Marine Biology (1998) 132: 691±701 Ó Springer-Verlag 1998

Y. Shlesinger á T. L. Goulet á Y. Loya Reproductive patterns of scleractinian in the northern Red Sea

Received: 2 February 1993 / Accepted: 9 March 1998

Abstract The majority of published accounts on ctinian with the data available on scleractinian scleractinian reproduction are from the tropical corals from other geographical regions. Paci®c and Caribbean, with very little information known about Red Sea species. This report examines variation in reproductive mode in 24 species of her- Introduction matypic corals (belonging to seven families) in the Gulf of Eilat, Red Sea. Eighteen species are hermaphroditic Knowledge of scleractinian coral reproduction has broadcasters, two are hermaphroditic brooders and progressively grown in the past 15 years. As Richmond three are gonochoric broadcasters. In the Pocillopor- and Hunter stated in a 1990 review, reproductive data idae, the gonads project into the body cavity, while in were available for 40% of known species from the the other six families the gonads reside inside the me- tropical Paci®c, 30% of Caribbean coral species and senteries. The number of gonads per in broad- only 6% of Red Sea species. Since the extensive reviews casting species follows family or genus lines. Fecundity by Richmond and Hunter (1990) and Harrison and (eggs per polyp) increases with polyp size. Brooding Wallace (1990), additional studies have been published species usually exhibit one or two gonads per polyp and on reproduction in corals from the tropical Paci®c each gonad contains only one to three oocytes. Oocyte (Glynn et al. 1991, 1994, 1996; Bermas et al. 1992; Dai et size varies widely and does not relate to mode of re- al. 1992; Shimoike et al. 1992; Stanton 1992; Stobart et production. The largest oocytes (diameter ˆ 450 lm) al. 1992; Ward 1992, 1995a, b; Tanner 1996; Sakai occur in the brooding coral Alveopora daedalea and in 1997), the Caribbean (Szmant 1991; Johnson 1992; Van broadcasting species of the genus (diame- Veghel 1993, 1994; Van Veghel and Bak 1994; Van Ve- ter ˆ 420 lm). Gonad morphology and gonochorism ghel and Kahmann 1994; Knowlton et al. 1997) and the versus hermaphroditism appear to be constrained phy- Gulf of Mexico (Gittings et al. 1992). However, infor- logenetically at the family or genus level. Lastly, this mation on the reproductive biology of corals from the report compares the data presented for Red Sea sclera- Red Sea is very limited (Loya 1976; Rinkevich and Loya 1979a, b; Shlesinger and Loya 1985, 1991; Kramarsky- Winter and Loya 1996; Kramarsky-Winter et al. 1997) and still lagging. Data on scleractinian coral reproductive modes such as variation in sexuality (gonochorism versus hermaph- Communicated by O. Kinne, Oldendorf/Luhe roditism), seasonality, and periodicity among coral Y. Shlesinger species have been used in an attempt to categorize the Environmental Department Municipality of Eilat, reproductive strategies of scleractinian corals. Several P.O. Box14, Eilat 88100, Israel hypotheses have been proposed. One hypothesis states T.L. Goulet that the reproductive variability is due to energetic Department of Biological Sciences, limitation (Kojis 1986; Ward 1995a). As reproductive State University of New York at Bu€alo, activity involves energetic expenditure, under certain Bu€alo, New York 14260, USA energetic conditions di€erent reproductive pathways Y. Loya (&) may exist. Fecundity and the ratio of male to female Department of Zoology, The George S. Wise Faculty of Life Sciences and the Porter Super-Center colonies may be regulated by a variety of internal and for Ecological and Environmental Studies, external processes (Rinkevich and Loya 1987; Ward Tel Aviv University, Ramat Aviv 69978, Israel 1995a). 692

Reproductive mode (brooding versus broadcasting) to obtain extensive comparative information, each species was may be determined by the coral's morphological traits sampled during several reproductive seasons. Data collected during the ®rst 4 years of the study (1980 to such as colony size, polyp size, oocyte diameter and 1984) were used to determine the spawning and gonad development gonad location (Rinkevich and Loya 1979a; Szmant periods of the coral species. Six large colonies (>15 cm diameter) 1986; Van Veghel and Kahmann 1994). Van Moorsel from each species were selected randomly on the reef and sampled (1983) hypothesized that reproductive requirements may monthly for 2 to 4 consecutive years. For branching corals, 5-cm modify skeletal characteristics, polyp size and number of long branches were collected. For massive corals, live tissue and skeleton approximately 10 cm2 in surface area were removed with a gonads. However, existing data show wide morpholog- hammer and chisel. Freshly collected samples were examined under ical variation and no linkage to reproductive mode a Nikon dissecting microscope to determine oocyte number, color (Kojis and Quinn 1982b; Harriott 1983a; Fadlallah and size in each gonad. These samples were then ®xed for 24 h in 1985; Wallace 1985; Harrison and Wallace 1990). 4% formaldehyde solution in sea water, and preserved in 70% alcohol. Corals were decalci®ed using formic acid/sodium citrate Reproductive modes may be dictated by phylogenetic solution (after Rinkevich and Loya 1979a). Decalci®ed tissue was constraints. Harrison (1985) summarized the available embedded in para®lm, cut into serial sections (6 lm thick), and data on reproductive features of coral species at various stained with Dela®eld hematoxylin and eosin. locations in the tropics, and noted the consistency of In addition to the monthly monitoring, in order to detect the process of gamete spawning or planula shedding, we conducted sexuality (gonochorism versus hermaphroditism), gonad daily in situ monitoring of ten tagged colonies of each species arrangement and anatomy within taxonomic groups. during their respective breeding seasons. Observations on released His thesis of shared traits due to shared ancestry has gonad products followed Shlesinger and Loya (1985). Based on the been partially supported by detailed descriptions of the data obtained in the ®rst 4 years, during the following 6 years, 15 scleractinian family (Wallace 1985). colonies of each species were sampled and examined only prior to their respective spawning periods. In order to quantify data on Reproductive mode may be externally controlled by gonad parameters, polyp and oocyte sizes were assessed from his- environmental factors. Stimson (1978) suggested that tological slides of decalci®ed polyps using a micrometer objective brooding or broadcasting patterns are determined by lens. Species were divided into three size classes: those with small depth below sea surface. Deep sea species are predomi- polyps (0.7 to 3.0 mm in diameter) in which a histological section contained 10 to 20 polyps each; species with medium-size polyps nantly broadcasters, while species in shallow water (3.0 to 6.0 mm in diameter) whose sections contained two to four brood planulae. Further research, however, has revealed polyps; and those with large polyps (6.0 to 20.0 mm in diameter) that both brooding and broadcasting species inhabit consisting of only one polyp per sample. We examined one section shallow water (Kojis and Quinn 1982a; Shlesinger and per colony for small- and medium-polyped species, and three or four sections per colony for large-polyped species. Maximum oo- Loya 1985; Harrison and Wallace 1990). Reproductive cyte diameter was obtained by measuring the largest oocyte ob- di€erences among species may result from habitat con- served in the histological sections. We counted the number of ditions in di€erent zoogeographic regions (Szmant 1986; gonads per polyp, and oocytes per gonad in both live tissue prep- Van Woesik 1995; Tanner 1996). arations and in serial histological sections. The mean number of Existing data are insucient to strongly support one oocytes per gonad was calculated from serial and cross sections through the entire polyp. In the present paper, the term ``fecundity'' of the above theories over the others. Additional com- refers to the number of oocytes per polyp. parative information on sexuality, fecundity and repro- ductive development are needed in order to determine the factors responsible for the observed reproductive Results patterns of stony corals (Harrison and Wallace 1990). This report summarizes a 10-year study on the re- Patterns of sexual development productive characteristics of 23 Red Sea scleractinian species. The studied species, in addition to Stylophora Most of the coral species studied in the present research pistillata, contribute approximately 70 to 80% of the (20 out of 23) were hermaphroditic (Table 1). In the total living coral cover in the Gulf of Eilat, Red Sea, and three gonochoric corals (Goniopora savignyi, lu- are therefore very important in this ecosystem (Loya tea and Pavona varians), sexuality was generally deter- 1972). Furthermore, the present study adds much needed mined at the colony level. In one sampled colony of data about scleractinian coral reproduction in the Red P. lutea, a few male polyps were observed in a pre- Sea. The results are discussed in light of di€erent repro- dominantly female colony. The main mode of repro- ductive pathways, with special emphasis on the question duction (21 out of 23 species) was broadcasting of of phylogenetic constraints on gonad parameters, and gametes (Table 1). The species caliendrum the relationship between reproductive strategy (brooding and Alveopora daedalea brood and release planulae [in versus broadcasting) and gonad morphology. addition to studied previously by Rinkevich and Loya (1979a, b) and also included in Table 1]. Materials and methods Gonad arrangement and morphology varied accord- ing to family (Table 1). Members of the This study was conducted on fringing reefs in the northern Gulf of exhibited a unique gonad arrangement. The gonads were Eilat, Red Sea (29°30¢N; 35°55¢E). Samples were collected from a found on stalks arising from the column wall in the body 5 km stretch of approximately 10 km south of the city of Eilat. The reproductive ecology of 23 common species of sclera- cavity (Table 1; Fig. 1A). Ova and spermaries co-oc- ctinian corals was examined over 10 years (1980 to 1990). In order curred within the same polyp, but were segregated be- 693

Table 1 Reproductive patterns of 24 scleractinian coral species Family, Sexuality Mode of Gonad Oocyte color during at Eilat, Red Sea (G go- species reproduction arrangement maturation nochoric; H hermaphroditic; Pocilloporidae B broadcasting gametes; P a brooding planulae; C gonads in Stylophora pistillata H P C Brown only body cavity; S gonads in me- Seriatopora caliendrum H P C Brown only senteries) Pocillopora verrucosa H B C White to cream Acroporidae Acropora eurystoma H B S Pink to white Acropora hemprichi H B S Pink to white Acropora humilis H B S Pink to white Acropora hyacinthus H B S Red to pink Acropora scandens H B S Pink to white Acropora variabilis H B S White to pink Astreopora myriophthalma H B S Red to purple Montipora erythraea H B S Brown to cream Faviidae Cyphastrea microphthalma H B S Green to brown favus H B S Green to red pentagona H B S Pink to red retiformis H B S Pink to red Platygyra lamellina H B S Green to red Alveopora daedalea H P S Brown only Goniopora savignyi G B S White to brown Porites lutea G B S Green to lilac Acanthastrea echinata H B S Green to orange lacrymalis H B S Brown to orange hemprichi H B S Orange to pink Oculinidae Galaxea fascicularis H B S White to pink Agariciidae a Results from studies of Pavona varians G B S White to cream Rinkevich and Loya (1979a, b) tween di€erent pairs of mesenteries (Fig. 1B). In the teries, which did not protrude out from the mesentery other six families, gonads were located within the me- wall (Fig. 2E, F). senteries (Table 1). In the Acroporidae, Faviidae, In broadcasting species, oogenesis was accompanied Mussidae and Oculinidae, the gonads ®lled the entire by color change in the developing oocytes. For example, mesenteries. Variation between these families occurred oocytes of Favia favus ®rst appeared green (with oocyte in the degree of segregation of testes and ovaries. Three diameter of 40 to 200 lm), then became greenish-red, levels of segregation were observed. and ®nally dark red (with a diameter of 360 lm) 2 weeks Faviids and the mussid Cynarina lacrymalis dis- prior to spawning. Oocytes of Acropora eurystoma played testes and oocytes intermingled throughout the changed from pink to white, while in Galaxea fascicul- mesentery without a distinct region for each gonad aris the color changed from white to pink (Table 1). (Fig. 1C, D, E). In the mussid Lobophyllia hemprichi, These color changes enabled determination of the mat- male and female gonads were arranged separately uration stage of a coral in situ by examination of female within the same mesentery. In the family Acroporidae, gonad color in gravid colonies. In brooding species, egg male and female gonads were segregated on di€erent color did not change throughout oogenesis, apart from mesenteries in each polyp, and occupied one row in each the progressive increase in the brownish color due to the mesentery. increase in zooxanthella numbers during maturation and In the Poritidae and Agariciidae, gonads created lo- embryogenesis. calized enlargements on only part of each mesentery Broadcasting species had annual gametogenic cycles (Fig. 2A). In the family Poritidae, gonads were arranged lasting approximately 6 to 7 months. The onset of in local enlargements which protruded out, and ap- oogenesis preceded spermatogenesis by 2 to 4 months peared as swellings or bulbs on the mesenteries (Fig. 3). Nevertheless, during the last 2 months of de- (Fig. 2B). These structures occurred in both gonochoric velopment, oocytes and testes matured synchronously and hermaphroditic species, and both male and female within colonies. Monthly changes in oocyte diameter gonads exhibited a similar bulbous appearance (Fig. 2C, conformed to either linear or exponential growth D). In contrast, the gonads of Pavona varians (Agarici- curves (Fig. 4). The linear curves indicate that most idae) appeared as small thickenings within the mesen- oocyte production occurred during the ®rst month of 694

oogenesis. These oocytes then gradually increased in during which all the oocytes are produced with very size until maturation. Linear growth curves were seen little increase in size. These oocytes then undergo a in oocytes of Montipora erythraea, Astreopora rapid acceleration of growth rate. Exponential growth myriophthalma, Favia favus and Galaxea fascicularis.In curves were recorded in oocytes of Acropora eurystoma, contrast, the exponential growth curves represent con- Acropora humilis, Goniastrea retiformis and Platygyra tinuous production of oocytes over the ®rst 3 months, lamellina. 695

Fig. 1 Histological sections of mature gonads of hermatypic corals in The gametogenic cycles in brooding species were the Red Sea. A Female gonad attached on a stalk (arrow)in di€erent from those in broadcasting species in their time Pocillopora verrucosa. B Separated ovaries and testes in the polyp of Pocillopora verrucosa. Intermingled gonads within the mesenteries of scale and degree of synchronization within the colony C Goniastrea retiformis, D Cyphastrea microphthalma and E Cynarina and population. Gonads of the brooders Seriatopora lacrymalis. F Longitudinal arrangement of spermatogonia and caliendrum and Alveopora daedalea matured in 2 to oogonia in the polyp of Acropora eurystoma. G Cross section illustrating spermaries and oocytes in di€erent mesenteries of A. Fig. 2 Anatomy of gonads in some gonochoric species in the Red Sea. eurystoma (Sp spermary; Oc oocyte; N oocyte nucleus; S mesentery) A Cross section of a female polyp of Porites lutea and B magni®cation of b an oocyte in the gonad of Porites lutea. C Ovaries and D spermatogonia of Goniopora savignyi. E Ovaries and F spermatogonia of Pavona varians.(Sp spermary; Oc oocyte; N oocyte nucleus; S mesentery) 696

Fig. 3 Reproductive patterns of 11 broadcasting species of scleractinian corals at Eilat in 1986. The last two species occur commonly at 15 to 30 m depth and are rare in shallow water. The period of gonad development is represented by a solid line with indications of the onset of oogenesis ($) and spermatogenesis (#). Further synchronized development of both gonads is indicated by the line following the $# symbol. Approximate spawning time, determined by disappearance of oocytes in the histological sections, is indicated by the symbol

3 months (Shlesinger and Loya 1985). Synchronization Eilat, polyp diameter was signi®cantly correlated with in the development of male and female gonads occurred the number of oocytes produced per polyp (Kendell's only in polyps which were in a similar reproductive coecient of rank correlation, P < 0.02). Broadcasters phase, in terms of initiating oocytes, maturation before in small-polyped families (Pocilloporidae, Acroporidae, fertilization, and stages during embryogenesis (Shle- Poritidae) produced a fairly low number of eggs per singer and Loya, unpublished data). Colonies of these polyp (20 to 75). In contrast, families with medium-sized brooding species, and even di€erent polyps within a polyps (Faviidae) had moderate egg production (105 to given colony, did not release planulae synchronously. 700 polyp)1), and large-polyped families (Mussidae, Oculinidae) exhibited very high egg production (1000 to 3550 polyp)1, Table 2). No signi®cant correlation was Fecundity versus polyp size found between polyp diameter and oocyte diameter (P > 0.05) or between oocyte diameter and mode of Among broadcasting corals, the number of ovaries per reproduction (P > 0.05). polyp was consistent within the small-polyped families Acroporidae (4 ovaries polyp)1) and Poritidae (12 ova- ries polyp)1). Additionally, the number of oocytes per Discussion and conclusions polyp and per gonad was also similar within these two families. In contrast, the two families with large polyps This study presents long-term (10 years) data on the (Faviidae, Mussidae) exhibited a wider variation in the reproductive characteristics of 24 scleractinian coral above gonad characteristics. The brooding species Sty- species in the Gulf of Eilat, Red Sea. The corals studied lophora pistillata, Seriatopora caliendrum and Alveopora comprise approximately 70 to 80% of the coral cover in daedalea developed only one or two ovaries per polyp, the Gulf of Eilat and therefore play an important role in with one to three oocytes per ovary. Thus, brooders this ecosystem. By monitoring all coral species at the produce only one to six eggs per polyp, while broad- same site, we were able to determine whether the coral casters may release tens to thousands of eggs per polyp reproductive characteristics exhibited phylogenetic, (Table 2). geographic patterns, or both. The present work provides At the family level, the number of ovaries and oocytes important information concerning approximate spawn- per polyp in corals in the Red Sea is similar to elsewhere ing times of 11 coral species (Fig. 3) in addition to the 12 (Table 3). A constant number of ovaries per broad- species previously reported by Shlesinger and Loya casting polyp is found in two additional small-polyped (1985). These results further support our contention that families: the Pocilloporidae (6) and Agariciidae (12) Red Sea corals exhibit temporal reproductive isolation (Tables 2, 3). Reported values of oocyte diameters de- (Shlesinger and Loya 1985). pend on whether measurements were made on live tissue Most of the species in the Red Sea reproduce during or histological sections. In broadcasting species from the summer months (Fig. 3; Shlesinger and Loya 1985). 697

of oocytes per spawning gonad were consistent within each family (Table 2). Therefore, these characteristics appear to be phylogenetic in origin, as suggested by Harrison (1985). In contrast, the rate of oocyte growth varied even within the same family (Fig. 4). Although the end result was the same, some species exhibited linear oocyte growth while others had exponential growth. These two strategies of oocyte growth varied in their initial ener- getic allocation. In species that exhibit linear oocyte growth, oocytes are synchronously formed during the ®rst month of oogenesis and then grow at a constant rate. In species that exhibit exponential oocyte growth, oocytes are produced during a prolonged period of about 3 months. Then, energy is channeled into in- creasing oocyte diameter until maturity. Harrison and Wallace (1990) mentioned that oocytes are obviously colored some weeks prior to spawning. The present report is the ®rst to indicate that oocytes of broadcasting coral species exhibit color change throughout maturation (Table 1). This feature can be applied as a ®eld tool to predict in situ, the approximate spawning time. No such color changes were observed in oocytes of brooding species. The di€erent modes of reproduction, brooding versus broadcasting, did not follow taxonomic lines (Table 1). Similar ®ndings were reported by Harrison (1985). The majority of the coral species in the present study (21 out of 23) broadcast gametes (Table 1). Only two species Alveopora daedalea and Seriatopora caliendrum brood and release planulae. The only other brooding species reported from the Red Sea is Stylophora pistillata (Rinkevich and Loya 1979a, b). For the Red Sea corals, the reproductive mode re¯ects variation in timing dur- ing gonad development. Oogenesis is long in broad- casting species (5 to 7 months) compared to a shorter time period (<3 months) in brooders. Broadcasters re- lease gametes in a short (1 to 4 d year)1) period with complete synchronization in the population. Brooders release planulae over a number of months and there is Fig. 4 Monthly increases in oocyte diameter during the oogenesis of only partial synchronization within the population. selected scleractinians in the Red Sea. Left: oocytes of species Furthermore, broadcasting species produce many (>10) exhibiting linear growth curves; right: exhibiting exponential growth. oocytes per polyp and many (>4 ) gonads per polyp Each month, for 5 to 6 months, 100 oocytes were measured for each species (Table 2). Conversely, brooders produce few (1 to 4) oocytes per polyp and have few (1 or 2) gonads per polyp (Table 2). In general, brooding species produce Two species in this study, Cynarina lacrymalis and Fa- few, large eggs, which allows them to provide supple- vites pentagona, started oogenesis in late summer with mentary nutrition for each planula. Thus, di€erent re- gamete release in the spring. Stylophora pistillata is the productive modes may have arisen in response to only other coral species from the Red Sea reported to energetic constraints or environmental pressures. have such a gametic cycle (Rinkevich and Loya 1979a). In attempting to understand brooding and broadcast Most of the studied species (20 out of 23) were her- spawning in corals, several studies have concluded that maphroditic (Table 1). In the three gonochoric species, reproductive mode and fecundity are linked to oocyte sexuality was determined at the colony level. Her- diameter and polyp size. Chia (1976) proposed that maphroditism or gonochorism followed family or genus broadcasting organisms tend to have smaller eggs and lines. Most species within a given family exhibited the higher fecundity than related species that exhibit pa- same gonad morphology such as gonad arrangement, rental care (brooding) and release large larvae. For Red structure and position in each polyp. In addition to the Sea corals, oocyte size had no relation to the mode of number of gonads in each spawning polyp, the number reproduction and varied widely. The brooding coral 698

Table 2 Quantitative characteristics of female gonads in Red Sea number of oocytes per polyp is derived from the average number of corals measured from histological sections. Oocyte diameter re- oocytes per gonad multiplied by the number of ovaries per polyp. presents the largest measurements in cross sections. Estimation of From each species, 30 colonies were sampled

Family, Polyp Oocyte No. of No. of Mean ‹ SD Estimated species diameter diameter ovaries oocytes oocytes oocytes (mm) (lm) polyp)1 gonad)1 gonad)1 polyp)1

Pocilloporidae Stylophora pistillataa, b 0.75 230 1±2 1±2 1.0 1±2 Seriatopora caliendruma 0.75 240 1±2 1 1.0 1±2 Pocillopora verrucosa 0.75 130 6 8±12 9.3 ‹ 1.3 56 Acroporidae Acropora eurystoma 0.75 420 4 5±8 5.2 ‹ 1.5 21 Acropora hemprichi 0.8±1.0 395 4 5±9 6.6 ‹ 1.7 27 Acropora humilis 0.7±1.0 395 4 5±8 6.6 ‹ 1.8 27 Acropora hyacinthus 0.75 375 4 4±6 5.1 ‹ 0.8 20 Acropora scandens 0.75 375 4 4±6 4.9 ‹ 1.2 20 Acropora variabilis 0.8±1.0 420 4 4±8 5.7 ‹ 1.6 23 Astreopora myriophthalma 2.5±3.0 395 4 8±15 10.7 ‹ 2.2 43 Montipora erythraea 0.75 290 4 4±10 6.7 ‹ 2.0 27 Faviidae Cyphastrea microphthalma 1.3±1.5 290 12 8±10 8.6 ‹ 0.8 105 Favia favus 5.2±6.5 395 18 20±60 38.5 ‹ 11.8 700 Favites pentagona 5.5±6.5 240 18 10±30 19.7 ‹ 6.9 355 Goniastrea retiformis 3.0±4.0 315 18 20±45 33.1 ‹ 7.0 600 Platygyra lamellina 4.5±5.5 370 18 12±60 41.4 ‹ 14.9 750 Poritidae Alveopora daedaleaa 0.8±1.2 450 1±2 1±3 2.2 ‹ 1.3 4 Goniopora savignyi 2.0±2.3 265 12 5±8 6.3 ‹ 1.9 75 Porites lutea 1.25 160 12 4±5 4.9 ‹ 1.6 60 Mussidae Acanthastrea echinata 10.0±12.0 300 24 20±62 46.6 ‹ 8.8 1000 Cynarina lacrymalis 16.0±20.0 265 60 45±120 79.7 ‹ 21.3 3550 Lobophyllia hemprichi 16.0±20.0 290 48 35±65 51.8 ‹ 10.1 2450 Oculinidae Galaxea fascicularis 5.0±7.0 395 36 48±230 60.4 ‹ 21.9 2160 Agariciidae Pavona varians 0.6±0.8 50 12 1±2 1.6 ‹ 0.8 18 a Brood planulae, unlike all other species which broadcast gametes b Results from studies of Rinkevich and Loya (1979a,b)

Alveopora daedalea and broadcasting species of the ge- ibbean corals large colony size and short annual nus Acropora had the largest oocytes (450 and 420 lmin spawning correlated with brooding species, while small diameter, respectively). Brooding species of Pocillopor- colony size, multiple planulating cycles per year and idae and Poritidae developed larger oocytes than the occupation of unstable habitats correlated with brood- broadcasting species in these families (Table 2). Oocyte ing species. Van Moorsel (1983) suggested that the diameter appears to vary widely within individual spe- number of sexual products may be a€ected by polyp cies at di€erent locations (Stimson 1976; Harriott 1983a) structure. Wallace (1985) found in Acropora species that or within genera (Wallace 1985; Kojis 1986), indicating oocyte diameter is inversely related to polyp fecundity. that more extensive comparative studies are needed. The The present study demonstrates that among scleractini- wide distribution of oocyte sizes within species may be ans in the Gulf of Eilat, the number of oocytes (i.e. due to either real di€erences between sites, or to diver- polyp fecundity) is positively correlated to polyp diam- gence in technical procedures (i.e. measurements by eter (Table 2). Nevertheless, the relationship between histological sections versus direct tissue measurements, egg number, egg size and polyp size is complex, and is see Wallace 1985). Comparison of oocyte diameters probably linked to the energetics of reproduction in each between geographical regions would be improved by species. Furthermore, recent research demonstrates that standardizing histological procedures and measure- mode of reproduction may vary in some species. For ments. example, Pocillopora damicornis (Ward 1992) and Go- Rinkevich and Loya (1979a) suggested that brooding niastrea aspera (Sakai 1997) exhibit broadcast spawning and broadcasting species were separated according to as well as brooding. At present there seems to be no polyp size, egg diameter and the anatomical sites of universal relationship between coral size, polyp size and/ gonads in the polyp. Szmant (1986) found that in Car- or egg size and mode of reproduction. 699

Table 3 Reproductive modes and fecundity in hermatypic corals. riott (1983a); J Szmant-Froehlich et al. (1985); K Babcock (1984); L The literature survey is based on available data of gonad para- Kojis and Quinn (1981); M Glynn et al. (1994); N Glynn et al. meters in scleractinians. Sources: A Rinkevich and Loya (1979a); B (1996); O Szmant-Froehlich et al. (1980); P Fadlallah (1982). All Harriott (1983b); C Stimson (1976); D Fadlallah (1985); E Szmant references used ®xed histological sections (P brooding planulae; B (1986); F Kojis (1986); G Wallace (1985); H Wyers (1985); I Har- broadcasting species)

Family, Mode of Oocyte No. of No. of No. of Source species reproduction diameter ovaries oocytes oocytes (lm) polyp)1 gonad)1 polyp)1

Pocilloporidae Stylophora pistillata P 230 1±2 1±2 A Pocillopora damicornis P 100 1±2 1 B Pocillopora damicornis P 30 6 3±4 18±24 C Pocillopora meandrina 30 6 18±20 108±120 C Pocillopora verrucosa B 150 6 60±90 D Acroporidae Acropora cervicornis B 300 4±6 6±8 E Acropora cuneata P 325 4 1±3 F Acropora ¯orida B 584 4 6±14 G Acropora granulosa B 534 4 6±23 G Acropora hyacinthus B 622 4 4±11 G Acropora longicyathus B 591 4 6±18 G Acropora loripes B 560 4 5±22 G Acropora nobilis B 571 4 2±12 G Acropora palifera P 325 4 1±3 F Acropora sarmentosa B 652 4 6±14 G Acropora valida B 633 4 3±11 G Montipora sp. 280 4 3±4 12±16 C Faviidae Cyphastrea ocellina P24C Diploria strigosa 330±370 10 H Diploria strigosa B 400 22±32 8±10 E Favia favus 360 1200 I Favia fragum P 250 9±22 1±2 J Goniastrea aspera B 350 1±13 K Goniastrea favulus B 510 1±13 L Montastraea annularis B 300 12 5±14 E Montastraea cavernosa B 350 24 12 E Poritidae Porites astreoides P 50 6±10 2 E Porites australiensis 150 12 4±8 72 I Porites compressa 120 12 3±4 36±48 C 120 12 3±4 36±48 C Porites lobata 140±170 60±75 M Porites lutea 180 12 4±8 72 I Mussidae Lobophyllia corymbosa 600 2800 I Mycetophyllia ferox P 300 12±24 2±4 E Siderastreidae Siderastrea siderea B 600 22±32 8±10 E Agariciidae Gardineroseris planulata 117 26±34 N Pavona explanata 12 20 240 C Pavona gigantea B 110 18±229 N Rhizangiidae Astrangia danae B 100±130 24 3000±4000 O Astrangia lajollaensis B 150 6000 P Dendrophylliidae Dendrogyra cylindrus B 300 10±30 E

Based on the evolution of sexual reproduction in sea reproduction, i.e. broadcasting of gametes. The advan- anemones (Chia 1976), we suggest that oviparity tage of this reproductive mode is long distance dispersal (broadcasting) is the ancestral mode of reproduction in due to the long planktonic larval period (Harrison and Hexacorallia, and viviparity (brooding) is a derived trait. Wallace 1990; Richmond and Hunter 1990). Evidently, most stony corals retain the ancestral mode of 700

Extreme physical disturbances which are character- istic of reef zones in shallow water may in¯uence the References evolution of reproductive modes (Stimson 1978; Szmant 1986). Species with large and massive colonies may Babcock RC (1984) Reproduction and distribution of two species of Goniastrea () from the prov- survive these physical disturbances by increasing energy ince. Coral Reefs 2: 187±204 for growth, and decreasing that for reproduction, while Bermas NA, Alino PM, Atrigenio MP, Uychiaoco A (1992) Ob- still broadcasting gametes. Species which have low servations on the reproduction of scleractinian and soft corals competitive abilities or require narrow and speci®c in the Philippines. In: Richmond RH (ed) Proc 7th int coral Reef Symp. Vol. 1. University of Guam, Mangilao, pp 443±447 conditions for settlement and recruitment may have Chia FS (1976) reproduction: patterns and adaptive shifted to a di€erent mode of reproduction, i.e. brood- radiation. In: Mackie GO (ed) Coelenterate ecology and be- ing. havior. Plenum Press, New York, pp 261±270 Szmant (1986) suggested that brooding, with the re- Dai CF, Soong K, Fan TY (1992) Sexual reproduction of corals in northern and southern Taiwan. In: Richmond RH (ed) Proc 7th sulting higher recruitment rates, appears to be an int coral Reef Symp. Vol. 1. University of Guam, Mangilao, adaptation evolved by small-size coral species that su€er pp 448±455 frequent and early colony mortality. Brooding may Fadlallah YH (1982) Reproduction ecology of the coral Astrangia provide a competitive edge during recruitment for some lajoleris in a kelp forest habitat. Oecologia 55: 379±388 r-strategist species, such as Stylophora pistillata (Loya Fadlallah YH (1985) Reproduction in the coral Pocillopora verru- cosa on the reefs adjacent to the industrial city of Yanbu (Red 1976). Brooding results in more rapid settlement and Sea, Saudi Arabia). In: Gabrie C et al. 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