Scientia Marina, Vol 74, No 3 (2010)

Reproductive pattern of an exploited dusky grouper Epinephelus marginatus (Lowe 1834) (Pisces: Serranidae) population in the western Mediterranean

Olga Reñones
Centro Oceanográfico de Baleares , Spain

Amalia Grau
LIMIA-D.G. Pesca, Govern de les Illes Balears , Spain

Xavier Mas
Centro Oceanográfico de Baleares , Spain

Francesc Riera
LIMIA-D.G. Pesca, Govern de les Illes Balears , Spain

Fran Saborido-Rey
Institute of Marine Research (CSIC) , Spain


The reproductive parameters of the dusky grouper, Epinephelus marginatus, in the Balearic Islands (western Mediterranean) were studied with a histological analysis of specimens caught by artisanal and recreational spear fisheries. The histological examination of the gonads showed that the dusky grouper spawning season extends from late spring to the end of summer with clear spawning peaks in July and August. The monthly variation of the hepatosomatic index (HSI) and the Le Cren condition index suggests that reserves for gonad development were obtained from the energy stored in the liver before spawning. Females reach maturation at 49 cm total length (TL) and 6 years, and transitional individuals start to occur before all females are matured. Males were the largest and oldest specimens but females were also present in the largest and oldest classes and there was a large sex, size and age overlap in the population. The fecundity data showed that the dusky grouper is a determinate spawner with asynchronous oocyte development. Potential fecundity ranged between 65 thousand and 8 million oocytes in females from 39 to 92 cm TL and from 6 to 42 years of age, with a mean relative fecundity of 334 x 103 oocytes kg-1. Females spawn an average of 10 batches during the spawning season, with a relative batch fecundity of 75 x 103 oocytes kg-1. Fecundity increased significantly with length, weight, age and HSI, while relative fecundity was only related to HSI. Based on the results obtained in the present study (long reproductive lifespan of females, influence of maternal attributes on fecundity and size at maturity) management measures for the species were evaluated.


Epinephelus marginatus; maturity; sex change; spawning; fecundity; Mediterranean

Full Text:



Allain, V. – 2001. Reproductive strategies of three deep-water benthopelagic fishes from the northeast Atlantic Ocean. Fish. Res., 51: 165-176. doi:10.1016/S0165-7836(01)00243-0

Alonso-Fernandez, A., R. Domínguez-Petit, M. Bao, C. Rivas and F. Saborido-Rey. – 2008. Spawning pattern and reproductive strategy of female pouting Trisopterus luscus (Gadidae) on the Galician shelf of north-western Spain. Aquat. Living Resour., 21: 383-393. doi:10.1051/alr:2008059

Berkeley, S.A., M.A. Hixon, R.J. Larson and M.S. Love. – 2004a. Fisheries sustainability via protection of age structure and spatial distribution of fish population. Fisheries, 29: 23-32. doi:10.1577/1548-8446(2004)29[23:FSVPOA]2.0.CO;2

Berkeley, S.A., C. Chapman and S.M. Sogard. – 2004b. Maternal age as a determinant of larval growth and survival in marine fish, Sebastes melanops. Ecology, 85(5): 1258-1264. doi:10.1890/03-0706

Bertoncini, A.A., L.F. Machado, M. Hostim-Silva and J.P. Barreiros. – 2003. Reproductive biology of the dusky grouper Epinephelus marginatus (Lowe, 1834). Bra. Arch. Biol. Technol., 46: 373-381.

Birkeland, C. and P.K. Dayton. – 2005. The importance in fishery management of leaving the big ones. Trends Ecol. Evol., 20(7): 356-358. doi:10.1016/j.tree.2005.03.015

Bouain, A. – 1980. Sexualité et cycle sexuel des mérous (Poissons, Téléostéens, Serranidae) des côtes du sud tunisien. Bull. Off. natn. Pêch. Tunisie, 4(2): 215-229.

Bouain, A. and Y. Siau. – 1983. Observations of the female reproductive cycle and fecundity of three species of groupers (Epinephelus) from the southeast Tunisian seashores. Mar. Biol., 73: 211-220. doi:10.1007/BF00406890

Bruslé, J. – 1985. Expose synoptique des donnés biologiques sur les mérous Epinephelus aeneus (Geoffroy Saint Hilaire, 1809) et Epinephelus guaza (Linnaeus, 1758) de l’océan Atlantique et de le Méditerranée. FAO Synopsis sur les pêches, 129: 1-64.

Chauvet, C. – 1988. Etude de la croissance du mérou Epinephelus guaza (Linné, 1758) des côtes tunisiennes. Aquat. Living Resour., 1: 277-288. doi:10.1051/alr:1988027

Coleman, F., C.C. Koenig and A. Collins. – 1996. Reproductive style of shallow-water groupers (Pisces: Serranidae) in the eastern Gulf of Mexico and the consequences of fishing spawning aggregations. Env. Biol. Fish., 47: 129-141. doi:10.1007/BF00005035

Coll, J., A. Garcia-Rubies, J. Moranta, J. Stefanni and B. Morales-Nin. – 1999. Efectes de la prohibició de la pesca esportiva sobre l’estructura poblacional de l’anfós (Epinephelus marginatus Lowe 1834, Pisces: Serranidae) en el Parc Nacional de Cabrera. Boll. Soc. Hist. Nat. Balears, 42: 125-138.

Coll, J., M. Linde, A. Garcia-Rubies, F. Riera and A.M. Grau. – 2004. Spear fishing in the Balearic Islands (west central Mediterranean): species affected and catch evolution during the period 1975-2001. Fish. Res., 70: 97-111. doi:10.1016/j.fishres.2004.05.004

Coll, J., A. Garcia-Rubies, G. Morey, O. Navarro, S. Martino, F. Riera and A.M. Grau. – 2007. The north of Minorca Marine Reserve (W-Mediterranean) as a tool for a suitable management of natural resources. The case of the dusky grouper Epinephelus marginatus (Lowe, 1834). In: P. Francour and J. Gradiot (eds.), Second International Symposium on the Mediterranean Groupers, May 10-13th 2007, pp. 55-58. Nice University Publication, Nice.

Desse, J. and N. Desse-Berset. – 1999. Préhistoire du mérou. Mar. Life, 9(1): 19-30.

Domínguez-Petit, R. – 2007. Study of reproductive potential of Merluccius merluccius in the Galician shelf. Ph.D. thesis, Univ. Vigo.

Fennessy, S.T. – 2006. Reproductive biology and growth of the yellowbelly rockcod Epinephelus marginatus (Serranidae) from South-East Africa. Afr. J. mar. Sci., 28(1): 1-11

Foucher, R.P. and R.J. Beamish. – 1980. Production of nonviable oocytes by pacific hake (Merluccius productus). Can. J. Fish. Aquat. Sci., 37: 41-48. doi:10.1139/f80-004

García-Charton, J.A., A. Perez-Ruzafa, P. Sánchez-Jerez, J.T. Bayle-Sempere, O. Reñones and D. Moreno-Lampreave. – 2004. Multi-scale spatial heterogeneity, habitat structure, and the effect of marine reserves on Western Mediterranean rocky reef fish assemblages. Mar. Biol., 144: 161-182. doi:10.1007/s00227-003-1170-0

Garvey, J.E., T.P. Herra and W.C. Leggett. – 2002. Protracted reproduction in sunfish: the temporal dimension in fish recruitment revisited. Ecol. Appl., 12(1): 194-205. doi:10.1890/1051-0761(2002)012[0194:PRISTT]2.0.CO;2

Grau, A., S. Crespo, F. Riera, S. Pou and M.C. Sarasquete. – 1996. Oogenesis in the amberjack Seriola dumerili Risso, 1810. An histological, histochemical and ultrastructural study of oocyte development. Sci. Mar., 60(2-3): 391-406.

Grau, A., M. Linde and A.M. Grau. – 2009. Reproductive biology of the vulnerable species Sciaena umbra (Pisces, Sciaenidae) Linnaeus, 1758. Sci. Mar., 73(1): 67-81. doi:10.3989/scimar.2009.73n1067

Greer-Walker, M., P.R. Witthames and I. Bautista de los Santos. – 1994. Is the fecundity of the atlantic mackerel (Scomber scombrus: Scombridae) determinate? Sarsia, 79: 13-26.

Gust, N. – 2004. Variation in the population biology of protogynous coral reef fishes over tens of kilometres. Can. J. Fish. Aquat. Sci., 61: 205-218. doi:10.1139/f03-160

Hamilton, S.L., J.E. Caselle, J.D. Standish, D.M. Schroeder, M.S. Love, J. Rosales-Casian and O. Sosa-Nishizaki. – 2007. Size-selective harvesting alters life histories of a temperate sex-changing fish. Ecol. Appl., 17(8): 2268-2280. doi:10.1890/06-1930.1 PMid:18213967

Harmelin, J.G. and M. Harmelin-Vivien. – 1999. A review on habitat, diet and growth of the dusky grouper, Epinephelus marginatus (Lowe, 1834). Mar. Life, 9(2): 11-20.

Harmelin-Vivien, M., J. García-Charton, J. Bayle-Sampere, E. Charbonel, L. Le Diréach, D. Ody, A. Pérez-Ruzafa, O. Reñones, P. Sánchez-Jerez and C. Valle. – 2007. Importance of marine reserves for the population dynamics of groupers (Epinephelidae) in the Western Mediterranean. P. Francour and J. Gradiot (eds.), In: P. Francour and J. Gradiot (eds.), Second International Symposium on the Mediterranean Groupers, May 10-13th 2007, pp. 91-94, Nice University Publication, Nice.

Harris, P.J., D.M. Wyanski, D.B. White and J.L. Moore. – 2002. Age, growth, and reproduction of scamp, Mycteroperca phenax, in the southwestern North Atlantic, 1979-1997. Bull. Mar. Sci., 70(1): 113-132.

Hawkins, J.P. and C.M. Roberts. – 2003. Effects of fishing on sex-changing Caribbean parrotfishes. Biol. Conserv., 115: 213-226. doi:10.1016/S0006-3207(03)00119-8

Heath, M.R. – 1992. Field investigations of the early life stages on marine fish. Adv. Mar. Biol., 28: 1-174. doi:10.1016/S0065-2881(08)60039-5

Heemstra, P. C. and J. E Randall. – 1993. Groupers of the world (Family Serranidae, Subfamily Epinephelidae). An annotated and illustrated catalogue of the grouper, rockcod, hind, coral grouper and lyretail species known. FAO Species catalogue. FAO Fish. Synop., 16(125): 1-382.

Hereu, B., D. Diaz, J. Pascual, M. Zabala and E. Sala. – 2006. Temporal patterns of spawning of the dusky grouper Epinephelus marginatus in relation to environmental factors. Mar. Ecol. Prog. Ser., 325: 187-194. doi:10.3354/meps325187

Hesp, A.A., R.P. Hobbs and I.C. Potter. – 2002. Infection of the gonads of Glaucosoma hebraicum by the nematode Phylometra lateolabracis: occurrence and host response. J. Fish. Biol., 60: 663-673.

Hunter, J.R., B.J. Maciewicz, N.C.H. Lo and C.A. Kimbrell. – 1992. Fecundity, spawning and maturity of female Dover sole, Microstomus pacificus, with an evaluation of assumptions and precision. Fish. Bull. U.S., 90: 101-128.

Hunter, J.R., N.C.H. Lo and H.J Leong. – 1985. Batch fecundity in multiple spawning fishes. In: R. Lasker, (ed.), An Egg Production Method for Estimating Spawning Biomass of Pelagic Fish: Application to the Northern Anchovy, Engraulis mordax. NOAA Tech. Rep. NMFS, 36: 67-77.

Irigoyen, A.J., D.E. Galva and L.A. Venerus. – 2005. Occurrence of dusky grouper Epinephelus marginatus (Lowe, 1834) in gulfs of northern Patagonia, Argentina. J. Fish. Biol., 67: 1741-1745. doi:10.1111/j.1095-8649.2005.00866.x

Kara, M.H. and F. Derbal. – 1999. Données biologiques sur le mérou Epinephelus marginatus (Lowe, 1834) des côtes algériennes. Mar. Life, 9(2): 21-27.

La Mesa, G., A. Longobardi, F. Sacco and G. Marino. – 2008. First release of hatchery juveniles of the dusky grouper Epinephelus marginatus (Lowe, 1834) (Serranidae: Teleostei) at artificial reefs in the Mediterranean: results from a pilot study. Sci. Mar., 72(4): 743-756. doi:10.3989/scimar.2008.72n4743

Lloret, J. and S. Planes. – 2003. Condition, feeding and reproductive potential of white seabream Diplodus sargus as indicators of habitat quality and the effect of reserve protection in the northwestern Mediterranean. Mar. Ecol. Prog. Ser., 248: 197-208. doi:10.3354/meps248197

Mackie, M.C. – 2003. Social induced sex-change in the half-moon grouper, Epinephelus rivulatus, at Ningaloo reef, Western Australia. Coral Reefs, 22: 133-142. doi:10.1007/s00338-003-0296-3

Mallol, S. and R. Goñi. – 2008. Rotación estacional de la pesca artesanal en la reserva marina de Cala Rajada y Llevant de Mallorca: herramientas de protección sobre las especies y hábitats. In: G. X.Pons (edit). V Jornades de Medi Ambient de les Illes Balears. Ponències i Resums, pp. 292. Soc. Hist. Nat. Balears, Palma de Mallorca.

Marino, G., E. Azzurro, A. Massari, G. Finoia and A. Mandich. – 2001. Reproduction in the dusky grouper from the southern Mediterranean. J. Fish. Biol., 58: 909-927. doi:10.1111/j.1095-8649.2001.tb00544.x

Marino, G., E. Panini, A. Longobardi, A. Mandich, M.G. Finoia, Y. Zohar and C.C. Mylonas. – 2003. Induction of ovulation in captive – reared dusky grouper, Epinephelus marginatus (Lowe, 1834), with a sustained –release GnRHa implant. Aquaculture, 219: 841-858. doi:10.1016/S0044-8486(03)00036-X

Marteinsdottir, G. and G.A. Begg. – 2002. Essential relationships incorporating the influence of age, size and condition on variables required for estimation of reproductive potential in Atlantic cod Gadus morhua. Mar. Ecol. Prog. Ser., 235: 235-256. doi:10.3354/meps235235

Moravec, F. and J.L. Justine. – 2005. Two species of Phylometra (Nematoda, Phylometridae) from serranid fishes off New Caledonia. Acta Parasitol., 50(4): 323-331.

Munday, P.L., P.M. Buston and R.R. Warner. – 2006. Diversity and flexibility of sex-change strategies in animals. Trends Ecol. Evol., 21(1): 89-95. doi:10.1016/j.tree.2005.10.020

Muñoz, R.C. and R.R. Warner. – 2003a. Alternative contexts of sex change with social control in the bucktooth parrotfish, Sparisoma radians. Environ. Biol. Fish., 68: 307-319. doi:10.1023/A:1027318422747

Muñoz, R.C. and R.R. Warner. – 2003b. A new version of the size-advantage hypothesis for the sex-change: Incorporating sperm competition and size fecundity skew. Am. Nat., 161: 749-761. doi:10.1086/374345 PMid:12858282

Murua, H. and F. Saborido-Rey. – 2003. Females reproductive strategies of marine fish species of the North Atlantic. J. Northw. Atl. Fish. Sci., 33: 23-31. doi:10.2960/J.v33.a2

Pears, R.J., J.H. Choat, B.D. Mapstone and G.A. Begg. – 2006. Demography of a large grouper, Epinephelus fuscoguttatus, from Australia’s Great Barrier Reef: implications for fishery management. Mar. Ecol. Prog. Ser., 307: 259-272. doi:10.3354/meps307259

Pelaprat, C. – 1999. Observations on the spawning behaviour of the dusky grouper Epinephelus marginatus (Lowe, 1834) in the north of Corsica (France). Mar. Life, 9(1): 59-65.

Reñones, O., R. Goñi, M. Pozo, S. Deudero and J. Moranta. – 1999. Effects of protection on the demographic structure and abundance of Epinephelus marginatus (Lowe, 1834). Evidence from the Cabrera Archipelago National Park (West-Central Mediterranean). Mar. Life, 9(2): 45-53.

Reñones, O. – 2007. Monitoring of groupers in a MPA with fishery management. In: J. García (ed.), Management of habitats and species in Mediterranean Marine Protected Areas, MedPAN Workshop nº7. pp. 15-17, MMA, Palma de Mallorca.

Reñones, O., C. Piñeiro, X. Mas, and R. Goñi. – 2007. Age and growth of the dusky grouper Epinephelus marginatus (Lowe 1834) in an exploited population of the Western Mediterranean. J. Fish. Biol., 71: 346-362. doi:10.1111/j.1095-8649.2007.01482.x

Rhodes, K.L. and Y. Sadovy. – 2002. Temporal and spatial trends in spawning aggregations of camouflage grouper, Epinephelus polyphekadion, in Pohnpei, federated states of Micronesia. Environ. Biol. Fish., 63: 27-39. doi:10.1023/A:1013840621820

Sadovy, Y.A., Rosario and A. Román. – 1994. Reproduction in an aggregating grouper, the red hind Epinephelus guttatus. Environ. Biol. Fish., 41: 269-286.

Sadovy, Y. and P.L. Colin. – 1995. Sexual development and sexuality in the Nassau grouper. J. Fish. Biol., 46: 961-976. doi:10.1111/j.1095-8649.1995.tb01401.x

Sanchez-Lizaso, J.L., R. Goñi, O. Reñones, J.A. García-Charton, R. Galzin, J.T. Bayle, P. Sanchez-Jerez, A. Rérez-Ruzafa and A. Ramos. – 2000. Density dependence in marine protected populations: a review. Environ. Conserv., 27: 144-158. doi:10.1017/S0376892900000187

Shapiro D.Y. – 1987. The reproduction in groupers. In: J.J. Polovina and S. Ralston (eds.), Tropical snappers and groupers: Biology and management of snappers and groupers, pp. 295-327. Westview Press Inc, Boulder, Colorado.

Shapiro, D., Y. Sadovy and M.A. McGehee. – 1993. Periodicity of sex change and reproduction in the red hind, Epinephelus guttatus, a protogynous grouper. Bull. Mar. Sci., 53(3): 1151-1162.

Sparre, P. and S.C. Venema. – 1992. Introduction to tropical fish stock assessment. Part 1 Manual. FAO Fish. Tech. Pap., 306.

Stearns, S.C. and R.E Crandall. – 1984. Plasticity for the age and size at sexual maturity: a life-history response to unavoidable stress. In: G.W. Potts and R.J. Wootton (eds.), Fish Reproductive Strategies and Tactics, pp. 13-30. Academic Press, New York.

Trippel, E.A. – 1995. Age at maturity as a stress indicator in fisheries. BioScience, 45: 759-771. doi:10.2307/1312628

Trippel, E.A. – 1999. Estimation of stock reproductive potential: History and challenges for Canadian Atlantic gadoid stock assessments. J. Northw. Atl. Fish. Sci., 25: 61-81. doi:10.2960/J.v25.a6

Warner, R.R. – 1975. The adaptative significance of sequential hermaphroditism in animals. Am. Nat., 109: 61-82. doi:10.1086/282974

Warner, R.R. – 1988. Sex change and the size advantage model. Trends Ecol. Evol., 3: 133-136. doi:10.1016/0169-5347(88)90176-0

Warner, R.R. and S.E. Swearer. – 1991. Social control of sex change in the bluehead wrasse Thalassoma bifasciatum (Pisces: Labridae). Biol. Bull., 181: 199-204. doi:10.2307/1542090

West, G. 1990. Methods of assessing ovarian development in fishes: a review. Aust. J. Mar. Freshw. Res., 41: 199-222. doi:10.1071/MF9900199

Wilk, S.J., W.W. Morse and L.L. Stehlik. – 1990. Annual cycles of gonado-somatic indices as indicators of spawning activity for selected species of finfish collected from the New York Bight. Fish. Bull., 88: 775-786.

Wootton, R.J. – 1990. Ecology of Teleost Fishes. Chapman and Hall, New York.

Zabala, M., A. García-Rubies, P. Louisy and E. Sala. – 1997a. Spawning behaviour of the Mediterranean dusky grouper Epinephelus marginatus (Lowe, 1834) (Pisces: Serranidae) in the Medes Islands Marine Reserve (NW Mediterranean, Spain). Sci. Mar., 61(1): 65-77.

Zabala, M., P. Louisy, A. García-Rubies and V. Gracia. – 1997b. Socio-behavioural context of reproduction in the Mediterranean dusky grouper Epinephelus marginatus (Lowe, 1834) (Pisces: Serranidae) in the Medes Islands Marine Reserve (NW Mediterranean, Spain). Sci. Mar., 61(1): 79-89.

Copyright (c) 2010 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Contact us

Technical support