Sexual Reproduction in the Tropical Corallimorpharian Rhodactis Rhodostoma
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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 be- tween 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 fe- males, 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 rep- lication 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.