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Sexual reproduction of the reef-building coral Diploria labyrinthiformis (scleractinia: Faviidae), in the Colombian Caribbean.


La reproduccion sexual del coral Diploria labyrinthiformis fue estudiada por primera vez. Analisis histologicos mensuales de muestras de D. labyrinthiformis extraidas en el Parque Nacional Natural Corales del Rosario (Caribe colombiano) entre mayo de 1997 a abril de 1998, muestran que es una especie hermafrodita, liberadora de gametos. Presenta un ciclo gametogenico anual de 10-11 meses para inversion en gonadas, en el cual la oogenesis comienza en agosto y termina en mayo-junio. La espermatogenesis es corta, ya que los paquetes espermaticos solo fueron observados en muestras de tejido del mes de mayo. En las muestras histologicas de mayo, un promedio de cuatro huevos maduros y seis paquetes espermaticos por mesenterio fertil fueron encontrados. El diametro promedio de los huevos fue de 297 [micron]m ([+ o -] 97 DS) y de 90 [micron]m ([+ o -] 33) para los paquetes espermaticos. La rapida maduracion de los huevos del estadio II al III coincidio con aumentos en la temperatura del aire, mayor numero de horas de sol por mes, disminucion en la velocidad del viento y ausencia de lluvias. El esfuerzo reproductivo de esta especie (14.07 [mm.sup.3]/[cm.sup.2]/ano) fue similar al de otras especies de Faviidae. Aunque la liberacion de gametos no fue observada en el campo, la ausencia de gonadas en las muestras histologicas del mes de junio sugieren que la liberacion ocurrio entre el 25 de mayo (cinco dias despues de luna llena) y el 24 de junio. Este evento coincidio con altas temperaturas del aire, bajas velocidades del viento y la iniciacion de la epoca lluviosa. El tiempo de liberacion de gametos en esta especie difiere de otras de la misma familia, conocidas para la region del Caribe.

Palabras clave: Diploria labyrinthiformis, reproduccion, gametogenesis, arrecifes coralinos, Caribe, Colombia.

Abstract: Sexual reproduction of the coral Diploria labyrinthiformis was studied for the first time. Monthly histological analyses at the Corales del Rosario National Park (Colombian Caribbean) from May 1997 to April 1998 show that D. labyrinthiformis is a hermaphroditic broadcasting species. It presents an annual gametogenic cycle with a 10-11 month period for gonad investment, in which oogenesis begins in August and ends in May-June. Spermiogenesis is short because sperm cysts were only observed in May tissue samples. In histological collected in May, an average of four mature eggs and six spermatic cysts per fertile mesentery were found. The mean diameter of mature eggs was 297 [micron]m ([+ o -] 97 SD) and 90 [micron]m ([+ o -] 33) for spermatic cysts. Rapid maturation of eggs from stage II to stage III coincides with increases in air temperature, high number of solar hours per month, decreases in wind velocity and absence of rainfall. Reproductive effort for D. labyrinthiformis (14.07 [mm.sup.3]/[cm.sup.2]/year) was similar to other Faviidae species. Although gamete release was not observed in the field, the absence of gonads in histological samples in June suggests spawning between May 25 (five days after full moon) and June 24. This event coincides with high air temperature, low number of solar hours per month, low wind velocity, and initiation of the rainy season. The earlier spawning time of this species differs from other species of the same family known for the Caribbean region. Rev. Biol. Trop. 52(4): 859-868. Epub 2005 Jun 24.

Key words: Diploria labyrinthiformis, coral reproduction, gametogenesis, Caribbean coral reefs, Colombia.


Studies on sexual reproduction of hermatypic corals have increased during the last two decades, with information of about 30% of the known species currently available. From 91 species of Faviidae within the Indo-Pacific region, information of only 40 species is known (Kojis and Quinn 1982, Harriot 1983, Harrison and Wallace 1990) and from 17 species of the Caribbean region, no more than eight species have been studied (Szmant 1986, Soong 1991, Acosta and Zea 1997).

Faviid species are mainly hermaphroditic and present gonads developing as local thickenings of the mesentery, in contrast with those of Pocilloporidae, which are connected by a short stalk to the mesenteries and projected into the body cavity (Rinkevich and Loya 1979) or those of Siderastrea siderea, which are attached to the mesenterial filaments (Alvarado and Guzman unpublished). In the Colombian Caribbean, information on the reproductive biology of corals is available for the following species: Porites porites (Hernandez and Manrique 1991), Acropora palmata (Garcia 1994), Acropora cervicornis (Sanjuan 1995), Tubastrea coccinea (Uscategui 1996) and Montastraea cavernosa (Acosta 1992, Acosta and Zea 1997) as well as on spawning season of Montastraea annularis and M. faveolata (Sanchez et al. 1999).

Diploria labyrinthiformis is a common species of the coral community in some areas of the Caribbean region and yet its reproductive biology is, so far, unknown. Previous studies on reproductive characteristics of Diploria strigosa (Wyers 1985, Szmant 1986, Wyers et al. 1991, Soong 1991) and Diploria clivosa (Soong 1991) document traits within the genus, such as reproductive patterns, gonadal arrangement, number of eggs per ovary, and size and shape of eggs. Gametogenic cycle of D. strigosa and spawning observations of D. strigosa and D. clivosa indicates a 9-10 month cycle with spawning occurring during the warmest season (July-September) synchronized with other faviid species. The only information we found in the literature is the release of traces of eggs from two colonies of D. labyrinthiformis in laboratory conditions, during late July (Wyers et al. 1991).

The present paper describes, for the first time, the reproductive pattern, mode of development, gametogenic cycle, gonadal arrangement, egg size, number of eggs per gonad, and reproductive effort of D. labyrinthiformis. These sexual characteristics were related to abiotic factors as well as compared with other species within the genus.


The study was carried out at the Isla Grande coral reef (Caribbean coast of Colombia), between May 1997 and April 1998. This island forms part of the Parque Nacional Natural Corales del Rosario, which is located between 10[grados]08'-10[grados]26, N and 75[grados]30'-75[grados]48, W (Fig. 1). The area lies within the Intertropical Convergence Zone, under trade winds that alternate from northwest to southeast. Three climatic seasons have been described for the area, a dry season, occurring between December and April and dominated by the Alisios winds; an intermediate season (mild rainfall) between May and July; and a rainy season (heavy rainfall), which occurs between August and November (Leble and Cuignon 1987). The annual average for seawater temperature is 27.5[grados]C; precipitation is 1 013.1 mm and salinity 35 [por millar] (Sanchez 1999).

Due to legal restrictions within the Protected Area, only three colonies per month were sampled. Each month, 5 days after full moon, two samples of 2.5 cm in diameter, per colony, were extracted from the center of three different colonies, located at depths of 7-12 m. These were fixed in Zenker solution for 24 hours, washed in running tap water for 24 hours and stored in 70% ethanol (Acosta and Zea 1997), until histological procedures. Tissue samples were dehydrated in alcohol and xylene series, embedded in Paraplast and serially sectioned at 6 pm. Sections, taken every 200-250 [micron]m, were stained with Heidenmhain's Azocarmine Aniline Blue (Luna 1968, Acosta and Zea 1997). Seven to nine slides with 4-8 sections each, and 20-56 mesenteries per section, were observed for each colony under light microscope. The slide containing the most reproductive material was used to estimate a) number of fertile mesenteries, b) total number of eggs and sperm cysts (Guzman and Holts 1993), and c) size and stage of these gametes. Since there is not a clear polyp differentiation in this species, all information is referred to area, where 1 [cm.sup.2] contains 12 to 15 mesenteries.

A number of 220 complete eggs were observed in order to define different development stages based on descriptions for other species (Wyers 1985, Delvoye 1988, Acosta 1992, Glynn et al. 1994, 1996). Three stages for oogenesis were defined using the following characteristics: l) presence of single mesogleal layer surrounding the egg; 2) presence and thickness of basal membrane surrounding the egg; 3) presence of cytoplasmatic material inside the egg (scarce or abundant cytoplasmatic material); 4) presence of vesicular cytoplasmatic inclusions (few or high--giving the egg a bubbly appearance); 5) maximum length of eggs using an ocular micrometer (Olympus, OSM-4, 10 X).

Reproductive effort was calculated with a modification of the Gonadal Index used by Szmant (1986): number of mesenteries per [cm.sup.2] x number of gonads per mesentery x maximum number of eggs per gonad x volume of eggs per [mm.sup.3] x number of cycles per year. The volume was calculated using the formula: V = 4/3[pi][r.sup.3].

Sunlight, air temperature, rainfall and wind velocity data for the study period (May 1997-April 1998) was provided by the Centro de Investigaciones Oceanograficas e Hidrograficas (CIOH) for two near-by sites (airport and Escuela Naval) (Fig. 1).


Diploria labyrinthiformis is a hermaphroditic broadcasting species with eggs and spermatic cysts within each mesentery (Fig. 2A). Eggs and spermatic cysts are located towards the aboral part of the mesentery (Fig. 2B). This species displays ah annual game-togenic cycle in which oogenesis begins in August and ends between May and June (Fig. 3). Spermiogenesis is short, since sperm cysts were observed only in tissue samples from May. Nevertheless, our observations suggest synchronous maturation between eggs and sperm cysts during May.

Oogenesis: Stage I oocytes were small, ovoid or rounded and the main characteristic was the presence of a thin, bluish-transparent mesogleal layer surrounding the egg (Fig. 2C). Cytoplasmatic material was absent (12%), scarce (86%), or abundant (2%). Mean diameter ofoocytes was 116.1 [micron]m ([+ o -] 36.5 S.D.), and range from 53.9 to 213.0 [micron]m (n = 44 oocytes). This stage was observed from August to April, with a peak in December (Fig. 3A).

Stage II oocytes were also small, ovoid or rounded (Fig. 2D), but with a basal membrane that thickened from November (11 [micron]m) to April (33 [micron]m). The majority had scarce cytoplasmatic material (67%), and the rest had either few vesicular cytoplasmatic inclusions or were empty. Mean oocyte diameter was 150.4 [micron]m ([+ o -] 32.6), and range from 57.7 to 209.6 [micron]m (n = 55 oocytes). This stage was observed from November to April, with a peak in March (Fig. 3B).

Stage III oocytes were enlarged, ovoid or irregular, with a well-defined basal membrane and with high vesicular cytoplasmatic inclusions giving them a bubbly appearance (Fig. 2E). Mean diameter was 297.2 [micron]m ([+ o -] 96.9), and range from 73.5 to 584.3 [micron]m (n = 121 oocytes). Mature eggs were only found in May (Fig. 3C).

In samples of June and July no eggs were found. This suggests that D. labyrinthiformis may have spawned between May 25 and June 24. Thus, this species has an annual reproductive cycle with a 10-11 months period for gonad investment.

Spermiogenesis: In May, spermatic cysts were only present on 85% of the mesenteries. In no case they were observed without eggs in the same mesentery, which confirms a hermaphroditic pattern. An average of six cysts per fertile mesentery were found, with a mean diameter of 90.1 [micron]m (+ 32.9), and range from 27.5 to 220.5 [micron]m, (n = 160 cysts). Cysts showed either dense (45%) or scarce (55%) cellular material (Fig. 2F).

Reproductive effort: On the total mesenteries observed (n = 705) for the one-year study period, 16% were fertile (n = 114), with 379 eggs and 208 spermatic cysts (complete and incomplete). The highest percentage of mature mesenteries was found in May (42%), bearing an average of four eggs per mesentery (range: 1-9; 21 per [cm.sup.2]) and six spermatic cysts per mesentery (range: 1-10; 21 cysts per [cm.sup.2]). The reproductive effort estimated by the gonad index obtained from mature eggs was 14.07 [mm.sup.3]/[cm.sup.2]/year (Table 1).


Reproductive type (hermaphroditic), mode of development (broadcaster), gonadal arrangement (oocytes and spermatic cysts in the same mesentery), oocyte mean size and shape, number of eggs per mesentery as well as duration of oogenesis seem to be conservative characteristics within any genus (Soong 1991) (Table 2). The similarity in the reproductive effort between the Faviidae species (Table 1) and particularly for D. labyrinthiformis (this study) and D. strigosa (Wyers 1985) further supports Soong's hypothesis.

Although the length of the oogenic cycle (10 months) is similar between D. labyrinthiformis and D. strigosa, the initiation of oogenesis and spawning month differs between the two species. These events occur earlier for D. labyrinthiformis populations in Colombia than for its congeneric species in Bermuda (Wyers 1985) and Puerto Rico (Szmant 1986) (Table 2). Gametogenesis and spawning differences for the same species have been attributed to latitude (Szmant 1986, Soong 1991, Van Veghel 1994, Acosta and Zea 1997, Knowlton et al. 1997), temperature, day length or both (Babcock 1995, Fan and Dai 1995, Fadlallah 1996, Ben-David-Zaslow et al. 1999), solar energy (Van Veghel 1994), current and winds regimes (Babcock et al. 1986) and rainfall (Acosta and Zea 1997).

The first visible egg in D. labyrinthiformis was found during August; while most stage I oocytes were found during October and November, which in Colombia coincides with the highest temperature (Fig. 4A). Rapid maturation of eggs (Stage II to Stage III) coincides with highest number of solar hours per month (Fig 4B) and rising temperatures, which happens during the dry season. Spawning occurs during June when wind velocity is lowest (Fig. 4C), and temperature is high. Thus, initiation and maturation of oocytes coincides with environmental conditions reported for species of the same family, by other authors for the Caribbean region (Szmant 1986, Soong 1991, Wyers et al. 1991, Van Veghel 1994, Acosta and Zea 1997, Sanchez et al. 1999). Nevertheless, gamete release does not occur during the months when most spawning events, known at low latitudes, take place (August-October) (Guzman and Holts 1993, Van Veghel 1994, Acosta and Zea 1997, Sanchez et al. 1999).


It is worthwhile noting that temperature range for the Caribbean region is 3.2[grados]C (Szmant 1986) and for Colombia, during the period studied, the temperature did not vary more than 1[grados]C (27.8[grados]C [+ or -] 0.4; 28.4[grados]C [+ or -] 0.21). As has been noted by other authors, rising temperatures might cue the initiation of gametogenesis in broadcasters, but gamete release is controlled by other factors such as photoperiod (Soong 1991, Szmant 1991), low tides (Kojis and Quinn 1981), low current regimes (Babcock et al. 1986), low winds and scarce rainfall (Watson et al. 2000). In accordance, Bassim et al. (2002) states that the effects of high seawater temperature do not affect fertilization rates of D. strigosa; while embryonic development and larval viability decrease dramatically where abnormally high sea surface temperatures occur during the spawning season.

The adaptive value of spawning in late May and early June for D. labyrinthiformis, may be related to appropriate settling space (Fan and Dai 1995), associated with reduction in algae cover caused by local conditions (Soong 1991, pers. obs. in the studied area) or low current regimes and low winds which may ensure that egg clumps will not be carried out by currents and thus, favor high rates of fertilization (Kojis and Quinn 1981), which are the environmental conditions at the study site during these months. Timing of reproduction is of taxonomic significance and may reflect species recognition problems within a group (Johnson 1992). Therefore, the difference in timing of gametogenic cycle in D. labyrinthiformis may represent a mechanism of reproductive isolation to prevent hybridization and maintain species boundaries within the genus (Miller and Babcock 1997), or a strategy for self fertilization, as has been reported for D. strigosa (Hagman et al. 1998). Finally, but not least, it is possible that the effects of El Nino event, which was present during 1997, could have affected the cycle of gametogenesis and hence, spawning. But even then, it remains unclear why this event should have affected this species and not others in the same site as M. annularis and M. faveolata that spawned during September and October (Sanchez et al. 1999), as has been reported through out the Tropical Caribbean region.


This work is part of the project "Reproduction, growth and transplantation survivorship of the coral species Montastraea annularis, Diploria labyrinthiformis and Porites astreoides in the National Natural Park Corales del Rosario, Colombian Caribbean", (Universidad Jorge Tadeo Lozano and COLCIENCIAS 1202-09-221-96). Research Permission No. 568, 15 de octubre de 1996, Ministerio del Medio Ambiente, Unidad Administrativa Especial del Sistema de Parques Nacionales Naturales. We thank J.A. Sanchez, O. Arenas, H. Charry, M. Gil and L. Chasqui, for their assistance during the whole course ofthis study. Also to Sport Baru, Centro de Investigaciones Oceanograficas e Hidrograficas (CIOH), ECOBUZOS and all those who helped in field or laboratory, as well as those who gave us logistic facilities in different phases of the research. We thank M. Zea and P. Yoshioka who proofread the English version and A. Acero, J. Cortes, H. Guzman and anonymous reviewers who helped improve the manuscript. Contribution to Marine Science No. 10 of Centro de Investigaciones Cientificas, Universidad de Bogota Jorge Tadeo Lozano.


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Elvira M. Alvarado Ch. (1) Rocio Garcia U. (2) Alberto Acosta (3)

(1) Centro de Investigaciones Cientificas (Museo del Mar), Universidad de Bogota Jorge Tadeo Lozano, Santafe de Bogota, D.C., Colombia. Fax: 57-1-2812840;

(2) Department of Marine Sciences, University of Puerto Rico -- Mayaguez Campus, P.O Box 908, Lajas P.R 00667;

(3) Pontificia Universidad Javeriana, K 7 No 43-82, Ed Carlos Ortiz. Oficina 502, Bogota, Colombia;

Received 26-IV-2002. Corrected 06-I-2003. Accepted 20-II-2003.

Comparison of reproductive effort within corals of Faviidae in the
Caribbean and Indo-Pacific

Region         Species                     Reproductive     Mode of
                                               Type       Development

Caribbean      Diploria labyrinthiformis        H             BC
               Diploria strigosa                H             BC
               Montastraea annularis            H             BC
               Montastraea cavernosa            G             BC
               Montastraea cavernosa            G             BC
               Favia fragum                     H             BR
Indo-Pacific   Platygyra sinensis               H             BC
               Goniastrea favulus               H             BC
               Goniastrea aspera                H             BC
               Favia favus                      G             BC

Region         Species                     Number of     Reproductive
                                            Cycles          Effort

Caribbean      Diploria labyrinthiformis       1             14.07
               Diploria strigosa               1          15.6-18.1
               Montastraea annularis           1             24.5
               Montastraea cavernosa           1             12.9
               Montastraea cavernosa           1              9.28
               Favia fragum                   12             27.4
Indo-Pacific   Platygyra sinensis              1             12.2
               Goniastrea favulus              1             15.3
               Goniastrea aspera               1             22.8
               Favia favus                     1             50

Region         Species                     Reference

Caribbean      Diploria labyrinthiformis   This study
               Diploria strigosa           Wyers (1985)
               Montastraea annularis       Szmant (1986)
               Montastraea cavernosa       Szmant (1986)
               Montastraea cavernosa       Acosta & Zea (1997)
               Favia fragum                Szmant (1986)
Indo-Pacific   Platygyra sinensis          Babcock et al. (1986)
               Goniastrea favulus          Babcock et al.(1986)
               Goniastrea aspera           Babcock et al. (1986)
               Favia favus                 Harriott (1983)

H: Hermaphroditic, G: Gonochoric, BC: Broadcasting, BR: Brooding.


Comparison of reproductive characteristics between species of the
genus Diploria

Species               Location     Latitude     Spawning

D. clivosa            Curazao         12        October
D. clivosa            Panama           9        August-Sept
D. labyrinthiformis   Bermuda         32        July
D. labyrinthiformis   Colombia        11        May/June?
D. strigosa           Bermuda         32        August-Sept
D. strigosa           Pto. Rico       18        August
D. strigosa           Panama           9        August

Species               Gametogenesis    # Eggs/    Egg Size ([micro]m
                                      Mesentery       [+ o -] SD)

D. clivosa            --                 --               --
D. clivosa            --                  6              600D
D. labyrinthiformis   *                   *              400 D
D. labyrinthiformis   Aug-May           4(H)      297 [+ o -] 97 (H)
D. strigosa           Nov-August         10       320 [+ o -] 40-370
                                                    [+ o -] 60 (H)
D. strigosa           Dec-June          8-10            400 (H)
D. strigosa           *                 4-10             600 D

Species               Reference

D. clivosa            Van Veghel 1993
D. clivosa            Soong 1991
D. labyrinthiformis   Wyers et al. 1991
D. labyrinthiformis   This Study
D. strigosa           Wyers 1985
D. strigosa           Szmant 1986
D. strigosa           Soong 1991

H: from histological preparations, D: Disecting microscope, * No data
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Author:Alvarado, Elvira M.; Garcia U., Rocio; Acosta, Alberto
Publication:Revista de Biologia Tropical
Date:Dec 1, 2004
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