Sexual Reproduction in the Tropical Corallimorpharian Rhodactis Rhodostoma

Invertebrate Biology 119(4): 361-369. 0 2000 American Microscopical Society, Inc.

Sexual reproduction in the tropical corallimorpharian Rhodactis rhodostoma

Nanette E. Chadwick-Furman,” Michael Spiegel, and Ilana Nir

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

Abstract. Polyps of the tropical corallimorpharian Rhodactis rhodostoma segregate sexes between center and edge positions within aggregations produced by clonal replication. On a reef flat at Eilat, northern Red Sea, infertile polyps and males occur mainly along the edges of clonal aggregations, while females mostly occupy central positions within each aggregation. In addition, on the inner to middle reef flat where polyps of this species are abundant, aggregations consist mostly of females. On the outer reef flat, where polyps are rare, a sampled aggregation consisted mostly of males and infertile polyps. Male polyps are significantly smaller than females, and the smallest polyps are infertile. Fecundity increases significantly with polyp size in females, but testis size and number do not vary with body size in males. Oocytes are present in polyps during most of the year and gradually increase in size until annual spawning in June- July during the period of maximum day length. Testes do not vary significantly in size during the year and remain a small proportion of body mass (<8%). In contrast, females invest up to 30% of their body mass into gonads during the months immediately before spawning. The annual spawning of gametes coincides with a temporary drop in the frequency of clonal replication by polyps. We estimate that each female polyp of R. rhodostoma may release up to 3000 large eggs (500 p,m in maximum diameter) each summer. The high investment of this corallimorpharian in sexual production of planktonic propagules may allow rapid dispersal to reef habitats distant from parent populations.

Additional key words: Cnidaria, coral reef, sea anemone, Red Sea, gonad index

Most research on sexual reproduction in actinian sea anemones, but are more closely related to scleractinian anemones has focused on species occurring in tem- corals (reviewed in den Hartog 1980). Little is known perate to cold-water environments (reviewed in Shick about the biology of corallimorpharians, even though 1991). In most of the >30 species of actinians exam- they are important occupiers of space in some tem- ined thus far, gametogenesis follows an annual cycle, perate and tropical benthic marine ecosystems (Chad- with polyps broadcasting gametes during spring to fall, wick 1991 ; Chadwick-Furman & Spiegel 2000). Pat- and the exact spawning period varying among species. terns of sexual reproduction have been investigated in In contrast, we know little about sexual reproductive only 2 species, both of which form large aggregations processes in tropical actinians. In one species exam- via clonal replication. In the temperate Corynactis cal- ined in Taiwan, polyps synchronously spawn gametes ifornica, all polyps in each clonal group are the same in mid-summer each year, during the period of peak sex, and gametogenesis leads to annual synchronous day length and temperature (Lin et al. 1992). Actinians spawning of gametes during winter (Holts & Beau- examined in Malaysia and Florida exhibit patterns of champ 1993). In contrast, in the tropical Rhodactis brooding, hermaphroditism, and diffuse spawning over ( = Discosoma) indosinensis, polyp size and sex are a long period each year (Jennison 1981; Dunn 1982). influenced by position within each clonal aggregation, The corallimorpharians are a group of soft-bodied with edge polyps small and male, and central polyps anthozoans that superficially resemble actinian sea larger and female (Chen et al. 1995b). This species follows an annual gametogenetic cycle in both sexes,

a Author for correspondence: Interuniversity Institute for with gamete spawning in midsummer during the pe- Marine Science, PO. Box 469, Eilat, Israel. E-mail: riod of peak seawater temperature and day length furman @ mail.biu.ac.il (Chen et al. 1995a). 362 Chadwick-Furman, Spiegel, & Nir

In the Red Sea and Indian Ocean, one of the dom- polyp was dissected to determine sex and reproductive inant corallimorpharians is Rhodactis (= Discosoma) state, and sex ratio was calculated. In 4 of the 16 pol- rhodostoma (EHRENBERG1934), which forms aggre- yps collected each month, all gonads and, in females, gations of various sizes mainly in shallow coral reef all oocytes were counted in whole preserved polyps. environments (den Hartog 1994; Chadwick-Furman Fecundity was defined as the number of oocytes per & Spiegel 2000). Polyps of R. rhodostoma replicate polyp. In addition, from October 1996 to June 1997 clonally by at least 3 distinct modes at a rate that (when gonads were large enough to manipulate), all permits them to rapidly monopolize large areas of the gonads were removed from 3 male and 3 female space on some reefs (Chadwick-Furman & Spiegel polyps each month. Gonads and polyps were dried 2000). In addition, polyps that contact stony-coral separately at 100°C for 24 h. Their preserved dry mas- competitors develop specialized marginal tentacles ses then were used to calculate a gonad index (GI), that damage their neighbors' tissues, after which the which was the relation of dry gonad mass to that of polyps move onto the coral skeletons and overgrow the entire animal, including gonads as well as the pol- them (Langmead & Chadwick-Furman 1999a). Rapid yp body (after Wedi & Dunn 1983). This index also clonal spread and aggressive damage to neighbors al- was used to determine reproductive effort and to assess low polyps of R. rhodostoma to become an alternate the rate of gonadal development during the year. Fi- dominant to stony corals in some disturbed reef areas nally, gonad samples were removed from an additional (Chadwick-Furman & Spiegel 2000). The ability of 6 of the 16 collected polyps each month for histolog- individuals of R. rhodostoma to become established ical analyses of gametogenesis. The tissues were im- on widely-separated reefs may depend largely on the bedded in paraffin blocks; 8-km sections were mount- extent of their investment in sexual production of dis- ed on slides and stained with hematoxylin and eosin persing planktonic larvae. We present here informa- for observation of gonad development (after Wedi & tion on patterns of sex ratio, gametogenesis, and Dunn 1983; Lin et al. 1992; Holts & Beauchamp mode of sexual reproduction in R. rhodostoma. We 1993). also discuss annual cycles of sexual reproduction vs. In each female, 5-50 oocytes that contained nuclei clonal replication, and the role of each process in the were measured each month. The maturity phases of ecology of this species. male gonads were not scored, because they did not show clearly distinct developmental phases throughout Methods the year (see below). All wet and dry masses given in the text were ob- Sexual reproduction in aggregations of the coralli- tained directly from preserved polyps, and not esti- morpharian Rhodactis rhodostoma was examined for mated from other parameters of polyp size. Statistical 2 years (July 1996-June 1998) on the shallow reef flat analyses were performed using the SAS program, ver- of the Japanese Gardens fringing reef inside the Coral sion 6. Before application of parametric tests, data Beach Nature Reserve at Eilat, Israel (northern Red were examined for normality and homogeneity of var- Sea, 29"30'3 1"N, 35'55'22"E). We randomly selected iances. Unless otherwise indicated, data are presented 4 aggregations, 2 on the inner reef flat, and 1 each on as means -+ 1 standard deviation. the middle and outer reef flat (in a separate study, dif- ferent aggregations were examined for clonal replica- Results tion, see Chadwick-Furman & Spiegel 2000). Each Gonads and sex ratio month we collected 16 polyps, 4 polyps from each of the same 4 aggregations. Within each aggregation, 2 Mature polyps of Rhodactis rhodostoma were either randomly selected polyps were collected from central male or female. Most mesenteries each bore a single positions, and 2 from along the edges (see Chadwick- gonad near the polyp base. Females were distinguished Furman & Spiegel 2000). The specimens were trans- by the presence of ovaries with developing oocytes, ferred to the nearby Interuniversity Institute for Marine which grew to fill much of the polyp before spawning Science in Eilat, anesthetized in 7.2% MgCl, at a ratio (Fig. 1A,B). Each preserved ovary contained a grape- of 1: 1 with seawater (for one hour or until the polyps like cluster of spherical, light-brown oocytes (Fig. became desensitized), and preserved in 10% formalin lC,D). Males had small white testes, each testis con- (after Sebens 1981; Wedi & Dunn 1983; Chen et al. sisting of a one-chambered sac (Fig. 1E,F). 1995a). Most female polyps were located in the center of After blotting off excess water, each preserved pol- aggregations, while most males were on the edges, and yp was weighed and the oral disk diameter was mea- the few polyps lacking gonads occurred mostly on the sured (modified after Wedi & Dunn 1983). Then each edges (Fig. 2). Of the polyps collected from the center Sexual reproduction in a corallimorpharian 363

Fig. 1. Gonads of the corallimorpharian Rhodactis rhodostoma. (A) Aboral view of preserved polyps with pedal disks removed, female on left with ripe ovaries and male on right with ripe testes. Scale bar, 1 cm. (B) Close-up of female polyp with ovaries on mesenteries. Visible are mesenteries, convoluted mesenterial filaments, and spherical oocytes. Scale bar, 1 mm. (C) A complete mesentery with an ovary containing 14 oocytes. Scale bar, 1 mm. (D) Histological section of an ovary showing developing oocytes in January 1997. In the largest oocyte, a nucleus (n) and dense yolk granules (g) are visible. Scale bar, 100 p,m. (E) Closeup of male polyp showing one testis (t), mesenteries, and mesenterial filaments. Scale bar, 1 mm. (F) A complete mesentery with testis (t). Scale bar, 1 mm. of aggregations, most were females (69.4%), some In 3 of the 4 aggregations examined, the number of were males (28.0%), and a few had no gonads (2.6%), females exceeded males, with a ratio of approximately giving a sex ratio of 2.5:l females to males in central 2:l females to males, because most polyps in central positions (Fig. 2A). In contrast, along the edge of ag- positions were female (Fig. 2A). The aggregation ex- gregations, most polyps were males (54.0%) and some amined on the outer reef flat differed from those in the were females (39.8%), giving a sex ratio of 0.7:l fe- other reef zones, in sex ratio. It was the only aggre- males to males (Fig. 2B). A higher proportion of pol- gation in which males exceeded females (ratio of only yps with no gonads (6.3%) occurred along the edges 0.3:l females to males), and it had the highest pro- of aggregations than in the centers. portion of polyps with no gonads (Fig. 2). The sex 364 Chadwick-Furman, Spiegel, & Nir ratio for all 4 aggregations together (N = 224 polyps) No gonads ElMale Female was 1.3:1 females to males. Sex ratios varied significantly both within and between examined aggregations 100 1 A. Center of aggregation (2-way Chi-square frequency test, x2 = 26.45 and 14.77, p<.OO1 for both variables, Fig. 2).

Size at sexual maturity All 3 of the measurements made on preserved polyps correlated strongly with those made on live polyps. The oral disk diameter of preserved polyps varied linearly with their oral disk diameter when live (linear regression test, r2 = .74, p<.OO1, N = 28 polyps). Polyps shrank when preserved by about 30% of their live oral disk diameter (live diameter = (1 SO? 0.3 1) X preserved diameter). The wet and dry mass of preserved polyps (M,,, and Mdry,expressed in grams) both increased exponentially with live oral disk diameter (Dhve,expressed in centimeters): M,,, = 0.06 D1,,2.44(r2 = .73, N = 96, p<.OOl) Mdly= 0.0071 D1,v2.54(r2 = 38, N = 36, p<.OO1) B. Edge of aggregation Thus, the wet mass of preserved polyps was used to estimate live polyp size, except in gonad index cal- 3 culations, where dry mass was used (see Methods). Above minimum reproductive size, the smallest re- producers were males and the largest were females (Fig. 3). Male polyps (preserved wet mass = 2.4 f- 0.9 g, N = 81 polyps) were significantly smaller than females (preserved wet mass = 3.3 t 1.0 g, N = 108 polyps), and infertile polyps (preserved wet mass = 1.5 +- 0.3 g, N = 10) were smallest of all (Multiple comparisons t-test, t = 1.97, LSD = 0.52, p<.05 for all pairs, Fig. 3). All fertile polyps in the smallest size class (<1 g> were males, and a11 polyps in the largest Inner reef Inner reef Md reef Outer reef size class (>6 g) were females (Fig. 3). In addition, #1 #2 the minimum size at maturity for males (0.6 g pre- Location of aggregation on reef flat served wet mass) was only half that for females (1.2 g preserved wet mass). Overall, sexual reproductive Fig. 2. Variation in sex ratio between 4 aggregations of the status varied significantly with polyp size (ANOVA, F corallimorpharian Rhoductis rhodostomu on a reef flat at Ei- = 33.66, pc.001). lat, northern Red Sea. Data are from October 1996 to June 1997 and January to May 1998, when gonads were well- Gonad development as a function of polyp size developed. In each of 8 possible positions, 26-29 polyps were collected total. N = 224 polyps were collected in all In females, fecundity (number of oocytes per polyp) positions (16 polyps each month X 14 months). (A) Polyps increased significantly with preserved polyp wet mass in the center of each aggregation. (B) Polyps along the edge (Fig. 4). This trend was due to the significant increase of each aggregation. in the number of oocytes per ovary with polyp size (Table 1). The number of oocytes in each ovary varied from 5 in the smallest polyp observed to 22 in the Males had 40-120 testes per polyp. The number of largest polyp observed. testes per polyp did not vary significantly with polyp Females had 70-180 ovaries per polyp, 1 each on size (Table 1). most of their mesenteries. The number of ovaries per Gonad index (the proportion of body mass devoted polyp did not vary significantly with polyp size (Table to gonads) did not correlate significantly with polyp 1). size, in either males or females (Table 1). Sexual reproduction in a corallimorpharian 365

50 each year (Fig. 5) but did not change in size during the year (Fig. 6). Sperms and oocytes apparently were spawned si- CA 40 multaneously in June-July each year, because testes 3e and oocytes both disappeared during the same period 30 in most polyps (Fig. 5A). Fertilization probably oc- 41 0 curred externally, as no fertilized eggs or developing et3 20 embryos were found within polyps. E During July and August each year, most polyps did 5 not have gonads. In July, a few females retained scat- z 10 tered large oocytes, but these disappeared by August, when new small oocytes began to develop (Fig. 5). 0 Histological examination of ovaries revealed devel- 012 34567oping oocytes with nuclei and dense yolk granules (Fig. 1D). However, histological sections of testes did Polyp size (preserved wet mass, g) not reveal a clear annual cycle of sperm development. Testes were present and distinguishable in male polyps Fig. 3. Variation in polyp size with sexual reproductive sta- during most of the year (Fig. 5A) but remained small tus in the corallimorpharian Rhoductis rhodostoma at Eilat, northern Red Sea. Data are from October 1996 to June 1997 and constant in size (Fig. 1E,F). and January to May 1998, when gonads were well-devel- The gonad index increased significantly over time oped. for females but not for males (Table 1, Fig. 6). Female gonad index rose sharply during spring 1997 (March to June), indicating rapid growth of oocytes during the Annual reproductive cycle months immediately before spawning (Fig. 6). Ovaries Oocytes were small but present in most polyps start- represented an investment of up to 30% of female pol- ing in September-October each year (Figs. 5, 6).They yp mass by the end of the reproductive cycle (20.7 ? increased in size gradually during the year, reaching a 8.2% in June 1997, Fig. 6). The gonad index of males maximum diameter of 500 km in June-July (Fig. 5). did not show a clear trend of increase over time, and Testes were also present and well-developed in remained low at <8% of male body mass throughout many polyps from September-October to June-July the entire period of spermatogenesis (4.6 k 2.6% in May 1997, Fig. 6).

N = 26 polyps Discussion 4000 y = 381.6~+ 396.7 Gonads and sex ratio fi 1 e r2 = .33 We demonstrate here an unusual pattern of sexual 30 30100 { .ck p < .O1 dispersion within clones of a tropical corallimorphar- rA -1 . a, ian. Sex ratio depends upon polyp position within ag- Yx 0 gregations of Rhodactis rhodostoma at Eilat, a pattern 8 2000 also known for R. indosinensis in Taiwan. In both spe- 5 cies, polyps in the center of aggregations are mostly ._0 large and female, while those along the edges are a .* . smaller and often male or infertile (Chen et al. 1995b; $ 1000 /. Chadwick-Furman & Spiegel 2000) (Fig. 2). In R. in- a, c4 *. dosinensis, the segregation of sex by position is even stronger than in R. rhodostoma, with almost all males 1 on the edges and all females in the center of aggre- o! I I I I I 1 gations (Chen et al. 1995b). Field experiments with R. 0 1 2 3 4 5 6 indosinensis have demonstrated that polyps change sex and size when cross-transplanted between central and Polyp size (preserved wet mass, g) edge positions (Chen et al. 1995b). Thus, in the 2 Fig. 4. Relationship of oocyte number (fecundity) to polyp members of this genus examined thus far, sexuality size in female polyps of the corallimorpharian Rhodactis appears to be determined by environment. rhodostoma. Actinian sea anemone polyps also may vary their 366 Chadwick-Furman, Spiegel, & Nir

Table 1. Gonadal characteristics of the corallimorpharian Rhoductis rhodostoma. Results are for Pearson’s correlation test, p-values give significance of the slope. GI = Gonad index (dry gonad mass/dry polyp mass), G, = gonad (testis or ovary) number per polyp, 0, = mean number of oocytes per ovary in each polyp, Mdry= polyp dry mass (g), M,,, = preserved polyp wet mass (g), Ti = time (months).

Males Females Factors N Slope Intercept r2 P N Slope Intercept r2 P

GI VS. M,,, 24 -0.001 0.02 .0002 .95 27 -0.12 0.17 .07 .18 0, vs. MW,, - - - - - 27 2.17 5.16 .24 .009 G, vs. M,,, 25 10.92 47.93 .14 .07 27 4.76 120.92 .03 .39 GI vs. Ti 24 0.0004 0.02 .04 .33 27 0.007 0.005 .68 .oo 1 condition and sexual status with position in aggrega- observed in R. rhodostoma (up to 30% of body mass tions. In the common aggregating actinian Anthopleu- invested into oocytes, Fig. 6) is greater than values ra elegantissima, mid-aggregation polyps are fertile reported for actinian sea anemones (reviewed by Shick and large, while edge polyps are mostly infertile and 1991). In addition, mature oocytes in R. rhodostoma smaller, but possess highly developed weaponry for (maximum diameter = 500 pm) are larger than those interclonal competition (Francis 1976). This pattern in- of most other corallimorpharians (Holts & Beauchamp dicates that polyps along the edges of aggregations 1993; Chen et al. 1995a) and actinians (Shick 1991). may allocate more energy into the defense of living Thus, female polyps of R. rhodostoma appear to al- space against competitors than into sexual reproduc- locate a relatively large proportion of their energy to- tion. Individuals of R. rhodostoma along the edges of ward sexual reproduction, especially during late spring aggregations also invest energy into spatial defense to summer (Fig. 6). Such high investment into sex may and the development of specialized weaponry (Lang- explain in part why most polyps produced oocytes mead & Chadwick-Furman 1999a,b), and thus may only under certain environmental conditions, such as have fewer resources left over for sexual reproduction those in the center of aggregations on the middle to than do polyps located in the center of aggregations. inner reef flat, while polyps under other, possibly less The low proportion of females in the aggregation optimal conditions often remained infertile or pro- examined on the outer reef flat (Fig. 2) may be due to duced sperm (Fig. 2). The high gonad index for fe- suboptimal conditions for R. rhodostoma in this hab- males of R. rhodostoma also may explain why mem- itat, where polyps of this species are rare in contrast bers of this species slow their fission rate just before to their abundance on the middle and inner reef flat spawning (Chadwick-Furman & Spiegel 2000), while (Chadwick-Furman & Spiegel 2000). those of a congener do not (Chen et al. 1995a). Each female polyp of R. rhodostoma produces up to 3000 Size at sexual maturity large eggs per year (Fig. 4), a high fecundity rate rel- Females are significantly larger than males in both ative to actinian sea anemones that are known to pro- the corallimorpharians R. rhodostoma (Fig. 3) and R. duce large eggs (Shick 1991). indosinensis (Chen et al. 1995a), as well as in some The pattern of development in R. rhodostoma may actinian sea anemone species that produce large eggs be classified as oviparous-planktonic-lecithotrophic (Shick 1991). The polyps of some species may need (Chia 1976; Shick 1991), in that large, yolk-rich eggs to achieve a relatively large minimum size before be- are released into the plankton. coming female, due to their high investment of energy and body space into large eggs (Jennison 1981 ; Shick Annual reproductive cycle 1991). Minimum sizes at maturity in R. rhodostoma The tropical corallimorpharian R. rhodostoma has (0.6 g preserved wet mass for males and 1.2 g for an annual cycle of sexual reproduction, with spawning females) are smaller than those known for R. indosi- of polyps during midsummer at Eilat (Fig. 5), when nensis (-3 g preserved wet mass, for males and -5 g days are longest and temperature is approaching its for females, calculated from figs. 2 and 3 in Chen et annual maximum (Chadwick-Furman & Spiegel al. 1995a). 2000). This annual pattern also occurs in R. indosensis in Taiwan (Chen et al. 1995a), and in littoral actinians, Gonad development as a function of polyp size most of which spawn at peak annual temperatures (re- We report here for the first time gonad index values viewed in Shick 1991). Experimental studies indicate for a corallimorpharian. The high gonad index that we that increasing photoperiod also may trigger rapid oo- Sexual reproduction in a corallimorpharian 367

A 0 No gonads El Male H Female

24 40 135 21 I8 so I04

M ,J JASONDJFM MJJASONDJFMA11 1996 1997 1998 I Fig. 5. Annual cycle of sexual reproduction in the corallimorpharian Rhoductis rhodostoma. The first annual cycle extended from the beginning of oocyte development in July-August 1996 to spawning in late June 1997. A second cycle began in August 1997. (A) Proportion of male and female polyps, and polyps lacking gonads, each month. N = 16 polyps examined each month. (B) Developmental cycle of oocyte growth. The number of oocytes measured each month is given above the bars. ND = no data obtained. In September 1996, oocytes were obtained from only 3 females for measurement of oocyte diameters.

cyte development in some actinians (Lin et al. 1992). cur during the summer when photoperiod, light inten- In the corallimorpharian R. rhodostoma, it appears that sity, and temperature are high, and thus optimal for lengthening photoperiod andor increasing sea temper- autrotrophic energy assimilation by symbiotic zooxan- ature may induce gametogenesis and spawning. thellae. Tropical actinians examined in Florida (Jen- Annual cycles of zooplanktonic food abundance nison 1981) and Malaysia (Dunn 1982) have poorly also may relate to cycles of sexual reproduction and defined and prolonged spawning seasons. In contrast, clonal replication in R. rhodostoma (see Chadwick- both actinians and corallimorpharians that occur in Furman & Spiegel 2000), although members of this more subtropical conditions such as Eilat and Taiwan genus appear to obtain much of their energy via pho- appear to have well-defined, synchronous spawning tosynthesis by their endosymbiotic zooxanthellae (den events that coincide with the optimal season for pho- Hartog 1980). Members of the corallimorpharian fam- tosynthesis each year (Lin et al. 1992; Chen et al. ily Discosomatidae, to which Rhodactis ( = Discoso- 1995a) (Fig. 5). At Eilat, many zooxanthellate scler- ma) belongs, all possess zooxanthellae, and they com- actinian corals also spawn their gametes in the summer pletely lack spirocysts, which are important in the during June-August (Shlesinger et al. 1998). capture of mobile prey (den Hartog 1980). Further- The polyps of tropical actinians and corallimor- more, their tentacles are non-retractile and lack the pharians, including those of R. rhodostoma, do not ap- musculature required for zooplankton capture, so al- pear to reduce their rates of fission during gametogen- though they possess an alternate mechanism to capture esis. Individuals of the actinian'AnthopZeurudixoniana prey, members of this group are thought to obtain rel- go through gametogenesis and clonal replication si- atively little energy via heterotrophy (Elliot & Cook multaneously, reaching maximal rates of both in the 1989). month of July (Lin et al. 1992). Polyps of the coral- In the 2 members of this family examined thus far, limorpharian R. indosinensis spawn in May-June and gamete growth and maximum clonal growth both oc- achieve maximum rates of clonal replication in July- 368 Chadwick-Furman, Spiegel, & Nir

pharians and actinians examined thus far, sperm rip- ening is accompanied by significant increases in testis size (Sebens 1981; Wedi & Dunn 1983; Holts & Beau- n champ 1993). v) +I 0.2 0X Conclusions -a E .e We conclude that polyps of this corallimorpharian 2 c release large numbers of energy-rich eggs during the 0 M season of optimal growth conditions for autotrophic 0.1 reef cnidarians. Strong investment into the sexual production of large dispersive propagules by polyps of this species allows them to colonize open space on shallow reefs distant from parent populations. After successful recruitment, founder polyps then may mo- 0.0 ,I,.,',.,., OND J FMAM J nopolize large areas of reef space via clonal production of extensive aggregations (Chadwick-Furman & Spie- gel 2000), followed by aggressive damage to and over- 1996 1997 growth of other benthic cnidarians (Langmead & Fig. 6. Changes in the gonad index of polyps of the coral- Chadwick-Furman 1999b). Polyps segregate sexual limorpharian Rhodactis rhodostoma between October 1996 and aggressive roles depending on their positions with- and June 1997. Gonad index was calculated by dividing dry in aggregations. This combination of reproductive and gonad mass by dry polyp mass. N = 3 polyps of each sex competitive strategies contributes to the dominance of examined each month, except during November, December, and January when only 2 males were examined each month. Rhodactis polyps in some shallow disturbed reef habitats in the Indo-Pacific region.

Acknowledgments. We thank the staff of the Interuniversity August (Chen et al. 1995a). Similarly, R. rhodostoma Institute for Marine Science in Eilat, especially Karen Tar- peaks in cloning in April-May (Chadwick-Furman & naruder for preparing the graphics. We also thank Rachel Spiegel 2000) and then spawns in late June (Fig. 5). Levi and Tami Anker of the Life Sciences Faculty at Bar Clonal actinians appear to vary latitudinally in their Ilan University, for assistance with statistical analyses and timing of sexual reproduction versus cloning. Tropical for preparing the photographic figures. The photographs in species may be less energy limited and so can carry Fig. 1 were taken by Amikam Shoob of Tel Aviv University. on both processes during the same season, in contrast The manuscript was improved by comments from Hudi Be- to temperate species that may confront seasons of star- nayahu, Allen Chen, and anonymous reviewers. Funding vation or physical stress, and so must adapt their en- was provided by a grant to N.E.C.-E from the Israel Science Foundation. This project was completed in partial fulfillment ergetic budget to more extreme conditions (reviewed of an M.Sc. degree by M.S. at Bar Ilan University. in Shick 1991). We observed in R. rhodostoma a temporary drop in fission rate during the months imme- References diately before and after the annual spawning event, Chadwick NE 1991. Spatial distribution and the effects of indicating that some aspect of the spawning process competition on some temperate Scleractinia and Coralli- may interfere with cloning (Chadwick-Furman & morpharia. Mar. Ecol. Prog. Ser. 70: 39-48. Spiegel 2000). Chadwick-Furman NE & Spiegel M 2000. Abundance and We did not document a clear annual cycle of testis clonal replication of the tropical corallimorpharian Rho- development in R. rhodostoma. However, our data dactis rhodostoma. Invertebr. Biol. 119: 351-360. strongly suggest an annual cycle, in that we found Chen CLA, Chen CP, & Chen IM 1995a. Sexual and asexual many males prior to the spawning of oocytes each reproduction of the tropical corallimorpharian Rhodactis year, and few immediately afterwards (Fig. 5A). In ( = Discosoma) indosinensis (Cnidaria: Corallimorpharia) actinian sea anemones, the release of sperms by males in Taiwan. Zool. Stud. 34: 29-40. 1995b. Spatial variability of size and sex in the trop- is known to induce spawning by females (reviewed in ical corallimorpharian Rhodactis ( = Discosoma) indosi- Shick 1991). Thus, synchronous egg release by fe- nensis (Cnidaria: Corallimorpharia) in Taiwan. Zool. Stud. males of R. rhodostoma also may be triggered by 34: 82-87. once-annual sperm release in the males. The uniform Chia FS 1976. Sea anemone reproduction: patterns and adap- size of testes throughout the year in R. rhodostoma tive radiations. In: Coelenterate Ecology and Behavior. (Fig. 6) is remarkable in that, in the few corallimor- Mackie GO, ed., pp. 261-270. Plenum Press, New York. Sexual reproduction in a corallimorpharian 369 den Hartog JC 1980. Caribbean shallow water Corallimor- Langmead 0 & NE Chadwick-Furman 1999a. Marginal ten- pharia. Zool. Verhan. 176: 1-83. tacles of the corallimorpharian Rhodactis rhodostoma. 1. - 1994. Sea anemones of the Seychelles. In: Oceanic Role in competition for space. Mar. Biol. 134: 479-489. Reefs of the Seychelles. Cruise Reports of the Netherlands 1999b. Marginal tentacles of the corallimorpharian Indian Ocean Programme. Vol. 2. Van der Land J, ed., Rhodactis rhodostoma. 2. Induced development and long- pp.75-79. Netherlands Geosciences Foundation, The term effects on coral competitors. Mar. Biol. 134: 491- Hague. 500. Dunn DF 1982. Sexual reproduction of two intertidal sea Lin J, Chen CP, & Chen IM 1992. Sexual and asexual re- anemones (Coelenterata: Actiniaria) in Malaysia. Biotro- production of Anthopleura dixoniana (Anthozoa: Actini- pica 14: 262-271. aria): periodicity and regulation. Mar. Biol. 112: 91-98. Elliott JL & Cook CB 1989. Die1 variation in prey capture Sebens KP 1981. Reproductive ecology of the intertidal sea behavior by the corallimorpharian Discosoma sanctitho- anemones Anthopleura xarzthogrammica (Brandt) and A. mae: mechanical and chemical activation of feeding. Biol. elegantissima (Brandt): body size, habitat, and sexual re- Bull. 176: 218-228. production. J. Exp. Mar. Biol. Ecol. 54: 225-250. Francis L 1976. Social organization within clones of the sea anemone Anthopleura elegantissima. Biol. Bull. 150: 361- Shick JM 1991. A Functional Biology of Sea Anemones. Chapman & Hall, London. 395 pp. 176-, -. Holts LJ & Beauchamp KA 1993. Sexual reproduction in Shlesinger y, Goulet TL, & Loya Y 1998. Reproductive pat- the corallimorpharian sea Corynactis californica terns of scleractinian corals in the northern Red Sea. Mar. in a central California kelp forest. Mar. Biol. 116: 129- Bid 132: 691-701. 136. Wedi SE & Dunn DF 1983. Gametogenesis and reproductive Jennison BL 1981. Reproduction in three species of sea periodicity of the subtidal sea anemone Urticina lofotensis anemones from Key West, Florida. Can. J. Zool. 59: (Coelenterata: Actiniaria) in California. Biol. Bull. 165: 1708-17 19. 458-472.