BULLETIN OF MARINE SCIENCE, 62(3): 897–904, 1998
897
CORAL REEF PAPER
SEXUAL REPRODUCTION OF THE SCLERACTINIAN CORAL
MERULINA AMPLIATA IN SOUTHERN TAIWAN
Tung-Yung Fan and Chang-Feng Dai
ABSTRACT
Sexual reproduction of the scleractinian coral Merulina ampliata in Nanwan Bay, south-ern Taiwan was studied from 1990 to 1993. M. ampliata is a hermaphroditic broadcast spawner. Colony size at sexual maturity was 5.0–10.0 cm in diameter. Mature egg size and fecundity were 210 µm and 952 eggs cm−2 yr−1, respectively. Monthly changes of
mean oocyte diameters and frequencies of colonies containing different stages of ga-metes indicated a brief annual gametogenic cycle. Oogenesis began in June 1991 and May 1992. Spermatogenesis began 1 mo later than oogenesis. Spawning occurred in September 1990 and 1991, and August and September 1992 during late summer to early autumn. Spawning of M. ampliata took place about 1 to 2 mo later in southern Taiwan than in Okinawa. The delayed reproduction of M. ampliata at the lower latitude (southern Taiwan) suggests that sea temperature may not operate as a primary factor controlling the reproductive seasonality of this species.
Knowledge of coral sexual reproduction has increased greatly since the findings of the mass spawning on the Great Barrier Reef and other Indo-Pacific locations (Harrison et al., 1984; Willis et al., 1985; Babcock et al., 1986; 1994; Hayashibara et al., 1993) as well as the temporal separation of coral reproduction in the Red Sea and the Caribbean (Shlesinger and Loya, 1985; Szmant, 1986). The majority of scleractinian corals are her-maphroditic broadcast spawners with an annual cycle of gametogenesis that culminates in a brief period of spawning (Harrison and Wallace, 1990; Richmond and Hunter, 1990). The synchronized sexual reproductive cycles of scleractinian corals have been related to various environmental factors (Harrison and Wallace, 1990). Environmental condi-tions may influence sexual reproduction as proximate factors which provide cues to syn-chronize reproductive cycles, and ultimate causes that exert selective pressure on the synchrony and timing of breeding within each species (Giese and Pearse, 1974; Oliver et al., 1988). Some studies suggest that seasonal variation in sea temperature or photoperiod may be the major proximate environmental factor controlling the annual cycle of repro-duction (Babcock et al., 1986; Harrison and Wallace, 1990; Soong, 1991), while others indicate that sea temperature may not operate as a primary factor controlling the season-ality of reproduction (Babcock et al., 1994; Fan and Dai, 1995). The spawning period of some species often varies between localities (Harrison and Wallace, 1990; Richmond and Hunter, 1990). Regional comparison of the spawning period of the same coral species offers an approach of discerning species responses to various environmental conditions (Oliver et al., 1988; Babcock et al., 1994; Fan and Dai, 1995).
Merulina ampliata (Ellis and Solander, 1786), a potentially large (1 to 2 m in diameter)
foliaceous species, is a widely distributed scleractinian on many Indo-Pacific coral reefs (Veron and Pichon, 1980) and is one of the most abundant species in some coral commu-nities in southern Taiwan (Dai, 1993). It was suggested that M. ampliata is an efficient space competitor and often dominates the reef slopes (Dai, 1990). However, the only information available about its reproductive biology is that it is a hermaphroditic spawner and that it participates in the mass spawning event on the reefs of Okinawa, the Great
Barrier Reef, and Western Australia (Willis et al., 1985; Babcock et al., 1986; 1994; Hayashibara et al., 1993).
Here we report the sexual reproductive characteristics and the gametogenesis of M.
ampliata in southern Taiwan. The month of spawning of M. ampliata in southern Taiwan
is compared with that in Okinawa, Japan (Hayashibara et al., 1993) and the environmen-tal factors controlling the reproductive seasonality of M. ampliata is discussed.
MATERIALSAND METHODS
Samples of 10 to 20 large coral colonies (>20 cm in diameter) were collected monthly from a population of Merulina ampliata in Nanwan Bay, southern Taiwan (21°55'N, 120°45'E) from Sep-tember 1990 to October 1992. Samples were fixed with 10% formalin in seawater for at least 24 h, rinsed in freshwater, decalcified in 8% formic acid, and stored in 70% alcohol. Tissue samples were dehydrated with increasing concentrations of alcohol, cleared with xylene, and embedded in Paraplast. Serial sections 6 to 8 µm thick were prepared and stained with Mayer’s hematoxylin and eosin. These tissue sections were examined for gamete development under a compound microscope at Figure 1. Seasonal cycle of mean oocyte diameters (A) and monthly changes in percentage of colonies containing gametes (B) for Merulina ampliata in Nanwan Bay, southern Taiwan. Numbers above bars indicate the number of colonies sampled.
899 FAN AND DAI: SEXUAL REPRODUCTION OF MERULINA AMPLIATA
magnifications up to 1000×. The length and width of at least six oocytes in nucleolar section were measured for each colony using a micrometer eyepiece. The monthly variation of oocyte size and percentages of colonies containing different developmental stages of gametes were used to deter-mine the seasonal pattern of gametogenesis and spawning among colonies. The mature egg size was represented by the mean of the oocytes collected prior to gamete disappearance.
Fecundity was estimated from counts of eggs per mesentery and numbers of polyps cm−2.
Num-ber of eggs per mesentery was calculated along the length of individual mesenteries from histologi-cal sections. Number of polyps cm−2 was calculated as the number of polyps in a circle of 2 cm in
diameter from areas of colony skeleton 2 cm away from the edge.
In 1993, coral samples of various sizes were collected in July, 1 to 2 mo prior to the month predicted for spawning at Nanwan Bay. Two diameters perpendicular to one another across the colony center were measured and their average was taken as the diameter of the colony. Samples were fixed, decalcified and then examined at magnification 64× under a dissecting microscope. Colonies were considered to be sexually mature if oocytes were visible under a dissecting micro-scope.
Sea surface temperatures at the study site were measured by divers using a thermometer (±0.5°C) around noon on each sampling day.
RESULTS
GAMETOGENESIS.—M. ampliata is a simultaneous hermaphrodite. The oocytes and
sper-maries develop within each of the 12 mesenteries between the retractor muscles and the mesenterial filaments. Five development stages of gametes were classified according to the histological characteristics and relative sizes of oocytes and spermaries. The stages were: (1) oogonia, (2) developing oocytes, (3) developing oocytes and early spermaries,
Figure 2. Percentage of colonies with oocytes per size class (mean diameter) for Merulina ampliata in Nanwan Bay, southern Taiwan. Numbers above bars indicate the number of colonies sampled.
(4) developing oocytes and spermaries, and (5) mature oocytes and spermaries. In Stage 1, few oogonia were found in the mesoglea of the mesenteries and the oogonia were <75
µm in diameter. The oogonium had a nucleus with a prominent nucleolus and a thin layer of cytoplasm. In Stage 2, the oogonia underwent vitellogenesis and increased to 75–150
µm in diameter. In Stage 3, the oocytes were 150–225 µm and the spermaries appeared. The spermaries were composed of several discrete sacs which contain a few spermatogo-nia. In Stage 4, the oocytes were 175–250 µm in diameter. The spermaries increased in diameter and the spermatocytes became more numerous and smaller. In Stage 5, the ma-ture oocytes reached a diameter of 200–275 µm. The sperm were arrayed in a bouquet with the heads located peripherally and the tails projecting toward the lumen.
MATUREEGGSIZEANDFECUNDITY.—Mean diameter of mature eggs was 214.2 ± 32.6 µm
(± 1SD, n = 158) in 1991 and 211.1 ± 28.6 µm (± 1SD, n = 74) in 1992. Based on the combined data of 1991 and 1992, mean number of eggs per mesentery was 13.8 ± 2.6 (± 1SD, ranged from 10 to 21, n = 37), mean number of polyps cm−2 was 5.7 ± 0.3 (± 1SD, n = 20), and annual fecundity estimated was 952 eggs cm−2.
REPRODUCTIVESEASONALITY.—Changes of mean oocyte diameters and frequencies of
colonies containing different stages of gametes in M. ampliata over each month of the 2 yrs indicated a clear annual gametogenic cycle (Fig. 1). Gametes were not found in samples taken monthly from October 1990 to May 1991 and from October 1991 to April 1992. Oocytes first appeared in June 1991 and May 1992, then increased in size from June to August in 1991 and from May to July in 1992 (Fig. 1A). Spermatogenesis started
ap-Figure 3. Spawning time of Merulina ampliata plotted against monthly mean of annual sea surface temperature in Nanwan Bay, southern Taiwan and Okinawa, Japan (from Hayashibara et al., 1993). The spawning periods in southern Taiwan were inferred from the histological data. Numbers above and below arrows indicate the year.
901 FAN AND DAI: SEXUAL REPRODUCTION OF MERULINA AMPLIATA
proximately 1 mo later than oogenesis (Fig. 1B). Most (>90%) or all colonies contained gametes from July to September in 1991 and from June to August in 1992. The sharp decline of colonies containing mature gametes occurred between September and October 1990 and 1991, and between August and October 1992. Since the coral samples were collected before the full moon during these months, the release of gametes most likely occurred in September 1990 and 1991, and in August and September 1992.
COLONYSIZEATSEXUALMATURITY.—Most colonies (>80%) of M. ampliata contain
ga-metes when reaching a size of >5.0 cm in diameter (Fig. 2). The minimum colony size at sexual maturity was 4.5 cm in diameter. All colonies larger than 20.1 cm in diameter were mature.
SEATEMPERATURE.—Sea surface temperature began to rise in February and reached its
peak in August (Fig. 3). Spawning of M. ampliata occurred after the warmest period in Nanwan Bay.
DISCUSSION
Gonad structure of M. ampliata is similar to that of other hermaphroditic broadcasting corals in the Pectiniidae and Faviidae from the Indo-Pacific reefs (Kojis and Quinn, 1981; 1982; Harriott, 1983; Babcock, 1984; Harrison and Wallace, 1990; Fan and Dai, 1995). In these families, oocytes and spermaries occur within the same mesentery, with oocytes developing early in the gametogenic cycle.
Colony size at sexual maturity of M. ampliata in southern Taiwan was >5.0 cm in diameter. Studies on recruitment and growth of M. ampliata colonies indicated that the minimum age at first reproduction was 4–5 yrs (Fan and Dai, unpubl. data). It is similar to that of Echinopora lamellosa, another common foliaceous coral in southern Taiwan (Dai, 1993; Fan and Dai, 1995) and other gamete-releasing species. They usually became re-productive mature at 4 yrs or older (Harrison and Wallace, 1990).
Mature egg size and annual egg volume production of M. ampliata (210 µm and 4.6 mm3 cm−2, respectively) were smaller than those of other gamete-releasing species except
Porites lutea and P. australiensis (Harriott, 1983; Harrison and Wallace, 1990). However, E. lamellosa produced comparable size and volume of eggs (215 µm and 3.7 mm3 cm−2, respectively) in southern Taiwan (Fan and Dai, 1995; unpubl. data). Thus, these two spe-cies allocate similar energy to reproduction.
M. ampliata has a brief annual reproductive cycle. Gametogenesis begins in May or
June (late spring to early summer) and is completed within 4 to 5 mo. The length of the gametogenic cycle of M. ampliata resembles that of E. lamellosa (see Fan and Dai, 1995), but is shorter than that of most other Indo-Pacific scleractinian corals (Harrison and Wallace, 1990). M. ampliata also undergoes gametogenesis and spawning at a time simi-lar to that of E. lamellosa (see Fan and Dai, 1995), but different from most other scleractinian corals in Nanwan Bay, southern Taiwan. Most spawning in Nanwan Bay occurs in late April or early May (Dai et al., 1992).
M. ampliata spawned during the full and the last quarter moon phases in Okinawa, the
Great Barrier Reef, and Western Australia (Willis et al., 1995; Babcock et al. 1986, 1994; Hayashibara et al., 1993). Spawning of M. ampliata in southern Taiwan also took place during this period. The consistence of timing of spawning suggests that spawning of M.
Spawning of M. ampliata in southern Taiwan occurred in late summer to early autumn (August to September) when the sea temperatures begin to decrease (Fig. 3). M. ampliata in Okinawa spawned in July and August 1990 and in July 1991 during the warmest period of the year (Hayashibara et al., 1993). Thus, spawning of M. ampliata in southern Taiwan (22°N) lagged 1 to 2 mo behind that in Okinawa (26°N).
The spawning pattern of M. ampliata is similar to that of E. lamellosa in northern and southern Taiwan (Fan and Dai, 1995) and the Caribbean coral Montastrea annularis (Van Veghel, 1994). The gametogenic initiation and spawning of E. lamellosa and M. annularis took place about 1 to 2 mo later at warmer localities than at colder localities in Taiwan and the Caribbean, respectively. The earlier reproductive seasons of M. ampliata, E.
lamellosa, and M. annularis on higher latitude reefs contradicts the hypothesis
concern-ing the role of sea temperature in the seasonality of reproduction (Orton, 1920; Giese and Pearse, 1974). Seasonal variation in photoperiod may operate as a possible proximate factor controlling the reproductive seasonality (Babcock et al., 1994) since latitudinal variation in reproductive seasonality of these species correlated with that in photoperiod. The timing of reproduction may reflect environmental conditions favorable for the sur-vival of larvae (Giese and Pearse, 1974). Perhaps the advantage for M. ampliata and E.
lamellosa to breed near the end of seasonal disturbances (typhoons and heavy rainfalls) is
to increase the substrate availability to larvae, to avoid the high mortality caused by dis-turbances and then to increase reproductive success (Fan and Dai, 1995). Environmental conditions during these months may be favorable for the survival of coral larvae is indi-cated by the fact that other sympatric foliaceous corals, including Echinophyllia aspera (Ellis and Solander, 1786) and Mycedium elephantotus (Pallas, 1766), also spawned in August and September (Fan and Dai, unpubl. data).
The life history of M. ampliata with a brief period of intense gametogenic activity may help to maintain its abundant population in southern Taiwan. In Nanwan Bay, algal cover-age showed a remarkable seasonal variation which was high in February to April and low in summer (Dai, 1991). These algae, mainly Codium sp., often cause damage to corals by shading, smothering, or sediment entrapping. Interspecific competition and repair of dam-aged tissue involve great investment of energy which may reduce growth rate and fecun-dity of corals (Rinkevich and Loya, 1985; Van Veghel and Bak, 1994; Ward, 1995). The gametogenesis of M. ampliata begins after the seasonal algal bloom could not only favor the growth of adults but also increase the reproductive output.
In conclusion, aspects of sexual reproductive characteristics of M. ampliata, such as the age at first reproduction, mature egg size, reproductive effort, timing and period of gametogenesis, and the latitudinal variation of spawning are similar to those of E. lamellosa. The delayed reproduction of M. ampliata in southern Taiwan, compared to that in Okinawa, suggests that sea temperature may not be a primary factor controlling the reproductive seasonality of this species.
ACKNOWLEDGMENTS
We thank Y.-C. Tsay, M.-C. Lin and D.-S. Chen for their assistance in the field. This study was supported by a grant from the National Science Council, R. O. C. (NSC 81-0209-B-002A-502).
903 FAN AND DAI: SEXUAL REPRODUCTION OF MERULINA AMPLIATA
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DATE SUBMITTED: September 5, 1995. DATE ACCEPTED: May 24, 1996.
ADDRESS: Institute of Oceanography, National Taiwan University, P. O. Box 23-13, Taipei, Taiwan,
