Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2023-03-02
Page range: 357-377
Abstract views: 780
PDF downloaded: 38

Integrative taxonomy of Imparfinis (Siluriformes, Heptapteridae) from the Upper Paraná River basin, Brazil, with description of a new species

1Instituto de Biociências, Universidade Estadual Paulista, R. Prof. Dr. Antonio C. W. Zanin, 250, 18618-689, Botucatu, Brazil
Instituto de Biociências, Universidade Estadual Paulista, R. Prof. Dr. Antonio C. W. Zanin, 250, 18618-689, Botucatu, Brazil
Instituto de Biociências, Universidade Estadual Paulista, R. Prof. Dr. Antonio C. W. Zanin, 250, 18618-689, Botucatu, Brazil
Instituto de Biociências, Universidade Estadual Paulista, R. Prof. Dr. Antonio C. W. Zanin, 250, 18618-689, Botucatu, Brazil
Instituto de Biociências, Universidade Estadual Paulista, R. Prof. Dr. Antonio C. W. Zanin, 250, 18618-689, Botucatu, Brazil
Catfishes Biodiversity Neotropical region Species delimitation Pieces

Abstract

The Neotropical family Heptapteridae comprises 228 valid species widely distributed in South America. Imparfinis is one of the most diverse genera of this family, with 25 valid species widely distributed, inhabiting streams from Costa Rica to Argentina. Old descriptions coupled with lack of recent systematic studies of the species of Imparfinis from the Upper Paraná river basin have led to a taxonomic impediment and hindered the advancement of studies in other areas, such as ecology, cytogenetic, phylogenetic, and evolution. We conducted the first integrative study analyzing both molecular and morphological data of Imparfinis from the Upper Paraná River basin. Our analyses strongly support the existence of four independent evolutionary lineages in this river system, three of them are the nominal species I. mirini, I. schubarti, and I. piperatus, and a new species from Goiás state described herein.

References

  1. Aitchison, J. (1986) The statistical analysis of compositional data. Vol. XII. Chapman and Hall, London and New York, 416 pp.

  2. Aguilera, G., Terán, G.E., Mirande, J.M., Alonso, F., Chumacero, G.M., Cardoso, Y., Bogan, S. & Faustino-Fuster, D.R. (2022) An integrative approach method reveals the presence of a previously unreported species of Imparfinis Eigenman and Norris 1900 (Siluriformes: Heptapteridae) in Argentina. Journal of Fish Biology, 101 (5), 1248–1261. https://doi.org/10.1111/jfb.15197

  3. Anjos, M.S., Bitencourt, J.A., Nunes, L.A., Sarmento-Soares, L.M., Carvalho, D.C., Armbruster, J.W. & Affonso, P.R.A.M. (2020) Species delimitation based on integrative approach suggest reallocation of genus in Hypostomini catfish (Siluriformes, Loricariidae). Hydrobiologia, 847, 563–578. https://doi.org/10.1007/s10 750-019-04121-z

  4. Azevedo-Santos, V.M., Britski, H.A., Oliveira, C. & Benine, R.C. (2019) Ichthyofauna of streams of the Rio Sapucaí basin, upper Rio Paraná system, Minas Gerais, Brazil. Biota Neotropica, 19 (1), e20180617. https://doi.org/10.1590/1676-0611-BN-2018-0617

    DOI: https://doi.org/10.1590/1676-0611-bn-2018-0617
  5. Benine, R.C., Mariguela, T.C. & Oliveira, C. (2009) New Moenkhauisia Eigenmann, 1903 (Characiformes: Characidae) with comments on the Moenkhausia oligolepis complex. Neotropical Ichthyology, 7 (2), 161–168. https://doi.org/10. 1590/S1679-62252009000200005

  6. Bockmann, F.A. (1998) Análise filogenética da família Heptapteridae (Teleostei, Ostariophysi, Siluriformes) e redefinição de seus gêneros. PhD Thesis. Universidade de São Paulo, Available from: https://repositorio.usp.br/item/001000413 (accessed 24 January 2023)

  7. Bockmann, F.A. & Castro, R. (2010) The blind catfish form caves of Chapada Diamantina, Bahia, Brazil (Siluriformes: Heptapteridae): description, anatomy, phylogenetic relationships, natural history, and biogeography. Neotropical Ichthyology, 8 (4), 673–706.

  8. Bockmann, F.A. & Slobodian, V. (2018) Family Heptapteridae—Three-barbeled catfishes. In: Sleen, P.V. & Albert, J.S. (Eds.), Field guide to the fishes of the Amazon, Orinoco and Guianas. Princeton University Press, Princeton, New Jersey, pp. 233–252.

  9. Brito, V. & Buckup, P.A. (2019) The fish fauna of the upper Piraí drainage, a transposed mountain river system in southeastern, Brazil. Check List, 15 (1), 235–247. https://doi.org/10.15560/15.1.235

  10. Castro, I.S. & Wosiacki, W.B. (2019) A new species of Imparfinis Eigenmann & Norris, 1900 (Siluriformes: Heptapteridae) from the Tapajós basin, Brazil. Zootaxa, 4701 (5), 461–472. https://doi.org/10.11646/zootaxa.4701.5.6

  11. De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56 (6), 879–886. https://doi.org/10.1080/10635150701701083

  12. Edgar, R.C. (2004) Muscle: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797. https://doi.org/10.1093/nar/gkh340

  13. Eigenmann, C.H. & Norris, A.A. (1900) Sobre alguns peixes de S. Paulo, Brazil. Revista do Museu Paulista, 4, 349–362.

  14. Faustino-Fuster, D.R., Mesa-Vargas, V., Lovejoy, N.R. & Lujan, N.K. (2021) Multi-Locus phylogeny with dense Guiana Shield sampling supports new suprageneric classification of the neotropical three-barbeled catfishes (Siluriformes: Heptapteridae). Molecular Phylogenetics and Evolution, 162, 1–14. https://doi.org/10.1016/j.ympev.2021.107 186

  15. Ferreira, M., Kavalco, K.F., Almeida-Toledo, L.F. & Garcia, C. (2014) Cryptic diversity between two Imparfinis species (Siluriformes, Heptapteridae) by cytogenetic analysis and DNA barcoding. Zebrafish, 11 (4), 306–317. https://doi.org/10.1089/zeb.2014.0981

  16. Frota, A., Message, H.J., Oliveira, R.C., Benedito, E. & Graça, W.J. (2019) Ichthyofauna of headwater stream from the rio Ribeira do Iguape basin, at the boundaries of the Ponta Grossa Arch, Paraná, Brazil. Biota Neotropica, 19 (1), e20180666. https://doi.org/10.1590/1676-0611-BN-2018-0666

  17. Gascon, C., Lougheed, S.C. & Borgard, J.P. (1998) Pattern of genetic population differentiation in four species Amazonian frogs: a test of the riverine barriers hypothesis. Biotropica, 30 (1), 104–119.

  18. Gery, J. (1962) Notes on the ichthyology of Surinam and other Guianas. The distribution pattern of the genus Hemibrycon, with a description of a new species from Surinam and an incursion into ecotaxonomy. Bulletin of Aquatic Biology, 3 (28), 65–80.

  19. Gomes, A.L. (1956) Descrição de uma nova espécie de “Luciopimelodinae” do Rio Mogi-Guaçu, Estado de São Paulo (Pisces, Nematognathi, Pimelodidae). Revista Brasileira de Biologia, 16 (4), 403–413.

  20. Haseman, J.D. (1911) Descriptions of some new species of fishes and miscellaneous notes on others obtained during the expedition of the Carnegie Museum to central South America. Annals of Carnegie Museum, 7 (3–4), 315–328.

  21. Ivanova, N.V., Dewaard, J.R. & Hebert, P.D. (2006) An inexpensive, automatic-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes, 6:998–1002. https://doi.org/10.1111/j.1471-8286.2006.01428.x

  22. Jennings, W.B., Ruschi, P.A., Ferraro, G., Quijada. C,C., Silva-Malanski, A.C.G., Prosdocimi, F. & Buckup, P.A. (2019) Barcoding the Neotropical freshwater fish fauna using a new pair if universal COI primers with a discussion of primer dimers and M13 primer tails. Genome, 62, 77–83. https://doi.org/10.1139/gen-2018-0145

  23. Jolliffe, I.T. (2002) Principal component analysis. Springer series in statistics. 2nd Edition. Springer, New York, New York, XXX + 488 pp.

  24. Kearse, M., Moir, R., Wilson, A., Stone-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199

  25. Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054

  26. Lutken, C.F. (1874) Siluridae novae Brasilie centralis a clarissimo J. Reinhardt in provincia Minas-gerais circa oppidulum Lagoa Santa, praecipue in flumine Rio das Velhas et affluentibus colectae, secundum caracteres essentiales, breviter descriptae a Chr. Lutken. Oversigt over det Kongelige Danske Videnskabernes Selskabs Forhandlinger og dets Medlemmers Arbeider, Kjøbenhavn, 1874 (1), 29–36.

  27. Menezes, N.A., Weitzman, S.H., Oyakawa, O.T., Lima, F.C.T, Castro, R.M.C. & Weitzman, M.J. (2007) Peixes de água doce da mata atlântica: Lista preliminar das espécies e comentários sobre conservação de peixes de água doce neotropicais. Museu de Zoologia, Universidade de São Paulo.São Paulo, 407 pp.

  28. Montoya-Burgos, J.I. (2003) Historical biogeography of the catfish genus Hypostomus (Siluroformes: Loricariidae), with implications on the diversification of Neotropical Icthyofauna. Molecular Ecology, 12, 1855–1867. https://doi.org/10.1046/j.1365-294X.2003.01857.x

  29. Ochoa, L.E., Melo, B.F., García-Melo, J.E., Maldonado-Ocampo, J.A., Souza, C.S., Albornoz-Garzón, J.G., Conde-Saldaña, C., Villa-Navarro, F., Ortega-Lara, A. & Oliveira, C. (2020) Species delimitation reveals an understimated diversity of Andean catfishes of the family Astroblepidae (Teleostei: Siluriformes). Neotropical Ichthyology, 18 (4), e200048. https://doi.org/10.1590/1982-0224-2020-0048

  30. Oyakawa, O.T. & Menezes, N.A. (2011) Checklist dos peixes de água doce do Estado de São Paulo, Brasil. Biota Neotropica, 11, 1–13. https://doi.org/10.1590/S1676060320 11000500002

  31. Pattengale, N.D., Alipour, M., Bininda-Emonds, O.R., Moret, B.M. & Stamatakis, A. (2010) How many bootstrap replicates are necessary? Journal of Computational Biology, 17, 337–354. https://doi.org/10.1089/cmb.2009.0179

  32. Patton, J.L., Da Silva, M.N.F. & Malcolm, J.R. (1994) Gene genealogy and differentiation among arboreal spiny rats (Rodentia: Echimyidae) of the Amazon basin: a test of the riverine barrier hypothesis. Evolution, 48 (4), 1314–1323. https://doi.org/10.1111/j.1558-5646.1994.tb05315.x

  33. Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21, 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x

  34. Puillandre, N., Brouillet, S. & Achaz, G. (2019) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources, 21, 609–620.

  35. Pereira, L.H., Castro, J.R.C., Vargas, P.M.H., Gomez, J.A.M. & Oliveira, C. (2021) 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

  36. Pereira, L.H., Hanner, R., Foresti, F. & Oliveira, C. (2013) Can DNA barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC Genetic, 14, 1–20. https://doi.org/10.1186/1471-2156-14-20

  37. Pereira, L.H., Maia, G.M.H., Hanner, R., Foresti, F. & Oliveira, C. (2011) DNA barcodes discriminate freshwater fishes from the Paraíba do Sul River Basin, São Paulo, Brazil. Mitochondrial DNA, 22, 71–79.

  38. Rannala, B. & Yang, Z. (2013) Improved reversible jump algorithms for Bayesian species delimitation. Genetics, 194, 245–253. https://doi.org/10.1534/genetic s.112.149039

  39. Reia, L., Vicensotto, A.M.P.F., Oliveira, C. & Benine, R.C. (2019) Taxonomy of Moenkhauia australis Eigenmann, 1908 (Characiformes, Characidae) with a discussion on its phylogenetic relationships. Zootaxa, 4688 (2), 213–231. https://doi.org/10.11646/zootaxa.4688.2.3

  40. Reia, L., Oliveira, C. & Benine, R.C. (2021) Moenkhausia andrica (Characiformes: Characidae): a new species from the Tapajós basin, Brazil, with minute fin hooklets in females. Journal of Fish Biology, 99 (4), 1380–1392. https://doi.org/10.1111/jfb.14847

  41. Ribolli, J., Filho, E.Z., Scaranto, B.M.S., Shibatta, O.A. & Machado, C.B. (2021) Cryptic diversity and diversification processes in three cis-Andean Rhamdia species (Siluriformes: Heptateridae) revealed by DNA barcoding. Genetic and Molecular Biology, 44 (3), e20200470. https://doi.org/10.1590/1678-4685-GMB-2020-0470

  42. Ribeiro, A.C., Lima, F.C.T., Riccomini, C. & Menezes, N.A. (2006) Fishes of the Atlantic Rainforest of Boracéia: testimonies of the Quaternary fault reactivation within a Neoproterozoic tectonic province in Southeastern Brazil. Ichthyological Exploration of Freshwaters, 17 (2), 157

  43. Roxo, F.F., Zawadzki, C.H., Alexandrou, M.A., Costa-Silva, G.J., Chiachio, M.C., Foresti, F. & Oliveira, C. (2012) Evolutionary and biogeography history of the subfamily Neoplecostominae (Siluriformes: Loricariidae). Ecology and Evolution, 2, 2438–2449. https://doi.org/10.1002/ece3.368

  44. R Core Team, R.F.F.S.C. (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.R-project.org/ (accessed 24 January 2023)

  45. Rstudio TEAM (2020) RStudio: Integrated development for R. RStudio, PBC, Boston, Massachusetts. Available from: https://www.rstudio.com/ (accessed 24 January 2023)

  46. Silva, G.S.C., Roxo, F.F., Melo, B.F., Ochoa, L.E., Bockmann, F.A., Sabaj, M.H., Jerep, F.C., Foresti, F., Benine, R.C. & Oliveira, C. (2021) Evolutionary history of Heptapteridae catfishes using ultraconserved elements (Teleostei, Siluriformes). Zoologica Scripta, 50 (5), 543–554. https://doi.org/10.1111/zsc.12493

  47. Silva, G.S.C., Melo, B.F., Oliveira, C. & Benine, R.C. (2016) Revision of the South American genus Tetragonopterus Cuvier, 1816 (Teleostei: Characidae) with description of four new species. Zootaxa, 4200 (1), 1–46. https://doi.org/10.11646/zootaxa.4200.1.1

  48. Stamatakis, A. (2014) RaxML version*: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033

  49. Struck, T.H. & Cerca, J. (2019) Cryptic species and their evolutionary significance. In: eLS. John Wiley Sons Ltd. Available from: https://doi.org/10.1002/9780470015902.a0028292 (accessed 24 January 2023)

  50. Struck, T.H., Jeffrey, L.F., Bendiksby, M., Birkeland, S., Cerca, J., Gusarov, V.I., Kistenich, S., Larsson, K., Liow, L.H., Nowak, M.D., Stedje, B., Bachmann, L. & Dimitrov, D. (2017) Finding evolutionary processes hidden in cryptic species. Trends of Ecology and Evolution, 2331, 153–163. https://doi.org/10.1016/j.tree.2017.11.007

  51. Thomas, M.R. & Sabaj, M.H. (2020) Heptapteridae: seven-finned catfishes. In: Warren, M.L. & Burr, B.M. (Eds.), Freshwater fishes of North America: Characidae to Poeciliidae. Vol. 2. The johns Hopkins University Press, Baltimore, Maryland, pp. 123–148.

  52. Taylor, W.R. & Van Dyke, G.C. (1985) Revised procedures for staining and clearing small and other vertebrates for bones and cartilage study. Cybium, 9 (2), 107–119.

  53. Vanables, W.N. & Ripley, B.D. (2002) Modern applied statistics with S. Springer-Verlag, New York, New York, XII + 498 pp.

  54. Xia, X., Xie, Z., Salemi, M. & Chen, L. (2003) Wang Y. An index of substitution saturation and its application. Molecular Phylogenetic and Evolution, 26 (1), 1–7. https://doi.org/10.1016/S1055-7903(02)00326-3

  55. Xia, X. & Lemey, P. (2009) Assessing substitution saturation with DAMBE. In: Lemey, P., Salemi, M. & Vandamme, A.M. (Eds.), The Phylogenetic Handbook. A practical approach to phylogenetic analysis and hypothesis testing. Cambridge University Press, Cambridge, pp. 615–630.

  56. Xia, X. (2018) DAMBE7: New and Improved Tools for Data Analysis in Molecular Biology and Evolution. Molecular and Biology Evolution, 35 (6), 1550–1552. https://doi.org/10.1093/molbev/msy073

    DOI: https://doi.org/10.1093/molbev/msy073