Reproductive biology of the dusky grouper (Epinephelus marginatus) at the southern limit of its distribution in the south-western Atlantic
Mario V. Condini A D , Luís F. Fávaro B , Antonio S. VarelaA Laboratório de Ictiologia, Instituto de Oceanografia, Universidade Federal de Rio Grande, C.P. 474, CEP: 96.201-900, Rio Grande – RS, Brazil.
B Laboratório de Reprodução de Comunidade de Peixes, Departamento de Biologia Celular, Universidade Federal do Paraná, CEP: 81.531-990, Curitiba, PR, Brazil.
C Instituto de Ciências Biológicas, Universidade Federal de Rio Grande, CEP: 96.201-900, Rio Grande – RS, Brazil.
D Corresponding author. Email: mvcondini@yahoo.com.br
Marine and Freshwater Research 65(2) 142-152 https://doi.org/10.1071/MF13120
Submitted: 28 November 2012 Accepted: 9 July 2013 Published: 25 September 2013
Abstract
We investigated the reproductive parameters of a dusky grouper Epinephelus marginatus population at the southern limit of its distribution in the south-western Atlantic. The analysed specimens were captured between January 2008 and April 2011 at Carpinteiro Bank (CB) (32°16′S; 051°47′W), a seamount located at the 20 m isobath ~16 nautical miles from the coast. The gonads of a total of 201 individuals (184 females, 16 males and 1 individual in sexual transition) with a total length (TL, mm) between 278 and 1160 mm were analysed microscopically. Histological analyses of the gonads suggested that the species is a partial spawner with a long spawning period (between November and March) and with a reproductive peak between November and January. The average female length at first maturity (L50) was 496 (TL, mm). We also observed partially spawned ovaries and partially spawned testes, which indicated reproductive activity, and we noted the presence of hyalinised follicles. These findings reveal that CB is the southernmost portion of the south-western Atlantic in which the dusky grouper reproduces. Additionally, an inshore-offshore comparison suggested that deeper (>20 m) rocky bottoms, such as the studied seamount, constitute higher quality habitats for this species when compared with littoral (<5 m) rocky reefs.
Additional keywords: length at first maturity, protogynous hermaphroditism, spawning seasonality.
References
Abreu, L., and Calliari, J. (2005). Paleocanais na plataforma continental interna do Rio Grande do Sul: evidências de uma drenagem fluvial pretérita. Revista Brasileira de Geofísica 23, 123–132.| Paleocanais na plataforma continental interna do Rio Grande do Sul: evidências de uma drenagem fluvial pretérita.Crossref | GoogleScholarGoogle Scholar |
Andrade, B. A., Machado, L. F., Hostim-Silva, M., and Barreiros, J. P. (2003). Reproductive biology of the dusky grouper Epinephelus marginatus (Lowe, 1834). Brazilian Archives of Biology and Technology 46, 373–382.
| Reproductive biology of the dusky grouper Epinephelus marginatus (Lowe, 1834).Crossref | GoogleScholarGoogle Scholar |
Bouchereau, J. L., Body, P., and Chauvet, C. (1999). Growth of the dusky grouper Epinephelus marginatus (Linnaeus, 1758) (Teleostei, Serranidae), in the Natural Marine Reserve of Lavezzi Islands, Corsica, France. Scientia Marina 63, 71–77.
Brulé, T., Renán, X., Colás-Marrufo, T., Hauyon, Y., and Tuz-Sulub, A. N. (2003a). Reproduction in the protogynous black grouper (Mycteroperca bonaci (Poey)) from the southern Gulf of Mexico. Fishery Bulletin 101, 463–475.
Brulé, T., Deniel, C., Colás-Marrufo, T., and Renan, X. (2003b). Reproductive biology of gag in the southern Gulf of Mexico. Journal of Fish Biology 63, 1505–1520.
| Reproductive biology of gag in the southern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
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 Fisheries Synopsis 129, 1–64.
Bruslé, J., and Bruslé, S. (1975). Ovarian and testicular intersexuality in two protogynous mediterranean groupers, Epinephelus aeneus and Epinephelus guaza. In ‘Intersexuality in the Animal Kingdom’. (Ed. R. Reinboth) pp. 222–227. (Springer Verlag: Berlin.)
Buchmann, F. S. C., Seeliger, M., Zanella, L., Madureira, L. S. P., Tomazelli, L. J., and Calliari, L. J. (2001). Análise batimétrica e sedimentológica no estudo do Parcel do Carpinteiro, uma paleolinha de praia pleistocênica na antepraia do Rio Grande do Sul, Brasil. Pesquisas 28, 109–115.
Bustos, R., Luque, A., and Pajuelo, J. G. (2010). Reproductive biology of the island grouper (Mycteroperca fusca) in the Canary Islands, northwest coast of Africa. Scientia Marina 74, 613–619.
| Reproductive biology of the island grouper (Mycteroperca fusca) in the Canary Islands, northwest coast of Africa.Crossref | GoogleScholarGoogle Scholar |
Cardoso, L., and Haimovici, M. (2011). Caracterização tecnológica, social, econômica e ecológica da atividade pesqueira sediada em Passo de Torres, Santa Catarina, Brasil. Boletim do Instituto de Pesca 37, 275–288.
Chauvet, C. (1988). Etude de la croissance du mérou Epinephelus guaza (Linné, 1758) des côtes tunisiennes. Aquatic Living Resources 1, 277–288.
| Etude de la croissance du mérou Epinephelus guaza (Linné, 1758) des côtes tunisiennes.Crossref | GoogleScholarGoogle Scholar |
Coleman, F., Koenig, C. C., and Collins, A. (1996). Reproductive style of shallow-water groupers (Pisces: Serranidae) in the eastern Gulf of Mexico and the consequences of fishing spawning aggregations. Environmental Biology of Fishes 47, 129–141.
| Reproductive style of shallow-water groupers (Pisces: Serranidae) in the eastern Gulf of Mexico and the consequences of fishing spawning aggregations.Crossref | GoogleScholarGoogle Scholar |
Coleman, F. C., Koenig, C. C., Huntsman, G. R., Musick, J. A., Eklund, A. M., McGovern, J. C., Chapman, R. W., Sedberry, G. R., and Grimes, C. B. (2000). Long-lived reef fishes: the grouper–snapper complex. Fisheries (Bethesda, Md.) 25, 14–21.
| Long-lived reef fishes: the grouper–snapper complex.Crossref | GoogleScholarGoogle Scholar |
Condini, M. V., Seyboth, E., Vieira, J. P., and Garcia, A. M. (2011). Diet and feeding strategy of the dusky grouper Mycteroperca marginata (Actinopterygii: Epinephelidae) in a man-made rocky habitat in southern Brazil. Neotropical Ichthyology 9, 161–168.
| Diet and feeding strategy of the dusky grouper Mycteroperca marginata (Actinopterygii: Epinephelidae) in a man-made rocky habitat in southern Brazil.Crossref | GoogleScholarGoogle Scholar |
Cornish, A., and Harmelin-Vivien, M. (2004). Epinephelus marginatus. 2006 IUCN Red List of Threatened Species. Available at www.iucnredlist.org [accessed 5 march 2012]
Craig, M. T., Sadovy de Mitcheson, Y. J., and Heemstra, P. C. (2011). ‘Groupers of the World: A Field and Market Guide.’ (Boca Raton: Florida.)
Cunha, M. E., Quental, H., Barradas, A., Pousão-Ferreira, P., Cabrita, E., and Engrola, S. (2009). Rearing larvae of dusky grouper, Epinephelus marginatus (Lowe, 1834), (Pisces: Serranidae) in a semi-extensive mesocosm. Scientia Marina 73, 201–212.
| Rearing larvae of dusky grouper, Epinephelus marginatus (Lowe, 1834), (Pisces: Serranidae) in a semi-extensive mesocosm.Crossref | GoogleScholarGoogle Scholar |
Domeier, M. L., and Colin, P. L. (1997). Tropical reef fish spawning aggregations: defined and reviewed. Bulletin of Marine Science 60, 698–726.
Fennessy, Y. S. T. (2006). Reproductive biology and growth of the yellowbelly rockcod Epinephelus marginatus (Serranidae) from South-east Africa. African Journal of Marine Science 28, 1–11.
| Reproductive biology and growth of the yellowbelly rockcod Epinephelus marginatus (Serranidae) from South-east Africa.Crossref | GoogleScholarGoogle Scholar |
Figueiredo, J. L., and Menezes, N. A. (1980). ‘Manual de peixes marinhos do sudeste do Brasil. III. Teleostei (2).’ (Museu de Zoologia, Universidade de São Paulo.)
Frias-Torres, S. (2006). Habitat use of juvenile goliath grouper (Epinephelus itajara) in the Florida Keys, USA. Endangered Species Research 2, 1–6.
| Habitat use of juvenile goliath grouper (Epinephelus itajara) in the Florida Keys, USA.Crossref | GoogleScholarGoogle Scholar |
Garvey, J. E., Herra, T. P., and Leggett, W. C. (2002). Protracted reproduction in sunfish: the temporal dimension in fish recruitment revisited. Ecological Applications 12, 194–205.
| Protracted reproduction in sunfish: the temporal dimension in fish recruitment revisited.Crossref | GoogleScholarGoogle Scholar |
Gerhardinger, L. C., Freitas, M. O., Bertoncini, A. A., and Hostim-Silva, M. (2006). Collaborative approach in the study of the reproductive biology of the dusky grouper Epinephelus marginatus (Lowe, 1834) (Perciformes: Serranidae). Acta Scientiarum. Biological Sciences 28, 219–226.
Gomes, I. D., and Araújo, F. G. (2004). Reproductive biology of two marine catfishes (Siluriformes, Ariidae) in the Sepetiba Bay, Brazil. Revista de Biologia Tropical 52, 143–156.
| 17357411PubMed |
Gust, N. (2004). Variation in the population biology of protogynous coral reef fishes over tens of kilometres. Canadian Journal of Fisheries and Aquatic Sciences 61, 205–218.
| Variation in the population biology of protogynous coral reef fishes over tens of kilometres.Crossref | GoogleScholarGoogle Scholar |
Harmelin, J. G., and Harmelin-Vivien, M. (1999). A review on hábitat, diet and growth of the dusky grouper Epinephelus marginatus (Lowe, 1834). Marine Life (Marseille) 9, 11–20.
Hastings, P. A. (1981). Gonad morphology and sex succession in the protogynous hermaphrodite Hemanthias vivanus (Jordan and Swain). Journal of Fish Biology 18, 443–454.
| Gonad morphology and sex succession in the protogynous hermaphrodite Hemanthias vivanus (Jordan and Swain).Crossref | GoogleScholarGoogle Scholar |
Hawkins, J. P., and Roberts, C. M. (2004). Effects of fishing on sex-changing Caribbean parrotfishes. Biological Conservation 115, 213–226.
| Effects of fishing on sex-changing Caribbean parrotfishes.Crossref | GoogleScholarGoogle Scholar |
Heemstra, C. P., and Randall, J. E. (1993). FAO Species catalogue. Groupers of the word (Family Serranidae, Subfamily Epinephelinae): An annotated and illustred catalogue of the grouper, rockcod, hind, coral grouper lyretail species known to date. FAO Fisheries Synopsis 125, 186–188.
Helfman, G. S., Collette, B. B., Facey, D. E., & Bowen, B. W. (2009). ‘The diversity of fishes: Biology, Evolution, and Ecology.’ (Wiley-Blackwell: West Sussex.)
Hunter, J. R., Maciewicz, B. J., Lo, N. C. H., and Kimbrell, C. A. (1992). Fecundity, spawning and maturity of female Dover sole, Microstomus pacificus, with an evaluation of assumptions and precision. Fishery Bulletin 90, 101–128.
Huntsman, G. R., Potts, J., Mays, R. W., and Vaughan, D. (1999). Groupers (Serranidae, Epinephelinae): Endangered apex predators of reef communities. In ‘Life in the Slow Lane: Ecology and Conservation of Long-lived Marine Animals’. (Ed. J. A. Musick) pp. 217–232. (American Fisheries Society Symposium.)
Irigoyen, A. J., Galván, D. E., and Venerus, L. A. (2005). Occurrence of dusky grouper Epinephelus marginatus (Lowe, 1834) in gulfs of northern Patagonia, Argentina. Journal of Fish Biology 67, 1741–1745.
| Occurrence of dusky grouper Epinephelus marginatus (Lowe, 1834) in gulfs of northern Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |
Kara, M. H., and Derbal, F. (1995). Morphome’ trie, croissance et mortalit e du Merou Epinephelus marginatus (Serranidae) des co^ tes de l’est algerien. Cahiers de Biologie Marine 36, 229–237.
Kara, M. H., and Derbal, F. (1999). Données biologiques sur le mérou Epinephelus marginatus (Lowe, 1834) des côtes algériennes. Marine Life (Marseille) 9, 21–27.
King, M. (1995). ‘Fisheries biology, assessment and management.’ (Blackwell Science: United Kingdom.)
La Mesa, G., Longobardi, A., Sacco, F., and Marino, G. (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. Scientia Marina 72, 743–756.
| 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.Crossref | GoogleScholarGoogle Scholar |
Linde, M., Grau, A. M., Riera, F., and Massutí-Pascual, E. (2004). Analysis of trophic ontogeny in Epinephelus marginatus (Serranidae). Cybium 28, 27–35.
López, V. G., and Orvay, F. C. (2005). Food habits of groupers Epinephelus marginatus (Lowe, 1834) and Epinephelus costae (Steindachner, 1878) in the Mediterranean Coast of Spain. Hidrobiológica 15, 27–34.
Machado, L., Bertoncini, A., Hostim-Silva, M., and Barreiros, J. P. (2003). Habitat use by the juvenile dusky grouper Epinephelus marginatus and its relative abundance, in Santa Catarina, Brazil. Journal of Ichthyology and Aquatic Biology 6, 133–138.
Machado, L. F., Daros, F. A. M. L., Bertoncini, A. A., Hostim-Silva, M., and Barreiros, J. P. (2008). Feeding ecology and trophic ontogeny in Epinephelus marginatus (Perciformes: Serranidae) from south Brazil. Cybium 32, 33–41.
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.
| Social induced sex-change in the half-moon grouper, Epinephelus rivulatus, at Ningaloo Reef, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Manooch, C. S. (1987). Age and growth of snappers and groupers. In ‘Tropical snappers and groupers: Biology and fisheries management’. (Eds J. J. Polovina and S. Ralston.) pp. 329–374. (Westview Press: Boulder, CO, USA.)
Marino, G., Azzurro, E., Massari, A., Finoia, M. G., and Mandich, A. (2001). Reproduction is the dusky grouper from the southern Mediterranean. Journal of Fish Biology 58, 909–927.
| Reproduction is the dusky grouper from the southern Mediterranean.Crossref | GoogleScholarGoogle Scholar |
Marino, G., Panini, E., Longobardi, A., Mandich, A., Finoia, M. G., Zohar, Y., and Mylonas, C. C. (2003). Induction of ovulation in captive – reared dusky grouper, Epinephelus marginatus (Lowe, 1834), with a sustained–release GnRHa implant. Aquaculture 219, 841–858.
| Induction of ovulation in captive – reared dusky grouper, Epinephelus marginatus (Lowe, 1834), with a sustained–release GnRHa implant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhs1Kmt7s%3D&md5=4d6d87e03cb8ea2e8609e4199fca6cccCAS |
Oliveira, E. C., and Fávaro, L. F. (2011). Reproductive biology of the flatfish Etropus crossotus (Pleuronectiformes: Paralichthyidae) in the Paranaguá Estuarine Complex, Paraná State, subtropical region of Brazil. Neotropical Ichthyology 9, 795–805.
| Reproductive biology of the flatfish Etropus crossotus (Pleuronectiformes: Paralichthyidae) in the Paranaguá Estuarine Complex, Paraná State, subtropical region of Brazil.Crossref | GoogleScholarGoogle Scholar |
Parrish, J. D. (1987). The trophic biology of snappers and groupers. In ‘Tropical Snappers and Groupers: Biology and Fisheries Management’. (Eds J. J. Polovina and S. Ralston.) pp. 405–463. (Westview Press: Boulder, CO, USA.)
Pulliam, H. R. (2000). On the relationship between niche and distribution. Ecology Letters 3, 349–361.
| On the relationship between niche and distribution.Crossref | GoogleScholarGoogle Scholar |
Reñones, O., Polunin, N. V. C., and Goni, R. (2002). Size related dietary shifts of Epinephelus marginatus in a western Mediterranean littoral ecosystem: an isotope and stomach content analysis. Journal of Fish Biology 61, 122–137.
| Size related dietary shifts of Epinephelus marginatus in a western Mediterranean littoral ecosystem: an isotope and stomach content analysis.Crossref | GoogleScholarGoogle Scholar |
Reñones, O., Piñeiro, C., Mas, X., and Goñi, R. (2007). Age and growth of the dusky grouper Epinephelus marginatus (Lowe 1834) in an exploited population of the western Mediterranean Sea. Journal of Fish Biology 71, 346–362.
| Age and growth of the dusky grouper Epinephelus marginatus (Lowe 1834) in an exploited population of the western Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar |
Reñones, O., Grau, A., Mas, X., Riera, F., and Saborido-Rey, F. (2010). Reproductive pattern of an exploited dusky grouper Epinephelus marginatus (Lowe 1834) (Pisces: Serranidae) population in the western Mediterranean. Scientia Marina 74, 523–537.
| Reproductive pattern of an exploited dusky grouper Epinephelus marginatus (Lowe 1834) (Pisces: Serranidae) population in the western Mediterranean.Crossref | GoogleScholarGoogle Scholar |
Sadovy, Y., and Shapiro, D. Y. (1987). Criteria for the Diagnosis of Hermaphroditism in Fishes. Copeia 1987, 136–156.
| Criteria for the Diagnosis of Hermaphroditism in Fishes.Crossref | GoogleScholarGoogle Scholar |
Sanches, E. G., Azevedo, V. G., and Costa, M. R. (2007). Criação da garoupa-verdadeira Epinephelus marginatus (Lowe, 1834) (Teleostei, Serranidae) alimentada com rejeito de pesca e ração úmida em tanques-rede. Atlantica 29, 121–126.
Seyboth, E., Condini, M. V., Albuquerque, C. Q., Varela, A. S., Velasco, G., Vieira, J. P., and Garcia, A. M. (2011). Age, growth, and reproductive aspects of the dusky grouper Mycteroperca marginata (Actinopterygii, Epinephelidae) in a man-made rocky habitat in southern Brazil. Neotropical Ichthyology 9, 849–856.
| Age, growth, and reproductive aspects of the dusky grouper Mycteroperca marginata (Actinopterygii, Epinephelidae) in a man-made rocky habitat in southern Brazil.Crossref | GoogleScholarGoogle Scholar |
Shapiro, D. Y. (1987). The reproduction in groupers. In ‘Tropical snappers and groupers: Biology and management of snappers and groupers’. (Eds. J. J. Polovina and S. Ralston.) pp. 295–327. (Westview Press: Boulder, CO, USA.)
Sluka, R. D., Chiappone, M., and Sullivan Sealey, K. M. (2001). Influence of habitat on grouper abundance in the Florida Keys, U.S.A. Journal of Fish Biology 58, 682–700.
| Influence of habitat on grouper abundance in the Florida Keys, U.S.A.Crossref | GoogleScholarGoogle Scholar |
Sokal, R. R., and Rohlf, F. J. (1995). ‘Biometry: the principles of statistics in biological research.’ (Freeman: New York.)
Thompson, R., and Munro, J. L. (1978). Aspects of the biology and ecology of Caribbean reef fishes: Serranidae (hinds and groupers). Journal of Fish Biology 12, 115–146.
| Aspects of the biology and ecology of Caribbean reef fishes: Serranidae (hinds and groupers).Crossref | GoogleScholarGoogle Scholar |
Webb, R. O., and Kingsford, M. J. (1992). Protogynous hermaphroditism in the half-banded sea perch, Hypoplectrodes maccullochi (Serranidae). Journal of Fish Biology 40, 951–961.
| Protogynous hermaphroditism in the half-banded sea perch, Hypoplectrodes maccullochi (Serranidae).Crossref | GoogleScholarGoogle Scholar |
Zabala, M., Garcia-Rubies, A., Louisy, P., and Sala, E. (1997a). Spawning behaviour of the Mediterranean dusky grouper Epinephelus marginatus (Lowe, 1834) (Pisces, Serranidae) in the Medes Islands Marine Reserve (NW Mediterranean, Spain). Scientia Marina 61, 65–77.
Zabala, M., Louisy, P., Garcia-Rubies, A., and Gracia, V. (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). Scientia Marina 61, 79–89.