Proceedings 9th International Coral Reef Symposium, Bali, Indonesia 23-27 October 2000

Reproduction of the solitary coral Scolymia wellsi Laborel (Cnidaria, Scleractinia) from the Abrolhos reef complex, Brazil

D. O. Pires1, C. B. Castro and C. C. Ratto ABSTRACT The sexuality, reproductive mode, and timing of reproduction of Scolymia wellsi were assessed by collecting specimens bimonthly during 1996 and sporadically in 1997 and 1999. S. wellsi is an hermaphroditic brooder species. Most specimens contained simultaneously oocytes in different stages of development and/or spermaries and planulae. Early stages of oogenesis were observed mostly from August through February. Late stages occurred from August through December. Only small spermatogonia were observed. The time span between early onset of oogenesis (August) and early occurrence of planulae (June) is similar to the time span between late onset of oogenesis (February) and late occurrence of planulae (December). These results suggest that S. wellsi has long breeding and planulation periods, lasting approximately 10-11 months, and with a single polyp bearing oocytes in different stages of development within a single breeding season.

Keywords Coral, Brazil, Reproduction, Scolymia, Game- The present study describes the reproductive cycle of togenesis S. wellsi and gathers the first data on the reproductive characteristics of the species. We provide evidence for a Introduction pattern of long breeding and planulation periods, with a single polyp presenting oocytes in different stages of Studies of sexual reproduction of reef corals have development within a single breeding season. greatly increased in the past two decades. However, data available from most reef areas or coral taxa remains Materials and methods limited. Information concerning the reproductive biology of some reef corals from the South Atlantic have just Scolymia wellsi was sampled from three reefs of the recently become available, including three sympatric Abrolhos Reefs Complex (Fig. 1). Field collections were congeneric species of Mussismilia, Favia gravida and conducted by SCUBA diving. Specimens were collected Siderastrea stellata (Pires et al. 1999, Calderon et al. bimonthly in 1996 (February/04-06, April/21, June/07, 2000, Lins de Barros et al. 2000). August/12, October/08, December/09) and sporadically in The present paper is part of an ongoing study that 1997 (May/25, June/12, October/31) and 1999 focuses on the sexual reproduction of corals from the (November/09). Although it was not logistically possible Brazilian coral reefs. It deals with Scolymia wellsi to collect in smaller time intervals, our sampling schedule Laborel 1967. The validity of this species has been was sufficient to reveal general trends in gamete and discussed recently, with suggestions that it could be a larvae development and spawning. form of S. cubensis Milne Edwards and Haime 1849 All study material was deposited in the Cnidaria (Fenner 1993, Veron 2000). However, this matter does Collection of the Museu Nacional/Universidade Federal not seem to be fully settled (see Cairns et al. 1999) and, do Rio de Janeiro. All samples were fixed in 10% therefore, the name most often used for Brazilian formalin-sea water in the field, decalcified in a solution of specimens is used herein (see Veron 2000). 10% formic acid and 5% formalin and then rinsed in Scolymia wellsi is a solitary, zooxanthellate coral, running tap water. Parts of decalcified polyps were occurring from southern Florida, the Bahamas, the processed for histological examination by standard Caribbean (Humann 1994), and off the coast of Brazil, techniques (Pires et al. 1999). Serial longitudinal sections from Pernambuco to Espírito Santo (Laborel 1969), and of 7 μm were stained in Mallory Triple Stain or Manuel Luís reefs (Leão-de-Moura 1999). In the hematoxylin-eosin and observed with a compound light Abrolhos reefs it occurs mainly on the side of reefs, on microscope under up to 500x magnification. Other parts vertical walls (Castro 1994), in areas with moderate or of the polyps were dissected under a binocular low degrees of luminosity, but it has also been found in stereoscope (up to 50x magnification) to examine the waters as deep as 110 meters (Laborel 1967). It is occurrence of gonads and developing planulae. common, but not abundant, often with a few individuals Initially five individuals were examined in each occurring close together, forming small clusters. sampling period. After an initial observation to determine The study area, the Abrolhos Reef Complex (18° S), the time of occurrence of mature gametes and/or planulae, is unique in many aspects, including the highest reef coral up to five additional individuals (total n = 10) from these diversity in Brazil. It also contains the southernmost periods were examined (August/96, October/96, structural coral reefs known in the Atlantic Ocean (Castro December/96, October/97, November/99). Timing of and Pires, in press).

1 Museu Nacional/UFRJ, Quinta da Boa Vista s/n, São Cristóvão, Rio de Janeiro, RJ, 20940-040, Brasil ,e-mail: [email protected]

spawning of gametes and planulation were inferred by the stages occurred together from October to December appearance of mature oocytes and planulae. within some single polyps. Mature oocytes (Fig. 2B) were found for extended periods, approximately five months (from August to December) in most of the observed polyps. The histological examination of S. wellsi revealed only a few instances where resorption of mature oocytes occurred (Fig. 2C). Mature oocytes lacked zooxanthellae and the maximum largest axis observed was 652 µm (in a polyp from November/99). Oocytes larger than 600 µm were also observed in samples from October/97. Female and male gametes differ in the timing of their developmental periods. The beginning of spermatogenesis took place from August to December. Only early stages of spermatogenesis were observed (Fig. 2D), but not all polyps collected in this period bore spermaries. The maximum number of immature spermaries per mesentery was 12 in a sample collected in August/96. All samples within this period (August through December) were collected at or up to 4 days before the new-moon. Gonads of both sexes were separated, but in the same mesenteries. Spermaries occurred closer to the oral disc, whereas the oocytes were located more basally in the polyps.

Fig.1 Map of study area. Abrolhos Reef Complex, Bahia, Brazil.

The largest axis of oocytes with a nucleolus in the histological section was measured using a calibrated micrometer. Ten oocytes from each individual were measured. Photomicrographs were obtained with an optical Olympus BH2 microscope. The classification of gametogenesis stages follows Pires et al. (1999).

Results

Scolymia wellsi is an hermaphroditic brooder species with a gametogenic cycle lasting approximately 10-11 months. Gametogenesis and the histological appearance of the gonads of S. wellsi are similar to that described for Mussismilia spp. (Pires et al. 1999). Gametogenesis was divided into three approximate stages of development according to Pires et al. (1999) and will not be elaborated Fig. 2 Gametogenic and embryogenic stages of Scolymia upon here. Oocytes were found throughout the year in all wellsi, Abrolhos Reef Complex: A – Stage 1 oocytes specimens examined. The earliest recognized female (May/97); B – Stage 3 oocytes (Aug/96); C – Arrow gamete (oogonia) was 12 μm (largest axis) (sample from indicates the resorption of an oocyte (Dec/96); D – Stage October/97) and was first detected in the mesenterial 1 spermaries and stage 3 oocytes (Aug/96); E – Embryo gastrodermis. Small oogonia consisted mostly of nuclei (Aug/96); F – Planulae (Nov/99). Scale bars = 100 µm. which contained distinct nucleoli. The maximum observed number of stage I oocytes (Fig. 2 A) per Zooxanthellate embryos (Fig. 2E) were observed in mesentery was 30, all of them inside the mesoglea some polyps from samples collected on August/96. (sample from February/96). The maximum observed Brooded larvae were observed in polyps where the number of oocytes per mesentery was 40, observed in a spermatogenesis had already began. Ciliated polyp collected on June/97. zooxanthellate planulae had well developed ectodermal, Oocytes at different developmental stages frequently endodermal and mesogleal layers, and presented two occurred in the same mesenterial septa. The three oogenic rudimentary mesenteric septa (Fig. 2F). The largest whole larva measured in histological preparations was 534 µm.

Larvae were observed in samples from August to there are even a few species in which both modes occur December. (Harrison 1985). The only two others species of mussids Spawning and larvae release were inferred to have reported as brooders are Isophyllia sp. and Mycetophyllia occurred in 1996 and 1997 during the second half of these ferox studied by Duerden (1902) and Szmant (1986), years. The only sample from 1999 (November) also respectively. contained mature oocytes and planulae (Fig. 3). The Only immature spermaries, at the beginning stage of probable periods of spawning and larval release occurred development, were observed in all polyps examined, during sea warming and increasing daylength ( Pires et al. occurring together with mature oocytes, embryos and 1999). planulae. It must be emphasized that all samples bearing spermaries were collected near the new moon and that they did not occur in all individuals from these samples. Such data suggest that spermatogenesis in Scolymia wellsi may develop within a short period (approximately one month), as r eported to other brooding coral species ( Harrison and Wallace 1990). In such case, spawning would follow a lunar cycle, probably occurring near the last-quarter moon. Mature oocytes and larvae occurred simultaneously between August and December, suggesting that larvae may be released repeatedly during an extended breeding season (Fig. 3). Mature gametes or planulae have been observed in some brooder species year-round (Harrison and Wallace 1990). Although recorded in August 96 and November 99, embryos were not seen in preparations from October 96, 97 and December 96. This fact is possible due to damages occurred in the preparations. Not Fig. 3 Scolymia wellsi. 1 = Stage 1 oocytes; 2 = Stage 2 all embryos and planulae had satisfactory histological oocytes; 3 = Stage 3 oocytes; ♂ = spermaries;  = results and commonly parts of them were destroyed, embryos; making difficult their observation and identification. = planulae. Open rectangle = range of oocytes Brooded larvae can often settle within hours after largest axis; vertical line = standard deviation; dot = mean release (Szmant 1986). The apparent distribution of S. of oocytes largest axis. Numbers in parentheses = number wellsi in small patches could be related to local of individuals examined, total number of oocytes recruitment, which may take place in the same habitat measured. where adults have been successful (Harrison and Wallace 1990) Discussion Acknowledgements The authors thank B. Segal, C. R. Hermaphroditism is the rule in the Mussidae. There Ventura, M. Lins de Barros, M. Medeiros, S. Pinto are reports of this condition in Acanthastrea (Willis et al. (Departamento de Invertebrados, Museu Nacional), C. A. 1985, Babcock et al. 1986, Heyward et al. 1987, Wilson Echeverría, E. Neves, and E. Viveiros de Castro for and Harrison 1997, Shlesinger et al. 1998), Cynarina helping in different phases of this study. This research (Shlesinger et al. 1998), Lobophyllia (Harriott 1983, was funded by the Conselho Nacional de Willis et al. 1985, Babcock et al.1986, Shlesinger et al. Desenvolvimento Científico e Tecnológico (CNPq), the 1998), Mussa (Steiner 1993), Mussismilia (Pires et al. Fundação de Amparo à Pesquisa do Estado do Rio de 1999), Mycetophyllia (Szmant 1986), Scolymia (Willis et Janeiro (FAPERJ), the Fundação Universitária José al. 1985, this paper) and Symphyllia (Marshall and Bonifácio (FUJB) and the Conselho de Ensino para Stephenson 1933, Willis et al. 1985, Babcock et al. 1986). Graduados (CEPG/UFRJ). Thanks are also extended to The only possible exception would be Isophyllia, with a the Brazilian Environmental Agency (IBAMA), for suspected gonochoric species (Duerden 1902). providing collecting permits. Willis et al. (1985) included some data on the sexual reproduction of the genus Scolymia in Australia, based on References aquaria observations. Unlike S. wellsi, the authors reported S. vitiensis as a broadcast spawner. Brooding in Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver S. wellsi had been previously indicated by Pires and JK, Wallace CC, Willis BL (1986) Synchronous Pitombo (1992) who studied the cnidae of mussids and spawning of 105 scleractinian coral species on the included observations on larvae of this species. Great Barrier Reef. Mar Biol 90: 379-394 Lack of a systematic trend in the mode of re- Cairns SD, Hoeksema BW, van der Land J (1999) List of production among corals has been suggested (Harrison Extant Stony Corals. Atoll Res Bull 459: 13-46 1985). Most families and genera contain species that are Calderon EN, Castro, CB, Pires DO (2000) Natação, broadcasters as well as species that are brooders, and assentamento e metamorfose de plânulas do coral

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