Lunar Patterns of Gametogenesis, Embryogenesis and Planulation in Puerto Rico

BULLETIN OF MARINE SCIENCE. 37(3): 880-892. 1985 CORAL REEF PAPER

SEXUAL REPRODUCTION OF FAVIA FRAGUM(ESPER): LUNAR PATTERNS OF GAMETOGENESIS, EMBRYOGENESIS AND PLANULATION IN PUERTO RICO

Alina Szmant-Froelich, Michael Reutter and Linda Riggs

ABSTRACT Several brooding scleractinian coral species are known to release planulae at certain phases ofthe moon. This study ofa brooding coral, Faviafragum, suspected of having a lunar cycle of planulation, had the objective of determining whether there was also a lunar periodicity in gametogenesis and embryogenesis. Histological examination of specimens collected at 2 to 4 day intervals over several lunar cycles revealed a lunar periodicity in the maturation of oocytes and a lunar cycle in spermatogenesis which ended with ovulation and presumably spawning of sperm about day 18 after the new moon. Embryos developed slowly, taking about 4 days to reach the planula stage. After brooding for about 3 weeks the mature planulae were expelled between days 6 and 15 after the new moon, with a peak on day 11. Under natural conditions, planulae were never retained past the end of the planulation period, which was followed closely by a new ovulation event. Therefore, the lunar periodicity in planulation is driven by a lunar cycle of gamete maturation and ovulation. The timing of this ovulation is about 4 to 5 days after the full moon, which is the same time many broadcasting corals are known to spawn.

Regardless of the mode of reproduction most coral species show a periodicity in their larval or gamete release. The timing of these events appears to be influ- enced by three physical factors: annual temperature variation, lunar/tidal cycles or variations in nocturnal illumination, and the diellight-dark cycle (Kojis and Quinn, 1981). These factors can act singly or in combination depending on the species. Virtually all brooding corals time larval release by some phase of the lunar cycle (Marshall and Stephenson, 1933; Harrigan, 1972; Stimson, 1978). Most coral reproductive studies have focused on gamete or planula release. Only recently have studies turned to the events preceding and immediately fol- lowing fertilization-gametogenesis and embryogenesis. Even though there is a renewed interest in coral reproduction, the gametogenic and embryogenic cycles of only a few species of coral are known (Stylophora pistillata-Rinkevich and Loya, 1979a; Astrangia danae-Szmant-Froelich et aI., 1980; Goniastrea australensis- Kojis and Quinn, 1981; Astrangia lajollaensis- Fadlallah, 1982; Balan- opyllia elegans and Paracyathus stearnsii-Fadlallah and Pearse, 1982a; 1982b respectively). To date there have been no reports on the gametogenesis or embryogenesis of a Caribbean coral. Several species of scleractinian coral have been observed to brood their embryos to the planula stage (Marshall and Stephenson, 1933; Duerden, 1904; Atoda, 1947; Fadlallah and Pearse, 1982; Rinkevich and Loya, 1979a; 1979b), and some of these brooding species have been reported to release their planulae (i.e., to planulate) at regular intervals in phase with the lunar cycle (Harrigan, 1972; Richmond and Jokiel, 1984). The above studies dealt exclusively with the release of the larvae, and thus the question remains as to whether mature planulae are present at all times and only the release of the larvae follows a lunar periodicity, or whether the production of planulae also follows a lunar cycle. Favia fragum is a small-sized (less than 5-cm diameter) western Atlantic reef coral that has long been known to planulate (Duerden, 1902), with recent studies

880 SZMANT·FROELlCH ET AL.: LUNAR REPRODUCTIVE PATTERNS 881

Table I. Criteria for classification of gametocytes and embryos into developmental stages (H-H refers to Heidenhain's azocarmine-aniline blue stain used in this study)

Stage Oocytes Spermaries Embryos 0 No ova in mesentery No spermaries in mesen- No planulae in coelenteron tery Enlarged interstitial cells Small clusters of intersti- Same size and staining properties with large nuclei in me- tial cells near or entering as egg, but free from mesen- soglea of mesentery mesoglea tery. Includes development up to the 2-layered gastula stage. II Accumulation of small Clusters of spermatocytes Early planula; mesoglea present. amount of cytoplasm with distinct spermary Oral pore and coelenteron around nuclei boundary; large nuclei form. No longer stains red. III Oocytes of variable size; Spermatocytes smaller Mesenteries forming as invagina- main period of vitello- with smaller nuclei; tions of mesoglea and endo- genesis number of cells within derm spermary much larger IV Oocytes full size with in- Spermatocytes with little Well-developed septa; mature dented nucleus; stains cytoplasm; tails not evi- planula dark red with H-H dent V Spermatozoa with tails; ready to spawn

indicating that planulation is more frequently observed at certain phases of the moon (Lewis, 1974). Lewis has described several aspects of the settlement behavior and the physiology of the planulae, but little else is known about this species' reproduction or ecology. Its distribution on the reef is generally restricted to the shallow reef flat, lagoon and upper fore-reef zones. It is often found in clusters of two to three colonies on pieces of rubble. Dumbbell shaped colonies are common, and give the impression that once separate colonies have fused. As part of an extensive study on the reproductive patterns of Caribbean reef corals, we undertook a study to examine gametogenesis and planula production in Pavia fragum. The objectives of this study were to determine whether 1) planulation in this species follows a lunar cycle, and 2) if so, was this a result of a lunar cycle in gametogenesis and embryogenesis. In addition, we wanted to determine whether the cycle was repeated year-round, and whether individual colonies were reproductive year-round.

MATERIALS AND METHODS

These studies were conducted out of the Magueyes Marine Laboratory of the University of Puerto Rico. Gametogenesis.-For the gametogenesis studies, 5 to 10 colonies of F. fragum were collected from the back-reef zones of several nearby reefs. Sampling was repeated every 2 to 4 days over 30- to 35- day periods in November/December 1982; February/March 1983; and July/August 1983. The di- mensions and numbers of polyps of each colony were recorded. The samples were fixed with Zenkers fixative (Yevich and Barzscz, in press) for 24 h and decalcified in a 10% HCl solution which contained small amounts of EDT A, sodium tartrate and sodium potassium tartrate. Tissues were washed for 24 h in tapwater to remove the acid, dehydrated in S-29 and cleared in UC-670 (Technicon Corp. histological dehydrating and clearing agents, respectively), and embedded in Paraplast. Polyps were oriented so that both longitudinal and cross sections were obtained. Sections 7-J.lmthick were stained with Heidenhain's azocarmine-aniline blue (Luna, 1968) and examined with a compound microscope (up to 1,000 x). Gametocytes and embryos found in each section were classified as to developmental stage according to the criteria in Table 1 and counted (Szmant-Froelich et aI., 1980). The number of 882 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.3, 1985

Figure 1. a. In situ planulation study. Colonies of Faviafragum were placed in chambers made out of acrylic tubing with nitex screen windows to allow water exchange. Chambers were secured to a cement platform. b. Close-up of expanded colony of F.fragum showing planulae lodged in the tentacles (arrows).

gametocytes counted for each colony varied considerably depending on the number of polyps sectioned, the orientation of the polyps and the chance that the section included a portion of a gonad bearing mesentery. While every effort was made to standardize our techniques as much as possible, it was obvious that it would be difficult to compare the absolute counts obtained for each colony. Therefore, the data from all colonies for each date were pooled and the percentages of the total oocytes, spermaries and embryos made up of each stage were calculated for each sampling date, The timing of release of the planulae was studied in both the laboratory and in situ. For the laboratory studies, colonies were individually placed in 500-ml plastic containers with Nitex screen windows (100-200 ILm mesh) suspended in an aquarium with running seawater. The number of planulae released the previous night were counted each morning, For the in situ studies, the colonies were placed into chambers, made out of 8-cm diameter acrylic tubing with 200 ILm mesh Nitex windows, which were fastened to a cement platform located at I-m depth on the back side of Enrique reef (Fig. la). Each day, the chambers were retrieved, the number of planulae released counted and the chambers cleaned. Exposure to air was kept to a minimum. The laboratory studies were repeated in November 1982, February, March, June, July, August, October and November 1983 and March 1984. The in situ studies were done simultaneously with the laboratory runs from August 1983 onwards. At the end of some of the studies (see details below) the colonies were fixed and examined histologically as above to determine whether any planulae still remained in the polyps. Sampling dates were converted to lunar day, with the new moon being day I of the lunar cycle; the gametogenic and planulation data were then plotted against lunar day.

RESULTS As is typical for scleractinian corals, the "gonads" (the aggregations of germ cells in Cnidaria are not true anatomical gonads (Werner, 1980), but will be referred to as such throughout this paper) form as thickenings of the mesenteries, mid-way between the longitudinal muscle bands and the mesenterial filaments. The germ cells which form the gonads are derived from a stock of interstitial cells; there is no "germ plasm" (German "Keimbahn") as in higher animals (Werner, 1980). The gametes develop in the mesogleal layer, which becomes stretched and indistinguishable by the time the gametes mature. In FaviaJragum, both oocytes and spermaries develop within the same mesentery, but oocytes tend to develop basally and spermaries distally. F. Jragum has between 9 and 22 mesenteries per polyp and all are capable of developing gonads. Practically all of the colonies observed had gonads; only two of them had no gonads at all. One of these was very small and had only two polyps. Six colonies had only female gonads. This, however, may have been caused by sectioning only the base where the female gonads are concentrated, since several colonies initially thought to have few or only female gonads were found to contain both sexes upon SZMANT-FROELICH ET AL.: LUNAR REPRODUCTIVE PATTERNS 883

OOGENESIS 100 STAGE

\.LJ I e" 80 ~ II C/) ::I: III U

Figure 3. Gametogenic stages of Faviajragum: a, Stage I oocyte next to mature oocyte; b, A Stage II oocyte before vitellogenesis has begun, and a Stage III oocyte with some yolk accumulation; c, Stage IV oocyte showing indentation of nucleus; d, Magnification of nuclear indentation showing extreme peripheral location of the nucleus; e, Stage III spermaries, Notice large size of spermatocyte nuclei; f, Stage IV spermaries, and halo around spermaries due to condensation of mesenterial material into the spermaries. This halo is also visible in (b) below the Stage II oocyte and in (e) just above the right spermary; g, Three Stage V spermaries next to a Stage IV oocyte. Notice three Stage III spermaries in lower center; h, Empty holes left in mesogiea by spawning of spermaries. Scale bar = 10 /otm in a, d, e, h; scale bar = 50 /otm in b, c, f, g. SZMANT-FROELlCH ET AL.: LUNAR REPRODUCTIVE PATTERNS 885

SPERMATOGENESIS STAGE

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0 4 20 24 28 () • LUNAR DAY • Figure 4. Summary of the lunar spermatogenic pattern in Faviafragum determined by the examination of histological samples collected over three lunar periods. See text for details. Stages as in Table I. dance just after the full moon, and were not found in any of the samples collected after day 18 of the lunar cycle (Fig. 2). Spermatogenesis. -Spermaries were classified into five developmental stages (Ta- ble 1). Spermatocytes were first observed in the endoderm near the mesoglea (Stage I). They were about 4 ~m in diameter and had the appearance of enlarged interstitial cells, but occurred in clusters of five to ten cells. These clusters then entered, or were engulfed, by the mesoglea (Stage 11).It appears that at this stage, spermary enlargement occurs by immigration of additional primary spermatocytes from the endoderm (Fig. 3f). Further growth of the spermaries occurs by division of the cells within each spermary (Stage III). Individual spermatocytes at this stage are smaller than in the previous stages, and their nuclei and cytoplasm are easily distinguishable (Fig. 3e). The nuclei then begin their condensation, and meiosis probably takes place, so that the spermatocytes become much smaller and have little cytoplasm (Stage IV) (Fig. 3f). Finally, the sperm tails become easily visible (Stage V) and often a lumen forms within the spermary (Fig. 3g). Stage I spermaries were present in small numbers throughout the lunar cycle, with peaks in relative abundance between days 6 to 26 ANM (Fig. 4). Stage II spermaries were present in small numbers (5-10%) from days 6 through 16, but increased in numbers dramatically to make up from 70 to 80% of the spermaries present from days 18 to 28 ANM. Stage III spermaries appeared in large numbers on day 28 and began to decrease in proportion after day 4 (Fig. 4). Stage IV spermaries were only present during days 6 through 18. Stage V spermaries were mature spermatozoa ready to be released and they were only found between days 10 and 18 ANM, which coincides with the period during which Stage IV oocytes were also present (Fig. 2). For several days after the disappearance of the Stage 886 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.3, 1985 r-

Figure 5. Embryogenic stages of Faviafragum: a, Two Stage I embryos with bumpy exteriors (- blastula stage); b, Early Stage II embryo. Interior layer is forming and coelenteron is almost open; c, Stage III planula showing stomadeum (arrow) and budding mesenteries; d, Zooxanthellae entering Stage III planula and concentrated in ectoderm around oral pore; e, Zooxanthellae crossing over from adult to larval tissues (arrows). Also notice mesenterial bud (m). Scale bar in b = 50 ~m for a-c; Scale bar in d = 30 ~m for d, e.

V spermaries there were signs of spawning, such as partially empty spermary sacs (Fig. 3h). Embryogenesis. - Embryonic development was subdivided into four stages (Table 1). Embryos were first seen in the coelenteron at the same time when the mature oocytes disappeared from the mesenteries. They were located at the base of the coelenteron near where the mature oocytes had been and had the same size and staining properties as the unreleased oocytes. Their surface was extremely bumpy indicating the presence of many cells (Fig. 5a). The earliest stage we found was a blastula-like stage. These embryos were solid (stereoblastula) and gastrulation appears to occur by delamination to form a stereogastrula. The ectodermal cells were more columnar and the endodermal layer appeared more syncytial. All embryos up to this point were classified as Stage I embryos. At this point the embryos began to grow in size and the red-staining yolk material became more dispersed, changing the appearance of the embryos. The ectodermal cells became distinctly columnar and a mesogleallayer became apparent (Stage II) (Fig. 5b). The embryos began to elongate and resembled early stage planulae seen in other species with external development (Szmant-Froelich et aI., 1980). The oral pore could be seen forming as an invagination of the ectoderm, and the SZMANT-FROELICH ET AL.: LUNAR REPRODUCTIVE PATTERNS 887 coelenteron began to open up as the endodermallayer became more organized. All early planulae up to this point of development were classified as Stage II. Zooxanthellae were first seen entering the embryos at about this stage. They appeared to enter the early planula through the ectoderm near the oral pore (Fig. 5d). Often the oral end ofa planula was found abutted to the parental endodermal tissues where there would be a concentration of zooxanthallae, as if they were preparing to transfer to the larva (Fig. 5e). The zooxanthellae were clearly more abundant in the planular ectodermal layer, at this point, than in the endoderm. They did not become exclusively endodermal until the end of Stage III. The first formation of mesenteries was discernible by strands of mesoglea ra- diating out into the endodermal syncytium. It appeared to occur first near the oral pore. The endoderm then appeared to organize around the mesogleal strands. Later mesenteries forming after the endodermal layer was well organized could also be seen to begin as an ingrowth of the mesogleallayer (Fig. 5e). All planulae with well developed coelenteron and budding mesenteries were classified as Stage III. The number of mesenteries continued to increase and usually six (3 complete pairs) had developed by the time planulation began (Fig. 5c). Mesenterial filaments also were already developed in the mature planulae. The latter were about 2 mm in length and 0.5 to 1.0 mm in width, but occasionally a colony would release numerous small planulae 1 mm in length and about 0.25 in width. The lunar cycle of embryogenesis is summarized in Figure 6a. This figure also shows the timing of occurrence of Stage IV oocytes and Stage V spermaries to demonstrate the close synchrony between the disappearance of the mature gametocytes and the appearance of the first embryos. These events can be seen to occur immediately after the disappearance of the Stage IV planulae at about day 17-18 ANM. It took the embryos about four days to reach the early planula stage. This is a much slower rate of development than that reported for externally developing larvae (Szmant-Froelich et aI., 1980; Kojis and Quinn, 1981; Krupp, 1983). The embryos were brooded for about 3 weeks before release. Planulation.-Planulae could be seen moving within the polyps at night when the polyps were expanded. They often moved up into the tentacles where they looked like tiny white sausages (Fig. 1b). Duerden (1902) reported thinking that the planulae might exit the polyps through the tentacles, but we were never able to observe them doing this. The planulae were surreptitiously released beginning 2 hours after dark. We were never able to observe one exiting a polyp, possibly because our flashlights disturbed their behavior. As reported by Lewis (1974), the newly released planulae swam around near the water surface, but began to explore the bottom and to settle early the next morning. During the first few days of each planulation cycle most of the newly released planulae were found swimming in the morning. Towards the end of the cycle, most of them were already loosely attached by the next morning. The first two planulation studies (November/December 1982, and February/ March 1983) were done by collecting 10 colonies every 2 to 4 days and counting the number of planulae released by each colony each day until it was replaced by a new colony. We noticed that colonies collected before day 6 ANM released no (or only 1 or 2) planulae the night of the day they were collected, while colonies collected after day 6 usually released many planulae that night. In other words, if mature planulae were present, the stress of collection resulted in the planulae being released soon after the first dark period. Not all planulae were released on the first night, however, and it was apparent that the planulation period peaked sometime from days 9 to 11 ANM. 888 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.3, 1985

100 u.... 0 A z 80 0 (/) I- W (/) C) 0 ~ I- 60 Cl.. (f) ~ 0 0 u >- c:: 40 I- CD Z \J.J ~ U W c:: 20 w Cl..

w 0 ..J w u o December B ~ >- lL.. ..J U • February 0 ::> o March z a:: 40 I- ~ w • June Z ..J > • July \J.J Cl.. 0 u t" October a:: ..J 0 *November w ~w 20 Cl.. I-(f) O~ I-w ..J w a:: 0 4 8 12 16 20 24 28 () 0 () • LUNAR DAY • Figure 6. Embryogenesis and planulation cycles of Favia fragum: a, Summary of embryogenesis pattern determined by the examination of histological samples collected over three lunar periods. (See text for details. Stages as in Table I.); b, Timing of planula release by colonies held in the laboratory.

All of the laboratory planulation trials done after these initial ones were done with colonies collected before day 6 ANM with the same 10 colonies being used without replacement throughout the test. The results of the laboratory planulation trials are summarized in Figure 6b. Planulation began as early as day 6 ANM and lasted as long as day 15 ANM, but most of the planulae were released between days 8 and 11 ANM. These results agree with the histological studies showing mature planulae present during that time, and a total absence of mature planulae in colonies collected after day 16 ANM. Planulation by corals kept in the laboratory for 3.5 months occurred during the expected planulation period for the first two cycles, but began about a week earlier (day 24, peaking on day 2) during the third and fourth cycles. Colonies used in the in situ studies planulated later and released fewer planulae than did laboratory colonies. Histological examination of these colonies at the SZMANT-FROELICH ET AL.: LUNAR REPRODUCTIVE PATTERNS 889 end of the planulation period revealed that many of their polyyps still had planulae while only a few polyps of the laboratory colonies did. We have no explanation for why the in situ conditions, which should have been more natural than the laboratory ones, interfered with planulation.

DISCUSSION

Gametogenic cycles have previously been described for only two brooding corals: the Red Sea coral Stylophora pistil/ata (Rinkevich and Loya, 1979a) and a Californian solitary coral Balanophyllia elegans (Fadlallah and Pearse, 1982a). The present study is the first to describe the gametogenic cycles of a species that planulates monthly throughout the year. Only three other species have been observed to planulate year-round on a lunar cycle: Pocil/opora damicornis (Atoda, 1947; Marshall and Stephenson, 1933 as Pocillopora bulbosa; Richmond and Jokiel, 1984), Cyphastrea oce/tina (Stimson, 1978) and Agaricia humilis (van- Moorsel, 1983). The results of the histological studies provide conclusive evidence for a lunar periodicity in gametogenesis. However, there are distinct differences between the oogenic and spermatogenic cycles. Oogenesis, as indicated by the differentiation of new primary oocytes, occurs pretty much throughout the cycle and large, almost mature oocytes probably remain through several lunar cycles. In other words, oocytes appear to take several months to grow to their mature size. Final maturation occurs for only one or two oocytes per mesentery each lunar cycle, and several other oocytes remain in each mesentery without ripening. Early spermaries (Stage I), while present throughout most of the cycle, must differentiate rapidly between days 16 to 18 in order to account for the large numbers of Stage II spermaries present in samples collected from days 18 to 20. Therefore, the results indicate that not just the final maturation of the spermaries, but the whole spermatogenic sequence occurs within a lunar cycle. Maturation of the oocytes is accompanied by a curious indentation of the nucleus. By the end of vitellogenesis the nucleus was always peripherally located so that the indentation was of the egg cortex as well as of the nucleus. This indentation has been seen in mature oocytes of several other coral species. We suggest that its function is to somehow facilitate fertilization. The gonads are located in the typical cnidarian position between the mesenterial retractor muscles and the mesenterial filaments (Hyman, 1940). Gonad maturation is synchronous within and between colonies. These conditions appear to be common among the Faviidae (Kojis and Quinn, 1982). There was no evidence of adolescent protandry as seen in other faviids (Rinkevich and Loya, 1979a; Kojis and Quinn, 1981); the smallest reproductive colonies found (5-10 polyps) had both male and female gametes. Rinkevich and Loya (1979a) suggested that corals in which the gonads matured within the mesentery would be expected to produce a larger number of large eggs which were broadcast. They suggested this mode of reproduction was limited to large-polyped (mostly massive) species. Small-polyped (mostly branching) species were expected to produce only a few small eggs in gonads that bulged into the gastric cavity. Internal fertilization and brooding was expected to further characterize these species. F. fragum has rela- tively large (about 5 mm) polyps, yet it produces a small number (only one or two per mesentery) of large eggs which are retained within the parent colony. F. fragum does not appear to follow the generalizations of Rinkevich and Loya (1979a), but provides further support for the suggestion by Szmant-Froelich et 890 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.3, 1985

al. (1980; also Szmant, in press) that relationships between polyp size, egg size and mode of reproduction can be fairly complicated. The earliest embryos were found near the bottom of the polyps' gastrovascular cavity indicating that fertilization took place without the oocytes moving far from their mesenterial position. It is possible that fertilization takes place while the egg is still within the endoderm, with the indentation serving as a site of easy pene- tration for the sperm. This could be a mechanism to prevent the wastage of unfertilized eggs, since it is unlikely that released eggs that were not fertilized could be recovered into the gonad. Mature ova that were not fertilized could then be maintained until the next spawning cycle. Whether self-fertilization can take place is unknown, but it is likely that it can and does. Favia fragum has a combination of life history traits characteristic of "weedy" or r-selected species (Loya, 1976; Stearns, 1976; 1977; Pianka, 1970). Colonies as small as 5 to 10 polyps had gonads. Laboratory growth rates would indicate these colonies to be less than 2 years old; therefore, this species begins reproduction early in life compared to many coral species (Connell, 1973; see review in Fadlallah, 1983; Szmant-Froelich, 1985a). Colonies seldomly get as large as a couple of hundred polyps, and many of the larger colonies have dead spots amidst the colony, suggesting that this species has poor ability to recover from lesions, and a short life span. It is only common in shallow depths, pre- dominantly in back-reef rubble areas, where it can be found growing on loose pieces of rubble as well as on more secure substrate. This is a zone and a micro- habitat that is frequently disturbed by intermediate sized storms that could result in high mortality to F. fragum. Water flow in these zones can be quite rapid, decreasing the chances of sperm from one colony reaching another. Therefore, the ability to self-fertilize could assure individual colonies some chance of passing on their genome to future generations before they are killed (Williams, 1975; Baker, 1959). This trait would also provide a selective advantage to planulae colonizing remote areas, as they could be founders for new populations. On the other hand, F. fragum produces many more sperm each lunar cycle than it needs to fertilize its own ova. This can be interpreted as a concerted effort to achieve some success at outcrossing (Williams, 1975; Smith, 1978). Brooding can also be seen as an adaptive trait for living in a frequently disturbed habitat. Maintenance of a population with high adult mortality requires high recruitment. Brooding the larvae until they are mature enough to settle will increase the chances of recruitment by these larvae into the same population of the parent. Brooding will also prevent much of the high mortality expected during planktonic larval development; high planktonic mortality may be responsible for the generally low recruitment rates reported for many dominant Caribbean coral species (Bak and Engel, 1979; Rylaarsdam, 1983; Sammarco, 1980) now known to be broadcasters with external development (Szmant-Froelich, 1984; Szmant, in press). Some broadcasting corals also have modes of reproduction that enable them to successfully compete for space in the reef-flat environment. The faviid Goniastrea australensis, for example, releases its eggs and spermaries in negatively buoyant, sticky clumps (Kojis and Quinn, 1981), which rapidly sink to the bottom adhering to algae and sediment. The lunar reproductive cycle in Favia fragum was repeated year-round, and seldomly was any individual coral or polyp found totally lacking of reproductive activity. This indicates that individual colonies are reproductively active every reproduction cycle. However, the number of planulae released by a given colony size varied greatly (manuscript in preparation), which may indicate large month SZMANT-FROELICH ET AL.: LUNAR REPRODUCTIVE PATTERNS 891

to month variation in reproductive effort due to physiological factors or success in fertilization, or it could indicate genetically determined differences in individual fecundity. Previous studies oflunar cycles in planulation of various coral species (Harrigan, 1972; Richmond and Jokiel, 1984) have implied that the lunar component is acting to synchronize the release of the planulae. The present study shows that the timing of the ovulation/spawning event seems to be much more closely syn- chronized with the lunar cycle than the timing of planulation. Ovulation occurs over at most a 2- to 3-day period, while planulation occurs over more than a week. Therefore, we suggest that the lunar forces are acting to synchronize the spawning event and that the planulae begin to dribble out about 3 weeks later as they mature. Similar lunar cycles in gametogenesis also may be found to be responsible for lunar planulation cycles in other species when they are examined more closely.

ACKNOWLEDGMENTS

This work was conducted out of the laboratory facilities of the University of Puerto Rico, Department of Marine Science, in La Parguera, P.R. We thank the director, Dr. M. Hernandez-Avila, and his staff for their interest and cooperation. We thank R. Armstrong, P. Hinds, S. Maddox and A. Mendez for donating their time and help with the planulation studies. Funded by NSF OCE-8208560 and OCE- 8315191.

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DATEACCEPTED: May 8, 1985.

ADDRESSES:(A.S.F.) Rosenstiel School of Marine and AtmospheriC Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149; (M.R.) Dept. of Oceanography, Florida State University, Tallahassee, Florida 32306; (L.R.) Dept. of Marine Science, University of Puerto Rico, Mayaguez, Puerto Rico 00708.