B). The significant variation in polyp size with position and orientation in aggregations (Fig. 6A, Table 1) may relate to differences in environmental conditions between microhabitats. The significantly larger size of Inner Middle Outer polyps in vertical than in horizontal orientations (Fig. 6A) may be due to less exposure to environmental 6o 1 stressors such as ultraviolet radiation and sedimenta- B tion on vertical reef surfaces. During extreme low I I tides, vertical polyps in reef depressions are less sus- ceptible to the drying effects of air than are those exposed on the upper horizontal surface of the reef flat. Similar variation in polyp size with habitat has been documented for intertidal actinians, where polyps increase in size with depth (Francis 1976), and with location in sheltered crevices or rocky depressions (Se- bens 1983). The larger size of polyps of R. rhodostoma in the center of aggregations, compared to those on the edg- Inner Middle Outer es, is similar to the pattern documented for R. indosinensis in Taiwan (Chen et al. 199%). In both species, Location of aggregation on reef flat most central polyps are large and female, while edge Fig. 6. Variation in (A) polyp size and (B) percent of cloning polyps are smaller and mostly male (Chen et al. 1995~; polyps with 3 factors: aggregation (located on inner, middle, Chadwick-Furman et al. 2000). In R. indosinensis, pol- or outer reef flat), position within aggregation (central or yps change size and sex when cross-transplanted, dem- edge), and orientation within aggregation (horizontal or ver- onstrating that position within an aggregation tical) in the corallimorpharian Rhoductis rhodostoma. At the influences gonadal development and body size (Chen time of peak cloning, in May 1997, 25 polyps were exam- et al. 1995~). ined from each of the 12 categories (N = 300, 25 per category). Variances in B are expressed as the 95% confidence Doubling time of polyps limit of the proportion of polyps observed to clone in each category, out of 25 polyps observed. Our analyses reveal that a high proportion of polyps of R. rhodostoma may be replicating at any given time (Fig. 4A), leading to the formation of large clones lat, possibly due to a diversion of energy from growth within a short period on the inner reef flat. It was not to sex during the summer season (Loya 1985). Other possible to determine the duration of or time since anthozoans are known to have different seasonal pat- each replication event because, in contrast to polyps terns of sexual reproduction and clonal replication of R. indosinensis (Chen et al. 1995b), those of R. (reviewed in Chadwick-Furman et al. 2000). In R. rhodostoma do not exhibit clear body scars after fis- rhodostoma and in other anthozoans, clonal growth sion or budding. However, these processes probably appears to be controlled by both exogenous (temper- are similar in duration to those in R. indosinensis, ature, light) and endogenous (sexual reproductive) which requires 1-2 months to complete of each act of factors. fission or budding (Chen et al. 199%). The highest Cloning in a corallimorpharian 359 proportion of replicating polyps observed in R. rho- Acknowledgments. We thank the staff of the Interuniversity dostoma (16.7% of polyps in May, Fig. 4A) is similar Institute for Marine Science in Eilat, especially Karen Tar- to that recorded for R. indosinensis (20.9% of polyps naruder for preparation of the graphics. We also thank Ra- during June-July, Chen et al. 1995b). chel Levi and Tami Anker of the Life Sciences Faculty at The doubling time of about 1 year calculated for Bar Ilan University, for help with statistical analyses and preparation of the photographic figures. The manuscript was polyps of R. rhodostoma at Eilat is slower than the 2 improved by comments from Hudi Benayahu, David Glas- month period estimated for the temperate corallimor- som, and 2 anonymous reviewers. Funding was provided by pharian Corynactis californica and for some actinians, a grant to N.E.C.-E from the Israel Science Foundation. This but is faster than rates of >1 year estimated for some project was completed in partial fulfillment for an MSc. scleractinian corals (Chadwick & Adams 1991 and ref- degree by M.S. at Bar Ilan University. erences therein). Our calculations for R. rhodostoma at Eilat predict a doubling time similar to that esti- References mated for aggregations of R. dawydofi in Malaysia (100-160% increase in number of polyps in 18 Benayahu Y & Loya Y 1977. Space partitioning by stony months, Ridzwan 1993). This may explain why dense corals, soft corals and benthic algae on the coral reefs of the northern Gulf of Eilat (Red Sea). Helgolander Wiss. populations of polyps of Rhodactis spp. have not pre- Meeresunters. 30: 362-382. viously been reported for these reefs. Carlgren 0 1949. A survey of the Ptychodactiaria, Coralli- Today, on some parts of the inner reef flat at Eilat, morpharia and Actiniaria. Kungl. Svenska Vetenskaps. aggregations of R. rhodostoma have become an alter- Handl. 1: 14-16. nate dominant (Figs. 1, 2) to the stony corals that were Chadwick NE 1991. Spatial distribution and the effects of major space occupiers before a recent disturbance competition on some temperate Scleractinia and Coralli- event (Loya 1990). This reef was exposed to a cata- morpharia. Mar. Ecol. Prog. Ser. 70: 39-48. strophic low tide in 1970, which caused a massive Chadwick NE & Adams C 1991. Locomotion, asexual re- death of stony corals and left most of the reef flat as production and killing of corals by the corallimorpharian bare, unoccupied substrate (Loya 1990). The large ag- Corynactis ca1i;fornica. 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