Sexual reproduction in the tropical corallimorpharian ...wp.auburn.edu/chadlab/wp-content/uploads/2015/10/Chadwick-Furm… · of the Japanese Gardens fringing reef inside the Coral

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 has focused on species occurring in temperate to cold-water environments (reviewed in Shick 1991). In most of the >30 species of actinians examined thus far, gametogenesis follows an annual cycle, with polyps broadcasting gametes during spring to fall, and the exact spawning period varying among species. In contrast, we know little about sexual reproductive processes in tropical actinians. In one species examined in Taiwan, polyps synchronously spawn gametes in mid-summer each year, during the period of peak day length and temperature (Lin et al. 1992). Actinians examined in Malaysia and Florida exhibit patterns of brooding, hermaphroditism, and diffuse spawning over a long period each year (Jennison 1981; Dunn 1982).

The corallimorpharians are a group of soft-bodied anthozoans that superficially resemble actinian sea

a Author for correspondence: Interuniversity Institute for Marine Science, PO. Box 469, Eilat, Israel. E-mail: furman @ mail.biu. ac.il

anemones, but are more closely related to scleractinian corals (reviewed in den Hartog 1980). Little is known about the biology of corallimorpharians, even though they are important occupiers of space in some temperate and tropical benthic marine ecosystems (Chad- wick 199 1 ; Chadwick-Furman & Spiegel 2000). Pat- terns of sexual reproduction have been investigated in only 2 species, both of which form large aggregations via clonal replication. In the temperate Corynactis californica, all polyps in each clonal group are the same sex, and gametogenesis leads to annual synchronous spawning of gametes during winter (Holts & Beau- champ 1993). In contrast, in the tropical Rhodactis ( = Discosoma) indosinensis, polyp size and sex are influenced by position within each clonal aggregation, with edge polyps small and male, and central polyps larger and female (Chen et al. 1995b). This species follows an annual gametogenetic cycle in both sexes, with gamete spawning in midsummer during the period of peak seawater temperature and day length (Chen et al. 1995a).

362 Chadwick-Furman, Spiegel, & Nir

In the Red Sea and Indian Ocean, one of the dominant corallimorpharians is Rhodactis (= Discosoma) rhodostoma (EHRENBERG 1934), which forms aggregations of various sizes mainly in shallow coral reef environments (den Hartog 1994; Chadwick-Furman & Spiegel 2000). Polyps of R. rhodostoma replicate clonally by at least 3 distinct modes at a rate that permits them to rapidly monopolize large areas of space on some reefs (Chadwick-Furman & Spiegel 2000). In addition, polyps that contact stony-coral competitors develop specialized marginal tentacles that damage their neighbors' tissues, after which the polyps move onto the coral skeletons and overgrow them (Langmead & Chadwick-Furman 1999a). Rapid clonal spread and aggressive damage to neighbors allow polyps of R. rhodostoma to become an alternate dominant to stony corals in some disturbed reef areas (Chadwick-Furman & Spiegel 2000). The ability of individuals of R. rhodostoma to become established on widely-separated reefs may depend largely on the extent of their investment in sexual production of dis- persing planktonic larvae. We present here informa- tion on patterns of sex ratio, gametogenesis, and mode of sexual reproduction in R. rhodostoma. We also discuss annual cycles of sexual reproduction vs. clonal replication, and the role of each process in the ecology of this species.

Methods

Sexual reproduction in aggregations of the corallimorpharian Rhodactis rhodostoma was examined for 2 years (July 1996-June 1998) on the shallow reef flat of the Japanese Gardens fringing reef inside the Coral Beach Nature Reserve at Eilat, Israel (northern Red Sea, 29"30'3 1"N, 35'55'22"E). We randomly selected 4 aggregations, 2 on the inner reef flat, and 1 each on the middle and outer reef flat (in a separate study, dif- ferent aggregations were examined for clonal replication, see Chadwick-Furman & Spiegel 2000). Each month we collected 16 polyps, 4 polyps from each of the same 4 aggregations. Within each aggregation, 2 randomly selected polyps were collected from central positions, and 2 from along the edges (see Chadwick- Furman & Spiegel 2000). The specimens were trans- ferred to the nearby Interuniversity Institute for Marine Science in Eilat, anesthetized in 7.2% MgCl, at a ratio of 1: 1 with seawater (for one hour or until the polyps became desensitized), and preserved in 10% formalin (after Sebens 1981; Wedi & Dunn 1983; Chen et al. 1995a).

After blotting off excess water, each preserved polyp was weighed and the oral disk diameter was measured (modified after Wedi & Dunn 1983). Then each

polyp was dissected to determine sex and reproductive state, and sex ratio was calculated. In 4 of the 16 polyps collected each month, all gonads and, in females, all oocytes were counted in whole preserved polyps. Fecundity was defined as the number of oocytes per polyp. In addition, from October 1996 to June 1997 (when gonads were large enough to manipulate), all the gonads were removed from 3 male and 3 female polyps each month. Gonads and polyps were dried separately at 100°C for 24 h. Their preserved dry masses then were used to calculate a gonad index (GI), which was the relation of dry gonad mass to that of the entire animal, including gonads as well as the polyp body (after Wedi & Dunn 1983). This index also was used to determine reproductive effort and to assess the rate of gonadal development during the year. Fi- nally, gonad samples were removed from an additional 6 of the 16 collected polyps each month for histological analyses of gametogenesis. The tissues were im- bedded in paraffin blocks; 8-km sections were mount- ed on slides and stained with hematoxylin and eosin for observation of gonad development (after Wedi & Dunn 1983; Lin et al. 1992; Holts & Beauchamp 1993).

In each female, 5-50 oocytes that contained nuclei were measured each month. The maturity phases of male gonads were not scored, because they did not show clearly distinct developmental phases throughout the year (see below).

All wet and dry masses given in the text were obtained directly from preserved polyps, and not esti- mated from other parameters of polyp size. Statistical analyses were performed using the SAS program, ver- sion 6. Before application of parametric tests, data were examined for normality and homogeneity of var- iances. Unless otherwise indicated, data are presented as means -+ 1 standard deviation.

Results Gonads and sex ratio

Mature polyps of Rhodactis rhodostoma were either male or female. Most mesenteries each bore a single gonad near the polyp base. Females were distinguished by the presence of ovaries with developing oocytes, which grew to fill much of the polyp before spawning (Fig. 1A,B). Each preserved ovary contained a grape- like cluster of spherical, light-brown oocytes (Fig. lC,D). Males had small white testes, each testis con- sisting of a one-chambered sac (Fig. 1E,F).

Most female polyps were located in the center of aggregations, while most males were on the edges, and the few polyps lacking gonads occurred mostly on the 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 were males (28.0%), and a few had no gonads (2.6%), giving a sex ratio of 2.5:l females to males in central positions (Fig. 2A). In contrast, along the edge of aggregations, most polyps were males (54.0%) and some were females (39.8%), giving a sex ratio of 0.7:l females to males (Fig. 2B). A higher proportion of polyps with no gonads (6.3%) occurred along the edges of aggregations than in the centers.

In 3 of the 4 aggregations examined, the number of females exceeded males, with a ratio of approximately 2:l females to males, because most polyps in central positions were female (Fig. 2A). The aggregation examined on the outer reef flat differed from those in the other reef zones, in sex ratio. It was the only aggregation in which males exceeded females (ratio of only 0.3:l females to males), and it had the highest proportion of polyps with no gonads (Fig. 2). The sex


ratio for all 4 aggregations together (N = 224 polyps) was 1.3:1 females to males. Sex ratios varied significantly both within and between examined aggregations (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 S O ? 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 = 3 8 , N = 36, p<.OO1)

Thus, the wet mass of preserved polyps was used to estimate live polyp size, except in gonad index cal- 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 size class (>6 g) were females (Fig. 3). In addition, the minimum size at maturity for males (0.6 g preserved wet mass) was only half that for females (1.2 g preserved wet mass). Overall, sexual reproductive status varied significantly with polyp size (ANOVA, F = 33.66, pc.001).

Gonad development as a function of polyp size

In females, fecundity (number of oocytes per polyp) increased significantly with preserved polyp wet mass (Fig. 4). This trend was due to the significant increase 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 largest polyp observed.

Females had 70-180 ovaries per polyp, 1 each on most of their mesenteries. The number of ovaries per polyp did not vary significantly with polyp size (Table 1).

No gonads E l Male Female

A. Center of aggregation 100 1

B. Edge of aggregation 3

Inner reef Inner reef M d reef Outer reef #1 #2

Location of aggregation on reef flat

Fig. 2. Variation in sex ratio between 4 aggregations of the corallimorpharian Rhoductis rhodostomu on a reef flat at Ei- lat, northern Red Sea. Data are from October 1996 to June 1997 and January to May 1998, when gonads were well- developed. In each of 8 possible positions, 26-29 polyps were collected total. N = 224 polyps were collected in all positions (16 polyps each month X 14 months). (A) Polyps in the center of each aggregation. (B) Polyps along the edge of each aggregation.

Males had 40-120 testes per polyp. The number of testes per polyp did not vary significantly with polyp size (Table 1).

Gonad index (the proportion of body mass devoted to gonads) did not correlate significantly with polyp size, in either males or females (Table 1).


50

CA 40 3 e

30 41 0

e t3 20 E 5 z 10

0 0 1 2 3 4 5 6 7

Polyp size (preserved wet mass, g) Fig. 3. Variation in polyp size with sexual reproductive status in the corallimorpharian Rhoductis rhodostoma at Eilat, northern Red Sea. Data are from October 1996 to June 1997 and January to May 1998, when gonads were well-developed.

Annual reproductive cycle

Oocytes were small but present in most polyps start- ing in September-October each year (Figs. 5 , 6) . They increased in size gradually during the year, reaching a maximum diameter of 500 km in June-July (Fig. 5).

Testes were also present and well-developed in many polyps from September-October to June-July

N = 26 polyps 4000 1 y = 3 8 1 . 6 ~ + 396.7

f i e 3 0 30 ck . rA

r2 = .33 p < .O1

100 { -1

a, Y x 0

8 2000 5 ._ 0 a $ 1000 a,

1 c4

.

/ .* . . * .

o ! I I I I I 1

0 1 2 3 4 5 6 Polyp size (preserved wet mass, g )

Fig. 4. Relationship of oocyte number (fecundity) to polyp size in female polyps of the corallimorpharian Rhodactis rhodostoma.

each year (Fig. 5) but did not change in size during the year (Fig. 6).

Sperms and oocytes apparently were spawned si- multaneously in June-July each year, because testes and oocytes both disappeared during the same period in most polyps (Fig. 5A). Fertilization probably occurred externally, as no fertilized eggs or developing embryos were found within polyps.

During July and August each year, most polyps did not have gonads. In July, a few females retained scat- tered large oocytes, but these disappeared by August, when new small oocytes began to develop (Fig. 5).

Histological examination of ovaries revealed developing oocytes with nuclei and dense yolk granules (Fig. 1D). However, histological sections of testes did not reveal a clear annual cycle of sperm development. Testes were present and distinguishable in male polyps during most of the year (Fig. 5A) but remained small and constant in size (Fig. 1E,F).

The gonad index increased significantly over time 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 months immediately before spawning (Fig. 6). Ovaries represented an investment of up to 30% of female polyp mass by the end of the reproductive cycle (20.7 ? 8.2% in June 1997, Fig. 6). The gonad index of males did not show a clear trend of increase over time, and remained low at <8% of male body mass throughout the entire period of spermatogenesis (4.6 k 2.6% in May 1997, Fig. 6).

Discussion Gonads and sex ratio

We demonstrate here an unusual pattern of sexual dispersion within clones of a tropical corallimorpharian. Sex ratio depends upon polyp position within aggregations of Rhodactis rhodostoma at Eilat, a pattern also known for R. indosinensis in Taiwan. In both species, polyps in the center of aggregations are mostly large and female, while those along the edges are smaller and often male or infertile (Chen et al. 1995b; Chadwick-Furman & Spiegel 2000) (Fig. 2). In R. indosinensis, the segregation of sex by position is even stronger than in R. rhodostoma, with almost all males on the edges and all females in the center of aggregations (Chen et al. 1995b). Field experiments with R. indosinensis have demonstrated that polyps change sex and size when cross-transplanted between central and edge positions (Chen et al. 1995b). Thus, in the 2 members of this genus examined thus far, sexuality appears to be determined by environment.

Actinian sea anemone polyps also may vary their


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 aggregations. In the common aggregating actinian Anthopleu- ra elegantissima, mid-aggregation polyps are fertile and large, while edge polyps are mostly infertile and smaller, but possess highly developed weaponry for interclonal competition (Francis 1976). This pattern in- dicates that polyps along the edges of aggregations may allocate more energy into the defense of living space against competitors than into sexual reproduction. Individuals of R. rhodostoma along the edges of aggregations also invest energy into spatial defense and the development of specialized weaponry (Lang- mead & Chadwick-Furman 1999a,b), and thus may have fewer resources left over for sexual reproduction than do polyps located in the center of aggregations.

The low proportion of females in the aggregation examined on the outer reef flat (Fig. 2) may be due to suboptimal conditions for R. rhodostoma in this habitat, where polyps of this species are rare in contrast to their abundance on the middle and inner reef flat (Chadwick-Furman & Spiegel 2000).

Size at sexual maturity

Females are significantly larger than males in both the corallimorpharians R. rhodostoma (Fig. 3) and R. indosinensis (Chen et al. 1995a), as well as in some actinian sea anemone species that produce large eggs (Shick 1991). The polyps of some species may need to achieve a relatively large minimum size before be- coming female, due to their high investment of energy and body space into large eggs (Jennison 198 1 ; Shick 1991). Minimum sizes at maturity in R. rhodostoma (0.6 g preserved wet mass for males and 1.2 g for females) are smaller than those known for R. indosinensis (-3 g preserved wet mass, for males and -5 g for females, calculated from figs. 2 and 3 in Chen et al. 1995a).

Gonad development as a function of polyp size

We report here for the first time gonad index values for a corallimorpharian. The high gonad index that we

observed in R. rhodostoma (up to 30% of body mass invested into oocytes, Fig. 6 ) is greater than values reported for actinian sea anemones (reviewed by Shick 1991). In addition, mature oocytes in R. rhodostoma (maximum diameter = 500 pm) are larger than those of most other corallimorpharians (Holts & Beauchamp 1993; Chen et al. 1995a) and actinians (Shick 1991). Thus, female polyps of R. rhodostoma appear to allocate a relatively large proportion of their energy to- ward sexual reproduction, especially during late spring to summer (Fig. 6). Such high investment into sex may explain in part why most polyps produced oocytes only under certain environmental conditions, such as those in the center of aggregations on the middle to inner reef flat, while polyps under other, possibly less optimal conditions often remained infertile or produced sperm (Fig. 2). The high gonad index for females of R. rhodostoma also may explain why members of this species slow their fission rate just before spawning (Chadwick-Furman & Spiegel 2000), while those of a congener do not (Chen et al. 1995a). Each female polyp of R. rhodostoma produces up to 3000 large eggs per year (Fig. 4), a high fecundity rate rel- ative to actinian sea anemones that are known to produce large eggs (Shick 1991).

The pattern of development in R. rhodostoma may be classified as oviparous-planktonic-lecithotrophic (Chia 1976; Shick 1991), in that large, yolk-rich eggs are released into the plankton.

Annual reproductive cycle

The tropical corallimorpharian R. rhodostoma has an annual cycle of sexual reproduction, with spawning of polyps during midsummer at Eilat (Fig. 5) , when days are longest and temperature is approaching its annual maximum (Chadwick-Furman & Spiegel 2000). This annual pattern also occurs in R. indosensis in Taiwan (Chen et al. 1995a), and in littoral actinians, most of which spawn at peak annual temperatures (reviewed in Shick 1991). Experimental studies indicate that increasing photoperiod also may trigger rapid oo-


A 0 No gonads El Male

135

J A S O N D J F M

1996

H Female

18

so I04 I 8

1 21

1 M J J A S O N D J F M A

1997 1998

24 40 I M ,J

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). In the corallimorpharian R. rhodostoma, it appears that lengthening photoperiod andor increasing sea temperature may induce gametogenesis and spawning.

Annual cycles of zooplanktonic food abundance also may relate to cycles of sexual reproduction and clonal replication in R. rhodostoma (see Chadwick- Furman & Spiegel 2000), although members of this genus appear to obtain much of their energy via pho- tosynthesis by their endosymbiotic zooxanthellae (den Hartog 1980). Members of the corallimorpharian family Discosomatidae, to which Rhodactis ( = Discoso- ma) belongs, all possess zooxanthellae, and they com- pletely lack spirocysts, which are important in the capture of mobile prey (den Hartog 1980). Further- more, their tentacles are non-retractile and lack the musculature required for zooplankton capture, so although they possess an alternate mechanism to capture prey, members of this group are thought to obtain relatively little energy via heterotrophy (Elliot & Cook 1989).

In the 2 members of this family examined thus far, gamete growth and maximum clonal growth both oc-

cur during the summer when photoperiod, light inten- sity, and temperature are high, and thus optimal for autrotrophic energy assimilation by symbiotic zooxanthellae. Tropical actinians examined in Florida (Jen- nison 1981) and Malaysia (Dunn 1982) have poorly defined and prolonged spawning seasons. In contrast, both actinians and corallimorpharians that occur in more subtropical conditions such as Eilat and Taiwan appear to have well-defined, synchronous spawning events that coincide with the optimal season for pho- tosynthesis each year (Lin et al. 1992; Chen et al. 1995a) (Fig. 5). At Eilat, many zooxanthellate scleractinian corals also spawn their gametes in the summer during June-August (Shlesinger et al. 1998).

The polyps of tropical actinians and corallimorpharians, including those of R. rhodostoma, do not appear to reduce their rates of fission during gametogenesis. Individuals of the actinian'AnthopZeuru dixoniana go through gametogenesis and clonal replication si- multaneously, reaching maximal rates of both in the month of July (Lin et al. 1992). Polyps of the corallimorpharian R. indosinensis spawn in May-June and achieve maximum rates of clonal replication in July-


n v)

+ I X 0 -a E .e

2 c 0 M

0.2

0.1

0.0 , I , . , ' , . , . ,

O N D J F M A M J

1996 1997

Fig. 6. Changes in the gonad index of polyps of the corallimorpharian Rhodactis rhodostoma between October 1996 and June 1997. Gonad index was calculated by dividing dry gonad mass by dry polyp mass. N = 3 polyps of each sex examined each month, except during November, December, and January when only 2 males were examined each month.

August (Chen et al. 1995a). Similarly, R. rhodostoma peaks in cloning in April-May (Chadwick-Furman & Spiegel 2000) and then spawns in late June (Fig. 5). Clonal actinians appear to vary latitudinally in their timing of sexual reproduction versus cloning. Tropical species may be less energy limited and so can carry on both processes during the same season, in contrast to temperate species that may confront seasons of star- vation or physical stress, and so must adapt their en- ergetic budget to more extreme conditions (reviewed in Shick 1991). We observed in R. rhodostoma a temporary drop in fission rate during the months immediately before and after the annual spawning event, indicating that some aspect of the spawning process may interfere with cloning (Chadwick-Furman & Spiegel 2000).

We did not document a clear annual cycle of testis development in R. rhodostoma. However, our data strongly suggest an annual cycle, in that we found many males prior to the spawning of oocytes each year, and few immediately afterwards (Fig. 5A). In actinian sea anemones, the release of sperms by males is known to induce spawning by females (reviewed in Shick 1991). Thus, synchronous egg release by females of R. rhodostoma also may be triggered by once-annual sperm release in the males. The uniform size of testes throughout the year in R. rhodostoma (Fig. 6) is remarkable in that, in the few corallimor-

pharians and actinians examined thus far, sperm rip- ening is accompanied by significant increases in testis size (Sebens 1981; Wedi & Dunn 1983; Holts & Beau- champ 1993).

Conclusions We conclude that polyps of this corallimorpharian

release large numbers of energy-rich eggs during the season of optimal growth conditions for autotrophic 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 monopolize large areas of reef space via clonal production of extensive aggregations (Chadwick-Furman & Spie- gel 2000), followed by aggressive damage to and over- growth of other benthic cnidarians (Langmead & Chadwick-Furman 1999b). Polyps segregate sexual and aggressive roles depending on their positions within aggregations. This combination of reproductive and competitive strategies contributes to the dominance of Rhodactis polyps in some shallow disturbed reef habitats in the Indo-Pacific region.

Acknowledgments. We thank the staff of the Interuniversity Institute for Marine Science in Eilat, especially Karen Tar- naruder for preparing the graphics. We also thank Rachel Levi and Tami Anker of the Life Sciences Faculty at Bar Ilan University, for assistance with statistical analyses and for preparing the photographic figures. The photographs in Fig. 1 were taken by Amikam Shoob of Tel Aviv University. The manuscript was improved by comments from Hudi Be- nayahu, Allen Chen, and anonymous reviewers. Funding was provided by a grant to N.E.C.-E from the Israel Science Foundation. This project was completed in partial fulfillment of an M.Sc. degree by M.S. at Bar Ilan University.

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