Scientia Marina, Vol 80, No 4 (2016)

Population genetic structure of an estuarine and a reef fish species exploited by Brazilian artisanal fishing

Regina H.G. Priolli
Fisheries and Food Institute, FIFO, PPG Ecomar, UNISANTA - Nepa, Capesca, UNICAMP , Brazil

Miklos M. Bajay
Department of Genetics, ESALQ, USP , Brazil

Renato A.M. Silvano
Fisheries and Food Institute, FIFO, PPG Ecomar, UNISANTA - Department of Ecology, UFRGS , Brazil

Alpina Begossi
Fisheries and Food Institute, FIFO, PPG Ecomar, UNISANTA - Nepa, Capesca, UNICAMP , Brazil


In this study, we used microsatellite markers to examine the genetic structures of Centropomus undecimalis (Bloch, 1792) and Epinephelus marginatus (Lowe, 1834) populations collected from artisanal fishing sites along a stretch of coastline in southeastern Brazil. Based on F-statistics, there was no significant genetic differentiation evident in any C. undecimalis samples (FST=0.012). However, Bayesian clustering, principal component analysis (PCA) and discriminant analysis of principal components (DAPC) results suggested that there were most likely two clusters, with no relation to geographic areas. The bottleneck results showed no significant values and the effective population sizes (Ne) for the two genetically differentiated groups were large and similar. In contrast, for E. marginatus populations, the microsatellite loci showed no population subdivisions. The FST value was low and non-significant (FST=0.008), a Bayesian analysis indicated one cluster, and a PCA showed that all samples from different geographical sites shared the same genetic structure. The bottleneck results exhibited significant differences, and a low Ne was observed. The results of the genetic study of these two species along the southeastern Brazilian coast suggest that the distinct genetic structure of each species should be taken into account as management units for the conservation of their genetic diversities.


small-scale fisheries; microsatellites; genetic diversity; common snook; dusky grouper; bottleneck

Full Text:



Able, K.W. 2005. A re-examination of fish estuarine dependence: Evidence for connectivity between estuarine and ocean habitats. Estuar. Coast. Shelf Sci. 64: 5-17.

Aliaume C., Zerbi A., Joyeux J., et al. 2000. Growth of juvenile Centropomus undecimalis in a tropical island. Environ. Biol. Fishes. 59: 299-308.

Almeida F.S., Fungaro M.H.P., Sodré L.M.K. 2001. RAPD and isoenzyme analysis of genetic variability in three allied species of catfishes (Siluriformes Pimelodidae) from the Tibagi river, Brazil. J. Zool. 253: 113-120.

Amorim P., Westmeyer M. 2016. Snapper and Grouper: SFP Fisheries Sustainability Overview 2015. Sustainable Fisheries Partnership Foundation. 18 pp. Available from:

Anderson A.B., Bonaldo R.M., Barneche D.R., et al. 2014. Recovery of grouper assemblages indicates effectiveness of a marine protected area in Southern Brazil. Mar. Ecol. Prog. Ser. 514: 207-215.

Andrade A.B., Machado L.F., Hostim-Silva M., et al. 2003. Reproductive biology of the dusky goruper Epinephelus marginatus (Lowe, 1834). Braz. Arch. Biol. Techn. 46: 373-381.

Andrello M., Mouillot D., Beuvier J., et al. 2013. Low connectivity between Mediterranean marine protected areas: a biophysical modeling approach for the dusky grouper Epinephelus marginatus. Plos One 8: e68564. PMid:23861917 PMCid:PMC3704643

Begossi A., Salivonchyk S.V., Hanazaki N., et al. 2012a. Fishers (Paraty, RJ) and fish manipulation time: a variable associated to the choice for consumption and sale. Braz. J. Biol. 72: 973-975. PMid:23295533

Begossi A., Salyvonchyk S., Nora V., et al. 2012b. The paraty artisanal fishery (southeastern Brazilian coast): ethnoecology and management of a social-ecological system (SES). J. Ethnobiol. Ethnomed. 8: 22-40. PMid:22738073 PMCid:PMC3476967

Benevides E.A., Vallinoto M.N.S., Fetter Filho A.F.H., et al. 2014. When physical oceanography meets population genetics: The case study of the genetic/evolutionary discontinuity in the endangered goliath grouper (Epinephelus itajara; Perciformes: Epinephelidae) with comments on the conservation of the species. Biochem. Syst. Ecol. 56: 255-266.

Bouchereau J.L., Body P., Chauvet C. 1999. Growth of the dusky grouper Epinephelus marginatus (Linnnaeus, 1758) (Teleostei, Serranidae), in the natural marine reserve of Lavezzi Islands, Corsica, France. Sci. Mar. 63: 71-77.

Brookfield J.F.Y. 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 5: 453-455. PMid:8688964

Caselle J.E., Hamilton S.L., Schroeder D.M., et al. 2011 Geographic variation in density, demography, and life history traits of a harvested, sex-changing, temperate reef fish. Can. J. Fish. Aquat. Sci. 68: 288-303.

Chapman R.W., Sedberry G.R., Koenig C.C., et al. 1999. Stock identification of gag, Mycteroperca microlepis, along the southeast coast of the United States. Mar. Biotechnol. 1: 137-146.

Chapuis M.P., Estoup A. 2007. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24: 621-631. PMid:17150975

Cornuet J.M., Luikart G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014. PMid:8978083 PMCid:PMC1207747

Damasceno J.S., Siccha-Ramirez R., Morales M.J.A., et al. 2015. Mitochondrial DNA evidences reflect an incipient population structure in Atlantic goliath grouper (Epinephelus itajara, Epinephelidae) in Brazil. Sci. Mar. 79: 419-429.

De Innocentiis S., Sola L., Cataudella S., et al. 2001. Allozyme and microsatellite loci provide discordant estimates of population differentiation in the endangered dusky grouper (Epinephelus marginatus) within the Mediterranean Sea. Mol. Ecol. 10: 2163-2175. PMid:11555259

De Oliveira J.N., Gomes G., do Rego P.S., et al. 2014. Molecular data indicate the presence of a novel species of Centropomus (Centropomidae - Perciformes) in the Western Atlantic. Mol. Phylogenet. Evol. 77: 275-280. PMid:24792089

De Souza A.S., Dias E.A. Jr., Galetti P.M. Jr., et al. 2015. Wide-range genetic connectivity of Coney, Cephalopholis fulva (Epinephelidae), through oceanic islands and continental Brazilian coast. An. Acad. Bras. Cienc. 87: 121-136. PMid:25806980

Dempster A.P., Laird N.M., Rubin D.B. 1977. Maximum likelihood from incomplete data via em algorithm. J. R. Stat. Soc. Ser. B. Methodol. 39: 1-38.

DeWoody J.A., Avise J.C. 2000. Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J. Fish. Biol. 56: 461-473.

Earl D.A., VonHoldt B.M. 2012. Structure Harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conserv. Genet. Resour. 4: 359-361.

Evanno G., Regnaut S., Goudet J. 2005. Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol. Ecol. 14: 2611-2620. PMid:15969739

Excoffier L., Laval G., Schneider S. 2005. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol. Bioinform. 1: 47-50.

Fitzpatrick B.M. 2009. Power and sample size for nested analysis of molecular variance. Mol. Ecol. 18: 3961-3966. PMid:19754511

Frankham R. 2010. Challenges and opportunities of genetic approaches to biological conservation. Biol. Conserv. 143: 1919-1927.

Ginestet C. 2011. GGPLOT2: Elegant Graphics for Data Analysis. J. R. Stat. Soc. Ser. A Stat. Soc. 174: 245-246.

Goudet J. 1995. FSTAT (Version 1.2): A computer program to calculate F-statistics. J. Hered. 86: 485-486.

Hereu B., Diaz D., Pasqual J., et al. 2006. Temporal patterns of spawning of the dusky grouper Epinephelus marginatus in relation to environmental factors. Mar. Ecol. Prog. Ser. 325: 187-194.

Hernandez-Vidal U., Lesher-Gordillo J., Contreras-Sanchez W.M., et al. 2014. Genetic variability of the Common Snook Centropomus undecimalis (Perciformes: Centropomidae) in connected marine and riverine environments. Rev. Biol. Trop. 62: 627-636. PMid:25102645

Hubisz M.J., Falush D., Stephens M., et al. 2009. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9: 1322-1332. PMid:21564903 PMCid:PMC3518025

Jakobsson M., Rosenberg N.A. 2007. Clumpp: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801-1806. PMid:17485429

Jombart T. 2008. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403-1405. PMid:18397895

Jombart T., Devillard S., Balloux F. 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010, 11: 94. PMid:20950446 PMCid:PMC2973851

King J.R., McFarlane G.A. 2003. Marine fish life history strategies: applications to fishery management. Fisheries Manag. Ecol. 10: 249-264.

Latch E.K, Dharmarajan G., Glaubitz J.C., et al. 2006. Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv. Genet. 7: 295-302.

Lopes P.F.M, Rosa E.M., Salyvonchyk S., et al. 2013. Suggestions for fixing top-down coastal fisheries management through participatory approaches. Mar. Policy 40: 100-110.

McClanahan T.R., Marnane M.J., Cinner J.E., et al. 2006. A comparison of marine protected areas and alternative approaches to coral-reef management. Curr. Biol. 16: 1408-1413. PMid:16860739

Mumby P.J., Harborne A.R., Brumbaugh D.R. 2011. Grouper as a Natural Biocontrol of Invasive Lionfish. PLoS One 6: e21510. PMid:21731769 PMCid:PMC3121772

Paradis E., Claude J., Strimmer K. 2004. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20: 289-290. PMid:14734327

Peery M.Z., Kirby R., Reid B.N., et al. 2012. Reliability of genetic bottleneck tests for detecting recent population declines. Mol. Ecol. 21: 3403-3418. PMid:22646281

Perera M.A., Mendoza M., Contreras W.M., et al. 2011. Reproductive biology of common snook Centropomus undecimalis (Perciformes: Centropomidae) in two tropical habitats. Rev. Biol. Trop. 59: 669-681.

Perera-Garcia M.A., Mendoza-Carranza M., Contreras-Sanchez W., et al. 2013. Comparative age and growth of common snook Centropomus undecimalis (Pisces: Centropomidae) from coastal and riverine areas in Southern Mexico. Rev. Biol. Trop. 61: 807-819. PMid:23885591

Peters K.M., Matherson R.E., Taylor R.G. 1998. Reproduction and early hsitory of common snook, Centropomus undecimalis (Bloch), in Florida. Bull. Mar. Sci. 62: 509-529.

Peterson M.S., Gilmore R.G. 1991. Eco-physiology of juvenile snook Centropomus undecimalis (Bloch) - Life-history implications . Bull. Mar. Sci. 48: 46-57.

Pinnegar J.K., Engelhard G.H. 2008. The 'shifting baseline' phenomenon: a global perspective. Rev. Fish. Biol. Fish. 18: 1-16.

Piry S., Luikart G., Cornuet J.M. 1999. Bottleneck: A computer program for detecting recent reductions in the effective population size using allele frequency data. J. Heredity 90: 502-503.

Priolli R.H.G., Stabelini N.S., Bajay M.M. 2014. Diversidade genética de uma espécie em perigo de extinção: a garoupa Epinephelus marginatus. In Begossi A., Lopes P.F.M. (eds), Comunidades pesqueiras de Paraty sugestões para manejo. RiMa Editora, São Carlos, pp. 27-40.

Pritchard J.K., Stephens M., Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959. PMid:10835412 PMCid:PMC1461096

R Development Core Team. 2015. R: A language and environment for statistical computing. The R Foundation for Statistical Computing. Vienna, Austria. Available online at

Ramirez M.A., Patricia-Acevedo J., Planas S., et al. 2006. New microsatellite resources for groupers (Serranidae). Mol. Ecol. Notes 6: 813-817.

Raymond M., Rousset F. 1995. GENEPOP (version-1.2) - population-genetics software for exact tests and ecumenicism. J. Heredity 86: 248-249.

Rice W.R. 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.

Rivera M.A.J., Graham G.C., Roderick G.K. 2003. Isolation and characterization of nine microsatellite loci from the Hawaiian grouper Epinephelus quernus (Serranidae) for population genetic analyses. Mar. Biotechnol. 5: 126-129. PMid:12876647

Ryman N., Palm S. 2006. POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol. Ecol Notes 6: 600-602.

Ryman N, Palm S, André C., et al. 2006. Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol. Ecol. 15: 2031-2045. PMid:16780422

Schunter C., Carreras-Carbonell J., Planes S., et al. 2011. Genetic connectivity patterns in an endangered species: The dusky grouper (Epinephelus marginatus). J. Exp. Mar. Biol. Ecol. 401: 126-133.

Seyoum S., Tringali M.D., Sullivan J.G. 2005. Isolation and characterization of 27 polymorphic microsatellite loci for the common snook, Centropomus undecimalis. Mol. Ecol. Notes 5: 924-927.

Shiozawa D.K., Kudo J., Evans R.P., et al. 1992. DNA extraction from preserved trout tissues. Gt. Basin Nat. 52: 29-34.

Silva-Oliveira G.C., do Rego P.S., Schneider H., et al. 2008. Genetic characterisation of populations of the critically endangered Goliath grouper (Epinephelus itajara, Serranidae) from the Northern Brazilian coast through analyses of mtDNA. Genet. Mol. Biol. 31: 988-994.

Silvano R.A.M., Begossi A. 2012. Fishermen's local ecological knowledge on Southeastern Brazilian coastal fishes: contributions to research, conservation, and management. Neotrop. Ichthyol. 10: 133-147.

Silvano R.A.M., MacCord P.F.L., Lima R.V., et al. 2006. When does this fish spawn? Fishermen's local knowledge of migration and reproduction of Brazilian coastal fishes. Environ. Biol. Fish. 76: 371-386.

Snedecor G.W., Cochran W.G. 1989. Statistical Methods, 8th ed. Iowa State University Press, Ames.

Spedicato M.T., Contegiacomo M., Carbonara P., et al. 1998. Artificial reproduction of Epinephelus marginatus aimed at the development of restocking techniques. Biol. Mar. Mediterr. 5: 1248-1257.

Taylor R.G., Whittington J.A., Grier H.J., et al. 2000. Age, growth, maturation, and protandric sex reversal in common snook, Centropomus undecimalis, from the east and west coasts of South Florida. Fish. Bull. 98: 612-624.

Tringali M.D., Bert T.M. 1996. The genetic stock structure of common snook (Centropomus undecimalis). Can. J. Fish Aquat. Sci. 53: 974-984.

Tringali M.D., Seyoum S., Wallace E.M., et al. 2008. Limits to the use of contemporary genetic analyses in delineating biological populations for restocking and stock enhancement. Rev. Fish. Sci. 16: 111-116.

Van Oosterhout C., Hutchinson W.F., Wills D.P.M., et al. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4: 535-538.

Vasconcellos A.V., Vianna P., Paiva P.C., et al. 2008. Genetic and morphometric differences between yellowtail snapper (Ocyurus chrysurus, Lutjanidae) populations of the tropical West Atlantic. Genet. Mol. Biol. 31: 308-316.

Waldie P.A., Almany, G.R., Sinclair-Taylor T.H., et al. 2016. Restricted grouper reproductive migrations support community-based management. R. Soc. Open Sci. 3: 150694. PMid:27069662 PMCid:PMC4821273

Waples R.S., Do C. 2008. LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol. Ecol. Resour. 8: 753-756. PMid:21585883

Copyright (c) 2016 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