, Volume 805, Issue 1, pp 75–88 | Cite as

From river to farm: an evaluation of genetic diversity in wild and aquaculture stocks of Brycon amazonicus (Spix & Agassiz, 1829), Characidae, Bryconinae

  • Roberta Cunha de Oliveira
  • Maria da Conceição Freitas Santos
  • Geraldo Bernardino
  • Tomas Hrbek
  • Izeni Pires Farias
Primary Research Paper


Brycon amazonicus is widely distributed in the Amazon basin. The species has traditionally been the focus of subsistence and commercial fisheries, and recently has become an important aquaculture species. Aquaculture relies on the removal of individuals from nature which form the basis of breeding stocks. The breeding stocks are often derived from local populations, but equally often are a mix of fishes from different regions or from other aquaculture stations. In this study, we found that B. amazonicus forms just one population in the central Amazon basin, and most animals in the aquaculture stations originated from this group. However, fishes from the Balbina aquaculture station represent another biological group, while the fishes in the experimental station of the Federal University of Amazonas are an admixed group. Fishes of the aquaculture stations are differentiated from each other and from the wild fish. Genetic diversity of the aquaculture fishes was not different from the wild fishes, and thus, inbreeding is unlikely to be a concern. Outbreeding depression, however, should be of concern given the observed levels of admixture in the aquaculture stocks. We conclude the article with recommendations for good practices to minimize the likelihood of inbreeding and outbreeding depression.


Genetic variability Microsatellite Matrinxã Amazon basin 



This research was supported by Grants from FINEP/DARPA (Convênio No. 01.09.0472.00) to IPF and GB. This study formed a portion of ROC PIBIC undergraduate program at UFAM. IPF and TH are supported by Bolsa de Pesquisa scholarship from CNPq, and ROC was supported by a fellowship from FAPEAM.

Supplementary material

10750_2017_3278_MOESM1_ESM.eps (809 kb)
Supplementary Figure S1 Schematic illustration of allelic frequencies at 10 studied microsatellite loci. Circles represent distinct alleles, and their areas are directly proportional to their frequencies. Supplementary material 1 (EPS 809 kb)


  1. Aguiar, J., H. Schneider, F. Gomes, J. Carneiro, S. Santos, L. R. Rodrigues & I. Sampaio, 2013. Genetic variation in native and farmed populations of Tambaqui (Colossoma macropomum) in the Brazilian Amazon: Regional discrepancies in farming systems. Anais da Academia Brasileira de Ciencias 85: 1439–1447.CrossRefPubMedGoogle Scholar
  2. Amado, M. V., I. P. Farias & T. Hrbek, 2011. A molecular perspective on systematics, taxonomy and classification amazonian discus fishes of the genus Symphysodon. International Journal of Evolutionary Biology 2011: 360654. doi: 10.4061/2011/360654.
  3. Ashikaga, F. Y., M. L. Orsi, C. Oliveira, J. A. Senhorini & F. Foresti, 2015. The endangered species Brycon orbignyanus: Genetic analysis and definition of priority areas for conservation. Environmental Biology of Fishes 98: 1845–1855.CrossRefGoogle Scholar
  4. Azevedo-Santos, V. M., O. Rigolin-Sá & F. M. Pelicice, 2011. Growing, losing or introducing? Cage aquaculture as a vector for the introduction of non-native fish in Furnas Reservoir, Minas Gerais, Brazil. Neotropical Ichthyology 9: 915–919.CrossRefGoogle Scholar
  5. Barroso, R. M., A. W. S. Hilsdorf, H. L. M. Moreira, A. M. Mello, S. E. F. Guimarães, P. H. Cabello & Y. M. Traub-Cseko, 2003. Identification and characterization of microsatellites loci in Brycon opalinus (Cuvier 1819)(Characiforme, Characidae, Bryconiae). Molecular Ecology Notes 3: 297–298.CrossRefGoogle Scholar
  6. Barroso, R. M., A. W. S. Hilsdorf, H. L. M. Moreira, P. H. Cabello & Y. M. Traub-Cseko, 2005. Genetic diversity of wild and cultured populations of Brycon opalinus (Cuvier, 1819) (Characiforme, Characidae, Bryconiae) using microsatellites. Aquaculture 247: 51–65.CrossRefGoogle Scholar
  7. da Batista, V. S., 1999. Biologia e administração pesqueira de alguns Characiformes explorados na Amazônia Central. Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus.Google Scholar
  8. da Batista, J., S. da & J. A. Alves-Gomes, 2006. Phylogeography of Brachyplatystoma rousseauxii (Siluriformes—Pimelodidae) in the Amazon Basin offers preliminary evidence for the first case of “homing” for an Amazonian migratory catfish. Genetics and Molecular Research 5: 723–740.PubMedGoogle Scholar
  9. Bernardino, R. M., J. A. Senhorini & C. L. Bock, 1993. Propagação artificial do matrinxã Brycon cephalus (Günther, 1869) (Teleostei, Characidae). Boletim Técnico CEPTA 6: 1–9.Google Scholar
  10. Castagnolli, N., 1992. Criação de peixes de água doce. FUNEP, Jaboticabal.Google Scholar
  11. Chistiakov, D. A., B. Hellemans & F. A. M. Volckaert, 2006. Microsatellites and their genomic distribution, evolution, function and applications: A review with special reference to fish genetics. Aquaculture 255: 1–29.CrossRefGoogle Scholar
  12. DeWoody, J. A., J. Schupp, L. Kenefic, J. Busch, L. Murfitt & P. Keim, 2004. Universal method for producing ROX-labeled size standards suitable for automated genotyping. Biotechniques 37: 348–352.PubMedGoogle Scholar
  13. Do, C., R. S. Waples, D. Peel, G. M. Macbeth, B. J. Tillett & J. R. Ovenden, 2014. NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Molecular Ecology Resources 14: 209–214. doi: 10.1111/1755-0998.12157.
  14. Earl, D. A. & B. M. VonHoldt, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.CrossRefGoogle Scholar
  15. Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology 14: 2611–2620.CrossRefPubMedGoogle Scholar
  16. Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.CrossRefPubMedGoogle Scholar
  17. Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131: 479–491.PubMedPubMedCentralGoogle Scholar
  18. Farias, I. P., J. P. Torrico, C. García-Dávila, M. D. C. F. Santos, T. Hrbek & J. F. Renno, 2010. Are rapids a barrier for floodplain fishes of the Amazon basin? A demographic study of the keystone floodplain species Colossoma macropomum (Teleostei: Characiformes). Molecular Phylogenetics and Evolution 56: 1129–1135.CrossRefPubMedGoogle Scholar
  19. Filho, L. C. S. & V. D. S. Batista, 2009. Dinâmica populacional da matrinxã Brycon amazonicus (Characidae) na Amazônia Central. Zoologia (Curitiba) 26: 195–203.CrossRefGoogle Scholar
  20. Frankham, R., J. D. Ballou & D. A. Briscoe, 2002. Introduction to Conservation Genetics. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  21. Flowers, J. M., S. C. Schroeter & R. S. Burton, 2002. The recruitment sweepstakes has many winners: Genetic evidence from the sea urchin Strongylocentrotus purpuratus. Evolution 56: 1445–1453.CrossRefPubMedGoogle Scholar
  22. Frederico, R. G., I. P. Farias, M. L. G. Araújo, P. Charvet-Almeida & J. A. Alves-Gomes, 2012. Phylogeography and conservation genetics of the Amazonian freshwater stingray Paratrygon aiereba Müller & Henle, 1841 (Chondrichthyes: Potamotrygonidae). Neotropical Ichthyology 10: 71–80.CrossRefGoogle Scholar
  23. Gilk, S. E., I. A. Wang, C. L. Hoover, W. W. Smoker, S. G. Taylor, A. K. Gray & A. J. Gharrett, 2004. Outbreeding depression in hybrids between spatially separated pink salmon, Oncorhynchus gorbuscha, populations: Marine survival, homing ability, and variability in family size. Environmental Biology of Fishes 69: 287–297.CrossRefGoogle Scholar
  24. Gomes, L. C. & J. R. Urbinati, 2005. Criação de matrinxã. In Baldisserotto, B. & L. C. Gomes (eds), Especies nativas para piscicultura no Brasil. Editora UFSM, Santa Maria: 149–174.Google Scholar
  25. Goulding, M., 1980. Fishes and the Forest: Explorations in Amazonian Natural History. University of California press, Los Angeles.Google Scholar
  26. Hoshiba, M. A., 2007. Enriquecimento da alimentação das larvas de Matrinxã (Brycon amazonicus) com aminoácidos. Universidade Estadual Paulista, Jaboticabal, Influência no crescimento inicial e sobrevivência das larvas.Google Scholar
  27. Hrbek, T., I. P. Farias, M. Crossa, I. Sampaio, J. I. R. Porto & A. Meyer, 2005. Population genetic analysis of Arapaima gigas, one of the largest freshwater fishes of the Amazon basin: Implications for its conservation. Animal Conservation 8: 297–308.CrossRefGoogle Scholar
  28. Hrbek, T., M. Crossa & I. P. Farias, 2007. Conservation strategies for Arapaima gigas (Schinz, 1822) and the Amazonian várzea ecosystem. Brazilian Journal of Biology 67: 909–917.CrossRefGoogle Scholar
  29. Huff, D. D., L. M. Miller, C. J. Chizinski & B. Vondracek, 2011. Mixed-source reintroductions lead to outbreeding depression in second-generation descendents of a native North American fish. Molecular Ecology 20: 4246–4258.CrossRefPubMedGoogle Scholar
  30. Hurtado-Alarcón, J. C., N. J. Mancera-Rodríguez & C. I. Saldamando-Benjumea, 2011. Genetic variability of Brycon henni (Characiformes: Characidae) in the middle basin of Nare and Guatapé Rivers, Magdalena River system, Colombia. Revista de Biología Tropical 59: 269–282.PubMedGoogle Scholar
  31. Hutchings, J. A. & D. J. Fraser, 2008. The nature of fisheries- and farming-induced evolution. Molecular Ecology 17: 294–313.CrossRefPubMedGoogle Scholar
  32. Jakobsson, M. & N. A. Rosenberg, 2007. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801–1806.CrossRefPubMedGoogle Scholar
  33. Junk, W. J., 1997. The Central Amazon System: Ecology of a Pulsing System. Springer, Berlin.CrossRefGoogle Scholar
  34. Kalinowski, S. T., 2005. Hp-Rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes 5: 187–189. doi: 10.1111/j.1471-8286.2004.00845.x.
  35. Leberg, P. L., 2002. Estimating allelic richness: Effects of sample size and bottlenecks. Molecular Ecology 11: 2445–2449.CrossRefPubMedGoogle Scholar
  36. Lima, F. C. T., 2003. Subfamily Bryconinae (Characins, Tetras). In Reis, R. E., S. O. Kullander & C. J. Ferraris (eds), RE Check List of the Freshwater Fishes of South and Central America. EDPURCS, Porto Alegre: 174–181.Google Scholar
  37. Machado, V. N., S. C. Willis, A. S. Teixeira, T. Hrbek & I. P. Farias, 2017. Population genetic structure of the Amazonian black flannelmouth characin (Characiformes, Prochilodontidae: Prochilodus nigricans Spix & Agassiz, 1829): contemporary and historical gene flow of a migratory and abundant fishery species. Environmental Biology of Fishes 100: 1–16. doi: 10.1007/s10641-016-0547-0.CrossRefGoogle Scholar
  38. Martin, C. W., M. M. Valentine & J. F. Valentine, 2010. Competitive interactions between invasive nile tilapia and native fish: The potential for altered trophic exchange and modification of food webs. PLoS ONE 5: e14395.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Matsumoto, C. K. & A. W. S. Hilsdorf, 2009. Microsatellite variation and population genetic structure of a neotropical endangered Bryconinae species Brycon insignis Steindachner, 1877: Implications for its conservation and sustainable management. Neotropical Ichthyology 7: 395–402.CrossRefGoogle Scholar
  40. McClelland, E. K. & K. A. Naish, 2006. What is the fitness outcome of crossing unrelated fish populations? A meta-analysis and an evaluation of future research directions. Conservation Genetics 8: 397–416.CrossRefGoogle Scholar
  41. Mennerat, A., F. Nilsen, D. Ebert & A. Skorping, 2010. Intensive farming: Evolutionary implications for parasites and pathogens. Evolutionary Biology 37: 59–67.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Naylor, R. L., R. J. Goldburg, J. H. Primavera, N. Kautsky, M. C. M. Beveridge, J. Clay, C. Folke, J. Lubchenco, H. Mooney & M. Trowll, 2000. Effect of aquaculture on world fish supplies. Nature 405: 1017–1024.CrossRefPubMedGoogle Scholar
  43. Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York, NY, 512 pp.Google Scholar
  44. Nei, M. & A. K. Roychoudhury, 1974. Sampling variances of heterozygosity and genetic distance. Genetics 76: 379–390.PubMedPubMedCentralGoogle Scholar
  45. Ortega, J. C. G., H. F. Júlio Jr., L. C. Gomes & A. A. Agostinho, 2014. Fish farming as the main driver of fish introductions in Neotropical reservoirs. Hydrobiologia 746: 147–158. doi: 10.1007/s10750-014-2025-z.
  46. Palstra, F. P. & D. J. Fraser, 2012. Effective/census population size ratio estimation: a compendium and appraisal. Ecology and Evolution 2: 2357–2365. doi: 10.1002/ece3.329.
  47. Pinto, L. G. Q., 2014. Potential Fish Species in Amazonia for National Aquaculture. The Fish Site:
  48. Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedPubMedCentralGoogle Scholar
  49. Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.CrossRefPubMedGoogle Scholar
  50. Rosenberg, N. A., 2004. DISTRUCT: A program for the graphical display of population structure. Molecular Ecology Notes 4: 137–138.CrossRefGoogle Scholar
  51. Sanches, A. & P. M. Galetti Jr., 2006. Microsatellites loci isolated in the freshwater fish Brycon hilarii. Molecular Ecology Notes 6: 1045–1046.CrossRefGoogle Scholar
  52. Sanches, A. & P. M. Galetti Jr., 2007. Genetic evidence of population structuring in the Neotropical freshwater fish Brycon hilarii (Valenciennes, 1850). Brazilian Journal of Biology 67: 889–895.CrossRefGoogle Scholar
  53. Sanches, A., P. M. Galetti Jr., F. Galzerani, J. Derazo, B. Cutilak Bianchi & T. Hatanaka, 2012. Genetic population structure of two migratory freshwater fish species (Brycon orthotaenia and Prochilodus argenteus) from the São Francisco River in Brazil and its significance for conservation. Latin American Journal of Aquatic Research 40: 177–186.CrossRefGoogle Scholar
  54. Santos, M. D. C. F., M. L. Ruffino & I. P. Farias, 2007. High levels of genetic variability and panmixia of the tambaqui Colossoma macropomum (Cuvier, 1818) in the main channel of the Amazon River. Journal of Fish Biology 71A: 33–44.CrossRefGoogle Scholar
  55. Schuelke, M., 2000. An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18: 233–234.CrossRefPubMedGoogle Scholar
  56. Sioli, H., 1967. Studies in Amazonian waters. Atas do Simpósio sobre a Biota Amazônica 3: 9–50.Google Scholar
  57. Sioli, H., 1984. The Amazon and its main affluents: hydrography, morphology of the river courses and river types. Limnology and Landscape Ecology of a Mighty Tropical River and its Basin. In Sioli, H. (ed.), The Amazon. Springer, New York: 127–165.CrossRefGoogle Scholar
  58. Smith, N. J. H., 1979. A Pesca no Rio Amazonas. INPA, Manaus.Google Scholar
  59. Templeton, A. R., 1986. Coadaptation and outbreeding depression. In Soulé, M. E. (ed.), Conservation Biology: The Science of Scarsity and Diversity. Sinauer Associates, Sunderland: 105–121.Google Scholar
  60. Wright, S., 1951. The genetical structure of populations. Annals of Eugenics 15: 323–354.CrossRefPubMedGoogle Scholar
  61. Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.CrossRefGoogle Scholar
  62. Waples, R. S. & C. Do, 2008. Ldne: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources 8: 753–756. doi: 10.1111/j.1755-0998.2007.02061.x.
  63. Yousefian, M. & A. Nejati, 2008. Inbreeding depression by family matching in rainbow trout (Oncorhynchus mykiss). Journal of Fisheries and Aquatic Science 3: 384–391.CrossRefGoogle Scholar
  64. Zengeya, T. A., M. P. Robertson, A. J. Booth & C. T. Chimimba, 2013. A qualitative ecological risk assessment of the invasive Nile tilapia, Oreochromis niloticus in a sub-tropical African river system (Limpopo River, South Africa). Aquatic Conservation: Marine and Freshwater Ecosystems 23: 51–64.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Roberta Cunha de Oliveira
    • 1
  • Maria da Conceição Freitas Santos
    • 2
  • Geraldo Bernardino
    • 3
  • Tomas Hrbek
    • 1
  • Izeni Pires Farias
    • 1
  1. 1.Laboratório de Evolução e Genética Animal (LEGAL), Departamento de GenéticaUniversidade Federal do Amazonas (UFAM)ManausBrazil
  2. 2.Departamento de BiologiaUniversidade do Estado do Amazonas (UEA)ManausBrazil
  3. 3.Secretaria de Pesca (SEPROR)ManausBrazil

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