BULLETIN OF MARINE SCIENCE, 73(3): 713–724, 2003
CORAL REEF PAPER
SEXUAL REPRODUCTION OF THE BRAZILIAN REEF CORAL
SIDERASTREA STELLATA VERRILL 1868 (ANTHOZOA,
SCLERACTINIA)
Monica Moraes Lins de Barros, Débora de Oliveira Pires
and Clovis Barreira e Castro
ABSTRACT
In the present study, the reproductive characteristics of the Brazilian endemic coral
Siderastrea stellata Verrill, 1868 were determined for the Abrolhos Reef Complex (18oS)
and Búzios (23oS). The reproductive pattern and mode of reproduction, sex ratio, gametogenesis and spawning season were determined by histological examination. Siderastrea
stellata was found to be a gonochoric brooder and oogenesis lasted approximately ten
months. Spawning occurred during February through the mid-March in the Abrolhos
Reef Complex, and December to early January in Búzios. Sea temperature is most likely
the major factor influencing the gametogenesis of this species and this latitudinal variation was probably related to the upwelling that occurs on Búzios during the summer.
Oocyte and larval characteristics indicated a relatively short dispersion phase such that
larvae settle near the parent habitat. These data may be useful for improving conservation
and management policies for Brazilian coral reefs.
The coral community from Brazil is characterized by the presence of archaic forms,
some of which are related to Tertiary forms (Leão, 1988). Fifteen scleractinian reef coral
species were described for Brazil (Castro, 1994), which correspond to only 1% of the
world’s coral diversity (Leão, 1997). Only one species of Siderastrea occurs in Brazil,
Siderastrea stellata Verrill, 1868, which is endemic to the South Atlantic (see Laborel,
1974, for a discussion on its occurrence in West Africa). This species is considered one of
the main coral builders in Brazilian reef areas (Echeverría et al., 1997; Leão et al., 1997):
S. stellata has been reported from the Parcel do Manuel Luiz (00∞53' S, 044∞16' W) to
Arraial do Cabo (23∞ S, 042∞ W). Probably the largest population of this species is present
at the Abrolhos Reef Complex, South of Bahia, Brazil (approximately 18∞S; Laborel,
1970; Castro, 1994). Part of this complex has been protected by a national marine park
and harbors the largest coral species richness in the South Atlantic (Gonchorosky et al.,
1989; Castro, 1994), including all reef coral species reported from Brazil to date. At
Búzios (approximately 23∞ S), an area approximately 1000 km to the south of Abrolhos
and close to the southern limit of S. stellata, contains a population of S. stellata on rocky
shores which included the largest colonies of this species ever reported (1.70 m).
The available information on the sexual reproduction of Siderastrea spp. is limited and
represented by punctuated data (Szmant, 1986; Soong, 1991; Soong and Lang, 1992).
The most detailed study on reproduction of Siderastrea concerns the embriogenesis of
Siderastrea radians from the West Indies done by Duerden (1904). Only one study has
been published on the sexual reproduction of Brazilian scleractinians (Pires et al., 1999),
and this work focused on the endemic coral genus, Mussismilia.
The goal of this study was to examine the sexual reproduction of S. stellata on the
Abrolhos Reef Complex and compare this to corals at another latitude at Búzios. The
reproductive pattern (gonochorism vs. hermaphroditism), mode of reproduction (brooder
Bulletin of Marine Science
© 2003 Rosenstiel School of Marine and Atmospheric Science
of the University of Miami
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vs. broadcast spawner), sex ratio and possible spawning season were estimated for these
two regions.
MATERIAL AND METHODS
Coral samples were taken in the Abrolhos Reef Complex (18o S), to diagnose the sexual reproduction characteristics of S. stellata and at Praia da Tartaruga, Búzios, RJ (23o S), to examine
latitudinal variation (Fig. 1). Samples from Abrolhos consisted of ten colonies taken bimonthly in
1996 (February 06, April 21; June 08, August 12, October 08, and December 09), sporadically in
1997 (March 24, May 25, June 12, October 31) and once in 1999 (March 08). Colonies of a given
sample were collected in one of several reef areas at most some 40 km distant from each other
(Viçosa Reef, 17∞58.30' S, 039∞15.40' W; Pontas Sul, 17∞53.88' S, 038∞58.48' W; Pedra de Leste,
17∞45.61' S, 039∞02.25' W and Pedra Lixa, 17∞46.10' S, 039∞02.73' W). Five–ten colonies were
collected in Búzios (22∞45.2' S, 041∞54.1' W) in 1999 (February 27; October 13; November 03;
December 15) and in 2000 (January 03). Whole colonies were collected using a hammer and a
chisel and fixed in a saline 10% formalin. Collected colonies were chosen haphazardly. Each collected colony was located at least one meter apart from all other collected colonies to avoid intraclonal
sampling. Also, collected colonies were at least 10 cm in diameter to avoid immature colonies.
The studied material was deposited in the Museu Nacional/Universidade Federal do Rio de Janeiro
(MNRJ). Initially, five colonies from each sample period were selected for histological procedures.
If necessary, more colonies were processed to standardize the data among the months (number of
oocyte measurements), or confirm results (oogenesis stage and sex ratio). Colonies were decalci-
Figure 1. Map of the studied areas.
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715
fied in a 5% formalin and 10% formic acid solution, and then rinsed in running tap water. A mean
of seven polyps was selected per colony, chosen from the central part of the colony to avoid sterile
zones (Hughes and Jackson, 1985; Rinkevich and Loya, 1985; Chornesky, 1989; Soong and Lang,
1992). Polyps were dehydrated, cleared and embedded in paraffin. Serial cross sections (5–8 mm)
were obtained using a manual micrometer (Reichert-Jung 820). Five slides per colony with three to
four histological sections each, were stained using Mallory’s Triple stain (Pantin, 1948). They were
observed under a binocular microscope (Olympus BH2).
The general conditions of tissues and gametes were described (qualitative data) and oocyte development classified into three stages, following Wourms (1987) and Pires et al. (1999). The evolution of the reproductive cycle was analyzed from line graphics showing the percentage of each
stage of oocytes over the study period. The spawning season was inferred indirectly by the disappearance of gametes, or the appearance of immature ones in the preparations.
Statistical analyses were undertaken using at least ten measurements of the largest axis size of
nuclei per colony (quantitative data; Lins de Barros et al., 2000a). Measurements were taken only
when the nucleolus was present in the histological section, using an eyepiece micrometer in an
optical microscope. Data were analyzed using the software package STATISTICA (StatSoft Inc.
1992). The data were analyzed using standard ANOVA techniques to determine whether colonies
were at the same stage of oocyte development, i.e., if the colonies were synchronized. Detection of
a significant difference was investigated with a Tukey post-hoc test to identify where the differences occurred (significance at P < 0.05).
Weekly mean sea surface temperatures (SST) from satellite data were obtained from the U.S.
National Oceanographic and Atmospheric Administration (NOAA) (Reynolds and Smith, 1994).
Data were used from grid points centered on 17∞30' S, 038∞30' W and 22∞30' S, 041∞30' W. The
former includes most of the area’s shallow platform (< 20 m depth), where the Abrolhos reef complex lies. The latter includes Cape Búzios. Land based temperatures for Arraial do Cabo (some 30
km south of Búzios) were obtained from Companhia Nacional de Álcalis, which collects hourly
data with an industrial thermometer (precision = 0.5∞ C) located at Ponta da Cabeça, Praia Grande.
This area is strongly influenced by upwelling waters.
The duration of daylight was based on sunrise and sunset hours in the studied area, calculated
using the coordinates 17∞30' S, 038∞30' W. Data were averaged by week to simplify graphical
comparisons with SST data. The spawning season of S. stellata in the Abrolhos Reef Complex was
related to SST and photoperiod data.
RESULTS AND DISCUSSION
Siderastrea stellata exhibited an annual reproductive cycle (Fig. 2). Due to this periodicity, the collecting interval was adequate to detect general trends in gamete development
and spawning.
No embryos were seen in the 20 mature colonies sampled in the Abrolhos Reef Complex, while planulae were observed in the gastrovascular cavity, or very close to the mouth,
ready to be released. These observations indicate the occurrence of internal fertilization
that results in a larva, characterizing S. stellata as a brooder species. The Caribbean species S. radians exhibits this mode of reproduction too, while S. siderea is a broadcast
spawner, releasing gametes to external fertilization (Szmant, 1986; Soong, 1991).
The studied materials of S. stellata (from the Abrolhos Reef Complex and Búzios)
contained only female gametes. Most coral species have spermaries for at least two consecutive months by the end of the reproductive cycle (Szmant, 1986; Soong, 1991) and
our sampling periods included months with oocytes in final stages of development in
consecutive months before spawning. The other two species of Siderastrea (S. siderea
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Figure 2. Representation of the reproductive cycle of Sideratrea stellata in the Abrolhos Reef
Complex, Brazil, based on the variation of the mean nucleus size during the study period. Number
in parenthesis on the x-axis indicates number of measured nuclei in the respective sample. Error
bars = standard deviation.
and S. radians, both from the Caribbean) are gonochoric (Szmant, 1986; Soong, 1991).
Therefore, we postulate that S. stellata is probably a gonochoric species too.
This available information about Siderastrea indicates that this genus follows Harrison’s
assumption (1985), that the pattern of reproduction (gonochorism vs. hermaphroditism)
is consistent among higher taxa, while the mode of reproduction (brooder vs. broadcast
spawner) can be very variable, even within populations of the same species.
A skewed sex ratio was estimated for S. radians (20 females: 1 male), while S. siderea
showed a sex ratio of 1:1 (Duerden, 1904; Szmant, 1986; Soong, 1991). The skewed sex
ratio present in S. radians, and probably in S. stellata is expected, since it occurs in other
brooders (Harrison and Wallace, 1990). Broadcast spawner species, on the other hand,
which are dependent on random mating, usually have a 1:1 sex ratio (Kramarsky-Winter
and Loya, 1998), as is the case of S. siderea (Szmant, 1986; Soong, 1991). Hypotheses
related to skewed sex ratios of corals include asexual propagation (Sammarco, 1982;
Chornesky and Peters, 1987), inbreeding (Hamilton, 1967), parthenogenesis (Hamilton,
1967), sex change in adults (Chornesky and Peters, 1987; Rinkevich and Loya, 1987),
eggs activated to develop by sperm of another species (Stenseth et al., 1985), or from
environmentally-determined sex (Charnov and Bull, 1977 in Soong, 1991). The absence
of males in the present study could be the result of analyzing an insufficient number of
mature colonies (Abrolhos – February 06, 1996 – 10 colonies; Abrolhos – March 03,
1999 – 10 colonies; Búzios – 15 December, 1999 – 2 colonies), associated with a large
deviation of the sex ratio.
As is typical for other scleractinian corals, the oogonia appeared in the endoderm of the
mesenteries. They migrated to a position in the mesogloea, mid-way between the longitudinal muscle bands and the mesenteric filaments (Hyman, 1940; Szmant-Froelich et al.,
1985). In a sexually mature polyp there were usually 48 mesenteries (complete and incomplete) that bore gonads. Each mesentery presented from three–seven mature oocytes.
The oogenesis of S. stellata was subdivided into three stages, according to histological
BARROS ET AL.: SIDERASTREA STELLATA REPRODUCTION
717
Figure 3. Oogenesis stages of Siderastrea stellata: A) Stage I oocyte (scale bars = 5 mm); B) Early
stage II oocyte (scale bars = 15 mm); C) Post stage II oocyte (scale bars = 22 mm); D) Stage IV
oocyte (scale bars = 50 mm); E) Larvae (scale bars = 50 mm ).
characteristics and relative size of oocytes and nuclei. Stage I (oogonia; Fig. 3A): A cloudy
cytoplasm, with no defined limits, stained a light rose, surrounds a conspicuous nucleus,
stained a lilac color, and a nucleolus, stained a strong red. At this stage, the oogonia can
be positioned in the endoderm of the mesentery, or in the mesogloea, which is represented by a thin layer (many times difficult to see). Larger oogonia measured approximately 70 mm, while the nucleus diameter ranged from 6–30 mm. Stage II (primary
oocyte; Figs. 3B,C): This was the longest oogenesis stage. This phase occurs after the
oocyte migration to the mesogloea, where the oocyte increases in size until the stage III,
prior to spawning. During the beginning of this stage (Fig. 3B), the cytoplasm was not
dense and was stained a rose color. The nucleus was in a central position and stained lilac.
By the end of this stage (Fig. 3C), the cytoplasm had become dense and stained pink, and
the nucleus (granulated and stained a lilac color) was in an intermediary position between
the center and the periphery of the oocyte. Some zooxanthellae were around the oocyte
and few inside the cytoplasm. During this stage, the endoderm thinned and showed some
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fragile parts near the gametogenic region. Oocyte diameter ranged from approximately
13–300 mm, while the nucleus ranged from 8–64 mm. Stage III (mature oocyte; Fig. 3D):
The cytoplasm was very dense, granulated, and stained a magenta color. The nucleus was
in the periphery of the oocyte. In the most advanced phase of this stage, a colorless region, in the form of a half-moon, could be seen between the nucleus and nucleolus. The
nucleus became granulated and acquired a half circle shape just before fertilization. In
some cases, the nucleolus showed subdivisions, and in other cases, more than one could
be seen in each oocyte. The oocyte was partially, or completely separated from the mesogloea and endoderm. The endoderm appear ripped in several regions, especially around
the gametogenic area. A great amount of reddish granules was found in the adjacent
endoderm, as well as a lot of zooxanthellae around and inside the oocyte. Oocyte diameter ranged from approximately 65–470 mm and the nucleus from 13–120 mm.
The oogenesis of S. stellata from Abrolhos probably began in April and lasted approximately 10–11 mo, with a small resting period between consecutive cycles. April and June
1996 were characterized by a small number of reproductive colonies, which required the
sample of ten colonies instead of only five. A small number of oocytes (4/10 in April
1996 and 3/10 in June 1996) in stage I was recorded. A concentration of interstitial cells
in the endoderm of the mesentery could also be seen. In August 1996, however, oocytes
in stage I disappeared, while oocytes in stage II were abundant, followed by oocytes in
stage III. During the next sample periods (October and December, 1996), the percentage
of stage II oocytes was still high, but that of stage III continuously increased (Fig. 4).
All colonies of 06 February 1996 contained mainly stage III oocytes (Fig. 4). Statistical analyses were carried to determine if these colonies were at the same stage of oocyte
development. These analyses were done using nucleus size, instead of oocyte size because S. stellata oocytes showed some microanatomical characteristics that could misrepresent the real size of the structure and lead to measurement errors. The nucleus, on
the other hand, did not exhibit such characteristics (Lins de Barros et. al., 2000a). During
the peak of the reproductive cycle (06 February 1996) four out of five colonies were at
the same stage of gametocyte development (ANOVA; P > 0.01). Moreover, the odd colony
Figure 4. Percentage of each oocyte stage of Siderastrea stellata colonies collected from Abrolhos
Reef Complex, Brazil, over given sample dates.
BARROS ET AL.: SIDERASTREA STELLATA REPRODUCTION
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was significantly different from only two other colonies (Tukey test: P = 0.542, 0.405,
0.036, and 0.009). Hence, the two colonies not significantly different from the odd colony
were in an intermediate phase of gametogenesis, with oocyte nucleus size not statistically
different from any other colony. These data suggest that there is a broad synchronization
in the gametogenesis and larval release among colonies of S. stellata, however, the data
are insufficient to drawn sound conclusions.
Larvae (Fig. 3E) were observed in the gastrovascular cavity of only three colonies
from the 20 mature colonies observed (ten in February 1996 and ten in March 1999). The
release of larvae of this species in the Abrolhos Reef Complex probably occurred between February and mid- March. On 23 April 1996, the oocytes were absent and the
majority of the polyps presented fragile regions on the endoderm, characteristic of the
occurrence of a recent spawning event. Observations based on materials collected on 08
March 1999 and 24 March 1997 corroborated these results: colonies comtained mainly
mature gametes and no gametes, respectively.
Colonies from Búzios contained larvae close to the mouth on 15 December 1999 and
03 January 2000, indicating that S. stellata probably releases larvae on successive days
during a prolonged spawning season. These results are in accordance with the most common relationship between mode of reproduction and periodicity of spawning in corals:
brooder coral species usually have multiple larvae release events over a year, or in a
single long period of the year (Fadlallah, 1983; Shlesinger and Loya, 1985; Richmond
and Hunter, 1990; Dai et al., 1992; Shlesinger et al., 1998).
Most corals have distinct breeding seasons and well-defined periods of gamete spawning, or planulae release (Harrison and Wallace, 1990). Both broadcast spawning and brooding species tend to exhibit seasonal and lunar patterns in timing of reproduction (Harrison
and Wallace, 1990). Sea temperature seems to be the major factor regulating the onset of
reproduction of most marine invertebrates (Jokiel and Guinther, 1978; Fadlallah, 1983;
Harrison et al., 1984; Richmond and Jokiel, 1984), while photoperiod is usually considered the main factor regulating the spawning (Harrison et al., 1984; Richmond and Jokiel,
1984; Fadlallah, 1985).
A latitudinal variation in the spawning season was observed between S. stellata populations from Búzios and Abrolhos: spawning of S. stellata also seemed to occur earlier on
Búzios (December to early January) than in Abrolhos (February to mid-March). Pires et
al. (1999) also observed a similar latitudinal asynchrony in M. hispida, with populations
from Búzios spawning before those from the Abrolhos. By 28 February 1999, corals from
Búzios had already spawned, while colonies from Abrolhos collected on 03 March 1999
were still in the peak of their gametogenic cycle. This variation occurred in opposition to
photoperiod variation between these two areas. In Abrolhos, larval release seems to occur
when the photoperiod is decreasing (Fig. 5), whereas, in Búzios, larval release occurs
around the summer solstice, when the photoperiod is the longest. Moreover, due to the
difference in latitude, colonies from Búzios experience larger photoperiod variation than
those at Abrolhos. This indicates that neither season (regarding photoperiod), nor absolute number of daylight hours is responsible for this latitudinal variation, suggesting that
photoperiod may not be a major force regulating the spawning season.
The summer season in the Búzios region is punctuated by an upwelling phenomenon,
which reduces SSTs by many degrees (Valentin and Moreira, 1978; Valentin et al., 1991).
Although there are anecdotal reports of upwelling influence in Búzios, the only available
SST satellite data are from Arraial do Cabo (Fig. 6), the area of strongest upwelling some
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Figure 5. Weekly mean sea surface temperature (SST) from satellite data, day length (number of
hours between sunrise and sunset), and probable spawning period of Siderastrea stellata (horizontal
bars) in the Abrolhos Reef Complex.
26 km south from Búzios. We believe the available SST satellite data are not adequate for
Búzios because this site is probably strongly influenced by the warm Brazilian Current.
On the other hand, the influence of upwelling is probably not as strong in Búzios as it is
in Arraial do Cabo. Siderastrea stellata at Búzios may spawn early to avoid these unusual
low sea temperatures in the summer that could compromise its reproductive success.
However, additional studies are needed to identify the proximate factor(s) that result in
this latitudinal difference.
Siderastrea stellata occurs in diverse reef ecozones, mainly shallow water habitats
(Laborel 1970, Leão, 1988). It was previously suggested that this species is resistant to
the major environmental stresses for a scleractinian coral species (extreme temperature,
high variation of salinity and intense sedimentation; Hartt in Laborel, 1970). The reproductive characteristics exhibited by S. stellata could be viewed as one of its adaptations
to tolerate the stressful conditions of shallow reefs.
The reproductive strategy of corals can be influenced by resource availability (food
and space), biotic interactions, and environmental conditions (Richmond, 1987). In the
Abrolhos Reef Complex, the shallow water coral community seems to be structured mainly
by abiotic factors (Lins de Barros et al., 2000b). Although S. stellata colonies are small in
the Abrolhos Archipelago (Segal-Ramos, 1998), because of their high frequency in the
area, S. stellata has one of the highest percentages of coral coverage in this habitat (Pitombo
BARROS ET AL.: SIDERASTREA STELLATA REPRODUCTION
721
Figure 6. Weekly mean sea surface temperature (SST) from satellite data and land-based methods,
near Búzios (Arraial do Cabo Region).
et al., 1988). This species also dominates the shallow habitats in Búzios, although colony
size is very large (pers. obs.).
The scenario at Abrolhos (large number of small colonies) may be the result of high
rates of mortality of larger colonies, related to a constant abiotic pressure in this environment (Bak and Engel, 1979; Kramarsky-Winter and Loya, 1998). Such a theoretical, high
adult mortality could be compensated for by an early onset of reproduction, with colonies
becoming mature only a few years after settlement (Van Moorsel, 1983; Kojis, 1986). It
could also be compensated for by high recruitment rates. Brooder species, as S. stellata,
seem to be well-adapted in occupying unstable habitats (Szmant-Froelich et al., 1985;
Szmant, 1986; Richmond, 1987). High settlement rates may be achieved through the
reproductive strategy of S. stellata to produce few (a mean of 5 per mesentery), large (up
to 470 mm) oocytes. Mature oocytes have zooxanthellae, which are inherited by the larvae, probably contributing to their nutrition (Richmond, 1987). It has been proposed that
oocytes with these characteristics most likely result in larvae with a non-feeding planktonic phase (Tomascik and Sander, 1987; Szmant, 1991). Therefore, larvae settlement
probably occurs soon after release (Fadlallah, 1983; Van Moorsel, 1983; Kojis, 1986;
Ward 1992). This strategy could contribute to decreases in the rate of larval mortality
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during planktonic dispersion (Bak and Egel, 1979; Szmant, 1986) and increase the local
recruitment rate (Szmant, 1986; Havenhand, 1995).
The current study presents the first data on the sexual reproduction of S. stellata. Although we were able to set forth new insights on this species life strategy, further studies
are necessary to complement the present information and analyze some of the proposed
hypotheses. These include minimum colony size at the onset of sexual reproduction,
settlement characteristics, and the structure and dynamics of populations. Reproductive
data provides important information to management and conservation programs, since
the reproductive characteristics of the organisms are strongly correlated with their distribution, maintenance, and ecological demands.
ACKNOWLEDGEMENTS
We thank E. Calderon, C.A. Echeverría, T.H. Moura de Melo, M. Medeiros, E. Neves, S. Pinto,
C. Ratto, B. Segal, C.R. Ventura, E. Viveiros de Castro, for helping in different phases of this study,
J.O. Nascimento (Observatório Nacional/CNPq), for data on sunrise and sunset hours, R.W. Reynolds
(NOAA), for help in obtaining SST satellite data, and F. Fernandes (IEAPM) for help in obtaining
land based SST data. This research was funded by Conselho Nacional de Desenvolvimento Científico
e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ),
Fundação Universitária José Bonifácio (FUJB), and Universidade Federal do Rio de Janeiro (UFRJ).
We also thank Brazilian Environmental Agency (IBAMA), for collecting permits.
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DATE SUBMITTED: September 29, 2000.
DATE ACCEPTED: November 8, 2002.
ADDRESSES: (M.M.L de B., D. de O.-P., C.B. e C.) Museu Nacional, Departamento de Invertebrados,
Quinta da Boa Vista, São Cristóvão, 20940-040, Rio de Janeiro, Brazil. CORRESPONDING AUTHOR: (M.M.L
de B.) Museu Nacional, Departamento de Invertebrados, Quinta da Boa Vista, São Cristóvão, 20.940040, Rio de Janeiro, Brazil. E-mail: <[email protected]>.