 Springer-Verlag 1997
Marine Biology (1997) 128: 141–148
A. Acosta · S. Zea
Sexual reproduction of the reef coral Montastrea cavernosa
(Scleractinia: Faviidae) in the Santa Marta area,
Caribbean coast of Colombia
Received: 19 April 1996 / Accepted: 24 September 1996
Abstract Sexual reproduction of the reef-building coral
Montastrea cavernosa was studied in the Santa Marta
area, Caribbean coast of Colombia, from October 1990
to October 1991. The area is subjected to a seasonal
upwelling–outwelling regime. From microscopical
analysis of tissue sections sampled each lunar month
around the full moon, it was confirmed that this is a
gonochoric, broadcasting species, with a single gametogenic cycle per year, and a 1:1 sex ratio. Oogenesis
began a few weeks after spawning, and extended for
11 mo. The onset of spermatogenesis occurred just before the full moon of June, later than at other localities
where sea-water temperatures during the first half of the
year are not as low. The amount of reproductive tissue
strongly increased in both sexes after July, in association
with an increase in sea-water temperature and a decrease
in photoperiod. The gonad index of fully mature female
colonies was about four times lower than at other localities, perhaps due to the stressful seasonal regime.
The male gonad index was lower than that of the female,
indicating sex-related differences in the rates of biomass
allocation to reproduction. As in other Caribbean localities, spawning occurred after the full moons of August and September. However, there was some evidence
of a third spawning episode after the full moon of October, possibly associated with a delay in the occurrence
of maximum sea-water temperatures in near-equatorial
localities compared to higher latitudes. The probability
of cross-fertilization in this species with a gonochoric
breeding system and a broadcasting mode of re-
Communicated by N.H. Marcus, Tallahassee
A. Acosta
Pontificia Universidad Javeriana, A.A. 59629 Bogotá DC,
Colombia
S. Zea (&)
Universidad Nacional de Colombia,
Departamento de Biologı́a, INVEMAR, AA 10–16,
Santa Marta, Colombia
production is favored by its balanced sex ratio, its
usually high within-reef zone abundance, and by localized and repeated spawning episodes, synchronized by
lunar phase.
Introduction
Sexual reproduction of reef-building corals has been
studied extensively (reviews by: Fadlallah 1983; Harrison and Wallace 1990; Richmond and Hunter 1990). In
the Caribbean Sea, ~30% of these species have been
studied, especially at Puerto Rico (Szmant et al. 1983,
1985; Szmant 1984, 1985, 1986, 1991), Panamá (Soong
1991; Guzmán and Holst 1993), Bermuda (Wyers 1984;
Wyers et al. 1991), Jamaica (Chornesky and Peters
1987), Barbados (Tomascik and Sander 1987), Curaçao
(Van Veghel 1994), and Florida (Szmant and Gassman
1990). However, there is still much to learn about geographic variability, or its lack, in those reproductive
traits (e.g. onset of gametogenesis, rates of allocation of
reproductive tissues, timing of spawning, etc.) that are
affected by environmental conditions.
Montastrea cavernosa is a gonochoric species, with a
long (F11 mo) oogenic cycle, and a shorter (F4 mo)
spermatogenic cycle that, in several localities across the
Tropical Western Atlantic, ends with the broadcasting
of gametes during evening hours, F1 wk after the full
moons of July to September (Szmant 1984, 1986, 1991;
Soong 1991; Wyers et al. 1991; Gittings et al. 1992; Van
Veghel 1993; Steiner 1995). Unlike the Caribbean areas
mentioned above, at Santa Marta, north-east Colombia,
reef corals are subjected to a stressful seasonal regime
that alternates between upwelling of low-temperature
waters, and outwelling of turbid, warm waters. To determine if this seasonal stress affects the reproductive
characteristics of M. cavernosa, we examined the progression of gametogenesis, fecundity, and spawning in
this species.
142
Materials and methods
Study area
The Santa Marta area in the north-east Colombian Caribbean
(11°15′ to 11°19′ N; 74°03′ to 74°13′W) forms part of the base of
the foothills of the Sierra Nevada de Santa Marta, which plunge
directly into the sea, forming a series of deep bays flanked by rocky
cliffs (Fig. 1). The area is characterized by low rainfall and upwelling of subsurface waters during the dry season (December to
April) due to the north-east trade winds. During the main rainy
season from September to November, significant outwelling of
warmer terrestrial runoff rich in inorganic and organic nutrients
occurs, lowering the coastal salinity (Márquez 1982). As a result,
coral reef development is mostly limited to a mid-depth (>5 to 10 m)
fringing belt, in which instead of the usual dominance of the
Montastrea annularis (Ellis and Solander, 1786) species-complex,
M. cavernosa (Linnaeus, 1758) is the main reef-builder (Antonius
1972; Acosta 1989; Zea 1993a, 1994).
Sampling was carried out at two sites, Punta de Betı́n in the
south-west and Bahı́a Gayraca (Gayraca Bay) in the north-east
(Fig. 1). Punta de Betı́n is a rocky peninsula on the northern side of
Santa Marta Bay. Its reef has been described by Erhardt and
Werding (1975), Acosta (1989), Liddell and Ohlhorst (1989), and
Zea (1994). Bahı́a Gayraca belongs to the complex of bays of the
Tayrona National Park, and is located some 16 km north-east from
Punta de Betı́n (Dı́az 1990).
Sampling
Samples of Montastrea cavernosa were collected by SCUBA on
each of 14 lunar months, at or close to the days of full-moon: 4
October, 2 November, 2 to 4 December 1990; 31 December 1990 to
3 January 1991; 30 and 31 January, 28 February, 30 March, 28
April, 28 May, 26 June, 24 and 25 July, 25 to 27 August, 23 and 24
September, 20 and 21 October 1991. At each reef site, between 5
and 17 m depth, 8 to 9 colonies were sampled (except for the 31
December 1990 to 3 January 1991 sample when only 4 colonies per
reef were sampled); the colonies were >20 cm maximum diameter,
and were spatially separated by at least 1 m. Growth form (encrusting/massive), color and size (maximum diameter) were noted,
and the number of polyps cm–2 was estimated. A single tissue
fragment, 5 cm diam × 2 cm thick, was taken by hand from the
center of each colony with a cylindrical steel corer driven by a
jackhammer. The same colony was never sampled twice. The total
number of colonies sampled was 216. Upon return to the diving
boat, tissues were fixed in Zenker solution.
Histological processing
After 24 h in fixative, samples were washed in running tap water
for another 24 h and then stored in 70% ethanol. Decalcifying was
carried out with 4% nitric acid and neutralizing in 5% sodium
sulfate solution (Guzmán and Holst 1993). Two 2 × 2 cm pieces,
each containing 1 to 4 polyps, were cut from each fragment and
embedded in paraffin after dehydration. Cross- and longitudinalsections, 10 lm thick, were cut from tissue blocks using a standard
microtome. The best 4 to 5 consecutive sections were chosen every
500 lm and mounted on glass slides. Sections were stained in
Heidenmhain’s azocarmine-anyline blue (Humason 1989).
Three polyps were generally examined from each colony (in a
few cases only 1 to 2 polyps were suitable for analysis) in crosssection with a microscope, and the number of mesenteries was
counted for each polyp. Ten mesenteries were haphazardly chosen
and examined for the presence of gonadal tissue. For each gonad,
the number of sex products (oocytes/eggs, spermaries or spermatic
cysts) were counted, and their size (maximum diameter) and developmental stage were noted. Quantitative variables were averaged
hierarchically for each gonad, polyp and colony. A per-colony
gonad index (volume of sex products per unit area of live tissue)
was calculated. Developmental stages were determined for female
and male sex products after the descriptions of Szmant et al. (1985)
and Szmant (1986, 1991), modified according to the ease with which
some stages could be distinguished. Thus, for oocytes, our Stage I
combined their Stages I (primary oocytes) and II (cytoplasm accumulation); our Stage II (vitellogenesis, up to 50% of cytoplasm
with yolk granules) covered the first half of their Stage III, while
our Stage III corresponded to the second half of theirs and included
Stage IV (eggs ready to spawn). For spermatic cysts, our Stage I
combined their Stages I (clusters of interstitial cells) and II (cysts
with membrane); our Stage II (concentric distribution of spermatocytes) was their Stage III; and our Stage III (spermatozoa at
the center) combined their Stages IV and V. Since the develop-
Fig. 1 Santa Marta area showing collecting sites (dashed line marks limits of Tayrona National Park)
143
mental stage of individual sex products was not uniform within and
between colonies at any given time, the percentage of eggs/cysts in
each stage was calculated from the total examined in each colony.
The behavior through time of the sample means of the above reproductive characteristics was used to infer the gametogenic cycle.
Spawning periods were indirectly assessed from histological
information. Colonies with a low absolute number of eggs/cysts, all
in Stage III, were assumed to have spawned within the previous
lunar month. Colonies with a still high number of large Stage III
eggs/cysts were assumed to be fully mature, ready to spawn within
the next lunar month. All other colonies were assumed to be still in
the process of maturation.
Environmental data
Daily (weekdays, 8:00 hrs) measurements of surface shore-salinity
(± 0.1& S) temperature (± 0.1 C°), and rainfall (± 1 mm) at Punta
de Betı́n, were averaged for the lunar month immediately preceding
the sampling date. Photoperiod (duration of daylight in hours) of
the days of full-moon at the nearby city of Barranquilla (10°59′N;
74°48′W) was obtained from the meteorological calendars of the
Instituto Colombiano de Hidrologı́a Meteorologı́a y Adecuación
de Tierras (1990, 1991). Environmental variables were not statistically correlated to reproductive characteristics; it was not possible
to evaluate the significance of the correlation coefficients because
the shortness of the time series prevented determination of their
autocorrelation structures (Box and Jenkins 1976). Thus, environ-
6
3
0
F M A M
J
J
A
S O
Female
Male
c
F M A M J
J
A S O
e
2.0
Gonad index
Percent of eggs
Gonad index
All colonies with reproductive tissues were either male or
female; thus sexes were separate (Fig. 2a). There were no
larvae in the gonads.
9
100
80
60
40
20
0
O N D D- J
J
Breeding system and reproductive mode
15
Female
2.5
The mean diameter of the sampled colonies of
Montastrea cavernosa was 50 cm (range 20 cm to 2 m).
Encrusting colonies constituted 61% of the total, while
the remaining 39% were massive and mound-shaped
colonies. Eleven different colors were noted, the most
frequent being green (26%), brown (20%), and red
(17%). Mean polyp density per colony varied between
0.36 and 1.99 polyps cm–2 colony area.
12
No gonads
d
Sampled population
18
O N D D- J
J
b
Results
Percent of cysts
Number of colonies
a
mental and reproductive data were compared graphically to reveal
possible relationships.
1.5
1.0
0.5
0
Male
100
80
60
40
20
0
0.4
O N D D- J
J
F M A M J
J
A S O
O N D D- J
J
1990
F M A M J
J
A S O
0.3
0.2
0.1
0
O N D D- J
J
1990
F M A M J
J
A S O
1991
1991
Month sampled (on day of full-moon)/year
Fig. 2 Montastrea cavernosa. Gametogenic cycle based on histological preparations from samples collected on days of full-moon between
October 1990 and October 1991. a Distribution of sexes; b, c percent
female eggs and percent male spermatic cysts, respectively, in each
developmental stage (h Stage I; n Stage II; s Stage III); d, e gonad
index of females and males, respectively. b, c means per colony; d, e
means (± SE)
144
Gametogenic cycle
There was one gametogenic cycle per year in both sexes.
The sampling period spanned the end of one cycle and
another complete cycle. The duration of the oogenic
cycle was F11 months. It began within 1 mo after the
last possible spawning episode, since of the colonies with
gonads sampled in November 1990, all female eggs were
already in Stage I (Fig. 2b). Development of eggs to
Stage II (yolk comprising up to 50% of the cytoplasm)
was evident in late December 1990 to early January 1991,
and development of Stage III eggs began in March 1991.
A marked increase in the mean gonad index did not
occur until after July 1991 (Fig. 2d).
In contrast, the spermatogenic cycle lasted only 2 to
4 mo. Male gonads, first evident in October and November 1990, disappeared until the full moon of June
(Fig. 2a), when testes with most spermatic cysts in
Stage I were observed (Fig. 2c). Stages II and III cysts
were evident from the beginning of the cycle, but the
latter constituted a large percent of the sex products only
after August 1991 (Fig. 2c). The mean gonad index increased from June through October (Fig. 2e). By and
after the full moon of October 1990 and 1991, most cysts
of male colonies were in Stage III.
gonad and 34 ± 5 gonads per polyp, data not shown),
resulting in a gonad index of 2.90 ± 0.97 mm3 eggs cm)2
tissue. On average, spermatic cysts of fully mature males
were smaller in diameter (109 ± 12 lm), and present in
greater numbers per polyp (364 ± 98; 12 ± 1.4 cysts per
gonad and 31 ± 7 gonad per polyp, data not shown),
resulting in a lower gonad index (0.32 ± 0.16 mm3 cysts
cm)1 tissue) than females. Thus, males allocated a lower
amount of biomass to reproduction. The timing of
maximum gonad development was the same for both
sexes, but the gonad index was greater for females than
for males (cf. Fig. 2d, e).
Spawning
The mean reproductive characteristics associated with
gonad maturation are given in Table 1. On average, eggs
of a fully mature colony were 346 ± 17 lm in diameter
and numbered 103 ± 24 per polyp (3 ± 0.5 eggs per
Spawning did not occur synchronously within the population, since maturing, fully mature and spawned colonies were found simultaneously on several sampling
dates (Table 2). In 1990, female spawning may have still
ocurred after the full moon of October (two fully mature, two spawned, Table 2), but not in November (all
with eggs in Stage I, initiating a new cycle). Fully mature
male colonies were also observed in October (five fully
mature, four spawned, Table 2), and spawning may
have still ocurred in November (a single colony with
large cysts was either still finishing maturation, or had
partially spawned: Table 2).
In 1991, all female spawning occurred after the full
moon of August (all still maturing: Table 2) and before
the full moon of October (all spawned). For males there
was no evidence of spawning before the full moon of
September (none spawned: Table 2), and there could
Table 1 Montastrea cavernosa. Reproductive characteristics of
maturing, fully mature, and spawned colonies sampled on/around
14 full-moon days between October 1990 and October 1991; for
criteria used to classify these categories, see ‘‘Materials and methods – Histological processing’’. Data are means ± SD (min.–
max.) for all colonies found in each category. Number of sex
products (eggs/cysts) are mean per-colony totals found in 1 to 3
(usually 3) polyps examined (n no. of colonies examined). Gonad
index calculated as volume of sex products per unit area of live
tissue
Reproductive characteristics of fully mature colonies
Variable
Female
Male
Maturing
Fully mature
Spawned
Maturing
Fully mature
Spawned
(n)
(93)
(8)
(8)
(31)
(10)
(5)
Egg/cyst diam (lm)
120 ± 63
(27–316)
346 ± 17
(320–379)
311 ± 55
(248–408)
66 ± 38
(20–152)
109 ± 12
(90–125)
112 ± 22
(78–135)
No. of eggs/cysts
per polyp
55 ± 31
(1–176)
103 ± 24
(62–139)
16 ± 21
(1–48)
116 ± 129
(3–388)
364 ± 98
(224–504)
100 ± 56
(1–138)
Gonad index
(mm3 eggs/cysts
cm–2 tissue)
0.13 ± 0.27
(0–1.86)
2.90 ± 0.97
(1.51–4.11)
0.57 ± 1.13
(0.02–3.30)
0.06 ± 0.11
(0–0.33)
0.32 ± 0.16
(0.09–0.59)
0.10 ± 0.08
(0–0.18)
Eggs/cysts in Stage I
10 ± 11
(0–52)
10 ± 11
(0–39)
12 ± 16
(0–58)
0
0
1±1
(0–2)
66 ± 12
(50–94)
0
24 ± 34
(0–140)
22 ± 58
(0–272)
19 ± 43
(0–149)
1±2
(0–6)
0
(0–1)
270 ± 55
(203–351)
1±1
(0–3)
3±3
(0–7)
76 ± 43
(0–109)
Stage II
Stage III
9 ± 11
(1–34)
145
Table 2 Montastrea cavernosa. Occurrence of maturing, fully mature and spawned colonies in 1990 and 1991 (other sampling months not
included because only quiescent and maturing colonies were found)
Sex
Sampling date/category
4 October
1990
2 November
1990
25 to 27
August
1991
23 and 24
September 1991
20 and 21
October 1991
Maturing Fully Spawned
mature
Maturing Spawned
Maturing
Maturing Fully
mature
Maturing Fully Spawned
mature
Females
0
2
2
9a
0
7
4b
6
0
0
6
Males
3
5
4
1c
0
8
4
2
2
3
1
Colonies
without gonads
d
7
e
1
4d
a
All just beginning oogenesis; assumed to have recently spawned
One was just beginning oogenesis; it was assumed to have recently spawned
c
Relatively low number of Stage III cysts (98) as if it had partially spawned, but several (41) Stage I cysts still present as if still maturing
d
Either females or males that had probably spawned completely and had not yet begun a new gametogenic cycle
e
Probably a still quiescent male (most males sampled were still in Stage I), but could have been female that had spawned completely (all
females sampled were in Stage III)
b
have been spawning after the full moon of October (in
the 20 and 21 October sample, only 1 of 6 colonies had
spawned).
Some of the females and males assumed to have
spawned were found with a number of Stage III eggs (up
to 34) or cysts (up to 109) (Table 1), perhaps indicating
that a single colony can spawn in several episodes
throughout the spawning period.
and outwelling season in the area (Fig. 3c; although
1991 was drier than average, continental runoff from the
mainland watersheds occurred), when surface temperatures were high (Fig. 3b) and salinities low (Fig. 3a).
Spawning in 1991 began when temperatures were still
rising and salinities falling, after the full moon of August, ending in 1990 when sea-water temperatures were
highest and salinities lowest.
Sex ratio
Discussion
One-hundred and nine female (50.5%), 46 male (21.3%)
and 61 (28.2%) colonies without gonads were sampled.
The observation that the smallest sampled colony
(20 cm) was female, and that female gonads began developing soon after spawning while male colonies appeared only later (Fig. 2a), led us to assume that most, if
not all, colonies without gonads were males. The possible exceptions to this were seven colonies without gonads
collected on 2 November 1990, one in the period 25 to 27
August 1991, and four in the period 20 to 21 October
1991 (Table 2), which may have been completely
spawned colonies of either sex. With this assumption and
subtracting the exceptions, the sex ratio was 109 females
(53.4%) to 95 males (46.6%), which was not significantly
skewed towards any sex (v2 = 0.96, p = 0.33).
Our study confirmed the findings of Soong (1991) and
Szmant (1991) that Montastrea cavernosa is a gonochoric species. Earlier reports (i.e. Gardiner 1902; Abe
1937; Szmant et al. 1983) had suggested that the species
is hermaphroditic.
The spermatogenic cycle of Montastrea cavernosa at
Santa Marta began after full moon in June 1991, while
at Puerto Rico in 1983 it began in April and May
(Szmant 1991). In contrast, Soong (1991) found early
stages of spermatic cysts at Panamá in December 1987.
These timing differences may be due to variation in the
criteria used to recognize the first stages of spermatogenesis. Nevertheless, relatively lower sea-water temperatures during the first half of the year both at Puerto
Rico (18° N, ca. ≥ 24 °C: data from Van Veghel 1994)
and Santa Marta (11° N; ca. ≥24 °C, due to upwelling)
than at Panamá (ca. 10° N; >26 °C, with highest temperatures around May: data from Keller and Jackson
1993), may be responsible for the differences. Furthermore, at Santa Marta, an increase from almost zero in
the rate of egg and cyst maturation (as measured by the
gonad index and its component variables, e.g. sexproduct quantity and diameter) was associated with an
increase in mean sea-water temperature after June.
Temperature controls coral gametogenic cycles and the
Relationship of reproductive characteristics
with environmental variables
Gonad maturation in both sexes (Fig. 2d, e) increased
with increasing temperature after the full moon of July
1990 (Fig. 3b). This increase also occurred when the
photoperiod began to shorten after the summer solstice
(Fig. 3d). Spawning took place during the main rainy
146
Salinity (‰)
a
Temperature (°C)
b
Rainfall (mm)
c
36
35
34
33
32
31
30
29
28
30
29
28
27
26
25
24
23
300
250
200
150
100
50
0
Photoperiod (h)
d 13:00
12:45
12:30
12:15
12:00
11:45
11:30
11:15
O N D D- J F M A M J J A S O
J
1990
1991
Month sampled (on day of full-moon)/year
Fig. 3 Surface salinity, surface temperature, and rainfall at Punta de
Betı́n, Santa Marta Bay, and photoperiod at nearby city of
Barranquilla. Mean (a, b) and total (c) weekday readings during
lunar month immediately preceding sampling date (full-moon); d data
for days of full-moon
periods of gamete or planulae liberation in many other
coral species (Kojis and Quinn 1981; Van Moorsel 1983;
Willis et al. 1985).
The onset of female gametogenesis in Montastrea
cavernosa and the reproductive characteristics of fully
mature females at Santa Marta were similar to those
reported for Puerto Rico (Szmant 1986, 1991) and Panamá (Soong 1991). Egg diameter (mean = 346 ± 18 lm
at Santa Marta vs 350 lm at Puerto Rico; 600 lm eggs
were reported from Panamá, but these were measured
under a dissecting microscope) and number of gonads
per polyp (34 ± 5 vs 24 at Puerto Rico and Panamá)
were similar, but the number of eggs per gonad was remarkably lower at Santa Marta (3 ± 0.5 vs 12 at Puerto
Rico and 10 to 20 at Panamá), resulting in a much lower
gonad index at Santa Marta (2.90 ± 0.97 mm3 cm–1 vs
12.94 mm3 cm–1 at Puerto Rico). As temperatures tend
to be as low at Puerto Rico as at Santa Marta during the
first half of the year, this difference might be due to the
stress of exposure to high turbidity and lower salinity
associated with outwelling during the rainy season at
Santa Marta (Zea 1994). The reproductive tissue biomass of other coral species is lower under conditions of
eutrophication (Tomascik and Sander 1987) and after
exposure to oil (Guzmán and Holst 1993).
This is the first study to examine the reproductive
characteristics of male Montastrea cavernosa. Sex-related similarities in the timing and differences in the rates
of biomass allocation to reproduction evident from our
data, may have ecological implications. Szmant (1991)
found that presumed differential energy expenses between sexes led to no differences in skeletal banding
patterns in M. cavernosa. In contrast, Ward (1995)
found faster growth rates and greater lipid storage after
reproduction in coral colonies of Pocillopora damicornis
that produced only sperm than in those that formed
both ova and sperm and brooded larvae.
As for most broadcasting species, Montastrea cavernosa has a single gametogenic cycle per year. However, its oogenic cycle contrasts strongly with that of
M. annularis, which lasts only 4 mo (Szmant 1991). This
longer period may permits a greater investment in the
quality and quantity of egg energy, producing a larger
egg (mean of fully mature colonies = 350 lm ± 120 lm
in M. cavernosa vs 300 lm in M. annularis: cf. Szmant
1986), which could increase survival time of the larvae
and, hence, enhance the dispersal potential.
Histological evidence of spawning in Montastrea cavernosa at Santa Marta corroborates simultaneous field
observations of its occurrence in the north-east Gulf of
Mexico after the full moon of September 1990 (Gittings
et al. 1992), and at Curaçao after the full moons of
August and September 1991 (Van Veghel 1993). Thus,
there is a common annual breeding period for this species over great latitudinal distances. Similar sea-water
temperatures throughout the Caribbean Sea were postulated as the causal mechanism (Steiner 1995). However, at Santa Marta there was some evidence for an
additional spawning episode in M. cavernosa after the
full moons of October 1990 and 1991. There was also a
delay of one lunar month at Curaçao in the spawning of
the M. annularis species complex (full moons of September and October) compared to localities further
north (full moons of July to September: Van Veghel
1994). The extended spawning period in M. cavernosa
may have been associated with the 1 to 2 month delay in
the occurrence of the annual maximum temperature in
near-equatorial latitudes such as Curaçao and Santa
Marta as a consequence of a reduction in the effective
solar energy in June (Van Veghel 1994). Indeed, coral
mass-spawning takes place in many areas when seawater temperature is at its highest (Babcock et al. 1986).
Besides temperature and related physical–chemical
variables, photoperiod may serve as an additional cue
for the onset and progress of reproductive activities
(Giese and Kanatani 1987). At higher tropical latitudes
where photoperiod may vary by ≥3 h, its increase as the
summer progresses has been associated with the onset of
reproductive activities in a marine gastropod mollusk
147
(Stoner et al. 1992). At Santa Marta, where photoperiod
changes by little more than 1 h, most of the volume of
female and male sex products of Montastrea cavernosa
was formed after the summer solstice, when daylength
started to decrease. Since there are no available data on
seasonal progress in the quantity of reproductive tissues
at other localities to compare with ours, it is not clear
whether such a small change in photoperiod can constitute an effective cue to reproductive activities. Perhaps
the more prolonged spawning season at Curaçao and
Santa Marta discussed above is due to a lower degree of
synchronization with photoperiod by colonies in these
areas than by colonies farther north.
Gonad development was asynchronous between and
within sexes in Montastrea cavernosa at Santa Marta as
well as at Puerto Rico (Szmant 1991). It was also apparent that only part of the colonies was engaged in
reproduction, and not all gametes were shed during a
given spawning episode. This strategy of partial shedding of gametes has been observed in some other gonochoric coral species (see review in Harrison and
Wallace 1990), and may serve to increase the probability
of overall cross-fertilization, especially if neighboring
colonies spawn synchronously and repeatedly throughout the season.
In Montastrea cavernosa there is no sex change and
there is no permanent sterility (Szmant 1991). This further supports our assumption that most colonies without
gonads were quiescent males, and our finding of a 1:1 sex
ratio at Santa Marta reefs (n = 204). At Panamá, the sex
ratio was 1:1 (n = 104), not counting infertile colonies,
but males could be sexed shortly after the spawning
season (Soong 1991). At Puerto Rico, sex ratio was originally 1:1, not counting infertile colonies (Szmant 1986),
but in a more recent sampling it was 1:2.4 (n = 140),
biased towards females (Szmant 1991). Perhaps, as in our
case, the sample contained colonies without gonads that
were quiescent males, since primary spermatocytes began
to appear in Puerto Rico around April and May, almost
as late as at Santa Marta. Thus, sex in M. cavernosa may
be determined genetically, due to the consistency of a 1:1
sex ratio across areas with different environmental conditions. This sex ratio would maximize the probability of
cross-fertilization in a gonochoric, broadcasting species
of high localized abundance. The latter is true for M.
cavernosa at Santa Marta (e.g. Zea 1993a, 1994) and
elsewhere (e.g. Liddell and Ohlhorst 1989).
The adaptive value of spawning by Montastrea cavernosa during the height of the rainy season at Santa
Marta may be related, as in the Red Sea (cf. Shlesinger
and Loya 1985), to an associated decrease in algal cover
and biomass (see Bula-Meyer 1990), thus enhancing the
availability of settling space for the coral larvae and
reducing for the newly settled young the likelihood of
competitive smothering. Also, it may be related to an
increase in suspended organic matter due to outwelling,
providing food for the young. Although very few recently settled corals were observed in the study area, it is
known that recruitment peaks at the height of the rainy
season in other groups of sessile invertebrates (cf. Garcı́a
and Salzwedel 1993; Zea 1993b).
Montastrea cavernosa contrasts with its congeners of
the M. annularis species complex (Szmant 1985, 1991;
Soong 1991; Van Veghel 1994), and with the majority of
species within the family Faviidae (Harrison 1985; Harrison and Wallace 1990) in being gonochoric. This points
toward a secondarily derived, adaptive change from simultaneous hermaphroditism to gonochorism in M. cavernosa. However, an examination of phylogenetic
relationships within the family has not been made to
confirm the direction of change. Contrasting breeding
systems have been reported for five genera of corals, including Montastrea, Siderastrea and Porites in the Caribbean (Szmant 1986; Tomascik and Sander 1987; see
review in Soong 1991). In broadcast spawners, gonochorism would be successful if the within-habitat sexratio is close to unity, if within-habitat abundance is high
enough, and/or if gamete broadcasting and dispersal
strategies are such as to guarantee cross-fertilization
(Williams 1975; Maynard-Smith 1978). As shown above,
these conditions are met by M. cavernosa with its balanced
sex ratio, its high, localized abundance, and its strategy of
partial shedding of gametes, synchronized by lunar phase.
Acknowledgements This paper includes portions of a thesis submitted by A. Acosta in partial fulfillment of the M.Sc. degree at the
Universidad Nacional de Colombia Graduate Program in Marine
Biology. The program is a joint project of the "Instituto Colombiano para el Desarrollo de la Ciencia y la Tecnologia ‘Francisco José de Caldas’" (COLCIENCIAS) and INVEMAR.
Financial support was received from COLCIENCIAS (Co–2105–
09–013–91), the "Comité de Investigaciones y Desarrollo Cientı́fico" of the Universidad Nacional de Colombia (803030), INVEMAR, and the Smithsonian Tropical Research Institute. We
thank I. Holst, H. Guzmán and N. Knowlton (Smithsonian), A.
Szmant (University of Miami), M. Van Veghel (Caribbean Marine
Biological Institute, Curaçao), L. Botero (INVEMAR), J.R.
Morales (COLCIENCIAS, Bogotá), H. Sánchez (CORPAMAG,
Santa Marta) and H. de Bonilla (Universidad Nacional, Bogotá)
for their help during the different stages of this research. S. Fowler
(International Atomic Energy Agency, Monaco) reviewed the
manuscript. An anonymous reviewer pointed out important details
that greatly helped improve the manuscript.
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