The use of an integrative approach to improve accuracy of species identification and detection of new species in studies of stream fish diversity

Abstract

In this study, we made an inventory of the stream and headwater ichthyofauna of the left bank of the Itaipu Dam Reservoir, located in the lower part of the Upper Paraná River basin, using an integrative approach of molecular and morphological data. The area is located in the western portion of the Paraná state in Brazil, in an area of about 8,000 km2 highly impacted by deforestation and intensive agriculture. For taxonomic identification of species, we used an identification key combined with the DNA barcoding approach. We found 48 species belonging to six orders, 13 families, and 37 genera. The Siluriformes and Characiformes were the most representative orders (75%) and the Characidae was the most representative family (20.8%). Nine species prevailed in this region, making up to 86% of all specimens collected. The integrative approach proved to be useful by allowing the unambiguous identification of all species, including those cases in which morphological characters were not conclusive for species identification, cases of cryptic species, and species with high morphological plasticity. In addition, the integrative approach highlighted six to 13 new putative species depending on the approach considered. Our study provides a relevant contribution to the knowledge of fish diversity in a poorly studied area of the Paraná River basin. We showed that the use of an integrative approach in inventory studies improves species identification and the discovery of new, cryptic, and overlooked species, being a powerful and necessary tool to quantify biodiversity.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Data availability

All sequences obtained were deposited in GenBank (accession numbers: MN879895—MN880048).

Code availability

Not applicable.

References

  1. Albert JS, Reis RE (2011) Historical biogeography of neotropical freshwater fishes. University of California Press, London

    Book  Google Scholar 

  2. Albert JS, Tagliacollo VA, Dagosta F (2020) Diversification of neotropical freshwater fishes. Annu Rev Ecol Evol Syst 51:27–53. https://doi.org/10.1146/annurev-ecolsys-011620-031032

    Article  Google Scholar 

  3. Albrecht M (2012) Influência da mata ciliar em parâmetros da ictiocenose e em aspectos populacionais de quatro espécies de peixes em riachos no sul do Brasil. Universidade do Vale do Rio dos Sinos, Rio Grande do Sul, Tese de mestrado

    Google Scholar 

  4. Allan JD, Castillo MM (2007) Stream Ecology: structure and function of running waters, 2nd edn. Springer, Netherlands

    Book  Google Scholar 

  5. Allan JD (2004) Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu Rev Ecol Syst 35(1):257–284. https://doi.org/10.1146/annurev.ecolsys.35.120202.110122

    Article  Google Scholar 

  6. April J, Mayden RL, Hanner R, Bernatchez L (2011) Genetic calibration of species diversity among North America´s freshwater fishes. PNAS 108(26):10602–10607. https://doi.org/10.1073/pnas.1016437108

    Article  PubMed  Google Scholar 

  7. Araújo MI, Delariva RL, Bonato KO, Silva JC (2011) Fishes in first order stream in Ivaí River drainage basin, Upper Paraná River Basin, Paraná state Brazil. Check List 7(6):774–777. https://doi.org/10.15560/11023

    Article  Google Scholar 

  8. Batista-Silva VF, Frota A, Kashiwaqui EAL, Abelha MCF, Bailly D, Gubiani EA, Graça WJ (2018) Ichthyofauna from three streams of the lower Iguatemi River in the Upper Paraná river basin, Brazil. Check List 14(2):363–378. https://doi.org/10.15560/14.2.363

    Article  Google Scholar 

  9. Bifi AG, Dias AC, Frota A (2017) Fish species (Osteichthyes: Actinopterygii) from two tributaries of the Rio do Peixe basin, Tupã municipality São Paulo state, Brazil. Check List 13(2):1–9. https://doi.org/10.15560/13.2.2063

    Article  Google Scholar 

  10. Buckup PA, Menezes NA, Ghazzi MS (2007) Catálogo das espécies de peixes de água doce do Brasil. Museu Nacional, Rio de Janeiro

    Google Scholar 

  11. Carvalho DC, Oliveira DAA, Pompeu OS, Leal CG, Oliveira C, Hanner R (2011) Deep Barcode divergence in Brazilian freshwater fishes: the case of the São Francisco River Basin. Mitochondr DNA 22(S1):80–86. https://doi.org/10.3109/19401736.2011.588214

    CAS  Article  Google Scholar 

  12. Casatti L, Langeani F, Castro RMC (2001). Peixes de riacho do Parque Estadual Morro do Diabo, bacia do alto rio Paraná, SP. Biota Neotropica, 1(1–2), 1–15. http://www.biotaneotropica.org.br/v1n12/pt/abstract?inventory+BN00201122001. Last accessed 27 Dec 2019. https://doi.org/https://doi.org/10.1590/S1676-06032001000100005.

  13. Castro RMC (1999). Evolução da ictiofauna de riachos sul-americanos: padrões gerais e possíveis processos causais. In Ecologia de Peixes de Riacho – Série Oecologia Brasiliensis. (EP Caramashi, R Mazzoni, PR Peres-Neto, eds). PPGE-UFRJ, Rio de Janeiro, p. 139–155.

  14. Castro RMC, Casatti L, Santos HF, Ferreira KM, Ribeiro AC, Benine RC et al (2003). Estrutura e composição da ictiofauna de riachos do Rio Paranapanema, sudeste e sul do Brasil. Biota Neotropica, 3(1), 1–31 http://www.biotaneotropica.org.br/v3n1/pt/abstract?article+BN01703012003. Last accessed 27 Dec 2019. https://doi.org/https://doi.org/10.1590/S1676-06032003000100007

  15. Castro MC, Casatti L, Santos HF, Melo ALA, Martins LSF, Ferreira KM, et al (2004). Estrutura e composição da ictiofauna de riachos da bacia do Rio Grande, no Estado de São Paulo, Sudeste do Brasil. Biota Neotropica, 4(1), 1–39. http://www.biotaneotropica.org.br/v4n1/pt/abstract?article+BN01704012004. Last accessed 27 Dec 2019. https://doi.org/https://doi.org/10.1590/S1676-06032004000100006

  16. Castro RMC, Casatti L, Santos HF, Vari RP, Melo ALA, Martins LSF, et al (2005). Structure and composition of the stream ichthyofauna of four tributary rivers of the Upper Rio Paraná basin, Brazil. Ichthyol. Explor. Fres., 16(3), 193–214. https://pfeil-verlag.de/wp-content/uploads/2015/05/ief16_3_01.pdf

  17. Claro-García A, Assega FM, Shibatta OA (2017) Diversity and distribution of ichthyofauna in streams of the middle and lower Tibagi river basin Paraná Brazil. Check List 14(1):43–53. https://doi.org/10.15560/114.1.43

    Article  Google Scholar 

  18. Costa-Silva GJ, Ashikaga FY, Dias CKS, Pereira LHG, Foresti F, Oliveira C (2018) DNA barcoding techniques used to identify the shared ichthyofauna between the Pantanal floodplain and Upper Paraná River. Mitochondr DNA 29(7):1063–1072. https://doi.org/10.1080/24701394.2017.1404046

    CAS  Article  Google Scholar 

  19. Cunico AM, Graça WJ, Agostinho AA, Domingues WM, Latini JD (2009) Fish, Maringá urban streams, Pirapó river drainage, Upper Paraná river basin Paraná state, Brazil. Check List 5(2):273–280. https://doi.org/10.15560/5.2.273

    Article  Google Scholar 

  20. Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85(3):407–415. https://doi.org/10.1111/j.1095-8312.2005.00503.x

    Article  Google Scholar 

  21. Dudgeon D, Arthington AH, Gessner MO, Kawabata Z, Knowler DJ, Lévêque C et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81(2):163–182. https://doi.org/10.1017/S1464793105006950

    Article  PubMed  Google Scholar 

  22. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughout. Nucleic Acids Res 32(5):1792–1797. https://doi.org/10.1093/nar/gkh340

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Felipe TRA, Súarez YR (2010). Caracterização e influência dos fatores ambientais nas assembleias de peixes de riachos em duas microbacias urbanas, alto rio Paraná. Biota Neotropica, 10(2), 143–151. http://www.biotaneotropica.org.br/v10n2/en/abstract?article+bn03810022010. Last accessed 27 Dec 2019. https://doi.org/https://doi.org/10.1590/S1676-06032010000200018

  24. Fernández L, Bechara JA (2010). An assessment of fish communities along a piedmont river receiving organic pollution (Aconquija Mountains, Argentina). Acta Biol. Colomb., 15(2), 79–100. http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0120-548X2010000200007

  25. Ferrer J, Malabarba LR (2013) Taxonomic review of the genus Trichomycterus Valenciennes (Siluriformes: Trichomycteridae) from the laguna dos Patos system. Southern Brazil Neotrop Ichthyol 11(2):217–246. https://doi.org/10.1590/S1679-62252013000200001

    Article  Google Scholar 

  26. Frézal LE, Leblois R (2008) Four years of DNA barcoding: current advances and prospects. Infect Genet Evol 8(5):727–736. https://doi.org/10.1016/j.meegid.2008.05.005

    CAS  Article  PubMed  Google Scholar 

  27. Fricke R, Eschmeyer WN, Van Der Laan R (2019). Eschmeyer´s catalog of fishes: genera, species, references. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp.Accessed. Accessed 27 Dec 2019.

  28. Froese R, Pauly D (2019). FishBase. World Wide Web electronic publication. www.fishbase.org. Accessed 27 Dec 2019.

  29. Frota A, Deprá GC, Petenucci LM, Graça WJ (2016). Inventory of the fish fauna from Ivaí river basin, Paraná state, Brazil. Biota Neotropica, 16(3), e20150151. http://dx.doi.org/https://doi.org/10.1590/1676-0611-BN-2015-0151. Last accessed 27 Dec 2019.

  30. Galves W, Shibatta O, Jerep F (2009) Estudos sobre a diversidade de peixes da bacia do alto rio Paraná: uma revisão histórica. Semina Ciências Biológicas e da Saúde 30(2):141–154. https://doi.org/10.5433/1679-0367.2009v30n2p141

    Article  Google Scholar 

  31. Galves W, Shibatta OA, Jerep FC (2007) Fish, Taquara river basin, northern of the state of Paraná, Brazil. Check List 3(3):353–359. https://doi.org/10.15560/3.3.253

    Article  Google Scholar 

  32. Gomes LC, Pessali TC, Sales NG, Pompeu PS, Carvalho DC (2015) Integrative taxonomy detects cryptic and overlooked fish species in a neotropical river basin. Genetica 143(5):581–588. https://doi.org/10.1007/s10709-015-9856-z

    Article  PubMed  Google Scholar 

  33. Goncalves CS, Braga FMS (2008). Diversidade e ocorrência de peixes na área de influência da UHE Mogi Guaçu e lagoas marginais, bacia do alto rio Paraná, São Paulo, Brasil. Biota Neotropica, 8(2), 103–114. http://www.biotaneotropica.org.br/v8n2/pt/abstract?article+bn02008022008. Accessed 27 Dec 2019. https://doi.org/https://doi.org/10.1590/S1676-06032008000200012

  34. Graça WJ, Pavanelli CS (2007) Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. Eduem, Maringá

    Google Scholar 

  35. Hebert PDN, Cywinska A, Ball SL, Ward JR (2003) Biological identifications through DNA barcodes. P Roy Soc B-Biol Sci 270(1512):313–321. https://doi.org/10.1098/rspb.2002.2218

    CAS  Article  Google Scholar 

  36. Hubert N, Hanner R, Holm E, Mandrak NE, Taylor E, Burridge M, Bernatchez L et al (2008) Identifying Canadian freshwater fishes through DNA barcodes. PLoS One 3(6):1–8. https://doi.org/10.1371/journal.pone.0002490

    CAS  Article  Google Scholar 

  37. Johnson NA, Smith CH, Pfeiffer JM, Randklev CR, Williams JD, Austin JD (2018) Integrative taxonomy resolves taxonomic uncertainty for freshwater mussels being considered for protection under the US endangered species. Act Sci Rep 8(15892):1–16. https://doi.org/10.5066/P9SRSHV2

    Article  Google Scholar 

  38. Junk WJ (2007) Freshwater fishes of South America: Their biodiversity, fisheries, and habitats – a synthesis. Aquat Ecosyst Health Manag 10(2):228–242. https://doi.org/10.1080/14634980701356733

    Article  Google Scholar 

  39. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120. https://doi.org/10.1007/BF01731581

    CAS  Article  Google Scholar 

  40. Kindt R, Coe R (2005). Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. http://www.worldagroforestry.org/output/tree-diversity-analysis. Accessed 27 Dec 2019.

  41. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Langeani F, Castro RMC, Oyakawa OT, Shibatta AO, Pavanelli CS, Casatti L (2007). Diversidade da ictiofauna do Alto Rio Paraná: composição atual e perspectivas futuras. Biota Neotropica, 7(3), 181–197. http://www.biotaneotropica.org.br/v7n3/pt/abstract?article+bn03407032007. Last accessed 27 Dec 2019. https://doi.org/https://doi.org/10.1590/S1676-06032007000300020

  43. Leite GFM, Silva FTC, Gonçalves JFJ, Salles P (2015) Effects of conservation status of the riparian vegetation on fish assemblage structure in neotropical headwater streams. Hydrobiologia 762(1):223–238. https://doi.org/10.1007/s10750-015-2351-9

    Article  Google Scholar 

  44. Lowe-McConnell RH (1999) Estudos ecológicos de comunidades de peixes tropicais. Universidade de São Paulo, São Paulo

    Google Scholar 

  45. Melo FAG, Buckup PA (2006) Astyanax henseli, a new name for Tetragonopterus aeneus Hensel, 1870 from southern Brazil (Teleostei: Characiformes). Neotrop Ichthyol 4(1):45–52. https://doi.org/10.1590/S1679-62252006000100003

    Article  Google Scholar 

  46. Meyer JL, Strayer DL, Wallace JB, Eggert SL, Helfman GS, Leonard NE (2007) The contribution of headwater streams to biodiversity in river networks. J Am Water Resour As (JAWRA) 43(1):86–103. https://doi.org/10.1111/j.1752-1688.2007.00008.x

    Article  Google Scholar 

  47. Mise FT, Message HJ, Pagotto JPA, Goulart E (2018) Environmental assessment in tropical streams by using abundance-biomass curves and W index in fish assemblages. Iheringia. Sér Zool 108:1–9. https://doi.org/10.1590/1678-4766e2018029

    Article  Google Scholar 

  48. Moreira-Filho O, Bertollo LA (1991). Astyanax scabripinnis (Pisces, Characidae): a species complex. Rev Bras Genet 14(2), 331–357. https://www.researchgate.net/publication/279618588

  49. Nelson JS, Crossman EJ, Espinosa-Pérez H, Findley LT, Gilbert CR, Lea RN, Willians JD (2004) Common and Scientific Names of Fishes from the United States, Canada, and Mexico, 6th edn. American Fisheries Society, Bethesda

    Google Scholar 

  50. Nwani CD, Becker S, Braid HE, Ude EF, Okogwu OI, Hanner R (2011) DNA barcoding discriminates freshwater fishes from southeastern Nigeria and provides river system-level phylogeographic resolution within some species. Mitochondr DNA 22(S1):43–51. https://doi.org/10.3109/19401736.2010.536537

    CAS  Article  Google Scholar 

  51. Ornelas-Garcia CP, Dominguez-Dominguez O, Doadrio I (2008) Evolutionary history of the fish genus Astyanax Baird & Girard (1854) (Actynopterigii, Characidae) in Mesoamerica reveals multiple morphological homoplasies. BMC Evol Biol 8(340):1–17. https://doi.org/10.1186/1471-2148-8-340

    CAS  Article  Google Scholar 

  52. Ota RR, Deprá GC, Graça WJ, Pavanelli CS (2018) Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotrop Ichthyol 16(2):e170094. https://doi.org/10.1590/1982-0224-20170094

    Article  Google Scholar 

  53. Padial JM, Miralles A, De La Riva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7(16):2–14. https://doi.org/10.1186/1742-9994-7-16

    Article  Google Scholar 

  54. Pereira AL, Ribeiro VR, Gubiani EA, Zacarkim CE, Cunico AM (2014) Ichthyofauna of urban streams in the western region of Paraná State, Brazil. Check List 10(3):550–555. https://doi.org/10.15560/10.3.550

    Article  Google Scholar 

  55. Pereira LHG, Hanner R, Foresti F, Oliveira C (2013) Can DNA Barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC Genet 14(20):1–14. https://doi.org/10.1186/1471-2156-14-20

    CAS  Article  Google Scholar 

  56. Pereira LHG, Maia GMG, Hanner R, Foresti F, Oliveira C (2011) DNA Barcodes discriminate fresh water fishes from the Paraíba do Sul River Basin, São Paulo, Brazil Mitochondr. DNA 22(S1):71–79. https://doi.org/10.3109/19401736.2010.532213

    CAS  Article  Google Scholar 

  57. Pereira MCB, Scroccaro JL (2010) Bacias hidrográficas do Paraná - Série histórica. SEMA, Curitiba

    Google Scholar 

  58. Pugedo ML, Andrade-NETO FR, Pessali TC, Birindelli JLO, Carvalho DC (2016) Integrative taxonomy supports new candidate fish species in a poorly studied neotropical region: the Jequitinhonha River Basin. Genetica 144(3):341–349. https://doi.org/10.1007/s10709-016-9903-4

    Article  PubMed  Google Scholar 

  59. Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Mol Ecol 21:1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x

    CAS  Article  PubMed  Google Scholar 

  60. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2013. URL http://www.R-project.org/.

  61. Reis RE, Kullander SO, Ferraris C (2003) Check list of the freshwater fishes of South and Central America (CLOFFSCA). Edipucrs, Porto Alegre

    Google Scholar 

  62. Ribeiro AO, Caires RA, Mariguela TC, Pereira LHG, Hanner R, Oliveira C (2012) DNA barcodes identify marine fishes of São Paulo State. Brazil Mol Ecol Resour 12(6):1012–1020. https://doi.org/10.1111/1755-0998.12007

    CAS  Article  PubMed  Google Scholar 

  63. Riedel A, Sagata K, Suhardjono YR, Tänzler R, Balke M (2013) Integrative taxonomy on the fast track-towards more sustainability in biodiversity research. Front Zool 10(15):1–9. https://doi.org/10.1186/1742-9994-10-15

    Article  Google Scholar 

  64. Ringuelet RA (1975). Zoogeografía y ecología de los peces de aguas continentales de la Argentina y consideraciones sobre las áreas ictiológicas de América del Sur. Ecosur, 2(3), 1–129. http://sedici.unlp.edu.ar/handle/10915/48003

  65. Rossini BC, Oliveira CAM, Melo FAG, Bertaco VA, Astarloa JMD, Rosso JJ et al (2016) Highlighting Astyanax Species Diversity through DNA Barcoding. PLoS ONE 11(12):1–20. https://doi.org/10.1371/journal.pone.0167203

    CAS  Article  Google Scholar 

  66. Rosso JJ, Magragaña E, Castro MG, De Astarloa M (2012) DNA barcoding neotropical fishes: recent advances from the Pampa Plain. Argentina Mol Ecol Resour 12(6):999–1011. https://doi.org/10.1111/1755-0998.12010

    CAS  Article  PubMed  Google Scholar 

  67. Savage JM (1995) Systematic and the biodiversity crisis. Bioscience 45(10):673–679. https://doi.org/10.2307/1312672

    Article  Google Scholar 

  68. Schaefer SA (1998) Conflict and resolution impact of new taxa on phylogenetic studies of Neotropical cascudinhos (Siluriformes: Loricariidae). In: Malabarba LR, Reis RE, Vari RP, Lucena ZMS, Lucena CAS (eds) Phylogeny and classification of Neotropical fishes. Edipucrs, Porto Alegre, pp 375–400

    Google Scholar 

  69. Schneider M, Aquino PPU, Silva MJM, Fonseca CP (2011) Trophic structure of a fish community in Bananal stream subbasin in Brasília National Park, Cerrado biome (Brazilian Savanna). DF Neotrop Ichthyol 9(3):579–592. https://doi.org/10.1590/S1679-62252011005000030

    Article  Google Scholar 

  70. Silveira SF (2002). Ecologia da comunidade aquática de um riacho de 1ª ordem da Mata Atlântica: Relações entre variáveis estruturais e bióticas em uma Reserva de Biosfera Tropical. Dissertation, Universidade Federal de São Carlos.

  71. Smith WS, Petrere MJ (2000). Caracterização limnológica da bacia de drenagem do rio Sorocaba, São Paulo, Brasil. Acta Limnol. Bras., 12, 15–27. https://www.ablimno.org.br/publiActa.php?issue=v12n2

  72. Súarez YR, Lima-Júnior SE (2009). Variação espacial e temporal nas assembleias de peixes de riachos na bacia do rio Guiraí, alto rio Paraná. Biota Neotropica, 9(1), 101–111. http://www.biotaneotropica.org.br/v9n1/en/abstract?article+bn01709012009. Accessed 27 Dec 2019. http://dx.doi.org/https://doi.org/10.1590/S1676-06032009000100012

  73. Strahler AN (1957) Quantitative analysis of watershed geomorphology. Eos Trans AGU 38(6):913. https://doi.org/10.1029/TR038i006p00913

    Article  Google Scholar 

  74. Terán GE, Benitez MF, Mirande JM (2020) Opening the Trojan horse: phylogeny of Astyanax, two new genera and resurrection of Psalidodon (Teleostei: Characidae). Zool J Linn Soc 190(4):1217–1234. https://doi.org/10.1093/zoolinnean/zlaa019

    Article  Google Scholar 

  75. Vilar AG, Van Dam H, Van Loon EE, Vonk JA, Van Der Geest HG, Admiraal W (2014) Eutrophication decreases distance decay of similarity in diatom communities. Freshwater Biol 59(7):1522–1531. https://doi.org/10.1111/fwb.12363

    Article  Google Scholar 

  76. Vörösmarty CJ, McIntyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P et al (2010) Global threats to human water security and river biodiversity. Nature 467:555–561. https://doi.org/10.1038/nature09440

    CAS  Article  PubMed  Google Scholar 

  77. Ward RD (2009) DNA barcode divergence among species and genera of birds and fishes. Mol Ecol Resour 9(4):1077–1085. https://doi.org/10.1111/j.1755-0998.2009.02541.x

    CAS  Article  PubMed  Google Scholar 

  78. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc B-Biol Sci 360(1462):1847–1857. https://doi.org/10.1098/rstb.2005.1716

    CAS  Article  Google Scholar 

  79. Wolff LL, Abilhoa V, Rios FSA, Donatti L (2009) Spatial, seasonal andontogenetic variation in the diet of Astyanax aff. fasciatus (Ostariophysi: Characidae) in an Atlantic Forest river, Southern Brazil. Neotrop Ichthyol 7(2):257–266. https://doi.org/10.1590/S1679-62252009000200018

    Article  Google Scholar 

  80. Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29(22):2869–2876. https://doi.org/10.1093/bioinformatics/btt499

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  81. Zorzal-Almeida S, Bini LM, Bicudo DC (2017) Beta diversity of diatoms is driven by environmental heterogeneity, spatial extent and productivity. Hydrobiologia 800:7–16. https://doi.org/10.1007/s10750-017-3117-3

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Itaipu Binacional Dam that provided part of field logistic to conduct this survey.

Funding

This work was supported by the Universidade Federal da Integração Latino-Americana (UNLA) under processes 137/2018/PRPPG, 80/2019/PRPPG; Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP under Grants 2018/20610-1, 2016/09204-6, 2014/26508-3; and Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq under Grant 306054/2006-0.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Luiz Henrique Garcia Pereira.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest related to the publication of this manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pereira, L.H.G., Castro, J.R.C., Vargas, P.M.H. et al. The use of an integrative approach to improve accuracy of species identification and detection of new species in studies of stream fish diversity. Genetica 149, 103–116 (2021). https://doi.org/10.1007/s10709-021-00118-6

Download citation

Keywords

  • Checklist
  • Conservation
  • DNA barcoding
  • Fishes
  • Fish distribution
  • Paraná River basin