Abstract
DEVELOPMENTAL BIOLOGY Animal Cells and Systems Vol. 16, No. 2, April 2012, 135144 a b, Sung-Jin Hwang and Jun-Im Song * a b Division of EcoScience, Womans University, Seoul 120-750, Korea; Department of Life Sciences, Ewha Womans University, Seoul 120-750, Korea (Received 17 May 2011; received in revised form 29 August 2011; accepted 1 September 2011) Dendronephthya castanea Utinomi, 1952 is a member of the family Nephtheidae, and dominates shallow waters adjacent to the southern part of Jejudo Island, Korea. This species is a gonochoric internal brooder with a sex ratio of 1:1, and releases planulae around the time of the full and new moon from July to September, when the seawater temperature peaks. The gametogenic cycle is annual, and oogenesis (12 months) is longer than spermatogenesis (45 months). No difference in reproductive features including sexuality, sex ratio, gametogenesis and gametogenic cycles was found between the sympatric species D. castanea and D. gigantea, and there was no temporal reproductive isolation. Investigation of the morphological taxonomy and molecular biology of these species indicates that they have very similar or identical traits, suggesting an absence of speciation and a need for taxonomic reclassification. Keywords: sexual reproduction; gametogenesis; Dendronephthya castanea; soft coral; Anthozoa Introduction Among the 250 species of the genus Dendro- nephthya, nine have been reported to occur in Korean Soft corals of the order Alcyonacea comprising five waters (Song 1976; Rho and Song 1977). These are families, 79 genera and approximately 1145 species are particularly abundant at 540 m depth adjacent to the fleshy mass octocorals with no skeletal axis (Daly et al. southern coast of Jejudo Island, where the sympatric 2007), and are distributed from tropical to temperate species D. castanea and D. gigantea dominate at 1025 regions. They are ecologically important and abundant m depth; however, it is difficult to distinguish them members of the biodiversity in coral reef and other because of their similar morphology (Figure 1). In this communities. These soft corals have three possible study we investigated the taxonomy of these two modes of sexual reproduction: broadcasting of ga- metes, internal brooding, and external surface brood- species by examining the reproductive features of D. ing (Benayahu and Loya 1983; Farrant 1986; Benayahu castanea, including sexuality, reproductive mode, ga- metogenesis and the reproductive cycle, and compared et al. 1990; Benayahu 1991). The reproductive mode differs among the various families; most species of the these features with those previously documented for family Alcyoniidae use the broadcast mode of repro- D. gigantea. duction, although the family Xeniidae shows only brooding behavior. In terms of sexuality, gonochorism predominates among soft coral species, although a few Materials and methods species show hermaphroditism (Benayahu et al. 1990; Collection of specimens Benayahu 1991; Achituv et al. 1992; McFadden and Jejudo Island (Figure 1) is located in the temperate Hochberg 2003; Hwang and Song 2007). The patterns zone but has a somewhat subtropical climate because of reproduction among alcyonaceans are summarized its coast is affected by the Tsushima Warm Current, in Table 1. which branches from the Kuroshio Current. Seawater Relative to the families Alcyoniidae and Xeniidae temperature in this area ranges from 13 to 288C (Korea there is limited information available regarding sexual Hydrographic and Oceanographic Administration; reproduction in the family Nephtheidae, even though KHOA) depending on the season. D. castanea mainly this family contains almost half of the known soft coral inhabits rock surfaces at 530 m depth. Small samples species (approximately 500). In particular, sexual of D. castanea (35 cm long) were cut from randomly reproductions has been described for only three species selected colonies (height 30 cm) at depths of 1030 m of the genus Dendronephthya (Dahan and Benayahu (accessed using SCUBA) in Munseom Island between 1997; Choi and Song 2007; Hwang and Song 2007), July 2003 and August 2007. Following collection the despite this genus having the majority of species samples were anesthetized with menthol, fixed in 45% (approximately 250) in the family Nephtheidae (Daly (v/v) neutral formalin diluted with seawater, and et al. 2007) and inhabiting tropical to temperate regions (Fabricius and Alderslade 2001). preserved in 70% (v/v) ethanol. *Corresponding author. Email: jisong@ewha.ac.kr ISSN 1976-8354 print/ISSN 2151-2485 online # 2012 Korean Society for Integrative Biology http://dx.doi.org/10.1080/19768354.2011.622486 http://www.tandfonline.com 136 S.-J. Hwang and J.-I. Song Table 1. Reproductive pattern documented in the literature on Alcyonacea. Sexuality Mode of reproduction Taxa Number of species G H G/H P BS EB IB U References Alcyoniidae 39 37 1 1 27 2 8 2 1,3,4,7,8,9,10,11, 15, 16 Alcyonium 11 9 1 1 5 1 4 1 1,3,8,9 Anthomastus 22 2 7, 16 Cladiella 11 1 4 Discophyton 11 1 9 Lobophytum 77 7 3, 11 Parerythropodium 11 1 3 Sarcophyton 55 5 3,10, 15 Sinularia 99 9 3 Thrombophyton 22 11 9 Nephtheidae 6 6 31 2 2,3,6,12,13,14 Litophyton 11 1 3 Scleronephthya 11 1 14 Dendronephthya 33 2 1 6,12,13 Capnella 11 1 2 Xeniidae 24 18 5 1 1 16 7 3,4,5 Xenia 15 12 3 10 5 3,4,5 Heteroxenia 41 2 1 4 3 Anthelia 22 1 1 3,4 Sympodium 11 1 3,4 Efflatounaria 11 1 3 Cespitularia 11 14 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, (14) Hwang and Song 2009, (15) Hellstrom et al. 2010, (16) Mercier and Hamel 2011. BS, broadcast spawner; EB, external brooder; G, gonochoric; H, hermaphroditic; G/H, gonochoric or hermaphroditic; IB, internal brooder; P, parthenogenetic; U, unknown. Dissection (Semi SV-6 or SV-11, Carl Zeiss) or a light microscope (BH-2, Olympus). The preserved specimens were dissected using a stereo- The overall sex ratio was determined by counting microscope (Semi SV-6, Carl Zeiss) to investigate the the number of female and male colonies during the sexuality of each colony and the external features of study period; more accurate ratios were calculated gametes. The gametogenic cycle was also investigated using the colonies from June to August throughout on a monthly basis by measuring the average length of the study period, when oocytes and spermaries were the longest and shortest axes of 30 gametes from each observed together. Deviation from a 1:1 sex ratio was colony using an image analyzer (Motic Image Plus 2.0 tested using the x goodness-of-fit test with the instrument, Motic China Group Co.); the average axis length was calculated to enable comparisons significance level set at PB0.05. Statistical analysis among months. The seawater temperature near the was carried out using SPSS version 17. collection site was recorded almost daily by the Korea Hydrographic and Oceanographic Administration (KHOA) throughout the study period. Results Sexuality and sex ratio All the D. castanea colonies examined microscopi- Images and data analysis cally were gonochoric. Among the total of 157 Images of living colonies in situ were taken using a colonies examined during the study period 87 were digital camera (5060-WZ, Olympus) with an under- female, 44 were male, and 26 contained small or water housing (Patima-7070, Patima Uw_Eng Co. no gametes (Figure 2). Female colonies were sig- Ltd.), and images of the collected specimens were nificantly more abundant than male colonies (sex obtained using a digital camera (G-7, Canon) prior ratio of 2:1), in contrast to the expected 1:1 ratio to fixation. All images of gametes were obtained using the Olympus camera attached to a stereomicroscope (including inactive colonies: x 31.132, df 2, Animal Cells and Systems 137 Figure 1. Colonies of sympatric species of Dendronephthya and map of study site. A. Colonies of D. castanea (left) and D. gigantea (right). B. Jejudo Island located in the southern part of Korea. C. Munseom Island located off the port of Seogwipo. P50.001; excluding inactive colonies: x 14.115, follicular layer and a prominent nucleus with a single df 1, P50.001). However, male colonies were nucleolus. The oocytes tended to change color as they observed mainly from late spring or early summer matured, from transparent to beige to ivory, and finally to autumn, while female colonies were present through- to vivid orange. The spermaries were initially transpar- out the year. Thus, only those colonies collected ent but became beige in color with maturity. between June and August were used to calculate the The gametes of D. castanea were classified into a sex ratio, excluding possible male colonies with small number of oogenic (five) and spermatogenic (four) or no gametes. Among the 76 colonies of D. castanea stages, depending on maturity (Table 2) and the collected between June and August in 20032007, 41 processes involved (Figure 3). In the oogenic stage, were female, 32 were male, and three were sexually the primary oocytes (stage I) were5 45 mm in diameter inactive. These data indicated a female to male sex (mean size 35.396.9 mm; mean9SD; n54), were ratio of 1.3:1, which was not significantly different clustered within the mesenterial filaments, had large from the expected 1:1 ratio (x 1.110, df 1, distinct nuclei, and were transparent as a consequence P 0.292). of the absence of cytoplasm. In stage II the nuclei of the oocytes were located on one side, and the color changed to beige as a result of the accumulation of Gametogenesis (gonad development) cytoplasm. At this stage the oocytes became individu- ally connected by pedicels to the mesenteries in the Gametogenic development in D. castanea was similar gastrovascular cavity, and their diameter ranged from to that of other alcyonaceans; the gametes originated in 46 to 100 mm (mean 79.9914.1 mm; n925). In stage mesenterial filaments within the polyp cavity. Immature III yolk synthesis (vitellogenesis) began. Yolk bodies gametes initially connected by pedicles to the mesen- accumulated around the nuclei in the oocytes, resulting teries were gradually transferred to the gastrovascular in a color change from beige to ivory. The maturing cavity, where they subsequently detached from the oocytes (diameter range 101180 mm; mean mesenteries as they matured. The spherical oocytes 130.5920.4 mm; n1947) became detached from the were evident by the presence of a well-developed 138 S.-J. Hwang and J.-I. Song Figure 2. Dendronephthya castanea. Percentage of colonies containing ooctyes, spermaries, and no gametes from 2003 to 2007. Number of colonies used in each month are indicated in parentheses. Colonies with no gamete are mentioned as unknown. mesenteries and entered a cavity covered by well aries in this stage ranged from 161 to 269 mm (mean developed follicular layers. In stage IV the oocyte size 211.9929.4 mm; n746). In stage IV the spermaries were mature, with diameters] 270 to 431 mm (mean rapidly increased because of ongoing yolk synthesis, 308.2932.9 mm; n 226). Late in this stage, the and the follicular layers became thicker. Synthesized spermaries were deep beige colored and not spherical, yolk bodies were apparent throughout the oocytes, and the spermatids metamorphosed into spermatozoa. resulting in a color change to orange. Late vitellogenic oocytes ranged from 181 to 299 mm in diameter (mean 235.3934.8 mm; n724). In stage V the mature oocytes were filled with yolk, resulting in a color Annual reproductive cycle change to vivid orange. These oocytes were] 300 mm D. castanea had a single annual reproductive cycle with to 490 mm in diameter (mean 355.8937.6 mm; n601). a clear difference between females and males. While In stage I of spermatogenesis, the immature spherical spermaries were only detected from late spring to early spermaries were embedded in mesenteries containing autumn (typically from May to September), oocytes clusters of spermatogonia, and their boundaries were were observed throughout most of the year during the indistinct. The spermaries were transparent in color study period; the exception was November 2004, when and5 45 mm in diameter (mean 34.197.1 mm; n67). no female colonies were collected. In stage II the boundaries of the spermaries were distinct In females stage I and II oocytes were found and they moved into the cavity, where they remain throughout most of the study period, although their attached to the mesenteries by pedicles. The spermaries relative frequency changed seasonally (Figure 4). In were opaque and filled with developing spermatocytes, 2003 the sum of the relative frequencies of these two and ranged in diameter from 46 to 160 mm (mean stages was comparatively low (0.190.04; mean9SD; 110.6930.6 mm; n497). In stage III the spermatocytes n 5) between July and November, but peaked in were arranged peripherally, resulting in hollow centers, December and remained high until the following March and began to develop into spermatids. The spermaries (mean 0.490.03; n3). A similar pattern was evident in changed from opaque to beige in color as the spermatids the successive years to August 2005. The frequency of accumulated, and late in this stage the spermaries and these two stages declined sharply to 0.07 in April 2004, mesenteries disconnected. The diameter of the sperm- and remained low until late August (mean 0.190.08; Table 2. Dendronephthya castanea. Range and mean diameter of gametes, which depends on stages (nnumber of gametes at each stage). Oocytes Spermaries Stage Range (mm) Mean9SD (mm) n Range (mm) Mean9SD (mm) n I 545 35.396.9 54 545 34.197.1 67 II 46100 79.9914.1 925 46160 110.6930.6 497 III 101180 130.5920.4 1947 161269 211.9929.4 746 IV 181299 235.3934.8 724 ]270 308.2932.9 226 V ]300 355.8937.6 601 Animal Cells and Systems 139 Figure 3. Dendronephthya castanea.. Development of gametes. A. Cluster of stage I oocytes. B. Stage II oocyte connected to mesentery by pedicle and stage III and stage IV enveloped with follicular layer. C. Fully matured stage V oocyte and planula. D. Cluster of stage I spermaries connected to mesentery and stage II to stage IV spermaries. Scale bar 50 mm (A) and 100 mm(B D). m, mesentery; O1, stage I oocyte; O2, stage II oocyte, O3, stage III oocyte, O4, stage IV oocyte, O5, stage V oocyte, p, pedicle, PL, planula, S1, stage I spermary, S2, stage II spermary, S3, stage III spermary; S4, stage IV spermary. n6). In September the frequency increased (peaking at In males, all the four spermary stages were observed together during brief periods that fluctuated somewhat 0.8 during October) and remained high until the following March (mean 0.590.18; n7), but between among the study years from 2003 to 2005 (Figure 5). April and August 2005 the frequency of these two oocyte The sum of the relative frequencies of stages I and II peaked in May 2004 (1.0) and June 2005 (0.7), but in stages was low (0.190.04; n4). Throughout every year 2003 the frequency peak observed in December was an in the study stage I and II oocytes increased in frequency outlier caused by observation of only two immature and then declined. In particular, the frequency of stages I spermaries. Maturing (stage III) and mature (stage IV) and II was sharply increased in December 2003 and spermaries were mainly observed from June to August September 2004, when stage IV and V oocytes were no during the study period, with mean frequencies of longer observed. The frequency of stage III oocytes also 0.590.18 (n7) and 0.290.16 (n7), respectively. fluctuated throughout the year. From 2003 to 2005 their frequency was high prior to and following summer (mean 0.690.18; n17), and low during summer (July Planulation and August; mean 0.190.03; n7). The frequency of this stage peaked in April 2004 and 2005 (0.9 and 0.7, The release of internally brooded planulae from the respectively), and then decreased steadily to August (B mother colonies of D. castanea was observed in both 0.1). In stage IV late vitellogenic oocytes were mainly field and aquarium specimens from July to August observed between April and September during the study 2003, in August 2004, and from August to September period (mean frequency 0.390.15, n14), and tend to in 2006, when mature oocytes (stage V) were largely be present at high frequencies (0.490.08; n9) during found (Figure 3C). In the field, release of ciliated summer, with a peak in June. Fully mature stage V orange planulae occurred during the full and new oocytes were found from June to November, were moon periods in July and August 2003, during the last abundant in July and August (mean frequency quarter of the moon in August 2004, and during the 0.590.04; n7), and peaked in frequency in August new and full moon in August and September 2006, from 2003 to 2005; after this the stage IV oocytes peaked respectively. Planulation of D. castanea was observed to in frequency. Planulae and mature oocytes were ob- co-occur with planulation of D. gigantea, and the served within the cavity in August 2004, suggesting the planulae were not morphologically distinguishable. In reproductive mode was internal brooding. aquaria the planulae were released continuously for 140 S.-J. Hwang and J.-I. Song Figure 4. Dendronephthya castanea. Monthly frequency of each oogenic stage from July 2003 to August 2005 (n4251oocytes). O1, stage I oocytes; O2, stage II oocytes, O3, stage III oocytes, O4, stage IV oocytes, O5, stage V oocytes, *, month with no collection. several days from branches cut off the mother colonies, 1970; Grigg 1977; Benayahu et al. 1990; Brazaeu and with the release showing no relation to lunar phase. Lasker 1990; Achituv et al. 1992; Lasker et al. 1996; Zeevi and Benayahu 1999; Orejas et al. 2007; Seo et al. 2008). Several members of the Alcyoniidae and Discussion Xeniidae are hermaphroditic, and a low level of hermaphroditism has been reported in the gonochoric Including the present study, reproduction of four species Sarcophyton glaucum (Sebens 1983; Benayahu species of the genus Dendronephthya has been reported, et al. 1990; Benayahu 1991; Schleyer et al. 2004), but all and three of them have been described from Jejudo the species belonging to the family Nephtheidae are Island (North Pacific Ocean) and one has been gonochoric (Farrant 1986; Benayahu et al. 1990; described from Eilat, in the Red Sea (Dahan and Dahan and Benayahu 1997; Choi and Song 2007; Benayahu 1997; Choi and Song 2007; Hwang and Song Hwang and Song 2007, 2009). 2007). The reproductive features of these four species With respect to sex ratio, female colonies of D. are summarized in Table 3. castanea were more abundant than male colonies All colonies of D. castanea examined in this study during the entire study period (ratio 2:1), but during were gonochoric, as previously reported for most octocorals including soft corals and gorgonians (Kinzie the breeding period (June to August) the sex ratio was Animal Cells and Systems 141 Figure 5. Dendronephthya castanea. Monthly frequency of each spermatogenic stage from July 2003 to August 2005 (n 1,536 speramries). S1, stage I spermaries, S2, stage II spermaries, S3, stage III spermaries; S4, stage IV spermaries;*, month with no collection. 1:1. This pattern was also observed in the sympatric and females for E. singularis (Santangelo et al. 2003; species D. gigantea. However, in spawners the sex ratio Tsounis et al. 2006; Gori et al. 2007). The sex ratio within is biased towards females in D. hemprichi, but is almost a population may be related to population density rather equal in D. spinulosa (unpublished data). Choi and than the reproductive mode for achieving optimal Song (2007) reported that in D. suensoni the sex ratio is fertilization (Brazeau and Lasker 1990; Santangelo biased towards females, but reproductively inactive et al. 1993; Tsounis 2005). D. castanea is extremely colonies were more abundant than the male colonies dominant in the study area together with D. gigantea, during their study, suggesting the possibility of an equal and the sympatric broadcasting species S. gracillimum is ratio. Other octocoral spawners that occur in Jejudo also very abundant (Hwang and Song 2009). The reproductive mode of both D. castanea and D. Island, including Anthoplexaura dimorpha and Calicogorgia granulosa, showed a sex ratio biased gigantea is internal brooding. The patterns of gamete towards females, but Scleronephthya gracillimum formation and arrangement in D. castanea are similar to those of other soft corals (Benayahu 1991; Cordes et al. showed an almost equal ratio (Cho 2008; Seo et al. 2008; Hwang and Song 2009). These studies strongly 2001; McFadden and Hochberg 2003; Hwang and Song suggest no correlation between sex ratio and mode of 2007, 2009). The size of gametes in the oogenic stages was almost the same for D. castanea and D. gigantea, reproduction in the soft corals. The sex ratios in some gorgonian species differ depending on the geographical while the gametes in each of the spermatogenic stages region. For example, the sex ratio of Corallium rubrum is were somewhat larger in D. castanea (Table 3; Hwang and Song 2007). The size of dendronephthyan gametes 1:1 in Costa Brava (Spain), but is biased towards females in Italy, and for both Paramuricea clavata and Eunicella does not show a strong correlation with the mode of singularis the ratio is 1:1 at the Medes Island, while at reproduction. The mature oocytes of the brooders D. Cape of Palos it is biased towards males for P. clavata castanea and D. gigantea (356938 mm and 346930 mm, 142 S.-J. Hwang and J.-I. Song Table 3. Comparison of reproductive features among four dendronephthyans Reproductive features D. castanea D. gigantea D. hemprichi D. suensoni Sexuality G G G G Sex ratio of female to male 2:1/1.3:1 (Jun to 1.5:1/0.9:1 (Jun to Aug) 3:2 (year-round) 2:1 (whole/specific period) Aug) Mode of reproduction IB IB BS BS Oogenic/spermatogenic period 12/45 12/35 Spermatogenesis rather 12/6 (month) rapid Size of matured oocyte/spermary 300490(356) /270 300480(346) /B 220(256) 260500/400 190 (249)/ (mean) (mm) 431(308) 160 (226) Gametogenic cycles/year 1 1 Year-round 1 Timing of planulation or JulSep JulSep Year-round SepOct spawning References Present work Hwang and Song 2007, Dahan and Benayahu Choi and Song present work 1997 2007 BS, broadcast spawner; G, gonochoric; IB, internal brooder; U, unknown. respectively) are larger than in the spawner D. suensoni and settlement of planulae is also enhanced in warmer (249936 mm), but the mature oocytes of D. hemprichi water, resulting in increased reproductive success (Ben- are 260 mm (maximum 500 mm), and other tropical David-Zaslow and Benayahu 1996; Nozawa and Har- and subtropical corals including Anthelia glauca, rison 2000; Fan et al. 2005). Planulation in D. castanea Sarcophyton glaucum, S. elegans and Lobophytum was also correlated with full and new moon phases of pauciflorum have mature oocytes 500 mminsize, the lunar cycle, as has been reported for D. gigantea suggesting a latitudinal gradient effect on the size of and many other soft corals (Kruger et al. 1998; gametes (Benayahu and Loya 1986; Dahan and Be- Schleyer et al. 2004; Hwang and Song 2007). nayahu 1997; Kruger et al. 1998; Fan et al. 2005; D. castanea differs morphologically from D. gigantea Hellstrom et al., 2010). In the case of C. rubrum the in colony growth form and anthocodial grade, which are major classification characters for the genus gamete size varies depending on the depth and region, Dendronephthya. All specimens in this study had the with gamete diameters being greater in shallow water and at low latitudes, suggesting the influence of a same anthocodial grade, coinciding with the original temperature gradient (Tsounis 2006). description of D. castanea from Korean waters, but the The gametogenic cycle was seasonal, and a differ- specimens had a glomerate and not an umbellate form, ence between female and male colonies was apparent, which differs from previous records (Utinomi 1952; Rho with longer oogenesis (biorhythms of 12 months) and and Song 1977). The holotype of D. castanea by shorter spermatogenesis (45 months). This is generally Utinomi (1952) and specimens described by Rho and consistent with gametogenesis observed in octocorals Song (1977) were very small (B 5 cm in height) relative (Benayahu and Loya 1986; Brazaeu and Lasker 1990; to our specimens ( 30 cm), and Utinomi (1952) Hwang and Song 2007, 2009; Seo et al. 2008; Hellstro ¨ m described different branching of the glomerate form in et al., 2010), although spermaries and oocytes are a large colony (paratype). In addition, the growth form present together throughout the year in some soft may be misleading as it can vary depending on the size corals (Kruger et al. 1998; Fan et al. 2005). The and condition (expanded or contracted) of the colony. gametogenic cycle of D. castanea was directly corre- Therefore, it was not surprising that our specimens were lated with seasonal factors including seawater tempera- morphologically identified not as a variant of D. ture, with marked fluctuations in the monthly mean gigantea but as D. castanea, although they were glome- diameter of gametes associated with changing seawater rate. However, we did not find differences between D. temperature throughout the study period (Figure 6). castanea and D. gigantea in terms of reproductive Planulation events were also observed and others may features including sexuality, reproductive mode, and have taken place when the seawater temperature the timing of reproduction (suggesting reproductive reached the annual peak between August and Septem- isolation) throughout the study. In addition, although ber. The regulation of sexual reproduction by this the evolution of mitochondrial DNA sequences is slow environmental factor is known in sympatric soft corals in the Anthozoa by the mismatch repair gene (msh1) and and the corals of temperate regions (Harii et al. 2001; the relatively recent divergence times among octocorals Neves and Pires 2002; Vermeij et al. 2004; Choi and (Pont-Kingdon et al. 1995; Shearer et al. 2002; Kim et al. Song 2007; Hwang and Song 2007, 2009). The survival 2008), the mitochondrial DNA sequences (18,730 bp) of Animal Cells and Systems 143 Figure 6. Dendronephthya castanea. Monthly mean diameter of oocytes and spermaries according to the seawater temperature (error bar SD). Left and right axes indicate mean diameter and seawater temperature, respectively. *, months with no collection. Sarcophyton glaucum (Quoy & Gaimard, 1833). Biol Bull these two species are identical (Kim 2008). Thus, these 170:3242. several studies strongly indicate the absence of specia- Benayahu Y, Weil D, Kleinman M. 1990. Radiation of tion between D. castanea and D. gigantea, and conse- broadcasting and brooding patterns in coral reef alcyo- quently suggest that D. castanea be incorporated into the naceans. Adv Invertebr Reprod 5:323328. Brazaeu DA, Lasker HR. 1990. Sexual reproduction and species D. gigantea. external brooding by the Caribbean gorgonian Briareum asbestinum. Mar Biol 104:465474. Cho IY. 2008. Biological studies of gorgonian coral Acknowledgements Calicogorgia granulosa (Anthozoa: Gorgonacea: Plexaur- This work was supported by the project titled ‘Sustainable idae) [master’s thesis]. Ewha Womans Univ. Conservation and Rehabilitation of Coral Resources in Choi E-J, Song J-I. 2007. Reproductive biology of the Korea’ funded by Ministry of Land, Transport and Maritime temperate soft coral Dendronephthya suensoni (Alcyona- Affairs of Korean Government to JIS. cea: Nephtheidae). Integ Biosci 11:215225. Cordes EE, Nybakken JW, VanDykhuizen G. 2001. Repro- duction and growth of Anthomastus ritteri (Octocorallia: References Alcyonacea) from Monterey Bay, California, USA. Mar Biol 138:491501. Achituv Y, Benayahu Y, Hanania J. 1992. Planulae brooding Dahan M, Benayahu Y. 1997. Reproduction of and acquisition of zooxanthellae in Xenia macrospiculata Dendronephthya hemprichi (Cnidaria: Octocorallia): (Cnidaria: Octocorallia). Helgo Meeresunters 46: year-round spawning in an azooxanthellate soft coral. 301310. Mar Biol 129:573579. Ben-David-Zaslow R, Benayahu Y. 1996. Longevity, compe- Daly M, Brugler MR, Cartwright P, Collins AG, Dawson tence and energetic content in planulae of the soft coral MN, Fautin DG, France SC, McFadden CS, Opresko Heteroxenia fuscescnens. J Exp Mar Biol Ecol 206:5568. DM, Rodriguez E, Romano SL, Stake JL. 2007. The Benayahu Y. 1991. Reproduction and developmental path- phylum Cnidaria: a review of phylogenetic patterns and ways of Red Sea Xeniidae (Octocorallia, Alcyonacea). diversity 300 years after Linnaeus. Zootaxa 1668:127182. Hydrobiologia 216/217:125130. Fabricius KE, Alderslade P. 2001. Soft corals and sea fans: a Benayahu Y, Loya Y. 1983. Surface brooding in the red sea comprehensive guide to the tropical shallow water genera soft coral Parerythropodium fulvum fulvum (Forska ˚l, of the central-west Pacific, the Indian Ocean and the Red 1775). Biol Bull 165:353369. Benayahu Y, Loya Y. 1986. Sexual reproduction of a soft Sea. Townsville: Australian Institute of Marine Science. coral: synchronous and brief annual spawning of p. 110111. 144 S.-J. Hwang and J.-I. Song Fan TY, Chou YH, Dai CF. 2005. Sexual reproduction of the Nozawa Y, Harrison PL. 2000. Larval settlement patterns, alcyonacean coral Lobophytum pauciflorum in southern dispersal potential, and the effect of temperature on Taiwan. Bull Mar Sci 76(1):143154. settlement of larvae of the reef coral, Platygyra daedalea, Farrant PA. 1986. Gonad development and the planuale of from the Great Barrier Reef. In: Moosa, editor et al., the temperate Australian soft coral Capnella gaboensis. Proc 9th Int Coral Reef Symp, Vol. 1. Bali, Indonesia. p. Mar Biol 92:381392. 409415. Gori A, Linares C, Rossi S, Coma R, Gili JM. 2007. Spatial Orejas C, Gili JM, Lo ´ pez-Gonza ´ lez PJ, Hasemann C, Arntz variability in reproductive cycle of the gorgonians WE. 2007. Reproduction patterns of four Antarctic Paramuricea clavata and Eunicella singularis (Anthozoa, octocorals in the Weddell Sea: an inter-specific, shape, Octocorallia) in the Western Mediterranean Sea. Mar and latitudinal comparison. Mar Biol 150:551563. Biol 151:15711584. Pont-Kingdon GA, Okada NA, Macfarlane JL, Beagley CT, Grigg RW. 1977. Population dynamics of two gorgonian Wolstenholme DR, Cavalier-Smith T, Clark-Walker D. 1995. corals. Ecology 58:278290. A coral mitochondrial mutS gene. Nature 375:109111. Harii S, Omori M, Yamakawa H, Koike Y. 2001. Sexual Rho B-J, Song J-I. 1977. A study on the classification of the reproduction and larval settlement of the zooxanthellate Korean Anthozoa 3. Alcyonacea and Pennatulacea. J coral Alveopora japonica Eguchi at high latitudes. Coral Kor Res Inst Liv 19:81100. Reefs 20:1923. Santangelo G, Abiatti M, Caforio G. 1993. Age structure and Hellstrom M, Kathryn DK, Benzie JAH. 2010. Multiple population dynamics in Corallium rubrum. In: Cicogna spawning events and sexual reproduction in the octocoral F, Cattaneo-Vietti R, editors. Red coral in the Mediter- Sarcophyton elegans (Cnidara: Alcyonacea) on Lizard Island, Great Barrier Reef. Mar Biol 157:383392. ranean Sea: art, history and science Min Ris Agr Al For, Hwang S-J, Song J-I. 2007. Reproductive biology and larval Rome. p. 131157. development of the temperate soft Dendronephthya Santangelo G, Carletti E, Maggi E, Bramnati L. 2003. gigantea (Alcyonacea: Nephtheidae). Mar Biol 152:273 Reproduction and population sexual structure of the overexploited Mediterranean red coral Corallium rubrum. Hwang SJ, Song JI. 2009. Sexual reproduction of soft coral, Mar Ecol Prog Ser 248:99108. Scleronephthya gracillimum, (Alcyonacea: Nephtheidae) Schleyer MH, Kruger A, Benayahu Y. 2004. Reproduction and based on long-term collection from Jejudo Island, Korea. the unusual condition of hermaphroditism in Sarcophyton Galaxea 11:155167. glaucum (Octocorallia, Alcyoniidae) in KwaZulu-Natal, Kim B. 2008. A population genetic study on the Korean South Africa. Hydrobiologia 530/531:399409. tideland snail, Batillaria cumingi and complete mitochon- Sebens KP. 1983. The larval and juvenile ecology of the drial DNA sequences of three octocorallian species temperate octocoral Alcyonium siderium Verrill. I. Sub- (Nephtheidae) [master’s thesis]. Ewha Womans Univ. stratum selection by benthic larvae. J Exp Mar Biol Ecol Kim B, Kong S-R, Song J-I, Won Y-J. 2008. Molecular 71:7389. phylogeny and divergence time estimation of the soft Seo SY, Hwang SJ, Song JI. 2008. Sexual reproduction of coral Dendronephthya gigantea (Alcyonacea: Nephthei- Anthoplexaura dimorpha (Gorgonacea: Octocorallia) dae). Korean J Syst Zool 24(3):327332. from Munseom, Jejudo Island, Korea. Anim Cell Syst Kinzie RA. 1970. The ecology of the gorgonians (Cnidaira; 12:231240. Octocorallia) of Discovery Bay, Jamaica [Ph.D. thesis]. Shearer TL, Van Oppen MJ, Romano SL, Worheide G. 2002. New Haven, CT: Yale University. Kruger A, Schleyer MH, Benayahu Y. 1998. Reproduction in Slow mitochondrial DNA sequence evolution in the Anthelia glauca (Octocorallia: Xeniidae). I. Gametogen- Anthozoa (Cnidaria). Mol Ecol 11(12):24752487. esis and larval brooding. Mar Biol 131:423432. Song JI. 1976. A study on the classification of the Korean Lasker HR, Kim K, Coffroth MA. 1996. Reproductive and Anthozoa 2. Alcyonacea. Korean J Zool 19(2):5162. genetic variation among Caribbean gorgonians: the Tsounis G. 2005. Demography, reproductive biology and differentiation of Plexaura kuna, new species. Bull Mar trophic ecology of red coral (Corallium rubrum L.) at the Sci 58:277288. Costa Brava (NW Mediterranean): ecological data as a McFadden CS, Hochberg FG. 2003. Biology and taxonomy tool for management [Ph.D. Thesis]. Univ of Bremen. of encrusting alcyoniid soft corals in the northeastern Tsounis G, Rossi S, Aranguren M, Gili J-M, Arntz W. 2006. Pacific Ocean with descriptions of two new genera Effects of spatial variability and colony size on the (Cnidaria, Anthozoa, Octocorallia). Invertebr Biol reproduction output and gonadal development cycle of 122(2):93113. the Mediterranean red coral (Corallium rubrum L.). Mar McFadden CS, Donahue R, Hadland BK, Weston R. 2001. A Biol 148:513527. molecular phylogenetic analysis of reproductive trait Utinomi H. 1952. Dendronephthya of Japan, I. evolution in the soft coral genus Alcyonium. Evolution Dendronephthya collected chiefly along the coast of Kii 55(1):5467. Peninsula. Seto Mar Biol Lab 2(2):121212, pl. 911. Mercier A, Hamel J-F. 2011. Contrasting eproductive strate- Vermeij MJA, Sampayo E, Broker K, Bak RPM. 2004. The gies in three deep-sea octocorals from eastern Canada: reproductive biology of closely related coral species: Primnoa resedaeformis, Keratoisis ornata, and gametogenesis in Madracis from the southern Caribbean. Anthomastus grandiflorus. Coral Reefs. doi: 10.1007/ Coral Reefs 23:206214. s0033801107248. Zeevi D, Benayahu Y. 1999. The gorgonian coral Acabaria Neves EG, Pires DO. 2002. Sexual reproduction of Brazilian biserialis: life history of a successful colonizer of artificial coral Mussismilia hispida (Verrill, 1902). Coral Reefs 21:161168. substrata. Mar Biol 135:473481.
Journal
Animal Cells and Systems
– Taylor & Francis
Published: Apr 1, 2012
Keywords: sexual reproduction; gametogenesis; Dendronephthya castanea; soft coral; Anthozoa
