Skip to main content
SpringerLink
Log in

Genetic evidences of non-reproductive shoaling in the freshwater fish Salminus brasiliensis

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Recent studies have identified patterns of genetic organization during schooling in the reproductive period of several Neotropical freshwater migratory fish. However, population segregation during non-reproductive periods is still unknown for most species. In this study, we investigated the genetic structure of populations of Salminus brasiliensis, a high-value large migratory freshwater fish, sampled during the non-reproductive season. We analysed 89 adults from Uruguay River Basin (Brazil) collected during the two consecutive non-reproductive periods, and assessed the genetic diversity levels using eleven microsatellite loci. Our results showed that populations are genetically structured, suggesting these fish can remain grouped likely due to a cooperative behaviour, not related to reproduction, in a typical shoaling behaviour. Besides, we found high genetic diversity for S. brasiliensis from the Turvo State Park area, highlighting the importance of this conservation unit as a relevant area for maintaining the genetic variability of S. brasiliensis in the Uruguay River.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aljanabi, S. M. & I. Martinez, 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic acids research 25: 4692–4693.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batista, J. S. & 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.

    PubMed  Google Scholar 

  • Braga-Silva, A. & P. M. Galetti, 2016. Evidence of isolation by time in freshwater migratory fish Prochilodus costatus (Characiformes, Prochilodontidae). Hydrobiologia 765: 159–167.

    Article  Google Scholar 

  • Carolsfeld, Y. & B. Harvey, 2003. Introduction: fishes of the floods. In Carolsfeld, J., B. Harvey, A. Baer & C. Ross (eds), Migratory fishes of South America: biology, fisheries and conservation status. International Development Research Centre and the World Bank, Victoria.

    Google Scholar 

  • Danzmann, R. G., M. M. Ferguson & D. L. G. Noakes, 1993. The genetic basis of fish behaviour. In Pitcher, T. J. (ed.), Behaviour of Teleost Fishes. Chapman & Hall, London.

    Google Scholar 

  • Delcourt, J. & P. Poncin, 2012. Shoals and schools: back to the heuristic definitions and quantitative references. Reviews in Fish Biology and Fisheries 22(3): 595–619.

    Article  Google Scholar 

  • Earl, D. & B. VonHoldt, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite v. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Falush, D. D., M. M. Stephens & J. K. Pritchard, 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567–1587.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Godoy, M. P., 1975. Peixes do Brasil, subordem Characoidei: bacia do rio Mogí Guassú. Editora Franciscana, Pirassununga.

    Google Scholar 

  • Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (v. 2.9. 3).

  • Goulding, M., 1980. The Fishes and the Forest: Explorations in Amazonian Natural History. University of California Press, Berkeley.

    Google Scholar 

  • Hatanaka, T. & P. M. Galetti Jr., 2003. RAPD markers indicate the occurrence of structured populations in a migratory freshwater fish species. Genetics and Molecular Biology 26: 19–25.

    Article  CAS  Google Scholar 

  • Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24(11): 1403–1405.

    Article  CAS  PubMed  Google Scholar 

  • Jombart, T., S. Devillard, A. B. Dufour & D. Pontier, 2008. Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101(1): 92–103.

    Article  CAS  PubMed  Google Scholar 

  • Jost, L., 2008. GST and its relatives do not measure differentiation. Molelucar Ecology 17: 4015–4026.

    Article  Google Scholar 

  • Jueterbock, A., P. Kraemer, G. Gerlach, J. Deppermann & M. A. Jueterbock, 2012. Package “DEMEtics”. Molecular Ecology 19: 3845–3852.

    Google Scholar 

  • Leberg, P. L., 2002. Estimating allelic richness: effects of sample size and bottlenecks. Molecular Ecology 11: 2445–2449.

    Article  CAS  PubMed  Google Scholar 

  • Lowe-McConnell, R. H., 1967. Ecological Studies in Tropical Fish Communities. Cambridge University Press, Cambridge.

    Google Scholar 

  • Lucas, M. C. & E. Baras, 2001. Migration of Freshwater Fishes. Blackwell Science, Oxford.

    Book  Google Scholar 

  • Myers, G. S., 1949. Usage of anadromous, catadromous and allied terms for migratory fishes. Copeia 1949: 89–97.

    Article  Google Scholar 

  • Peakall, R. & P. E. Smouse, 2006. Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.

    Article  Google Scholar 

  • Pereira, L. H. G., F. Foresti & C. Oliveira, 2009. Genetic structure of the migratory catfish Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) suggests homing behaviour. Ecology of Freshwater Fish 18: 215–225.

    Article  Google Scholar 

  • Pitcher, T. J., 1983. Heuristic definitions of fish shoaling behaviour. Animal Behavior 31: 611–613.

    Article  Google Scholar 

  • Pitcher, T. J., 1986. Functions of shoaling behaviour in teleosts. In Pitcher, T. J. (ed.), The Behaviour of Teleost Fishes. Springer, Boston.

    Chapter  Google Scholar 

  • Pitcher, T. J. & J. K. Parrish, 1993. Functions of shoaling behaviour in teleosts. In Pitcher, T. J. (ed.), Behaviour of Teleost Fishes. Chapman & Hall, London.

    Chapter  Google Scholar 

  • Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team, R., 2017. R: A Language and Environment for Statistical Computing. Vienna, R Foundation for Statistical Computing.

    Google Scholar 

  • Raymond, M. & F. Rousset, 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of heredity 86: 248–249.

    Article  Google Scholar 

  • Reynalte-Tataje, D. A., A. P. Nuñer, M. C. Nunes, V. Garcia, C. A. Lopes & E. Zaniboni-Filho, 2012. Spawning of migratory fish species between two reservoirs of the upper Uruguay River, Brazil. Neotropical Ichthyology 10(4): 829–835.

    Article  Google Scholar 

  • Ribeiro, M. B. L. B., 1983. As migrações dos jaraquis (Pisces, Prochilodontidae) no rio Negro, Amazonas, Brasil. Masters Dissertation, INPA/FUA. Manaus, 192 p.

  • Ribolli, J., D. J. Hoeinghaus, J. A. Johnson, E. Zaniboni-Filho, P. D. de Freitas & P. M. Galetti, 2017. Isolation-by-time population structure in potamodromous Dourado Salminus brasiliensis in southern Brazil. Conservation Genetics 18: 67–76.

    Article  Google Scholar 

  • Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.

    Article  PubMed  Google Scholar 

  • Rueda, E. C., P. Carriquiriborde, A. M. Monzón, G. M. Somoza & G. Ortí, 2013. Seasonal variation in genetic population structure of sábalo (Prochilodus lineatus) in the Lower Uruguay River. Genetica 141: 401–407.

    Article  PubMed  Google Scholar 

  • Ruschel, A. R., R. O. Nodari & B. M. Moerschbacher, 2007. Woody plant species richness in the Turvo State park, a large remnant of deciduous Atlantic forest, Brazil. Biodiversity Conservation 16: 1699–1714.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Schork, G., S. Hermes-Silva, L. F. Beux, E. Zaniboni-Filho & A. P. O. Nuñer, 2012. Diagnóstico da pesca artesanal na usina hidrelétrica de machadinho, alto Rio Uruguai – Brasil. Boletim do Instituto de Pesca 38: 97–108.

    Google Scholar 

  • Schork, G., S. Hermes-Silva & E. Zaniboni-Filho, 2013. Analysis of fishing activity in the Itá reservoir, Upper Uruguay River, in the period 2004-2009. Brazilian Journal of Biology 73: 559–571.

    Article  CAS  Google Scholar 

  • Schuelke, M., 2000. An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18(2): 233–234.

    Article  CAS  PubMed  Google Scholar 

  • Slatkin, M., 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457–462.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Weir, B. S. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.

    CAS  PubMed  Google Scholar 

  • Zaniboni-Filho, E., 1985. Biologia da reprodução do matrinxã, Bricon cephalus (Günther, 1869) (Teleostei: Characidae). Masters dissertation, INPA/FUA. Manaus, Brazil, 134 p.

  • Zaniboni-Filho, E. & U. H. Schulz, 2003. Migratory fishes of the Uruguay River. In Carolsfeld, J., B. Harvey, A. Baer & C. Ross (eds), Migratory Fishes of South America: Biology, Fisheries and Conservation Status. International Development Research Centre and the World Bank, Victoria.

    Google Scholar 

  • Ziober, S. R., D. A. Reynalte-Tataje & E. Zaniboni-Filho, 2015. The importance of a conservation unit in a subtropical basin for fish spawning and growth. Environmental Biology of Fishes 98: 725–737.

    Article  Google Scholar 

Download references

Acknowledgements

JR acknowledges the financial support provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Programa de Doutorado Sanduíche no Exterior (PDSE) (process1592/81-2). PMGJ thanks Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Grant 2010/52315-7), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, 308385/2014-4) and Sistema Nacional de Pesquisa em Biodiversidade (SISBIOTA-Brazil, MCTI/CNPq 563299/2010-0). EZF thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Grant 302860/2014-2). We are grateful to Laboratório de Biologia e Cultivo de Peixes de Água Doce (LAPAD) of Universidade Federal de Santa Catarina (UFSC), Pedro Iaczinki and local fishermen for help with fish collections. The authors thank the two anonymous reviewers for valuable contributions improving the manuscript. Research was conducted under Animal Care Protocol PP00788.

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Ecologia e Recursos Naturais, Universidade Federal de São Carlos, Rodovia Washington Luís Km 235, São Carlos, SP, 13565-905, Brazil

    Josiane Ribolli

  2. Laboratório de Biologia e Cultivo de Peixes de Água Doce, Departamento de Aquicultura, Universidade Federal de Santa Catarina, Rodovia SC 406, 3532, Lagoa do Peri, Florianópolis, SC, Brazil

    Josiane Ribolli & Evoy Zaniboni-Filho

  3. Laboratório de Biodiversidade Molecular e Conservação, Departamento de Genética e Evolução, Universidade Federal de São Carlos, Rodovia Washington Luís Km 235, São Carlos, SP, 13565-905, Brazil

    Josiane Ribolli, Patricia D. Freitas & Pedro M. Galetti Jr.

Authors
  1. Josiane Ribolli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Evoy Zaniboni-Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patricia D. Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pedro M. Galetti Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Josiane Ribolli.

Additional information

Handling editor: Christian Sturmbauer

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1 (PDF 159 kb)

10750_2018_3550_MOESM2_ESM.tif

Fig. S2 Plots displays mean log-likelihood values (LnP (D)) and Evanno´s Delta K generated in STRUCTURE HARVESTER based in 89 Salminus brasiliensis from Uruguay River Basin. STRUCTURE analysis was performed with six independent runs for K = 1-10 were performed at 500,000 Markov Chain Monte Carlo (MCMC) repetitions after a burn-in period of 300,000 iterations. Delta K results indicated that samples comprise two populations (K = 2) (TIFF 17982 kb)

10750_2018_3550_MOESM3_ESM.tif

Fig. S3 Discriminant Analysis of Principal Components (DAPC). (a) Density of individual scores on the first discriminant function, with groups represented in red (Pop-2011) and blue (Pop-2011). (b) Membership probabilities (in bar plots), represent individuals in different clusters. (TIFF 119 kb)

Table S4 (DOCX 21 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ribolli, J., Zaniboni-Filho, E., Freitas, P.D. et al. Genetic evidences of non-reproductive shoaling in the freshwater fish Salminus brasiliensis. Hydrobiologia 815, 65–72 (2018). https://doi.org/10.1007/s10750-018-3550-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3550-y

Keywords

Search

Navigation