Sexual development and demography of the rock hind Epinephelus adscensionis, a protogynous grouper, in the south-west Atlantic
Simone Marques A and Beatrice P. Ferreira A
+ Author Affiliations
- Author Affiliations
A Universidade Federal de Pernambuco, Departamento de Oceanografia, Recife 50740-550, Brazil.
B Corresponding author. Email: simonemarbio@gmail.com
Marine and Freshwater Research 69(2) 300-312 https://doi.org/10.1071/MF17016
Submitted: 25 January 2017 Accepted: 1 August 2017 Published: 13 October 2017
Abstract
This study reports on the pattern of sexual development and demography of Epinephelus adscensionis sampled on the north-east coast of Brazil. The species is a protogynous hermaphrodite, with males (26–44-cm total length, TL) transitioning from mature females (20–33 cm TL). This species presented multiple spawning, with peaks in the gonadosomatic index indicating that the spawning period of the rock hind occurred along 3 months per year, where for 2008 was between August and October, and for 2009 was between July and September. Age was determined from otoliths and periodicity was validated from captive fish treated with tetracycline. The resulting von Bertalanffy growth parameters were as follows: theoretical maximum length (L∞) 34.82 cm TL, growth coefficient (k) 0.26 and theoretical age at L = 0 (t0) 0.86 years. The size and age at sexual maturity for females were 20 cm TL and 4 years. The total rate of mortality was 0.28 year–1. Older fish were males and had a maximum longevity of 15 years. This species is an important resource for local communities, but is also currently caught by trap fisheries, which have been expanding in recent decades in response to demands of export markets. Lack of monitoring and management of these and other reef fisheries in north-east Brazil makes fishing sustainability uncertain.
Additional keywords: mortality, otolith, sex change, validation.
References
Afonso, P., Porteiro, F. M., Santos, R. S., Barreiros, J. P., Worms, J., and Wirtz, P. (1999). Coastal marine fishes of Sao Tome Island (Gulf of Guinea). Arquipélago – Life and Marine Sciences 17A, 65–92.Beamish, R. J., and Fournier, D. A. (1981). A method for comparing the precision of a set of age determinations. Canadian Journal of Fisheries and Aquatic Sciences 38, 982–983.
| A method for comparing the precision of a set of age determinations.Crossref | GoogleScholarGoogle Scholar |
Beçak, W., and Paulete, J. (1976). ‘Técnicas de citologia e histologia.’ (Livros Técnicos e Científicos: São Paulo, Brazil.)
Berkeley, S. A., Hixon, M. A., Larson, R. J., and Love, M. S. (2004). Fisheries sustainability via protection of age structure and spatial distribution of fish populations. Fisheries 29, 23–32.
| Fisheries sustainability via protection of age structure and spatial distribution of fish populations.Crossref | GoogleScholarGoogle Scholar |
Berkes, F., Hughes, T. P., Steneck, R. S., Wilson, J. A., Bellwood, D. R., Crona, B., and Nyström, M. (2006). Globalization, roving bandits, and marine resources. Science 311, 1557–1558.
| Globalization, roving bandits, and marine resources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XislGrsLk%3D&md5=9a483b32ece4c4e4efa28eb72ca3ce68CAS |
Beverton, R. J. H., and Holt, S. J. (1957). On the dynamics of exploited fish populations. Fishery Investigations Series II, number 19, Springer Science & Business Media, London, UK.
Bullock, L. H. and Smith, G. B. (1991). ‘Seabasses (Pisces: Serranidae).’ (Florida Marine Research Institute: St Petersburg, FL, USA.)
Burton, M. L., Potts, J. C., and Carr, D. R. (2012). Age, growth, and natural mortality of rock hind, Epinephelus adscensionis, from the Gulf of Mexico. Bulletin of Marine Science 88, 903–917.
| Age, growth, and natural mortality of rock hind, Epinephelus adscensionis, from the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Burton, M. L., Potts, J. C., and Carr, D. R. (2015). Age, growth, and natural mortality of yellowfin grouper (Mycteroperca venenosa) from the southeastern United States. PeerJ 3, e1099.
| Age, growth, and natural mortality of yellowfin grouper (Mycteroperca venenosa) from the southeastern United States.Crossref | GoogleScholarGoogle Scholar |
Campana, S. W. (2001). Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. Journal of Fish Biology 59, 197–242.
| Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods.Crossref | GoogleScholarGoogle Scholar |
Carter, A. B., Davies, C. R., Mapstone, B. D., Russ, G. R., Tobin, A. J., and Williams, A. J. (2014). Effects of region, demography, and protection from fishing on batch fecundity of common coral trout (Plectropomus leopardus). Coral Reefs 33, 751–763.
| Effects of region, demography, and protection from fishing on batch fecundity of common coral trout (Plectropomus leopardus).Crossref | GoogleScholarGoogle Scholar |
Carvalho, R. A. A., Cunha, F. E. A., Montezuma, A. M. N., and de Araújo, M. E. (2014). Captura e processamento de peixes recifais no estado do Rio Grande do Norte, Brasil. Acta of Fisheries and Aquatic Resources 1, 91–103.
Carvalho-Filho, A. (1999). Badejos, chernes, garoupas e mero. In ‘Peixes da Costa Brasileira’. (Ed. A. Carvalho-Filho.) pp. 97–111. (Melro: São Paulo, Brazil.)
Caselle, J. E., Hamilton, S. L., Schroeder, D. M., Love, M. S., Standish, J. D., Rosales-Casian, J. A., and Sosa-Nishizaki, O. (2011). Geographic variation in density, demography, and life history traits of a harvested, sex-changing, temperate reef fish. Canadian Journal of Fisheries and Aquatic Sciences 68, 288–303.
| Geographic variation in density, demography, and life history traits of a harvested, sex-changing, temperate reef fish.Crossref | GoogleScholarGoogle Scholar |
Cheung, W. W., Pitcher, T. J., and Pauly, D. (2005). A fuzzy logic expert system to estimate intrinsic extinction vulnerabilities of marine fishes to fishing. Biological Conservation 124, 97–111.
| A fuzzy logic expert system to estimate intrinsic extinction vulnerabilities of marine fishes to fishing.Crossref | GoogleScholarGoogle Scholar |
Choat, J. H., and Robertson, D. R. (2002). Age-based studies on coral reef fishes. In ‘Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem’. (Ed. P. F. Sale.) pp. 57–80. (Academic Press: San Diego, CA, USA.)
Choat, J. H., Kritzer, J. P., and Ackerman, J. L. (2009). Ageing in coral reef fishes: do we need to validate the periodicity of increment formation for every species of fish for which we collect age-based demographic data? In ‘Tropical Fish Otoliths: Information for Assessment, Management and Ecology’. (Eds B. S. Green, B. D. Mapstone, G. Carlos, and G. A. Begg.) pp. 23–48. (Springer: London, UK.)
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 25, 14–21.
| Long- lived reef fishes: the grouper–snapper complex.Crossref | GoogleScholarGoogle Scholar |
de Araújo, J. N., and Martins, A. S. (2006). Age and growth of coney (Cephalopholis fulva) from the central coast of Brazil. Journal of the Marine Biological Association of the United Kingdom 86, 181–187.
| Age and growth of coney (Cephalopholis fulva) from the central coast of Brazil.Crossref | GoogleScholarGoogle Scholar |
Erisman, B. E., Craig, M. T., and Hastings, P. A. (2009). A phylogenetic test of the size-advantage model: evolutionary changes in mating behavior influence the loss of sex change in a fish lineage. American Naturalist 174, E83–E99.
| A phylogenetic test of the size-advantage model: evolutionary changes in mating behavior influence the loss of sex change in a fish lineage.Crossref | GoogleScholarGoogle Scholar |
Erisman, B. E., Craig, M. T., and Hastings, P. A. (2010). Reproductive biology of the Panama graysby Cephalopholis panamensis (Teleostei: Epinephelidae). Journal of Fish Biology 76, 1312–1328.
| Reproductive biology of the Panama graysby Cephalopholis panamensis (Teleostei: Epinephelidae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvpsFSgug%3D%3D&md5=09b37a6eee14e6f170b2eb674e32c0c6CAS |
Ferreira, B. P. (1993). Reproduction of the inshore coral trout Plectropomus maculatus (Perciformes: Serranidae) from the central Great Barrier Reef, Australia. Journal of Fish Biology 42, 831–844.
Ferreira, B. P. (1995). Reproduction of the common coral trout Plectropomus leopardus (Serranidae: Epinephelinae) from the Great Barrier Reef, Australia. Bulletin of Marine Science 56, 653–669.
Ferreira, B. P., and Maida, M. (2006). ‘Monitoramento dos recifes de coral do Brasil.’ (Ministério do Meio Ambiente: Brasília, Brazil.)
Ferreira, B. P., and Russ, G. R. (1994). Age validation and estimation of growth rate of the coral trout, Plectropomus leopardus (Lacepede 1802), from Lizard Island, Northern Great Barrier Reef. Fishery Bulletin 92, 46–57.
Freire, K. M. F., Aragão, J. A. N., Araújo, A. R. R., Ávila-da-Silva, A. O., Bispo, M. C. S., and Velasco, G. (2015). Reconstruction of catch statistics for Brazilian marine waters (1950–2010). Fisheries Catch Reconstructions for Brazil’s Mainland and Oceanic Islands, Fisheries Centre Research Reports 23, 3–30.
Gasparini, J. L., and Floeter, S. R. (2001). The shore fishes of Trindade Island, western South Atlantic. Journal of Natural History 35, 1639–1656.
| The shore fishes of Trindade Island, western South Atlantic.Crossref | GoogleScholarGoogle Scholar |
Grandcourt, E. M., Abdessalaam, T. Z. A., Francis, F., and Shamsi, A. T. A. (2005). Population biology and assessment of the orange-spotted grouper, Epinephelus coioides (Hamilton, 1822), in the southern Arabian Gulf. Fisheries Research 74, 55–68.
| Population biology and assessment of the orange-spotted grouper, Epinephelus coioides (Hamilton, 1822), in the southern Arabian Gulf.Crossref | GoogleScholarGoogle Scholar |
Grandcourt, E. M., Al Abdessalaam, T. Z., Francis, F., Al Shamsi, A. T., and Hartmann, S. A. (2009). Reproductive biology and implications for management of the orange-spotted grouper Epinephelus coioides in the southern Arabian Gulf. Journal of Fish Biology 74, 820–841.
| Reproductive biology and implications for management of the orange-spotted grouper Epinephelus coioides in the southern Arabian Gulf.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjnt1yitw%3D%3D&md5=0a13cf5fe8080246667b02e855b79ca6CAS |
Green, B. S., Mapstone, B. D., Carlos, G., and Begg, G. A. (2009). ‘Tropical Fish Otoliths: Information for Assessment, Management and Ecology.’ (Springer: Dordrecht, Netherlands).
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, P. C., and Randall, J. E. (1993). FAO Species Catalogue. Vol. 16. Groupers of the World (Family Serranidae, Subfamily Epinephelinae). An Annotated and Illustrated Catalogue of the Grouper, Rockcod, Hind, Coral Grouper and Lyretail Species Known to Date. FAO Fisheries Synopsis125.’ (FAO: Rome, Italy.)
Hostim-Silva, M., Bertoncini, Á. A., Machado, L. F., Gerhardinger, L. C., Daros, F. A., Barreiros, J. P., and Godoy, E. (2006). ‘Peixes de Costão Rochoso de Santa Catarina. I. Arvoredo.’ (Universidade do Vale do Itajaí: Itajaí, Brazil.)
Huang, B., Banzon, V. F., Freeman, E., Lawrimore, J., Liu, W., Peterson, T. C., and Zhang, H. M. (2015). Extended reconstructed sea surface temperature version 4 (ERSST. v4). Part I: upgrades and intercomparisons. Journal of Climate 28, 911–930.
| Extended reconstructed sea surface temperature version 4 (ERSST. v4). Part I: upgrades and intercomparisons.Crossref | GoogleScholarGoogle Scholar |
Instituto Chico Mendes de Conservação da Biodiversidade (2014). Lista de espécies ameaçadas. Available at http://www.icmbio.gov.br/portal/faunabrasileira/lista-de-especies-dados-insuficientes [Verified 6 October 2017].
King, M. (1997). ‘Fisheries Biology, Assessment and Management.’ (Blackwell Science: London, UK.)
Kline, R. J., Khan, I. A., and Holt, G. J. (2011). Behavior, color change and time for sexual inversion in the protogynous grouper (Epinephelus adscensionis). PLoS One 6, e19576.
| Behavior, color change and time for sexual inversion in the protogynous grouper (Epinephelus adscensionis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFCktbg%3D&md5=85d5ced141a2a3b7ab62f1acc79f5d0dCAS |
Liu, M., and Sadovy, Y. (2004). Early gonadal development and primary males in the protogynous epinepheline, Cephalopholis boenak. Journal of Fish Biology 65, 987–1002.
| Early gonadal development and primary males in the protogynous epinepheline, Cephalopholis boenak.Crossref | GoogleScholarGoogle Scholar |
Lombardi-Carlson, L. A., Fitzhugh, G. R., and Mikulas, J. J. (2002). Red grouper (Epinephelus morio) age–length structure and description of growth from the eastern Gulf of Mexico: 1992–2001. Contribution Series 2002–02, National Marine Fisheries Service, Southeastern Fisheries Science Center, Panama City, FL, USA. Available at http://sedarweb.org/docs/wsupp/S12RD03%20age%20growth.pdf [Verified 4 August 2017].
Luckhurst, B. E., Barnes, J. A., and Sadovy, Y. (1992). Record of an unusually large red hind, Epinephelus guttatus (pisces: serranidae) from Bermuda with comments on its age. Bulletin of Marine Science 51, 267–270.
Marques, S., and Ferreira, B. P. (2010). Composição e características da pesca de armadilhas no litoral Norte de Pernambuco – Brasil. Boletim Técnico-Científico do CEPENE 18, 49–60.
Marques, S., and Ferreira, B. P. (2011). Sexual development and reproductive pattern of the Mutton hamlet Alphestes afer (Teleostei: Epinephelidae): a dyandric hermaphroditic reef fish. Neotropical Ichthyology 9, 547–558.
| Sexual development and reproductive pattern of the Mutton hamlet Alphestes afer (Teleostei: Epinephelidae): a dyandric hermaphroditic reef fish.Crossref | GoogleScholarGoogle Scholar |
Marques, S., and Ferreira, B. P. (2016). Age and growth of the mutton hamlet Alphestes afer, with a review of the size and age of sex change among epinephelids. Journal of Fish Biology 89, 1009–1025.
| Age and growth of the mutton hamlet Alphestes afer, with a review of the size and age of sex change among epinephelids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC28fpsVeksQ%3D%3D&md5=45f293b8d74c42f76647e93c414c98a9CAS |
Martins, A. S., Olavo, G., and Costa, P. A. S. (2005). Recursos demersais capturados com espinhel de fundo no talude superior da região entre Salvador (BA) e o Cabo de São Tomé (RJ). In ‘Pesca e potenciais de exploração de recursos vivos na região central da Zona Econômica Exclusiva brasileira’. (Ed. P. A. S. Costa.) pp. 109–128. (Museu Nacional: Rio de Janeiro, Brazil.)
Munday, P. L., Buston, P. M., and Warner, R. R. (2006). Diversity and flexibility of sex-change strategies in animals. Trends in Ecology & Evolution 21, 89–95.
| Diversity and flexibility of sex-change strategies in animals.Crossref | GoogleScholarGoogle Scholar |
Nagahama, Y. (1983). The functional morphology of teleost gonads. In ‘Fish Physiology, IX (Part A).’ (Eds W. S. Hoar, D. J. Randall, and E. M. Donaldson.) pp. 223–275. (Academic Press: London, UK.)
Oliveira Freitas, M. O., de Moura, R. L., Francini-Filho, R. B., and Minte-Vera, C. V. (2011). Spawing patterns of commercially important reef fish (Lutjanidae and Serranidae) in the tropical western South Atlantic. Scientia Marina 75, 135–146.
| Spawing patterns of commercially important reef fish (Lutjanidae and Serranidae) in the tropical western South Atlantic.Crossref | GoogleScholarGoogle Scholar |
Palmer, C. L., Farsky, R. A., Gardner, C., and Lombardi-Carlson, L. A. (2006). The use of an otolith reference collection to monitor age reader precision for red grouper (Epinephelus morio). SEDAR 12-DW-01, Contribution 2006–11, Panama City Laboratory, St Petersburg, FL, USA.
Pinheiro, H. T., Martins, A. S., and Gasparini, J. L. (2010). Impact of commercial fishing on Trindade Island and Martin Vaz Archipelago, Brazil: characteristics, conservation status of the species involved and prospects for preservation. Brazilian Archives of Biology and Technology 53, 1417–1423.
| Impact of commercial fishing on Trindade Island and Martin Vaz Archipelago, Brazil: characteristics, conservation status of the species involved and prospects for preservation.Crossref | GoogleScholarGoogle Scholar |
Pinheiro, H. T., Ferreira, C. E. L., Joyeux, J.-C., Santos, R. G., and Horta, P. A. (2011). Reef fish structure and distribution in a south-western Atlantic Ocean tropical island. Journal of Fish Biology 79, 1984–2006.
| Reef fish structure and distribution in a south-western Atlantic Ocean tropical island.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38%2FltFamsQ%3D%3D&md5=272790cbdd367005098d31036efecd45CAS |
Potts, J. C., and Manooch, C. S. (1995). Age and growth of red hind and rock hind collected from North Carolina through the Dry Tortugas, Florida. Bulletin of Marine Science 56, 784–794.
Ribeiro, F. P. (2006). A pesca de peixes demersais com armadilhas no nordeste do Brasil. In ‘Monitoramento dos recifes de coral do Brasil’. (Eds B. P. Ferreira and M. Maida.) pp. 71–72. (Ministério do Meio Ambiente : Brasília, Brazil.)
Rocha, L. A., and Rosa, R. S. (2001). Baseline assessment of reef fish assemblages of Parcel Manuel Luiz Marine State Park, Maranhão, north-east Brazil. Journal of Fish Biology 58, 985–998.
Rocha, L., Ferreira, B., Choat, J. H., Craig, M. T., Sadovy, Y., and Bertoncini, A. A. (2008). Epinephelus adscensionis (Butterfish, Deady, Graysby, Hind, Jack, Rock Grouper, Rock Hind). In ‘The IUCN Red List of Threatened Species 2008’, ver. 3.1, e.T132819A3460202. (International Union for Conservation of Nature and Natural Resources.) Available at http://www.iucnredlist.org/details/132819/0 [Verified 15 March 2016].
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 |
Sadovy de Mitcheson, Y., and Liu, M. (2008). Functional hermaphroditism in teleosts. Fish and Fisheries 9, 1–43.
| Functional hermaphroditism in teleosts.Crossref | GoogleScholarGoogle Scholar |
Sadovy de Mitcheson, Y., Craig, M. T., Bertoncini, A. A., Carpenter, K. E., Cheung, W. W. L., Choat, J. H., Cornish, A. S., Fennessy, S. T., Ferreira, B. P., Heemstra, P. C., Liu, M., Myers, R. F., Pollard, D. A., Rhodes, K. L., Rocha, L. A., Russell, B. C., Samoilys, M. A., and Sanciangco, J. (2013). Fishing groupers towards extinction: a global assessment of threats and extinction risks in a billion dollar fishery. Fish and Fisheries 14, 119–136.
| Fishing groupers towards extinction: a global assessment of threats and extinction risks in a billion dollar fishery.Crossref | GoogleScholarGoogle Scholar |
Schwamborn, S. H. L., and Ferreira, B. P. (2002). Age structure and growth of the dusky damselfish, Stegastes fuscus, from Tamandaré reefs, Pernambuco, Brazil. Environmental Biology of Fishes 63, 79–88.
| Age structure and growth of the dusky damselfish, Stegastes fuscus, from Tamandaré reefs, Pernambuco, Brazil.Crossref | GoogleScholarGoogle Scholar |
Shapiro, D. Y. (1987). Reproduction in groupers. In ‘Tropical Snappers and Groupers – Biology and Fisheries Management’. (Eds J. J. Polovina and S. Ralston.) pp. 295–327. (Westview Press: Boulder, CO, USA.)
Siau, Y. (1994). Population structure, reproduction and sex-change in a tropical East Atlantic grouper. Journal of Fish Biology 44, 205–211.
| Population structure, reproduction and sex-change in a tropical East Atlantic grouper.Crossref | GoogleScholarGoogle Scholar |
Teixeira, S. F., Ferreira, B. P., and Padovan, I. P. (2004). Aspects of fishing and reproduction of the black grouper Mycteroperca bonaci (Poey, 1860) (Serranidae: Epinephelinae) in the Northeastern Brazil. Neotropical Ichthyology 2, 19–30.
| Aspects of fishing and reproduction of the black grouper Mycteroperca bonaci (Poey, 1860) (Serranidae: Epinephelinae) in the Northeastern Brazil.Crossref | GoogleScholarGoogle Scholar |
Vijay Anand, P. E., and Pillai, N. G. K. (2002). Reproductive biology of some common coral reef fishes of the Indian EEZ. Journal of the Marine Biological Association of India 44, 122–135.
