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Issue: Vol. 5432 No. 4: 3 Apr. 2024
Type: Article
Published: 2024-04-03
DOI: 10.11646/zootaxa.5432.4.4
Page range: 535-554
Abstract views: 137
PDF downloaded: 1

A systematic assessment of Leporinus tigrinus (Characiformes: Anostomidae) using morphological and molecular data

Programa de Pós-Graduação em Ciências Biológicas; Universidade Estadual de Londrina; Londrina; Paraná; Brazil.
Laboratório de Sistemática Molecular; Departamento de Biologia Animal e Vegetal; Universidade Estadual de Londrina; Rodovia Celso Garcia Cid; Km 380; CEP 86057-970; Londrina; Paraná; Brazil.
Museu de Zoologia; Universidade Estadual de Londrina; Rodovia Celso Garcia Cid; Km 380; CEP 86057-970; Londrina; Paraná; Brazil.
Anostomidae Taxonomy Neotropical region species delimitation analyses Ostariophysi

Abstract

Leporinus tigrinus was described based on specimens collected in the rio Tocantins basin, and was only recently recorded at the rio Xingu, rio Tapajós and upper rio Paraná basins. So far, no study has compared specimens of all these distinct drainages focusing on understanding whether all these populations truly belong to a single species or may consist instead in a species complex. Our study focused on investigating the intraspecific variation within Leporinus tigrinus using morphological and molecular data. Both morphology and molecular analyses support that all samples belong to a single species widespread in the rio Araguaia, rio Tocantins, rio Xingu and rio Tapajós. In addition, the population occurring at upper rio Paraná is considered to be allochthonous, originating from the rio Araguaia/Tocantins. A comprehensive morphological description of the species, including osteological illustrations and descriptions are provided, as well as a comparative diagnosis with similar-looking species.

References

  1. Albert, J.S., Tagliacollo, V.A. & Dagosta, F. (2020) Diversification of Neotropical freshwater fishes. Annual Review of Ecology, Evolution, and Systematics, 51, 27–53. https://doi.org/10.1146/annurev-ecolsys-011620-031032
  2. Aljanabi, S.M. & Martinez, I. (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic acids research, 25 (22), 4692–4693. https://doi.org/10.1093/nar/25.22.4692
  3. Andrade, M.C., Jégu, M. & Giarrizzo, T. (2016) Tometes kranponhah and Tometes ancylorhynchus (Characiformes: Serrasalmidae), two new phytophagous serrasalmids, and the first Tometes species described from the Brazilian Shield. Journal of Fish Biology, 89 (1), 467–494. https://doi.org/10.1111/jfb.12868
  4. Anjos, M.S., Bitencourt, J.A., Nunes, L.A., Sarmento-Soares, L.M., Carvalho, D.C., Armbruster, J.W. & Affonso, P.R. (2020) Species delimitation based on integrative approach suggests reallocation of genus in Hypostomini catfish (Siluriformes, Loricariidae). Hydrobiologia, 847, 563–578. https://doi.org/10.1007/s10750-019-04121-z
  5. Bemis, W.E., Hilton, E.J., Brown, B., Arrindell, R., Richmond, A.M., Little, C.D., Grande, L., Forey, P.L. & Nelson, G.J. (2004) Methods for preparing dry, partially articulated skeletons of osteichthyans, with notes on making Ridewood dissections of the cranial skeleton. Copeia, 2004 (3), 603–609. https://doi.org/10.1643/CI-03-054R1
  6. Bertaco, V.A., Jerep, F.C. & Carvalho, F.R. (2011) A new characid fish, Moenkhausia aurantia (Ostariophysi: Characiformes: Characidae), from the upper rio Tocantins basin in Central Brazil. Zootaxa, 2934 (1), 29–38. https://doi.org/10.11646/zootaxa.2934.1.3
  7. Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in ecology & evolution, 22 (3), 148–155. https://doi.org/10.1016/j.tree.2006.11.004
  8. Birindelli, J.L.O. & Britski, H.A. (2013) Two new species of Leporinus (Characiformes: Anostomidae) from the Brazilian Amazon, and redescription of Leporinus striatus Kner 1858. Journal of Fish Biology, 83 (5), 1128–1160. https://doi.org/10.1111/jfb.12206
  9. Birindelli, J.L.O. & Sidlauskas, B.L. (2018) Preface: How far has Neotropical Ichthyology progressed in twenty years?. Neotropical Ichthyology, 16 (3), e180218. https://doi.org/10.1590/1982-0224-20180128
  10. Birindelli, J.L.O., Melo, B.F., Ribeiro-Silva, L.R., Diniz, D. & Oliveira, C. (2020) A new species of Hypomasticus from Eastern Brazil based on morphological and molecular data (Characiformes, Anostomidae). Copeia, 108 (2), 416–425. https://doi.org/10.1643/CI-19-335
  11. Borodin, N.A. (1929) Notes on some species and subspecies of the genus Leporinus Spix. Memoirs of the Museum of Comparative Zoology, 50 (3), 269–290. https://doi.org/10.5962/bhl.title.49345
  12. Britski, H.A. (1997) Descrição de duas espécies novas de Leporinus dos rios Araguaia e Tocantins, e comentários sobre as demais espécies do gênero assinaladas na bacia (Ostariophysi, Characiformes, Anostomidae). Comunicações do Museu de Ciências e Tecnologia da PUCRS, Série Zoologia, 10, 27–43. [in Portuguese]
  13. Britski, H.A. & Birindelli, J.L.O. (2016) Redescription of Leporinus altipinnis, a senior synonym of L. falcipinnis, and comments on L. holostictus (Characiformes: Anostomidae). Ichthyological Exploration of Freshwaters, 27 (1), 25–40.
  14. Britski, H.A. & Garavello, J.C. (1978) Sobre Leporinus octofasciatus Steindachner da bacia do Paraná (Pisces, Anostomidae). Papéis Avulsos de Zoologia, 31, 237–250. [in Portuguese]
  15. Burns, M.D., Chatfield, M., Birindelli, J.L.O. & Sidlauskas, B.L. (2017) Systematic assessment of the Leporinus desmotes species complex, with a description of two new species. Neotropical Ichthyology, 15 (2), e160166. https://doi.org/10.1590/1982-0224-20160166
  16. Camargo, M., Giarrizzo, T. & Isaac, V. (2004) Review of the geographic distribution of fish fauna of the Xingu river basin, Brazil. Ecotropica, 10 (2), 123–147.
  17. Cavaretto, R.C., Souza-Shibatta, L., Celestino, L.F., Silva, P.S., Shibatta, O.A., Sofia, S.H., Makrakis, S. & Makrakis, M.C. (2020) Evidence for the unexpected dispersal of Leporinus tigrinus Borodin, 1929 through hydroelectric dams in the most regulated Neotropical river basin. Aquatic Invasions, 15 (3), 497–513. https://doi.org/10.3391/ai.2020.15.3.09
  18. Costa, W.J.E.M., Mattos, J., Lopes, S., Amorim, P. & Katz, A. (2022) Integrative taxonomy, distribution and ontogenetic colouration change in Neotropical mountain catfishes of the Trichomycterus nigroauratus group (Siluriformes: Trichomycteridae). Zoological Studies, 61, 11. https://doi.org/10.6620/ZS.2022.61-11
  19. 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
  20. Ezard, T., Fujisawa, T. & Barraclough, T. (2021) splits: SPecies’ LImits by Threshold Statistics. R package version 1.0-20/r56. Available from: https://R-Forge.R-project.org/projects/splits/ (accessed 21 February 2022)
  21. Fisch-Muller, S., Mol, J.H.A. & Covain, R. (2018) An integrative framework to reevaluate the Neotropical catfish genus Guyanancistrus (Siluriformes: Loricariidae) with particular emphasis on the Guyanancistrus brevispinis complex. PLoS One, 13 (1), e0189789. https://doi.org/10.1371/journal.pone.0189789
  22. Fricke, R., Eschmeyer, W.N. & Fong, J.D. (2023) Eschmeyer's Catalog of Fishes: genera/species by family/subfamily. Available from: https://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp (accessed 24 March 2023)
  23. Froehlich, O., Cavallaro, M., Sabino, J., Súarez, Y.R. & Vilela, M.J.A. (2017) Checklist da ictiofauna do estado de Mato Grosso do Sul, Brasil. Iheringia, Série Zoologia, 107, e2017151. [in Portuguese] https://doi.org/10.1590/1678-4766e2017151
  24. Garavello, J.C. (1979) Revisão taxonômica do gênero Leporinus Spix, 1829 (Ostariophysi, Anostomidae). Unplub. Doctoral thesis, Instituto de Biociências, Universidade de São Paulo, São Paulo, 451 pp. [in Portuguese]
  25. Garavello, J.C. & Britski, H.A. (2003) Family Anostomidae. In: Reis, R.E., Kullander, S.O. & Ferraris Jr., C.J (Eds.), Check list of the freshwater fishes of South and Central America. Edipucrs, Porto Alegre, pp. 71–84.
  26. Garavello, J.C., Ramirez, J.L., Oliveira, A.K.D., Britski, H.A., Birindelli, J.L.O. & Galetti Jr., P.M. (2021) Integrative taxonomy reveals a new species of Neotropical headstanding fish in genus Schizodon (Characiformes: Anostomidae). Neotropical Ichthyology, 19 (4), e210016. https://doi.org/10.1590/1982-0224-2021-0016
  27. García-Melo, J.E., Oliveira, C., da Costa Silva, G.J., Ochoa-Orrego, L.E., Garcia Pereira, L.H. & Maldonado-Ocampo, J.A. (2019) Species delimitation of neotropical Characins (Stevardiinae): Implications for taxonomy of complex groups. PLoS One, 14 (6), e0216786. https://doi.org/10.1371/journal.pone.0216786
  28. Géry, J. (1977) Characoids of the world. TFH Publications, Neptune City, 672 pp.
  29. Géry, J. (1999) A new anostomid species, Leporinus bleheri n. sp., from the Rio Guaporé-Iténez basin, with comments on some related species (Teleostei: Ostariophysi: Characiformes). Aqua, Journal of Ichthyology and Aquatic Biology, 3 (3), 105–112.
  30. Giarrizzo, T., Oliveira, R.R.S., Andrade, M.C., Gonçalves, A.P., Barbosa, T.A.P., Martins, A.R., Marques, D.K., Santos, J.L.B., Frois, R.P.S., Albuquerque, T.P.O., Montag, L.F.A., Camargo, M. & Sousa, L.M. (2015) Length–weight and length–length relationships for 135 fish species from the Xingu River (Amazon Basin, Brazil). Journal of Applied Ichthyology, 31 (2), 415–424. https://doi.org/10.1111/jai.12677
  31. Gomes, L.C., Pessali, T.C., Sales, N.G., Pompeu, P.S. & Carvalho, D.C. (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
  32. Guimarães, K.L.A., Lima, M.P., Santana, D.J., de Souza, M.F.B., Barbosa, R.S. & Rodrigues, L.R.R. (2022) DNA barcoding and phylogeography of the Hoplias malabaricus species complex. Scientific Reports, 12 (1), 1–15. https://doi.org/10.1038/s41598-022-09121-z
  33. Hammer, Ø., Harper, D.A. & Ryan, P.D. (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia electronica, 4 (1), 1–9.
  34. Higuchi, H. (1996) An updated list of ichthyological collecting stations of the Thayer Expedition to Brazil (1865–1866). Available from: https://mcz.harvard.edu/files/mcz/files/higuchi_1996_thayer_formated_prelim.pdf (accessed 3 February 2024)
  35. Isbrücker, I.J.H. (1973) Status of the primary homonymous South American catfish Loricaria cirrhosa Perugia, 1897, with remarks on some other loricariids (Pisces, Siluriformes, Loricariidae). Annali del Museo Civico di Storia Naturale di Genova, 79, 172–191.
  36. Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120. https://doi.org/10.1007/BF01731581
  37. Kullander, S.O. (2003) Family Cichlidae. In: Reis, R.E., Kullander, S.O., Ferraris Jr., C.J (Eds.), Check list of the freshwater fishes of South and Central America. Edipucrs, Porto Alegre, pp. 605–654.
  38. Langeani, F., Castro, R.M.C., Oyakawa, O.T., Shibatta, O.A., Pavanelli, C.S. & Casatti, L. (2007) Diversidade da ictiofauna do Alto Rio Paraná: composição atual e perspectivas futuras. Biota Neotropica, 7 (3), 181–197. [in Portuguese] https://doi.org/10.1590/S1676-06032007000300020
  39. Lima, F.C.T. (2004) Brycon gouldingi, a new species from the rio Tocantins drainage, Brazil (Ostariophysi: Characiformes: Characidae), with a key to the species in the basin. Ichthyological Exploration of Freshwaters, 15, 279–287.
  40. Lucinda, P.H., Freitas, I.S., Soares, A.B., Marques, E.E., Agostinho, C.S. & de Oliveira, R.J. (2007) Fish, Lajeado reservoir, rio Tocantins drainage, state of Tocantins, Brazil. Check List, 3 (2), 70–83. https://doi.org/10.15560/3.2.70
  41. Luo, A., Ling, C., Ho, S.Y. & Zhu, C.D. (2018) Comparison of methods for molecular species delimitation across a range of speciation scenarios. Systematic Biology, 67 (5), 830–846. https://doi.org/10.1093/sysbio/syy011
  42. Mahnert, V., Géry, J. & Muller, S. (1997) Leporinus falcipinnis n. sp., a new species from the lower rio Tapajos basin, Para, Brazil (Pisces, Characiformes, Anostomidae). Revue suisse de Zoologie, 104 (4), 837–844. https://doi.org/10.5962/bhl.part.80025
  43. Myers, G.S. (1950) Studies on South American fresh-water fishes. II. The genera of anostomine characids. Stanford Ichthyological Bulletin, 3 (4), 184–198.
  44. Ohara, W.M., Lima, F.C.T., Salvador, G.N. & Andrade, M.C. (2017) Peixes do rio Teles Pires: diversidade e guia de identificação. Gráfica Amazonas e Editora Ltda–EPP, Aparecida de Goiânia, 408 pp. [in Portuguese]
  45. Pavanelli, C.S., da Graça, W.J., Zawadzki, C.H., Britski, H.A., Vidotti, A.P., Avelino, G.S. & Veríssimo, S. (2007) Fishes from the Corumbá Reservoir, Paranaíba River drainage, upper Paraná River basin, State of Goiás, Brazil. Check List, 3 (1), 58–64. https://doi.org/10.15560/3.1.58
  46. Pereira, L.H., Hanner, R., Foresti, F. & Oliveira, C. (2013) Can DNA barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna?. BMC Genetics, 14 (1), 1–14. https://doi.org/10.1186/1471-2156-14-20
  47. Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W. & Vogler, A.P. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55 (4), 595–609. https://doi.org/10.1080/10635150600852011
  48. Puillandre, N., Brouillet, S. & Achaz, G. (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources, 21 (2), 609–620. https://doi.org/10.1111/1755-0998.13281
  49. R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.R-project.org/ (accessed 21 February 2022)
  50. Ramirez, J.L., Birindelli, J.L.O., Carvalho, D.C., Affonso, P.R.A.M., Venere, P.C., Ortega, H., Carrillo-Avila, M., Rodríguez-Pulido, J.A. & Galetti Jr., P.M. (2017) Revealing hidden diversity of the underestimated neotropical ichthyofauna: DNA barcoding in the recently described genus Megaleporinus (Characiformes: Anostomidae). Frontiers in Genetics, 8, 149. https://doi.org/10.3389/fgene.2017.00149
  51. Ramirez, J.L., Birindelli, J.L.O. & Galetti Jr., P.M. (2017) A new genus of Anostomidae (Ostariophysi: Characiformes): diversity, phylogeny and biogeography based on cytogenetic, molecular and morphological data. Molecular Phylogenetics and Evolution, 107, 308–323. https://doi.org/10.1016/j.ympev.2016.11.012
  52. Ramirez, J.L., Carvalho‐Costa, L.F., Venere, P.C., Carvalho, D.C., Troy, W.P. & Galetti Jr., P.M. (2016) Testing monophyly of the freshwater fish Leporinus (Characiformes, Anostomidae) through molecular analysis. Journal of Fish Biology, 88 (3), 1204–1214. https://doi.org/10.1111/jfb.12906
  53. Ramirez, J.L. & Galetti Jr., P.M. (2015) DNA barcode and evolutionary relationship within Laemolyta Cope 1872 (Characiformes: Anostomidae) through molecular analyses. Molecular Phylogenetics and Evolution, 93, 77–82. https://doi.org/10.1016/j.ympev.2015.07.021
  54. Ramirez, J.L., Santos, C.A., Machado, C.B., Oliveira, A.K., Garavello, J.C., Britski, H.A. & Galetti Jr., P.M. (2020) Molecular phylogeny and species delimitation of the genus Schizodon (Characiformes, Anostomidae). Molecular Phylogenetics and Evolution, 153, 106959. https://doi.org/10.1016/j.ympev.2020.106959
  55. Reis, R.B., Frota, A., Deprá, G.D.C., Ota, R.R. & da Graça, W.J. (2020) Freshwater fishes from Paraná State, Brazil: an annotated list, with comments on biogeographic patterns, threats, and future perspectives. Zootaxa, 4868 (4), 451–494. https://doi.org/10.11646/zootaxa.4868.4.1
  56. Sabaj, M.H. (2020) Codes for natural history collections in ichthyology and herpetology. Copeia, 108 (3), 593–669. https://doi.org/10.1643/ASIHCODONS2020
  57. Santos, C.J., Tencatt, L.F.C., Ota, R.R. & da Graça, W.J. (2013) Second record of Leporinus tigrinus Borodin, 1929 (Characiformes: Anostomidae) in the Upper Paraná River basin, Brazil. Check List, 9 (6), 1543–1544. https://doi.org/10.15560/9.6.1543
  58. Santos, G.M.D. & Jégu, M. (1989) Inventário taxonômico e redescrição das espécies de anostomídeos (Characiformes, Anostomidae) do baixo rio Tocantins, PA, Brasil. Acta Amazonica, 19, 159–213. [in Portuguese] https://doi.org/10.1590/1809-43921989191213
  59. Sidlauskas, B.L., Assega, F.M., Melo, B.F., Oliveira, C. & Birindelli, J.L.O. (2021) Total evidence phylogenetic analysis reveals polyphyly of Anostomoides and uncovers an unexpectedly ancient genus of Anostomidae fishes (Characiformes). Zoological Journal of the Linnean Society, 194 (2), 626–669. https://doi.org/10.1093/zoolinnean/zlab016
  60. Sidlauskas, B.L. & Birindelli, J.L.O. (2017) Family Anostomidae. In: van der Sleen, P. & Albert, J.S. (Eds.), Field guide to the fishes of the Amazon, Orinoco, and Guianas. Princeton University Press, Princeton, New Jersey, pp. 82–89.
  61. Sidlauskas, B.L. & Vari, R.P. (2008) Phylogenetic relationships within the South american fish family Anostomidae (Teleostei, Ostariophysi, Characiformes). Zoological Journal of the Linnean Society, 154 (1), 70–210. https://doi.org/10.1111/j.1096-3642.2008.00407.x
  62. Soares, I.M., Azevedo-Santos, V.M. & Benine, R.C. (2017) Redescription of Moenkhausia megalops (Eigenmann, 1907), a widespread tetra from the Amazon basin (Characiformes, Characidae). Zoosystematics and Evolution, 93 (2), 255–264. https://doi.org/10.3897/zse.93.10837
  63. Tamura, K., Stecher, G. & Kumar, S. (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular biology and evolution, 38 (7), 3022–3027. https://doi.org/10.1093/molbev/msab120
  64. Taylor, W.R. & Van Dyke, G.C. (1985) Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9 (2), 107–119.
  65. Toledo-Piza, M., Baena, E.G., Dagosta, F.C.P., Menezes, N.A., Ândrade, M., Benine, R.C., Bertaco, V.A., Birindelli, J.L.O., Boden, G., Buckup, P.A., Camelier, P., Carvalho, F.R., Castro, R.M.C., Chuctaya, J., Decru, E., Derijst, E., Dillman, C.B., Ferreira, K.M., Merxem, D.G., Giovannetti, V., Hirschmann, A., Jégu, M., Jerep, F.C., Langeani, F., Lima, F.C.T., Lucena, C.A.S., Lucena, Z.M.S., Malabarba, L.R., Malabarba, M.C.S.L., Marinho, M.M.F., Mathubara, K., Mattox, G.M.T., Melo, B.F., Moelants, T., Moreira, C.R., Musschoot, T., Netto-Ferreira, A.L., Ota, R.P., Oyakawa, O.T., Pavanelli, C.S., Reis, R.E., Santos, O., Serra, J.P., Silva, G.S.C., Silva-Oliveira, C., Souza-Lima, R., Vari, R.P. & Zanata, A.M. (2024) Checklist of the species of the Order Characiformes (Teleostei: Ostariophysi). Neotropical Ichthyology, 22 (1), e230086. https://doi.org/10.1590/1982-0224-2023-0086
  66. Ward, R.D., Hanner, R. & Hebert, P.D.N. (2009) The campaign to DNA barcode all fishes, FISH‐BOL. Journal of Fish Biology, 74 (2), 329–356. https://doi.org/10.1111/j.1095-8649.2008.02080.x
  67. Ward, R.D., Zemlak, T.S., Innes, B.H., Last, P.R. & Hebert, P.D.N. (2005) DNA barcoding Australia's fish species. Philosophical Transactions of the Royal Society B: Biological Sciences, 360 (1462), 1847–1857. https://doi.org/10.1098/rstb.2005.1716
  68. Weitzman, S.H. (1962) The osteology of Brycon meeki, a generalized characid fish, with an osteological definition of the family. Stanford Ichthyological Bulletin, 8, 1–77.
  69. Winterbottom, R. (1980) Systematics, osteology and the phylogenetic relationships of fishes of the Ostariophysan subfamily Anostominae (Characoidei, Anostominae). Royal Ontario Museum, Life Sciences Contribution, 123, 1–112. https://doi.org/10.5962/bhl.title.52085
  70. Zawadzki, C.H., Birindelli, J.L.O. & Lima, F.C.T. (2008) A new pale-spotted species of Hypostomus Lacépède (Siluriformes: Loricariidae) from the rio Tocantins and rio Xingu basins in central Brazil. Neotropical Ichthyology, 6 (3), 395–402. https://doi.org/10.1590/S1679-62252008000300012
  71. 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
  72. Zuanon, J.A.S. (1999) História natural da ictiofauna de corredeiras do rio Xingu, na região de Altamira, Pará. Unpub. Doctoral thesis, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, 200 pp. [in Portuguese]