<I>Goniastrea Australensis

BULLETIN OF MARINE SCIENCE. 31(3): 558-573, 1981

ASPECTS OF SEXUAL REPRODUCTION AND LARVAL DEVELOPMENT IN THE SHALLOW WATER HERMATYPIC CORAL, GONIASTREA A USTRALENSIS (EDWARDS AND HAIME, 1857)

Barbara L. Kojis and Norman J. Quinn

ABSTRACT Sexual reproduction and larval development in Goniastrea australensis. a shallow water hermatypic coral. were studied from September 1977 to November 1980 on Heron Island reef. Australia. G. australensis is a simultaneous hermaphrodite with ovary and testis intermingled on the same mesentery. Gonad development occurred synchronously within and between colonies. An annual spring spawning season of approximately 2 days was observed. Gametes were released between 1600-1800 h on neap low tides between the full and last quarter moon phases. Fertilization is probably external; eggs from a single polyp were released in clumps held together by mucus and sperm were freely released. Egg clumps were negatively buoyant and sticky, adhering to objects when contact was made. Sperm and eggs were usually released simultaneously from the same polyp. Laboratory experiments indicated that self-fertilization was possible with apparently normal larval development and settlement. In aquaria ciliated larvae developed in approximately 2 days and settlement commenced 17 days after spawning. Reproduction began in colonies with an arithmetic mean radius of !.5-2.0 cm. aged 4+ years. While G. aU.I'tralen.l'i.\· did not planulate, the mode and timing of spawning and larval development substantiated Stimson's (1978) hypothesis that the mode of reproduction in hermatypic corals may be related to habitat. but not his prediction that corals characteristic of the reef flat would begin to sexually reproduce at an early age and planulate.

It has been assumed from studies of sexual reproduction in hermatypic corals that they are viviparous and release planulae (Hyman, 1940; Wells, 1954). How- ever, it has been noted that the release of planulae has not been observed in most species of coral, including species in which gonads were present at some time during the studies (Connell, 1973; Stimson, 1978). The most comprehensive report of sexual reproduction in a non-planulating hermatypic coral was the study of Favia pallida (Marshall and Stephenson, 1933) (nomenclature of Faviidae is in accordance with Veron and Pichon, 1976). The presence of gonads in November and absence in December 1928 indicated a relatively brief spawning period, contrasting with the long, often year-round, period of larval release found in known planulating species, and suggested that gamete release and external fertilization may have occurred. Stimson (1978) synthesized information from his own and previous studies on the presence or absence of planula release and habitat distribution of corals and compared reproduction among corals in shallow and deep water. He hypothesized that the mode of reproduction in hermatypic corals is related to habitat and predicted that corals characteristic of the reef flat would begin to sexually reproduce at an early age and characteristically planulate while deep water corals would have alternate modes of reproduction, probably seasonal gamete release. The sexual reproduction, larval development, distribution and abundance of Goniastrea australensis were studied on Heron Island, Australia, to augment the meager data on the life history of hermatypic corals and to test Stimson's hypothesis. G. australensis (Fig. 1) is a massive hermatypic coral widely distributed in the Western Pacific (Veron, 1974; Veron et al., 1977). It has been recorded as 558 KOJIS AND QUINN: SEXUAL REPRODUCTION IN GONIASTREA 559

Figure I. Reef flat colony of Gon;(lstre(l (lustra/ens;s on Heron Island reef. present in a variety of habitats from the reef flat to the deeper water of the reef slope (Veron et a\., 1977). On Heron and Wistari Reefs of the Capricorn Group, Great Barrier Reef (23°27'S, 1510155'E), G. australensis is largely restricted to major shallow water habitats: lagoon, inner and outer reef flat and crest. It is rarely found on the reef slope and then only in water less than 5 m deep.

MATERIALS AND METHODS Gonads

Reproduction was studied from September 1977 to November 1980 on the reef flat at Heron Island. Ten colonies (> 15 cm diameter) at each of three different sites (total 30 colonies) were individually tagged on the inner reef flat (Fig. 2). Sites were more than 200 m apart to allow determination of variation in the timing and mode of reproduction within the same general habitat. In addition, large untagged colonies from the outer reef flat, crest and lagoon were sampled to assess variation in the mode and timing of reproduction with habitat. Colonies were sampled monthly between September ]977 and November 1978 by removing samples of approximately 5 to 20 polyps with a hammer and chisel. Samples were fixed in 10% sea water formalin in the field and 24 h later transferred to a fresh solution of 10% formalin for storage. Preserved whole samples were decalcified in Gooding and Stewart's solution and initially treated as follows: (I) single polyps were embedded in "Tissue Prep," sectioned at a nominal thickness of 8 J.tm, stained either with Mayer's hematoxylin and eosin or Heidenhain's hematoxylin, and examined for the presence of gonads; (2) other polyps from the same samples were then dissected and observed using a binocular dissecting microscope. It was found that eggs (2-530 J.tm diameter) and sperm clusters could be seen in both calcified and decalcified polyps if the mesenteries were removed and gently squashed on a slide. Eggs and testes nearing maturity were visible in the field with the naked eye when the mesenteries were exposed. Five entire colonies with ripe gonads were repeatedly split and examined to determine whether gonad development was synchronized throughout a colony.

Spawning

Additional colonies from the reef flat were maintained in aquaria with unfiltered, running sea water and plankton netting filtering the run-off from the outlets. Colonies on the reef flat were periodically sampled to determine if they spawned at the same time. The convention of numbering days according to the lunar cycle has been adopted for comparative purposes (Atoda, 1947a; Stimson, 1978), i.e. new moon is lunar day I; first quarter, day 8; full moon, day 15: last quarter, day 22. 560 BULLETIN OF MARINE SCIENCE, VOL. 31, NO.3, \98\

--- REEF CREST./

---'"' ..•• -- ... t N

500m

IlIIIIJ Beachrock

Figure 2. Map of sample and transect sites on Heron Island reef.

Larval Settlement and Development

To estimate the approximate time from spawning to development of mobile, ciliated larvae, all colonies were removed from aquaria the morning following spawning, leaving the spawn in the aquaria, In 1978, ciliated larvae were transferred to and maintained in 2-4 I clean plastic aquaria containing glass slides and pieces of dried coral rubble. Aquaria were ventilated to provide air and increase water movement; the latter may enhance larval settlement (Harrigan, 1972). As larvae adhered to the bottom and sides of aquaria, unfiltered sea water was changed twice a week by siphoning. Plastic film was placed over the tops of aquaria to reduce evaporation and keep the containers clean. In 1979, another laboratory trial was made to determine the interval between spawning and settlement and whether normal larvae developed from self-fertilized eggs. Fifty to 200 larvae from aquaria with single colonies (self-fertilized) and two or more colonies (possibly cross-fertilized) were held in covered 2-1large-mouth jars and provided with air for short intervals. Prior to placing larvae inside, aquaria were conditioned in sea water for several days. Once larvae had settled and metamorphosed, the polyps were fed by running unfiltered sea water into aquaria for several hours daily. The aquaria with polyps were cleaned periodically by removing algae and sediment with the fingertips. To compare rates of development, larvae were collected from the substrate surrounding colonies known to have spawned in the field and in aquaria respectively on the same day and were observed, using a dissecting microscope 16 and 40 h after spawning. Samples of larvae were collected, fixed in 3-4% gluteraldehyde in phosphate buffer or filtered sea water, stored in 0.1 M (pH 7.2) phosphate buffer and embedded in Spurr's medium. Semi-thin sections (3-5 ILm) were cut with an ultra-microtome and stained with 0.3% toluidine blue, a metachromatic stain which stains mucin an intense pink (Humason, 1972).

Colony Size and Reproduction

To determine the approximate size at the onset of reproduction, 101 colonies were measured and sampled. The arithmetic mean radius (x) of colonies in situ was found by measuring the height KOJIS AND QUINN: SEXUAL REPRODUCTION IN GONIASTREA 561

Table I. The arithmetic mean radius (x), standard deviation (SO), and coefficient of variation (CV%) for repeated size samples of 6 colonies of GOlliaslrea auslralellsis

Colonies 6 x (cm) \.89 3.67 5.63 6.27 6.56 7.56 SO 0.07 0.15 0.29 0.]0 0.21 0.11 CV% 3.7 4.] 5.2 \.6 3.2 1.5

(distance from the point of attachment to the tip of the colony), length (greatest diameter at right angles to the height) and width (greatest diameter at right angles to both the height and length). Wooden calipers and ruler were used to measure coral colonies. The calipers prevented damage to coral skeletal projections. Hughes and Jackson (1980) found that partial colony mortality distorted the linear relationship between size and age among reef corals. Partial colony death commonly occurred in G. auslralellsis (personal observation). Thus the arithmetic mean radius (x) was used in preference to the geometric mean radius (Gm) (Loya, 1976b) because the Gm decreases in relation to X as differences in I, wand h measurements increase. While we used x to consider the effect of age, present data indicate only the effect of size on reproduction, irrespective of age, and do not indicate whether age will induce the onset of reproduction or increase fecundity at a smaller size than would occur if growth were not impaired. Six ill silU colonies were consecutively measured eight times by the same person to determine the error inherent in the size measurements. The colonies were measured four times on one day and four more times the next day. The mean error at the 95% confidence leve] was ±0.3 cm (Table I). No significant difference between the variance of the measurements was observed (F Test; P > 0.05). The mean coefficient of variation was 3.1% with measurements of large colonies being as variable as small colonies. Variation in colony measurements was probably associated with the errors in measuring irregularly shaped colonies. Each measured colony was sampled for gonads shortly before spawning. When gonads were abundant, samples were examined in the field; when there were few or no gonads, samples were examined using a dissecting microscope. Each sample was assigned a gonad index value based on the criteria in Table 2.

Distribution, Abundance and Size

Five transects were made perpendicular to the beach, extending from the beach rock, across the reef flat to the inner edge of the crest (Fig. 2). All coral colonies ]0 cm either side of the transect were identified to species or genus and the distance each colony paralleled the line was measured. A 20 cm wide transect was used to reduce the effect of patchiness on measurements of distribution and abundance. Additionally, the length, width and height of all colonies of G. ausrralellsis in Transect 2 were measured.

Table 2. Female and male gonad abundance values for GOlliaslrea auslralellsis

Gonnd Female Gonads: Male Gonads: Abundance Average No. of A verage Size of Values Eggs Mesentery 1 Testis Mesentery"-'

o Non-reproductive Non-reproductive 0.5

Figure 3. Polyps of Goniastrea austra/ensis split through the center exposing oocytes and sperm clusters: 0, oocytes; sc, sperm clusters.

RESULTS Gonads G. australensis is a simultaneous hermaphrodite with ovary and testis mter- mingled in the same mesentery (=gonad) (Figs. 3 and 4) (Favia pallida; Marshall and Stephenson, 1933). Gametogenesis occurred over approximately 9 months of the year. In most colonies oocytes were first observed in March, except in one instance when they were present in a sample collected in the beginning of Feb- ruary, Oocytes did not begin developing in all mesenteries of a colony concur- rently, although nearly all mesenteries of sexually mature colonies contained ova shortly before spawning. As vitellogenesis proceeded, the eggs changed in color from white to brown, The mean diameter of 20 eggs measured in 1978 immediatel y

Figure 4. Cross section through the mesenteries of a polyp of GOIl;astrea australells;s showing male and female gonads approximately 2 weeks before spawning: m, mesentery; n, nucleolus; nu, nucleus; 0, oocytes; sc, sperm clusters. Kons AND QUINN: SEXUAL REPRODUCTION IN GONIASTREA 563

Table 3. Tide times' for Heron Island during the spawning period of Goniaslrea auslraJensis in 1978, 1979 and 1980

1978 1979' 1980

Moon's Time of Spawn- Moon's Time of Spawn- Moon's Time of Sp.nvn- Age2 Date Low Tide ing Age Date Low Tide ing Age Dale Low Tide iog

15 16 Nov. 15.11 NA 15 5 Nov. 15.03 15 24 Oct. 14.33 16 17 Nov. 15.43 NA 16 6 Nov. 15.24 NA 16 25 Oct. 15.18 17 18 Nov. 16.15 A 17 7 Nov. 16.24 NA 17 26 Oct. 16.05 18 19 Nov. 16.52 AF 18 8 Nov. 17.07 NA 18 27 Oct. 16.54 t 19 20 Nov. 17.37 AF 19 9 Nov. 18.00 A 19 28 Oct. 17.50 AF 20 21 Nov. 18.43 A 20 10 Nov. 19.09 AR 20 29 Oct. 19.03 NA 21 22 Nov. 19.58 A 21 11 Nov. 20.30 A 21 30 Oct. 20.30 NA 22 23 Nov. 21.05 A 22 12 Nov. 21.35 A 22 31 Oct. 21.45 NA 23 24 Nov. 21.58 A 23 13 Nov. 22.24 A 23 I Nov. 22.39 NA

A. spawning observed in aquaria; F. spawning observed in the field: R, remnants of spawning observed in the field; NA, colonies in aquaria did not spawn. I Department of Harbours and Marine. Queensland, Australia, 1978, 1979, 1980. , Dala are reported according 10 the lunar calendar used by Aloda (1947) . • Rough seas and high winds prevented spawning observations on the reef flat. t Field samples indicated that some colonies spawned on this date.

after release was 510 JLm (450-530 JLm). Testes were not present until late Sep- tember/early October. Five colonies examined for intra-colony synchrony in November 1978 had ripe gonads in approximately the same abundance in nearly all polyps, including those at the edge of the colonies. Gonads were only absent in polyps bordering regions recently damaged or severely infected by algae. Progressive gonad development synchronized in all colonies, was apparent in monthly samples taken throughout one year from individually tagged colonies. All colonies observed, including tagged colonies at all three sites and untagged colonies from the outer reef flat, crest and lagoon, showed synchrony of gonad development.

Spawning G. australensis released ova and sperm in November 1977, 1978, and 1979 and during the end of October 1980. In 1977, samples collected on 6 November had ripe gonads; no gonads were present on 6 December. Spawning was observed in aquaria (1978; 1979; 1980) and in the field (1978; 1980). In all observations gametes were released during the afternoon low tide commencing at approximately 1600 h and continuing until approximately 1800 h EST, with the majority being released between 1600-1700 h (Table 3). In 1978, the bulk of spawning in the field probably occurred between 18-20 November. Spawning in this species was observed in the field at Lord Howe Island at approximately 1630 h during mid-January 1977 (T. Donne and L. Zell, personal communication). Sexually mature colonies spawned annually. In tagged colonies sampled over successive years (N = 10, 1977, 1978, 1979; N = 20, 1977, 1978) gonads were present in all samples at the beginning of November but absent at the end of November/beginning of December. In eggs fixed in formalin immediately after spawning, sectioned and stained, no germinal vesicle was present and cell division had not begun. Thus ova probably developed shortly before spawning and fertilization could have occurred prior to, during or after spawning. No distinct fertilization membrane was seen at any stage. 564 BULLETIN OF MARINE SCIENCE. YOLo 31. NO.3. 1981

Figure 5. GOI1;astrea allstralel1s;s, eggs and sperm being released from polyps: e, eggs; s. sperm.

During a single daily spawning period, ova and sperm may be released simultaneously (Fig. 5) or separately. Field colonies spawned in 1 or 2 days. In contrast, colonies held in aquaria for 3 or more days prior to spawning released gametes for up to 1 week, though not on every day. Additionally, polyps from different sections of the same colony spawned on different days. Lengthy spawning in aquaria may have been an experimentally induced artifact. In the field and in the aquarium, eggs were retained in a mucous matrix on the surface of each polyp (Fig. 5) until the polyp had completed egg release. The egg clumps were sticky and negatively buoyant adhering to the substratum on contact, often adhering to the short strands of filamentous algae surrounding many of the colonies (Fig. 6). Egg color was similar to the sediment trapped between algal strands and to the foraminiferan epifauna. Clumps free in the water sank slowly and in still water rested on the sand surrounding spawning colonies (Fig. 7). Caught in currents, eggs were carried until they came in contact with the substratum and adhered. Light microscope observations of live sperm indicated that sperm had a single, motile flagellum and triangular head, and were released unconstrained instead of in discrete packets as occurs in some alcyonarians (Gohar, 1940).

Larval Development and Settlement In 1979, eggs from all aquaria developed into mobile, ciliated larvae in approximately 2 days irrespective of whether the eggs were cross-fertilized or self-fertilized. Water temperature was measured and compared in the aquaria and on the reef flat on 2 days and no significant difference was found (daily range 23.5- 27.soC). Larval development was similar in aquaria and on the reef flat. Larval development was similar to the anemone Adamsia palliata (Gemmill, 1920). Developing larvae of G. australensis became ciliated and mobile at the KOllS AND QUINN: SEXUAL REPRODUCfION IN GONJASTREA 565

Figure 6. Colony of GOl/ias/rea alls/ralel/sis on the reef flat surrounded by recently spawned eggs adhering to the substratum: e, eggs. gastrula stage. Larvae sampled 65 h after spawning had small scattered mucous glands in the zone of future ectoderm. By day 7, larvae had a well developed ectodermal layer separated from the embryonic endoderm by a layer of mesoglea, a stomodeum and mesenterial filaments. Mucous glands were large and abundant in the ectoderm, especially in the thickened aboral region. Larvae sampled on days 12, 15, 17 and 22 showed less rapid, but continuing, development. Zooxan- thellae were not observed in eggs or larvae. In 1978, larvae were held in aquaria for 23 days, but none settled. In 1979,

Figure 7. Negatively buoyant egg clumps resting on the sand: ec, egg clumps. 566 BULLETIN OF MARINE SCIENCE, VOL. 31, NO.3, 1981

Figure 8. Developing larvae of Goniasrrea ausrralellsis adhering to algae and sand: dl, developing larvae.

three larvae which had developed from self-fertilized eggs settled ]7 days after spawning and 3 days later 20 larvae from potentially cross-fertilized eggs settled. Others settled on subsequent days. When the experiments were terminated 47 days after the initial spawning, most juvenile corals and a number of unmeta- morpho sed larvae were alive. No budding had occurred. In the laboratory experiment to test how long larvae remained benthic, colonies spawned and egg clumps attached to filamentous algae on the bricks or settled on the sand. Most developing larvae remained benthic for 5 days after spawning (Fig. 8). On the morning of day 6, larvae were seen swimming and from then on the number of benthic larvae decreased markedly. It is not known if the larvae were lost at the outlet, died or settled. Colony Size and Reproduction This species is a protandrous hermaphrodite. Colonies smaller than 2.5 cm were usually male (Fig. 9), or if hermaphroditic, eggs were only sporadically present intermingled with sperm clusters. As the size of colonies increased, the percentage of colonies with gonads increased (Table 4) as did the size of testes and the number of eggs per gonad.

Distribution, Abundance and Size The transect data indicated that G. australensis is common and widely distributed on the reef flat of Heron Island (Table 5), where it is the fifth most abundant species and comprises 4.4% of the live coral cover. Similarly, Grassle (] 973) found G. australensis ranked sixth in abundance on the reef flat, but was not common on either the crest or slope. Distinguishable colonies ranged from 0.5 cm to small microatolls approximately 30 cm greatest radius. Colonies measured in Transect 2 ranged from 0.5-13,9 cm x with a mean size of 4.5 cm x (N = 45). (Table 6). KOllS AND QUINN: SEXUAL REPRODUCTION IN GONIASTREA 567

-H.ronlllonCl

I. - -Lor4 HOWlIllQnd.

M M

Ar.tnmellC ~can r,jC:llS lcrr> TIME (months)

Figure 9. Plot of gonad abundance against the arithmetic mean radius of Goniastrea austra/ensis: (x), colonies with testes only: (e) hermaphroditic colonies. Figure 10. Oceanic surface temperatures near Heron Island (averaged over 12 years, 1966-1977) and Lord Howe Island (averaged over 2 years, 1977-1978) (CSIRO, Cronulla, Australia) and spawning times for Gonillstre(l (lustra/ensis (..••).

DISCUSSION This is the first report of a study of sexual reproduction, larval development and life history strategy of a hermatypic coral that releases gametes. Gamete release may be widespread among the Scleractinia. There have recently been reports of gamete release and external development of larvae in two species of ahermatypic coral from temperate waters, Astrangia danae (Szmant-Froelich et aI., 1980)and Paracyathus stearnsii (Fadlallah and Pearse, MS1). Gamete release, simultaneous hermaphroditism and annual protogynous gonad development may be common amongst the members of the Faviidae. Eggs were released in aquaria colonies of Favia favus (Shlesinger in Rinkevich and Loya, 1979a). At Heron Island, Kojis and Quinn (1980) observed a brief annual spawning season in Fav- ites abdita and Leptoria phrygia. Simultaneous hermaphroditism and protogynous, annual gonad development have been rep'orted in Favia pallida at Low Isles, Great Barrier Reef (Marshall and Stephenson, 1933), Favia fragum (Duerden, 1902) and Favia favus (Rinkevich and Loya, 1979a). Associated with simultaneous hermaphroditism is the possibility of self-fertilization. G. australensis may commonly self-fertilize, since ova and sperm are released simultaneously. Self-fertilization in sessile animals, such as corals, ensures against reproductive wastage, since an "individual will always be certain of suc- cessful contact with a reproductively capable individual, namely itself' (Tomlin- son, 1966), regardless of population density. Thus, it may be especially im- portant in the colonization of new habitats and the recolonization of old habitats after a catastrophe which eliminates all but a few widely spaced individuals. A strong indicator of reproductive mode in hermatypic corals may be the number of eggs per gonad (Rinkevich and Loya, 1979a). Faviid species that release gametes are strongly fecund having more than seven eggs per gonad shortly before spawning. G. australensis had a maximum of 13 eggs per gonad. In contrast, Stylophora pistil/ata, a planulating species had only one or, rarely, two mature eggs per gonad (Rinkevich and Loya, 1979a).

1 Fadlallah, Y., and J. S. Pearse, MS. Sexual reproduction in solitary corats: synChronous gametogenesis and broadcast spawning in Puracyarhus sreurnsii. 568 BULLETIN OF MARINE SCIENCE, VOL. 31, NO, 3. 1981

Table 4, Percentage of sexually reproducing colonies in similar size classes for Goniastrea austra- /ensis and Stylophora pistil/ara (Rinkevich and Loya, 1979b) (x = arithmetic mean radius, Om = geometric mean radius)

Goniastrea australensis Stylophora pi.\,tillara

Size Classes % of Colonies Size Classes % of Colonies K (em) N Reproductive Gm(em) N Reproductive

0.51-1.00 19 0 1.01-1.50 4 0 1.01-1.50 33 3.0 1.51-2.00 15 33.3 1.51-2.00 25 32.2 2.01-2.50 10 40.0 2,01-2.50 22 54.2 2.51-3.00 14 35,7 3.01-3.50 15 60.0 2.51-4.00 13 69.2 3.51-4.00 7 100,0 4.01-4,50 9 77.8 4.01-4.50 10 90.0 4.51-6.00 9 88.9 4,51-6.00 36 86,1 6.01-20.00 18 100.0 6.01-8,50 14 92.9

It has been suggested that the failure to detect planulation in corals may be because (1) colonies of some species may not spawn every year (Connell, 1973), (2) death may follow reproduction (Marshall and Stephenson, 1933) and (3) colonies studied were sexually immature (Stimson, 1978). Data from this study dis- count all of the above. Colonies of G. australensis have been shown to spawn annually, 3 years in succession, and thus colony death is not related to reproduction. Also, while planulating species, e.g. Stylophora pistil/ata, become sexually reproductive at an earlier age than G. australensis, the colony sizes of both species are similar. The size at the onset of reproduction is small (x = 1.51-2.00 cm) and if this is true for other species, the possibility that all colonies inspected were juveniles is unlikely. Indeed, failure to detect planulation may be because (1) many corals do not planulate, they release gametes, and (2) gamete release is brief, occurring annually. Korringa (1947) listed three factors which determine the time of reproduction in marine invertebrates: annual temperature variation, lunar tidal cycle or vari- ations in nocturnal illumination, and the day-night (light/dark) cycle. The timing of spawning in G. australensis appears to be influenced by all three factors. Annual periodicity of spawning has been correlated with "a definite temperature, which is a physiological constant for the species, or ... a definite temperature change, at either the maximum or minimum temperature of the locality" (Orton, 1920). Gonad maturation in G. australensis may be influenced by the rapid spring temperature rise beginning in September, with final ripening occurring only when a minimum temperature of approximately 23-24°C is reached (Fig. 10). At Lord Howe Island the rapid spring temperature rise begins in November

Table 5. Relative abundance of Goniastrea austra/ell.I'is in transects 1-5 on Heron Island reef flat

Transect No. % Live Coral Cover

I 4.1 2 4.9 3 3.1 4 8.2 5 3.7 KOJIS AND QUINN: SEXUAL REPRODUCTION IN GONIASTREA 569

Table 6. Size distribution of Goniastrea australellSis on Heron Island reef flat along Transect 2 (x = arithmetic mean radius)

Size Classes

il (em) N % of TOlal N

0-1.00 2 4.4 1.01-2.00 6 13.3 2.01-3.00 9 20.0 3.01-4.00 9 20.0 4.01-5.00 4 8.9 5.01-6.00 5 11.1 6.01-10.00 5 11.1 10.01-14.00 5 11.1 and 23-24°C is not reached until January. This could explain why spawning at Lord Howe Island is 2 months later than at Heron Island. Timing of spawning is associated with the lunar cycle in a numb.er of invertebrate species, e.g., the echinoid Centrechinus (Diadema) setosus (Fox, 1924)and the polychaete Platynereis dumerilii (Hauenshild, 1955; 1956). Timing of spawning is also correlated with the lunar cycle in a number of planulating coral species (Stimson, 1978). Colonies of G. australensis spawned for 3 consecutive years between the full and last quarter moon phases at the end of October or in No- vember on the afternoon low tides. The lunar cycle appears to influence the particular time of the month, while the day-night cycle may influence the time of day or on which low tide in the semi-die I cycle spawning occurs (Table 7). Time to settlement of larvae in hermatypic corals is probably influenced by three factors: (1) presence of an appropriate substrate, (2) suitable environmental conditions (Harrigan, 1972; Chia and Bickell, 1977) and (3) the time from release of planulae or gametes to the development of mature larvae (i.e., ready to settle) (Rinkevich and Loya, 1979a). Settling and metamorphosis in many planulating hermatypic corals occurred only when larvae were at an advanced developmental stage, i.e., three to six complete mesenteries (e.g., Siderastrea radians, IsophyLlia dipsacea, Duerden, 1902; Fungia actiniformis var. palawensis, Abe, 1937; Po- cillopora damicornis, Atoda, 1947a; and Acropora bruggemanni, Atoda, 1951a). The larvae of Stylophora pistil/ata were released with or without mesenteries, but settled only at the HaIcampoides stage (Rinkevich and Loya, 1979a). Some larvae of S. pistil/ata were ready to settle immediately upon release, while settlement in others was delayed until development was completed. Few of the species studied had larvae able to settle at an early developmental stage, e.g., Galaxea aspera had no mesenteries (Atoda, 1951b) and Faviafragum had only one pair of complete mesenteries before attachment (Duerden, 1902). Although the stage of larval development at which settlement occurs is not known in G. australensis, the relatively lengthy period from larval release to settlement as compared with many larvae releasing species may be attributed in part to time to larval maturity. It may be that the minimum time to settlement of 17 days in aquaria is comparable with that occurring on the reef flat since Abe (1937) found in Palau that Goniastrea aspera settled in aquaria between 16 and 23 days after release. In G. australensis gonads were present in most polyps irrespective of their position in the colony. This contrasts with the distribution of gonads in branching species. In Pocil/opora damicornis (Harrigan, 1972) and Stylophora pistil/ata 570 BULLETIN OF MARINE SCIENCE, VOL. 31, NO.3, 1981

Table 7. Reproductive periods for eight planulating species of hermatypic coral

Length of A nnua) Larval Species Author Location Lat. Release Period

Cyphastrea ocel/ina Stimson, 1978 Hawaii All year Favia fragum Duerden, 1902 Caribbean 22°N All year Fungia actiniformis Abe, 1937 Palau 200N 8 months Ga/axea aspera Atoda, 1951b Palau 8°N All year Manicina areo/ata Duerden, 1902 Caribbean 8°N All year Pocil/opora damicornis Atoda, 1947b Palau 200N All year caespitosa Pocil/opora damicornis Marshall and Stephenson, 1933 Low Isles, Great 8°N All year Barrier Reef 17°S Pocil/opora damicornis Harrigan, 1972 Hawaii 22°N All year Seriatopora hystix Atoda, 1951c Palau 8°N All year Stylophora pistil/ata Atoda, 1947b Palau 8°N All year Stylophora pistil/ata Rinkevich and Loya, 1979b Eilat, Red Sea 29°N 8 months

(Rinkevich and Loya, ]979b) gonads are more plentiful in the mid-section of the branch, while in Acropora palifera they may be absent up to 1.5 cm from a growing tip (personal observation). This difference in gonad distribution may be related to the uniform growth of massive species versus the localized growth in branching species (Wood-Jones, 19]0; Buddemeier and Kinzie, 1976). For ex- ample, skeletal density bands of the massive coral Porites lobata indicated that growth occurred over most of the corallum (Isedale, 1977). Since there are no prescribed regions in which growth is concentrated (cf. branching species), energy in all polyps of reproductively mature colonies is directed both to gonad development and growth. Decrease in growth rate has been correlated with increase in size in a number of corals and it is generally accepted that calcification in corals is most rapid in younger, smaller, colonies (Connell, 1973; Buddemeier and Kinzie, 1976). In Favia pallida (Marshall and Stephenson, 1933), Stylophora pistillllta (Rinkevich and Loya, 1979b) and G. australensis, larger colonies were more fecund than smaller colonies. It may be that decreasing growth rate is caused by the onset of sexual reproduction and the increasing fecundity associated with increasing size. A colony initially directs all its energy toward maintenance and growth until it attains a size where the threat of death owing to predation, competition and overgrowth diminishes and it can apportion some of its energy to reproduction. As a colony continues to increase in size, it can channel a larger proportion of energy to reproduction. When determining the annual fecundity of a coral, a number of factors must be taken into consideration. First, polyp fecundity (i.e., number of eggs per gonad) may increase as the colony grows larger, Second, if fecundity varies among polyps of a colony, the ratio of reproductive to non-reproductive parts of a colony will need to be determined as well as whether this ratio varies with size/age. Third, while planulating species release larvae for long periods (Table 7), gamete releasing faviids have a brief annual spawning period, Individual colonies of planulating species have not been followed through a reproductive season to determine how many larvae may be released by a polyp, and thus present knowledge of fecundity is confined to the number of larvae found in a polyp at anyone time. The simultaneous presence of eggs, sperm and larvae in polyps of Stylophora pistillata (Rinkevich and Loya, 1979a) and Favia fragu1n (Duerden, 1902) indi- KOJIS AND QUINN: SEXUAL REPRODUCTION IN GONIASTREA 571

cates that there may be more than one cycle of larval development and release within a polyp in a year. Stimson (1978) hypothesized that the release of planulae in shallow water corals enables them to retain recruits in fast moving shallow water by allowing rapid settlement. G. australensis is a shallow water reef coral that does not planulate although it exhibits a mode of spawning and larval development that encourages the retention of recruits on the reef flat. Spawning occurs before and during low tide when the current is least and water depth shallow. During low tides, water only just covers the coral heads ensuring that egg clumps will remain near the substrate and not be carried by currents above the coral heads, a possibility during high tide when the reef flat may be covered by 2 m of water. Egg clumps are sticky and negatively buoyant, adhering to the substrate. Thus, developing larvae remain near the parental colony. Ectodermal mucous gland development enables the larvae to adhere readily to surfaces (Chia and Bickell, 1977). The color of developing larvae provides effective camouflage in the benthic habitat and possibly diminishes predation. Stimson (1978) also suggested that corals characteristic of reef flats differ from deeper water corals in simple demographic characters, such as age, at the onset of reproduction. Stylophora pistil/ata, an r strategist (Loya, 1976a), characterizes the reef flat in the Red Sea (Loya, 1972) and appears to be typical of the shallow water corals discussed by Stimson. A comparison of size at first reproduction between S. pistil/ata and G. australensis suggests that while linear size is similar, age differs. S. pistil/ata first reproduces when less than 2 years of age (Rinkevich and Loya, 1979b) while G. australensis, extrapolating from Woodhead's (1971) growth data, does not begin reproducing until 4 to 7 years of age. With increasing linear size, the differences in age between similar sized colonies of these two species become more marked. Species characteristic of reef flats that primarily form new colonies by means of sexual reproduction may have various modes of reproduction that reduce planktonic life to a minimum and retain larvae on the reef flat. Some species, such as Stylophora pistil/ata (Loya, 1976a) and Pocil/opora damicornis (Harri- gan, 1972), planulate and are r strategists. They have a relatively small maximum colony size, early age at the onset of reproduction and possibly large reproductive effort (year-round presence of gonads and/or larvae). Others, such as G. australensis, release gametes and are K strategists. They have a relatively large maximum colony size, delayed age at first reproduction and smaller reproductive effort (i.e., gonads present only part of the year). Such species may be adapted to the range of environmental conditions occurring on the reef flat over decades, if not centuries. Edmondson (1928) tested a number of Hawaiian reef flat corals for their ability to resist fluctuations in salinity, temperature and exposure and found species of the family Faviidae to be among the most tolerant. These data do not invalidate Stimson's hypothesis that different modes of reproduction are adaptive in different habitats. However, results show that planulation is not the only mechanism that can achieve this end and that demographic characteristics of shallow water corals and thus their position on the rand K continuum may vary.

ACKNOWLEDGMENTS

We thank Drs. R. Endean and C. Plowman of the University of Queensland, Brisbane, Australia; Dr. D. C. Potts of the University of California, Santa Cruz, and Dr. R. Reichelt, Australian Institute of Marine Science, Townsville, Australia, for their critical reading of the manuscript. We would also like to thank Dr. R. Endean for his suggestions regarding experimental design and Mss. V. Harriot, 572 BULLETIN OF MARINE SCIENCE, VOL. 31, NO.3, 1981

L. Keyes, I. Stejskal and many others for their assistance in the field. This study was supported financially by grants from the University of Queensland, The Great Barrier Reef Marine Park Au- thority and the Ecological Society of Australia. The use of the Heron Island Research Station facilities and oceanographic data from CSIRO, Cronulla, Australia, is gratefully acknowledged.

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DATEACCEPTED: March 24, 1981.

ADDRESSES: Zoology Departmenl. University of Queensland, Saint Lucia, Queensland 4067, Aus- tralia; PRESENTADDRESS:(N.J.Q.) Fisheries Department, Papua New Guinea University of Tech- noloK.\'. P.O. Box 793. Lae. Papua New Guinea.