Galaxea, Journal of Coral Reef Studies 11: 155-167（2009）

Original paper

Sexual reproduction of soft coral, Scleronephthya gracillimum, (Alcyonacea: Nephtheidae) based on long-term collection from Jejudo Island, Korea

Sung Jin HWANG and Jun Im SONG*

Division of EcoScience, College of Natural Sciences, Ewha Womans University, Seoul, Republic of Korea

* Corresponding author: J.I. Song E-mail: [email protected]

Communicated by Makoto Tsuchiya

Abstract The soft coral Scleronephthya gracillimum Introduction (Alcyonacea: Octocorallia), a member of family Nephth­ eidae, is abundant in the southern part of Jejudo Island, Soft corals, of the order Alcyonacea, are ecologically Korea. To examine the sexual reproductive pattern, important sessile members of coral reef communities, and monthly collections and histological studies were con­ are distributed from tropical to temperate regions. These ducted from June 2003 to October 2007. The sexual re­ corals have three modes of sexual reproduction, namely productive pattern of the genus Scleronephthya was de­ the broadcasting of gametes, internal brooding, and ex­ scribed for the first time in the present study, which es­ ternal surface brooding involving planulae (Farrant 1986; tablished that S. gracillimum is a gonochoric broadcaster, Benayahu et al. 1990; Benayahu 1991; Cordes et al. 2001). with the sex ratio of 1:1. The gametogenic cycle was an­ The reproductive patterns of alcyonaceans are summarized nual, and a difference between female and male colonies in Table 1. The reproductive mode of soft corals varies was apparent, with biorhythms of 12 and 5-7 months re­ among different family groups; gonochorism is generally spectively. Gametogenesis and spawning are related to dominant in soft coral species, although a few species are seasonal factors such as seawater temperature and algal hermaphroditic (Sebens 1983; Benayahu et al. 1990; blooms. Actual spawning event occurred, and others may Achituv et al. 1992; McFadden et al. 2001; McFadden and have taken place, when seawater temperature attained an Hochberg 2003; Choi and Song 2007; Hwang and Song annual peak between August and September. The actual 2007). Most species belonging to the family Alcyoniidae spawning occurred in the field at 10 a.m. on September 3, employ the broadcast mode of reproduction. In the family 2006, 4 days before the full moon. Xeniidae, by contrast, only brooding behavior has been described, although the examination about reproductive Keywords sexual reproduction, gametogenesis, Scleronephthya mode has not been finished yet. gracillimum, soft coral, Anthozoa Generally, the production and development of gametes is similar in most soft corals. Gametes are formed in the mesenteries, and then move into the gastrovascular cavity, where they mature (Benayahu 1991; McFadden and Hochberg 2003). Broadcast spawning events of corals are 156 Hwang and Song: Sexual reproduction of soft coral

Table 1 Reproductive pattern reported in the literature on Alcyonacea

Number Sexuality Mode of reproduction Taxa References of species G H G/H P BS EB IB U Alcyoniidae 37 35 1 - 1 26 2 7 2 1,3,4,7,8,9,10,11 Alcyonium 11 9 1 - 1 5 1 4 1 1,3,8,9 Anthomastus 1 1 - - - - - 1 - 7 Cladiella 1 1 - - - 1 - - - 4 Discophyton 1 1 - - - - - 1 - 9 Lobophytum 7 7 - - - 7 - - - 3,11 Parerythropodium 1 1 - - - - 1 - - 3 Sarcophyton 4 4 - - - 4 - - - 3,10 Sinularia 9 9 - - - 9 - - - 3 Thrombophyton 2 2 - - - - - 1 1 9 Nephtheidae 6 6 - - - 3 1 2 - 2,3,6,12,13 Litophyton 1 1 - - - - - 1 - 3 Scleronephthya 1 1 1 present Dendronephthya 3 3 - - - 2 - 1 - 6,12,13 Capnella 1 1 - - - - 1 - - 2 Xeniidae 24 18 5 1 - - 1 16 7 3,4,5 Xenia 15 12 3 - - - - 10 5 3,4,5 Heteroxenia 4 1 2 1 - - - 4 - 3 Anthelia 2 2 - - - - - 1 1 3,4 Sympodium 1 1 - - - - - 1 - 3,4 Efflatounaria 1 1 - - - - 1 - - 3 Cespitularia 1 1 ------1 4 References: (1) Sebens 1983, (2) Farrant 1986, (3) Benayahu et al. 1990, (4) Benayahu 1991, (5) Achituv et al. 1992, (6) Dahan and Benayahu 1997, (7) Cordes et al. 2001, (8) McFadden et al. 2001, (9) McFadden and Hochberg 2003, (10) Schleyer et al. 2004, (11) Fan et al. 2005, (12) Choi and Song 2007, (13) Hwang and Song 2007. BS broadcast spawner, EB external brooder, G gonochoric, H, hermaphroditic G/H gonochoric or hermaphroditic, IB internal brooder, P parthenogenetic, U unknown.

usually synchronous and seasonal, although only a low temperate regions (Fabricius and Alderslade 2001), and level of synchrony is apparent in temperate species only one species, Scleronephthya gracillimum (Kükenthal, (Harrison et al. 1984; Benayahu and Loya 1986; Harrison 1906), has been reported in Korean waters to date (Song and Wallace 1990; Benayahu 1991; Ben-David-Zaslow et 1976). In the present report, reproductive features such as al. 1999; Kapela and Lasker 1999; Cordes et al. 2001; sexuality, reproductive mode, gametogenesis, and the Schleyer et al. 2004). reproductive cycle, are described for S. gracillimum for Limited information is available regarding the sexual the first time. reproduction of Nephtheidae, compared with that on Alcyoniidae and Xeniidae. Also, most studies on repro­ duction have been conducted in only a few geographical Materials and methods regions, mainly the Red Sea, the Australian Great Barrier Reef, and the Northeastern Pacific Ocean (Benayahu et Collection of specimens al. 1990; Benayahu 1991; McFadden et al. 2001; Mc­ Colonies of S. gracillimum are abundant on the south Fadden and Hochberg 2003). The genus Scleronephthya, coast of Jejudo Island (Fig. 1) in Korea, located in the a member of the family Nephtheidae, inhabits tropical-to- temperate zone but with a somewhat subtropical climate Hwang and Song: Sexual reproduction of soft coral 157

Fig. 1 Colonies of Scleronephthya gracillimum and map of the study site. A Colonies spawned eggs in the field on September 3, 2006. B Jejudo Island is located in the most southern part of Korea

because the coast is affected by the Tsushima Warm length and width were cut from preserved specimens, Current branching from the Kuroshio Current. Colonies decalcified in 10% (w/v) EDTA solution for 5 days, and live mainly on the vertical surfaces of rocks in our study then dehydrated in a graded series of ethanol baths. area, where seawater temperatures range from 14-26℃ Dehydrated tissues were cleared with a mixture of xylene depending on season. Long (5-6 cm) fragments were and ethanol, embedded in paraffin, and cut into sections collected from randomly selected colonies (height ＞30 of 10 µm thick using a microtome. Serial sections were cm) located at depths of 10 m and 30 m by researchers stained with Harris hematoxylin and eosin Y and mounted wearing SCUBA apparatus, between June 2003 and using Shandon Synthetic Mountant (Thermo). Sections October 2007. After collection, samples were anesthetized were observed under an Olympus BH-2 microscope. with menthol for 4-6 hours, and were then fixed in 4-5% (v/v) neutral formalin, diluted with seawater, for 24 hours. Images and analysis Finally, samples were transferred into 70% (v/v) ethanol Photographs of living colonies in water were taken for preservation. with an Olympus 5060-WZ digital camera fitted with an Underwater Patima 7070 Housing, and all images of Dissection and histology gametes and histological sections were obtained using the Each preserved specimen was examined under a Zeiss same camera attached to stereomicroscopes (Semi SV-6 (Semi SV-6) stereomicroscope to determine the sexuality and SV-11 instruments) or a light microscope (Olympus of each colony and the external features of gametes. To BH2 instrument). The sex ratio was determined by count­ investigate gametogenic cycles, the longest and shortest ing the numbers of female and male colonies from June to axes of about 30 gametes from each colony were meas­ October throughout study periods, when oocytes and ured using an image analyzer (Motic Image Plus 2.0 in­ spermaries were observed together. The χ2 goodness-of-fit strument) on a monthly basis, and an average axis length test was used to test for deviation from a 1:1 sex ratio, was calculated. Seawater temperature near the collection using SPSS (version 12). site was recorded monthly by Korea Hydrographic and Oceanographic Administration (KHOA) during the entire study period. Histology was employed to identify gametogenic stages and the reproductive mode. Tissues 0.5-1.0 cm in both 158 Hwang and Song: Sexual reproduction of soft coral

Results The earliest oocytes, in stage I, were in the mesoglea of mesenteries and were smaller than 50 µm in diameter, Sexuality and sex ratio with an average size of 39.2±8.1 µm (mean±SD, n＝98) All S. gracillimum colonies analyzed microscopically (Fig. 2a). These oocytes contained large distinct nuclei, and histologically were determined to be gonochoric. and were transparent because of a lack of cytoplasm. As Among the total of 269 colonies examined during the the oocytes grew into stage II, the color changed to cream entire study period, 131 were female, 79 male, and 59 as a result of accumulation of cytoplasm, and one-sided contained small or no gametes. Female colonies were nuclei were seen. At this stage, oocytes were observed in significantly more abundant than male colonies, with a the gastrovascular cavity and were individually connected sex ratio of 1.76:1. However, male colonies were observed to mesenteries by pedicles (Fig. 2a). The diameter of only from late spring or early summer to fall. On the other oocytes ranged from 51-149 µm with a mean value of hand, female colonies were present throughout the year. 112.2±24.5 µm (n＝1,515). At stage III, vitellogenesis Thus, only 85 female and 75 male colonies obtained (yolk synthesis) commenced, and yolk bodies accumulated between June and October were used to calculate the around the nuclei of oocytes, resulting in a color change precise sex ratio, excluding possible male colonies with from cream to light orange. The maturing oocytes became small or no gametes. This sex ratio was not significantly detached from the mesenteries, entering into a cavity different from 1:1 (χ2＝90.625, df＝1, P＝0.429). covered by follicular layers (Fig. 2b); the oocytes ranged in diameter from 150-199 µm, with a mean of 169.8± Gametogenesis (gonadal development) 13.5 µm (n＝590). In stage IV, yolk bodies were contin­ Development of gametes in S. gracillimum was similar uously synthesized, and spread throughout the entire to that in other alcyonaceans; gametes originated from oocyte (Fig. 2c), so that the color of oocytes became gastrodermal mesenteries within the polyp cavity. Imma­ gradually deeper. Late vitellogenic oocytes ranged from ture gametes gradually moved into the gastrovascular 200-299 µm in diameter, with a mean of 255.2±29.8 µm cavity, being initially connected to the mesenteries by (n＝464). Fully mature oocytes, in stage V, were vivid pedicles, and then detached from the mesenteries as they dark orange in color and were over 300 µm in diameter, matured. with a maximum of 473 µm and an average of 346.2± Oogenesis. Oocyte was easily defined microscopically by 35.0 µm (n＝370) (Fig. 2d). These oocytes were covered the presence of a transparent follicular layer and a with a well-developed follicular layer. Embryos and prominent nucleus with a single nucleolus. Spherical planulae were not observed when oocytes were at this oocytes tended to change from transparent to cream in stage within the cavity. color, and then to vivid orange, as they matured. The Spermatogenesis. The development of spermaries was development of oocytes was classified into five stages, classified into four stages depending on maturity, as shown depending on maturity, as shown in Table 2. in Table 2. Spermaries at the earliest stage were embedded

Table 2 Range and mean diameter of gametes, which depends of stages (n number of gametes at each stage) Hwang and Song: Sexual reproduction of soft coral 159

Fig. 3 Development of spermaries. A Stage I spermaries em­ Fig. 2 Development of oocytes. A Stage I oocytes embedded bedded in the mesentery containing clusters of spermatogonia. B in the mesentery and stage II oocyte connected to mesentery by Stage II and stage III spermaries filled with spermatocytes. C pedicle. B Stage III oocytes enveloped with follicular layers. C Spermatocytes arranged at the periphery of stage III spermaries. Stage IV oocyte contained numerous yolk bodies. D Fully D Stage IV spermary with a convolution of spermatozoa at the matured stage V oocyte. The scale bar＝100 µm, O1 stage I on-side. The scale bar＝50 µm, M mesentery, S1 stage I sper­ oocyte, O2 stage II oocyte, O3 stage III oocyte, O4 stage IV mary, S2 stage II spermary, S3 stage III spermary S4 stage IV oocyte, O5 stage V oocyte, P pedicle spermary in mesenteries containing clusters of spermatogonia, and matozoa at the on-side of spermaries was observed before the boundaries of the spermaries were unclear (Fig. 3a). sperm was released (Fig. 3d). Stage I spermaries were spherical and were less than 50 µm in diameter, with a mean of 43.2±5.3 µm (n＝52). Gametogenic cycle and spawning In stage II, spermaries were filled with developing sper­ Annual reproductive cycle (oogenic and spermatogenic matocytes and moved into the cavity, where they remain cycle). S. gracillimum showed a single annual reproductive attached to the mesenteries by pedicles (Fig. 3b). These cycle, with a clear difference between females and males. opaque spermaries had distinct boundaries and ranged in Whereas spermaries were detected only between June and diameter from 51-99 µm, with a mean of 76.9±14.1 µm December in 2003, June and October in 2004, April and (n＝350). In stage III, spermatocytes were arranged at August in 2005, June and October in 2006, and May and the periphery of spermaries, resulting in hollow centers October in 2007, oocytes were observed throughout the (Fig. 3b, c), and began to develop into spermatids. The year, except when collections were not possible. sper­maries changed from opaque to tinted cream in color In females, oocytes of stages I and II were found as spermatids accumulated. The diameter of spermaries throughout most of the study period, although their rela­ ranged from 100-174 µm, with a mean of 134.3±20.2 µm tive frequency changed with the season (Fig. 4). In June (n＝1,047). In stage IV, spermaries attained their full size 2003, the sum of the relative frequencies of these two and were completely mature, with diameters in excess of stages was comparatively high at 0.8, and this sum 175 µm, with a maximum of 281 µm and a mean of 203.0 subsequently dropped sharply, to under 0.1, between July ±23.4 µm (n＝281). Late in this stage, spermatids began and August. By late September, the two stages of oocytes to metamorphose into spermatozoa in these cream-colored recorded the highest combined frequency of 1.0, and this spermaries. Tails began to be displayed, and the sper­ high frequency was continuously maintained until the matozoa formed a parallel array. A convolution of sper­ following May, with an average of 0.9 (±0.10, n＝9). A 160 Hwang and Song: Sexual reproduction of soft coral

Fig. 4 Monthly frequency of each oogenic stage from June 2003 to October 2007 (n＝3037 oocytes). O1 stage I oocytes, O2 stage II oocytes, O3 stage III oocytes, O4 stage IV oocytes, O5 stage V oocytes, * month with no collection

similar pattern, with small fluctuations, appeared in suc­ 2006, and June 2007, with a mean frequency of 0.5± cessive years up to and including October 2007. Stage I 0.14 (n＝5). Generally, stage V oocytes tended to peak in and II oocytes showed a rise, followed by a fall, in frequency 1-2 months after the peak in stage IV oocytes, frequency over the course of any year. The sum of the with fluctuation in each year. frequencies of stages I and II was low at 0.2±0.23 In males, stages I and II were observed between April (mean±SD, n＝16) between June and August, abruptly and December, with fluctuation in each year, throughout increased in September to a high of 0.7±0.22 (n＝24), the entire study period (Fig. 5). The sum of the relative which lasted for 9 months until the following May, and frequencies of these stages peaked every June between then decreased again from June. Stage III showed a low 2004 and 2007, but in 2003 the frequency peak was frequency throughout the year, with a mean of 0.2±0.13 observed in November. However, only small numbers of (n＝40). No frequency fluctuation pattern was observed spermaries were found between October and December for this stage. Late vitellogenic oocytes, in stage IV, were 2003: 11 in October, 3 in November, and 30 in December. found mainly between June and September, showing a Thus, if the data from October to December 2003 are mean frequency of 0.3±0.21 (n＝21). Frequency peaks ignored, stage I and II spermaries showed the highest in stage IV oocytes in each year were recorded in July of frequency in June, as occurred from 2004 to 2007. The 2003 and 2004, June of 2005 and 2006, and August mean frequency of stage I and II spermaries was notably 2007, with minimum and maximum frequencies of 0.3 elevated, at 0.7±0.25 (n＝5), every June from 2004 to and 0.8 in 2003 and 2007, respectively. Fully mature 2007, but from July of each year the frequency sharply oocytes, in stage V, were observed from June to Septem­ decreased, to a mean of 0.1±0.12 (n＝14). Stage III ber, and were abundant in July and August at an average spermaries were usually apparent during the entire period frequency of 0.3±0.20 (n＝11). Stage V oocyte levels when male colonies were present, but were particularly peaked in August 2003, July 2004, July 2005, August abundant from July to October, with a mean frequency of Hwang and Song: Sexual reproduction of soft coral 161

Fig. 5 Monthly frequency of each spermatogenic stage from June 2003 to October 2007 (n＝1730 speramries). S1 stage I spermaries, S2 stage II spermaries, S3 stage III spermaries, S4 stage IV spermaries, * month with no collection

0.7±0.23 (n＝20). Mature spermaries, in stage IV, were In 2003, the number of mature oocytes (stage V) and found between June and October, with a mean frequency the total number of oocytes fell abruptly between August of 0.3±0.20 (n＝15). Stage IV spermaries displayed dis­ and September (Fig. 6). Mature spermaries were observed tinct rise and fall patterns, suggesting that reproductive only from July to September, and the number of sper­ events were underway. In July and September 2003, the maries declined between August and October (Fig. 7). frequency of stage IV spermaries peaked, and then drop­ Thus, it is reasonable to infer that a spawning event may ped to zero. Similar patterns were also evident in 2004 have occurred between August and September 2003. In and 2005, with peaks in July followed by rapid declines. 2004, mature oocytes and spermaries were not found after Such a rise and fall pattern was recorded twice in 2006, September, and the numbers of oocytes and spermaries with peaks in June and late August. Also, an additional decreased from September, suggesting that spawning small peak was observed, together with a high frequency occurred in September. In 2005, the numbers of mature of stage III spermaries, in October 2006, but the number oocytes and spermaries fell rapidly between July and of spermaries rapidly declined from September, suggest­ August, indicative of the spawning of gametes. However, ing the termination of reproductive events. Rise-and-fall the total numbers of oocytes and spermaries did not patterns were also noted between August and September decrease, and oocytes of stage IV and spermaries of stage 2007. III were abundant, suggesting an additional spawning Spawning of gametes (inferred and observed spawning event in September even though sampling was not per­ events). An actual spawning event was observed on Sep­ formed. The actual spawning occurred in the field at 10 tember 3, 2006, in the field, and no embryos or planulae a.m. on September 3, 2006, 4 days before the full moon, were found in histological sections or dissected colonies, and several potential spawning events might be inferred suggesting that broadcast spawning is the reproductive from decreases in mature gametes between the middle of mode of S. gracillimum. August and the end of September. Thus, declines in both 162 Hwang and Song: Sexual reproduction of soft coral

Fig. 6 Total number of mature and entire oocytes from June 2003 to October 2007. O5 stage V oocytes, WO whole oocytes, * month with no collection

Fig. 7 Total number of mature and entire spermaries from June 2003 to October 2007. S4 stage IV spermaries, WS whole spermaries, * month with no collection Hwang and Song: Sexual reproduction of soft coral 163 the number of mature gametes and in the total number of sodes, termed mass spawning, in the Indo-Pacific and gametes indicated that spawning might have occurred Great Barrier Reef regions (Harrison et al. 1984; Babcock between the end of August (from 1 day after the full moon) et al. 1986: Alino and Coll 1989). During mass spawning, to the middle of September (to 1 day before the new vast numbers of colonies of many species release huge moon), in 2007. quantities of eggs and sperm over just 1 night. However, temperate corals have a tendency to exhibit a somewhat low level of synchrony in spawning, and display prolong­ Discussion ed gametogenesis, whereas spawning events in tropical corals are synchronous (Benayahu 1991; Ben-David- The sexual reproductive pattern of the genus Zaslow et al. 1999; Cordes et al. 2001). S. gracillimum Scleronephthya has been identified for the first time in the contained mature gametes continuously during the months present study, which established that S. gracillimum is a of summer and early fall, and gametes of different gonochoric broadcaster. To date, very little information on developmental stages were observed together within the sexual reproduction in the family Nephtheidae has been same polyp during reproductive periods. These observa­ available, compared to that for other soft corals in the tions suggest relatively asynchronous spawning in our families Alcyoniidae and Xeniidae (Table 1). Gonochorism study population, perhaps reflecting the continuous re­ is known to be the dominant reproductive pattern in soft lease of gametes. Dendronephthya suensoni and Antho­ corals and also in most gorgonians (Grigg 1977; Benayahu plexaura dimorpha (respectively a soft coral and a et al. 1990; Brazaeu and Lasker 1990; Benayahu 1991; gorgonian) are sympatric with S. gracillimum, and show Achituv et al. 1992; Zeevi and Benayahu 1999; Lasker et similar spawning patterns during reproductive periods al. 1996; Schleyer et al. 2004; Orejas et al. 2007; Seo et al. (Choi and Song 2007; Seo et al. 2008). Also, Dendro­ 2008). Whereas hermaphroditism is observed in several nephthya gigantea, another sympatric species, released species of Alcyoniidae and Xeniidae, only gonochorism planulae continuously from summer to early fall (Hwang is found in Nephtheidae (Sebens 1983; Farrant 1986; and Song 2007). Benayahu et al. 1990; Benayahu 1991; Dahan and Thus, corals with asynchronous spawning need to em­ Benayahu 1997; Choi and Song 2007; Hwang and Song ploy a supplementary strategy to increase the possible low 2007). level of fertilization resulting from asynchrony. Control In soft corals, sexuality varies according to geograph­ of sperm density may efficiently optimize fertilization ical region. For example, Heteroxenia elizabethae is a rate, and sperm density can be affected both by dilution gonochoric coral in the Great Barrier Reef, Australia, but and the distance between female and male colonies. Ac­ is hermaphroditic in the Red Sea. Also, Sarcophyton tual spawning of S. gracillimum was observed in the field glaucum shows a low level of hermaphroditism in South when the current was weak, and spawning also occurs Africa, but gonochorism in the Red Sea (Benayahu et al. during periods of slow current in other corals; this 1990; Schleyer et al. 2004). The distribution of S. gracil­ minimizes dilution of sperm in water (Kapela and Lasker limum is fairly wide, from tropical to temperate regions 1999; Neves and Pires 2002; Penland et al. 2004). In the (Song 1976, researcher’s observation), which suggests natural habitat, the colonies of S. gracillimum completely that the sexuality of this species may differ geograph­ cover the surface of the rock, thus prohibiting establish­ ically. ment of other coral species. This high population density To optimize fertilization, and consequently to increase in a restricted space may result from asexual reproduc­ the success of reproduction in broadcasting species, tion, which may increase the frequency of fertilization, as spawning events usually occur synchronously (Benayahu has been noted in another broadcast-spawning gorgonian, and Loya 1986; Harrison and Wallace 1990; Kapela and Plexaura kuna (Coffroth and Lasker 1998). However, Lasker 1999; Schleyer et al. 2004). Especially, reef- detailed enumeration of female and male colony numbers building corals show a high synchrony of spawning epi­ in the clonal population is necessary for further study of 164 Hwang and Song: Sexual reproduction of soft coral the reproductive strategy of S. gracillimum. Song 2007; Hwang and Song 2007). However, no re­ The spawning time of S. gracillimum approximately lationship between duration of gonadal development and coincides with the full moon, occurring 4 days before a reproductive mode is apparent. full moon in 2006 and in the interval 1 day after full moon In temperate regions, sexual reproduction, including to 1 day before the new moon in 2007, which is in line gametogenesis and spawning, is directly correlated with with the behavior of other spawning corals (Harrison et al. seasonal factors such as seawater temperature (Harii et 1984; Schleyer et al. 2004; Carroll et al. 2006). However, al. 2001; Neves and Pires 2002; Vermeiji et al. 2004). it is unclear why S. gracillimum spawned eggs in the The monthly mean diameter of oocytes and spermaries morning on September 3, 2006, as most other spawning in S. gracillimum increased and decreased in line with corals release eggs and sperm after sunset (Harrison et al. fluctuations in seawater temperature throughout our en- 1984; Lasker et al. 1996; Dahan and Benayahu 1997; tire study period (Fig. 8). Especially, spermaries were Ryland and Westphalen 2004). observed only during the warmer seasons, and mature The pattern of gonadal formation and arrangement in gametes were found only after elevation of seawater S. gracillimum is similar to those of other soft corals temperature to 19-21℃ in June and July. Actual spawning (Benayahu 1991; Cordes et al. 2001; McFadden and event occurred, and others may have taken place, when Hochberg 2003; Hwang and Song 2007). Gametes are seawater temperature attained an annual peak between produced in the mesenteries, and enter the gastrovascular August and September. In the sympatric soft corals D. cavity but remain attached to the mesenteries by pedicles. gigantea, D. suensoni, and A. dimorpha, a similar repro­ After migration into the cavity, gametes rapidly mature, ductive cycle and release pattern of planulae or gametes and the connections between gametes and mesenteries are over the same period correlated with rises and falls in eliminated as the gametes grow. seawater temperature (Choi and Song 2007; Hwang and The gametogenic cycle was seasonal, and a difference Song 2007; Seo et al. 2008). Also, the survival and set­ between female and male colonies was apparent, with tlement of planulae were enhanced in warmer water, biorhythms of 12 and 5-7 months respectively. Oocytes resulting in increased reproductive success (Ben-David- developed throughout the year, whereas spermaries Zaslow and Benayahu 1996; Nozawa and Harrison 2000; formed only during a particular interval that was princi­ Fan et al. 2005). pally summer-to-fall (June to October) in S. gracillimum. In addition, S. gracillimum is an azooxanthellate coral The cycle of gonadal development was thus similar to that which requires food resources for survival, growth, and of other corals, with a short period of spermatogenesis reproduction, and thus feeds on phyto- and zooplankton in compared to that of oogenesis (Goldberg and Hamilton water (Fabricius et al. 1995a, b). Acabaria biserialis, the 1974; Benayahu and Loya 1984; Alino and Coll 1989; azooxanthellate gorgonian of the Red Sea, released Brazaeu and Lasker 1990; Harii et al. 2001), although planulae after an algal bloom, which suggests that planula spermaries and oocytes are present together all year round survival is increased by such episodes (Zeevi and in some soft corals (Kruger et al. 1998; Fan et al. 2005). Benayahu 1999). Major and minor algal blooms occurred Oogenesis usually takes over 1 year, and the duration in May and September during reproductive periods at our varies among soft corals and with respect to geographical study site (Choa and Lee 2000). These blooms may form region in the same species. For example, oogenesis takes a direct nutrient resource encouraging gametogenesis in 11-12 months in Parerythropodium f. fulvum, but 18-24 adult colonies of S. gracillimum, and also facilitating months in Sinularia humesi, S. leptoclados, S. mayi, and survival and growth of offspring. Litophyton arboreum. In S. glaucum, oogenesis requires 16-18 months in Africa and 22-23 months in the Red Sea. All of Lobophytum paciflorum, D. gigantea, and D. Conclusion suensoni require 12 months for oogenesis (Benayahu et al. 1990; Schleyer et al. 2004; Fan et al. 2005; Choi and The sexual reproductive pattern of Scleronephthya Hwang and Song: Sexual reproduction of soft coral 165

Fig. 8 Monthly mean diameter of oocytes and spermaries according to the seawater temperature (error bar＝SD). * month with no collection

gracillimum has been identified for the first time in the like to gratefully thank Yeon Kyu Jung and Digital Eco present study, focused in sexuality, reproductive mode, Photo Club (DEPC) for providing photo of spawning. We gametogenesis, and the reproductive cycle. also acknowledge HE Song, HN Kim, and JJ Park for - Scleronephthya gracillimum is a gonochoric broad­ their help in the experiment. caster, with the sex ratio of 1:1. - The oogenic cycle is longer than the spermatogenic cycle, with biorhythms of 12 and 5-7 months respec­ References tively. - Gametogenesis and spawning is related to seasonal Achituv Y, Benayahu Y, Hanania J (1992) Planulae brooding factors such as seawater temperature and algal blooms. and acquisition of zooxanthellae in Xenia macrospiculata - Spawning approximately occurs around the time of full (Cnidaria: Octocorallia). Helgo Meeresunters 46: 301- moon. 310 Alino PM, Coll JC (1989) Observations of the synchronized mass spawning and post settlement activity of octocorals on the Great Barrier Reef, Australia: biological aspects. Acknowledgements Bull Mar Sci 45: 697-707 Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, This research was supported by a grant from Sustain­ Wallace CC, Willis BL (1986) Synchronous spawning of able Conservation and Rehabilitation of Coral Resources 105 scleractinian coral species on the Great Barrier Reef. in Korea Program Funded by Ministry of Land, Transport Mar Biol 90: 379-394 and Maritime Affairs of Korean Government. We would 166 Hwang and Song: Sexual reproduction of soft coral

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