Advertisement

Species diversity in Gymnogeophagus (Teleostei: Cichlidae) and comparative biogeography of cichlids in the Middle Paraná basin, an emerging hotspot of fish endemism

  • Oldřich Říčan
  • Štěpánka Říčanová
  • Klára Dragová
  • Lubomír Piálek
  • Adriana Almirón
  • Jorge Casciotta
ADVANCES IN CICHLID RESEARCH III
  • 71 Downloads

Abstract

We address the diversity of two species groups of the cichlid genus Gymnogeophagus in the Middle Paraná basin using molecular phylogeography and traditional morphological characters and conclude that they are composed of a higher diversity of endemic species than previously thought. The nominal Gymnogeophagus setequedas is found non-monophyletic with each phylogeographic lineage endemic to a single tributary of the Middle Paraná (Rio Acaray, Rio Monday, the Itaipu area). Prime candidates for the origin of the species in the G. setequedas group are waterfalls that separate most of the tributaries from the Middle Paraná River. The postulated waterfall- and rapids-driven fragmentation of Gymnogeophagus in the studied area falls into a narrow time window coinciding with the Pleistocene epoch. We further demonstrate that the endemism in Gymnogeophagus shows a high degree of biogeographical congruence with other sympatric cichlid genera. The Middle Paraná basin has up to 27 globaly endemic species of cichlid fishes in three genera and 21 of these species are endemics of single tributaries of the Middle Paraná. As a final consideration we address threats to the long term survival of the still poorly known but clearly highly endemic and endangered fish fauna of the Middle Paraná basin.

Keywords

Freshwater fishes Endemism Putative new species Phylogeography Molecular-clock dating Conservation 

Notes

Acknowledgements

We thank Soledad Gouric for the pictures of the LPJ and the authorities of Ministerio de Ecología y Recursos Naturales Renovables de la Provincia de Misiones for the awarded fishing permits. Financial support was provided by the Czech Science Foundation (GAČR) (Grant Number 14-26060P) to ŠŘ and by Comisión de Investigaciones Científicas de la provincia de Buenos Aires (CIC), Facultad de Ciencias Naturales y Museo (UNLP) and Administración de Parques Nacionales.

Supplementary material

10750_2018_3691_MOESM1_ESM.doc (2.4 mb)
Supplementary material 1 (DOC 2495 kb). Fig. S1. Map of the Paraná basin featuring the Middle Paraná section and parts of the Upper and Lower sections. White bars show boundaries of the Middle Paraná section. Note the floodplain nature of both the Lower and Upper Paraná as opposed to the canyon-type nature of the Middle Paraná. Note that the nature of the Itaipú area drainage is of a similar nature as the rest of the Middle Paraná but that the canyon of the Middle Paraná in the Itaipú area is flooded by the Itaipú reservoir. The arrow shows the Itaipú dam. The Itaipú area is now part of the Upper Paraná basin because the Itaipú reservoir flooded the Setequedas falls (upper bar) that used to separate the Middle and Upper Paraná sections. The different geomorphological nature of the Middle Paraná explains its high endemism compared to the faunas of both the Lower and Upper Paraná. Fig. S2. Phylogenetic relationships within Gymnogeophagus based on the cytb marker from BEAST analysis (as in Fig. 2) showing support values instead of dating. Fig. S3. Phylogenetic relationships within Gymnogeophagus showing species delimitation results based on the GMYC analysis (red branches are based on this analysis intraspecific, black branches are interspecific). The upper inset figure shows the single treshold line and the lower inset figure the single treshold peak. Because of this the multiple threshold analysis (not shown) provided identical results to the single treshold analysis. The focal species groups are colored as in Fig. 2. The tree is the same ultrametric tree from BEAST analysis as in Fig. 2 and Fig. S2

References

  1. Abell, R., M. L. Thieme, C. Revenga, M. Bryer, M. Kottelat, N. Bogutskaya, B. Coad, N. Mandrak, S. C. Balderas, W. Bussing, M. L. J. Stiassny, P. Skelton, G. R. Allen, P. Unmack, A. Naseka, R. Ng, N. Sindorf, J. Robertson, E. Armijo, J. V. Higgins, T. J. Heibel, E. Wikramanayake, D. Olson, H. L. López, R. E. Reis, J. G. Lundberg, M. H. Sabaj Pérez & P. Petry, 2008. Freshwater ecoregions of the World: a new map of biogeographic units for freshwater biodiversity conservation. BioScience 58: 403–414.CrossRefGoogle Scholar
  2. Albert, J. S., P. Petry & R. E. Reis, 2011. Major Biogeographic and Phylogenetic Patterns. In: Historical Biogeography of Neotropical Freshwater Fishes. In Albert, J. S. & R. E. Reis (eds), Historical Biogeography of Neotropical Freshwater Fishes. University of California Press, Berkeley CA: 21–57.CrossRefGoogle Scholar
  3. Agostinho, A. A., S. M. Thomaz & L. C. Gomes, 2004. Threats for biodiversity in the floodplain of the Upper Paraná River: effects of hydrological regulation by dams. Ecohydrology and Hydrobiology 4: 255–268.Google Scholar
  4. Agostinho, A. A., F. M. Pelicice, A. C. Petry, L. C. Gomes & H. F. Júlio Jr., 2007. Fish diversity in the upper Paraná River basin: habitats, fisheries, management and conservation. Aquatic Ecosystem Health Management 10(2): 174–186.CrossRefGoogle Scholar
  5. Agostinho, A. A., L. C. Gomes, N. C. L. Santos, J. C. G. Ortega & F. M. Pelicice, 2016. Fish assemblages in Neotropical reservoirs: colonization patterns, impacts and management. Fisheries Research 173: 26–36.CrossRefGoogle Scholar
  6. Agostinho, A. A., S. M. Thomaz & L. C. Gomes, 2005. Conservation of the biodiversity of Brazil’s inland waters. Conservation Biology 13: 616–652.Google Scholar
  7. Azpelicueta, M., G. Aguilera & J. M. Mirande, 2011. Heptapterus mbya (Siluriformes: Heptapteridae), a new species of catfish from the Paraná river basin, in Argentina. Revue Suisse de Zoologie 118: 319–327.CrossRefGoogle Scholar
  8. Baumgartner, G., C. S. Pavanelli, D. Baumgartner, A. G. Bifi, T. Debona & V. A. Frana, 2012. Peixes do baixo rio Iguaçu. Eduem, Maringá.CrossRefGoogle Scholar
  9. Bertonatti, C. & J. Corcuera, 2000. Situación ambiental Argentina. Fundación Vida Silvestre, Buenos Aires.Google Scholar
  10. Bonetto, A. A., J. R. Wais & H. P. Castello, 1989. The increasing damming of the Paraná basin and its effects on the lower reaches. River Research and Applications 4: 333–346.Google Scholar
  11. Burress, E. D., F. Alda, A. Duarte, M. Loureiro, J. W. Armbruster & P. Chakrabarty, 2017. Phylogenomics of pike cichlids (Cichlidae: Crenicichla): the rapid evolution and trophic diversification of an incipient species flock. Journal of Evolutionary Biology.  https://doi.org/10.1111/jeb.13196.Google Scholar
  12. Burress, E. D., L. Piálek, J. R. Casciotta, A. Almirón, M. Tan, J. W. Armbruster & O. Říčan, 2018. Island- and lake-like parallel adaptive radiations replicated in rivers. Proceedings of the Royal Society B, Biological sciences 285: 20171762.CrossRefPubMedGoogle Scholar
  13. Carstens, B. C. & T. A. Dewey, 2010. Species delimitation using a combined coalescent and information-theoretic approach: an example from North American Myotis bats. Systematic Biology 59: 400–414.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Casciotta, J. R., S. E. Gómez & N. Toresani, 1995. ‘Cichlasoma’ tembe, a new cichlid species from the río Paraná basin, Argentina (Osteichthyes: Labroidei). Ichthyological Exploration of Freshwaters 6: 193–200.Google Scholar
  15. Casciotta, J. R., S. E. Gómez & N. Toresani, 2000. Gymnogeophagus che, una nueva especie de la familia Cichlidae de la cuenca del río Paraná (Perciformes: Labroidei). Revista Museo Argentino de Ciencias naturales n.s. 2: 53–59.Google Scholar
  16. Casciotta, J., A. Almirón, L. Piálek, S. Gómez & O. Říčan, 2010. Crenicichla ypo (Teleostei: Cichlidae), a new species from the middle Paraná basin in Misiones, Argentina. Neotropical Ichthyology 8: 643–648.CrossRefGoogle Scholar
  17. Casciotta, J., A. E. Almirón & S. E. Gómez, 2006. Crenicichla yaha sp. n. (Perciformes: Labroidei: Cichlidae), a new species from the río Iguazú and arroyo Urugua-í basins, northeastern Argentina. Zoologische Abhandlungen 56: 107–112.Google Scholar
  18. Casciotta, J., A. Almirón, D. Aichino, S. Gómez, L. Piálek & O. Říčan, 2013. Crenicichla taikyra (Teleostei: Cichlidae), a new species of pike cichlid from the middle rio Parana, Argentina. Zootaxa 3721: 379–386.CrossRefPubMedGoogle Scholar
  19. Casciotta, J., A. Almirón, L. Ciotek, P. Giorgis, O. Říčan, L. Piálek, K. Dragová, Y. Croci, M. Montes, J. Iwaszkiw & A. Puentes, 2016. Visibilizando lo invisible. Un relevamiento de la diversidad de peces del Parque Nacional Iguazú, Misiones. Argentina. Historia Natural (Tercera Serie) 6: 5–77.Google Scholar
  20. Casciotta, J., A. Almirón, L. Piálek & O. Říčan, 2017a. Gymnogeophagus taroba (Teleostei: Cichlidae), a new species from the río Iguazú basin, Misiones, Argentina. Historia Natural (Tercera Serie) 7: 5–22.Google Scholar
  21. Casciotta, J., A. Almirón, Š. Říčanová, K. Dragová, L. Piálek, F. Alonso & O. Říčan, 2017b. First record of Gymnogeophagus lipokarenos Malabarba, Malabarba & Reis, 2015 (Teleostei: Cichliformes) from Argentina. Ichthyological Contributions of PecesCriollos 54: 1–5.Google Scholar
  22. Concheiro Pérez, G. A., O. Říčan, G. Ortí, E. Bermingham, I. Doadrio & R. Zardoya, 2007. Phylogeny and biogeography of 91 species of heroine cichlids (Teleostei: Cichlidae) based on sequences of the cytochrome b gene. Molecular Phylogenetics and Evolution 43: 91–110.CrossRefPubMedGoogle Scholar
  23. Drummond, A. J. & A. Rambaut, 2007. BEAST: bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Farias, I. P., G. Ortí, I. Sampaio, H. Schneider & A. Meyer, 2001. The cytochrome b gene as a phylogenetic marker: the limits of resolution for analyzing relationships among cichlid fishes. Journal of Molecular Evolution 53: 89–103.CrossRefPubMedGoogle Scholar
  26. Fontaneto, D., E. A. Herniou, C. Boschetti, M. Caprioli, G. Melone, C. Ricci & T. G. Barraclough, 2007. Independently evolving species in asexual bdelloid rotifers. PLoS Biology 5: e87.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Fujisawa, T. & T. G. Barraclough, 2013. Delimiting species using single-locus data and the generalized mixed yule coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Systematic Biology 62: 707–724.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Galindo-Leal, C. & I. de Gusmão Câmara, 2003. Atlantic Forest hotspot status: An overview. En: C. Galindo-Leal y de Gusmão Câmara, I. (eds), The Atlantic Forest of South America: Biodiversity status, threats, and outlook, pp. 3–12.Google Scholar
  29. Giraudo, A. F., E. Krauczuk, V. Arzamendia & H. Povedano, 2003. Critical analysis of protected areas in the Atlantic Forest of Argentina. In Galindo-Leal I. & I. de Guzmão Câmara (eds), The Atlantic Forest of South America: biodiversity status, threats, and outlook: 245–261.Google Scholar
  30. Guerrero, R. A., E. M. Acha, M. B. Framiňan & C. A. Lasta, 1997. Physical oceanography of the Río de la Plata Estuary, Argentina. Continental Shelf Research 17: 727–742.CrossRefGoogle Scholar
  31. Haq, B. U., J. Hardenbol & P. R. Vail, 1987. Chronology of Fluctuating Sea Levels since the Triassic. Science 235: 1156–1167.CrossRefPubMedGoogle Scholar
  32. Huelsenbeck, J. P. & F. Ronquist, 2001. MrBayes: bayesian inference of phylogenetics trees. Bioinformatics 17: 754–755.CrossRefPubMedGoogle Scholar
  33. Ilves, K. L., D. Torti & H. López-Fernández, 2017. Exon-based phylogenomics strengthens the phylogeny of Neotropical cichlids and identifies remaining conflicting clades (Cichliformes: Cichlidae: Cichlinae). Molecular Phylogenetics and Evolution in press.  https://doi.org/10.1016/j.ympev.2017.10.008.Google Scholar
  34. Ingenito, L. F. S., L. F. Duboc & V. Abilhoa, 2004. Contribução ao conhecimento da ictiofauna da bacia de alto rio Iguaçu, Paraná, Brasil. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR 7: 23–36.Google Scholar
  35. Ingenito, L. F. S., M. S. Ghazzi, L. F. Duboc & V. Abilhoa, 2008. Two new species of Rineloricaria (Siluriformes: Loricariidae) from the rio Iguaçu basin, southern Brazil. Neotropical Ichthyology 6: 355–366.CrossRefGoogle Scholar
  36. Júlio Júnior, H. F., C. D. Tós, A. A. Agostinho & C. S. Pavanelli, 2009. A massive invasion of fish species after eliminating a natural barrier in the upper rio Paraná basin. Neotropical Ichthyology 7: 709–718.CrossRefGoogle Scholar
  37. Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. Duran, T. Thierer, B. Ashton, P. Mentjies & A. Drummond, 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Koerber, S., T. O. Litz & J. M. Mirande, 2017a. CLOFFAR - update 4 - supplement to Checklist of the Freshwater Fishes of Argentina. Ichthyological Contributions of PecesCriollos 55: 1–11.Google Scholar
  39. Koerber, S., H. S. Vera-Alcaraz & R. E. Reis, 2017b. Checklist of the Fishes of Paraguay (CLOFPY). Ichthyological Contributions of PecesCriollos 53: 1–99.Google Scholar
  40. Kullander, S. O., 1998. A phylogeny and classification of the South American Cichlidae (Teleostei: Perciformes). In Malabarba, L. R., R. E. Reis, R. P. Vari, Z. M. S. Lucena & C. A. S. Lucena (eds), Phylogeny and classification of Neotropical fishes. Edipucrs, Porto Alegre: 461–498.Google Scholar
  41. Kullander, S. O., 2009. Crenicichla mandelburgeri, a new species of cichlid fish (Teleostei: Cichlidae) from the Paraná river drainage in Paraguay. Zootaxa 2006: 41–50.Google Scholar
  42. Kullander, S. O. & C. A. S. Lucena, 2013. Crenicichla gillmorlisi, a new species of cichlid fish (Teleostei: Cichlidae) from the Paraná river drainage in Paraguay. Zootaxa 3641: 149–164.CrossRefPubMedGoogle Scholar
  43. Langeani, F., R. M. C. Castro, O. T. Oyakawa, O. A. Shibatta, C. S. Pavanelli & L. Casatti, 2007. Diversidade da ictiofauna do Alto Rio Paraná: composição atual e perspectivas futuras. Biota Neotropica 7: 181–197.CrossRefGoogle Scholar
  44. López, H. L., C. C. Morgan & M. J. Montenegro, 2002. Ichthyological ecoregions of Argentina. División Zoología La Plata, Argentina, División Zoología Vertebrados, Museo de La Plata., 71pp.Google Scholar
  45. López, H. L., A. M. Miquelarena & R. C. Menni, 2003. Lista comentada de los peces continentales de la Argentina. ProBiota - Serie Técnica y Didáctica 5.Google Scholar
  46. López-Fernández, H., K. O. Winemiller & R. L. Honeycutt. 2010. Multilocus phylogeny and rapid radiations in Neotropical cichlid fishes (Perciformes: Cichlidae: Cichlinae). Molecular Phylogenetics and Evolution 55: 1070–1086.CrossRefPubMedGoogle Scholar
  47. Loureiro, M., M. Zarucki, L. R. Malabarba & I. González-Bergonzoni, 2016. A new species of Gymnogeophagus Miranda Ribeiro from Uruguay (Teleostei: Cichliformes). Neotropical Ichthyology 14: 155–164.CrossRefGoogle Scholar
  48. Malabarba, L. R., M. C. Malabarba & R. E. Reis, 2015. Descriptions of five new species of the Neotropical cichlid genus Gymnogeophagus Miranda Ribeiro, 1918 (Teleostei: Cichliformes) from the rio Uruguay drainage. Neotropical Ichthyology 13: 637–662.CrossRefGoogle Scholar
  49. Malabarba, M. C., L. R. Malabarba & C. del Papa, 2010. Gymnogeophagus eocenicus (Perciformes: Cichlidae), an Eocene cichlid from the Lumbrera Formation in Argentina. Journal of Vertebrate Paleontology 30: 341–350.CrossRefGoogle Scholar
  50. Matschiner, M., Z. Musilová, J. M. I. Barth, Z. Starostová, W. Salzburger, M. Steel & R. Bouckaert, 2017. Bayesian phylogenetic estimation of clade ages supports trans-Atlantic dispersal of cichlid fishes. Systematic Biology 66: 3–22.CrossRefPubMedGoogle Scholar
  51. Mirande, J. M. & S. Koerber, 2015. Checklist of the Freshwater Fishes of Argentina (CLOFFAR). Ichthyological Contributions of PecesCriollos 36: 1–68.Google Scholar
  52. Monaghan, M. T., R. Wild, M. Elliot, T. Fujisawa, M. Balke, D. G. J. Inward, D. C. Lees, R. Ranaivosolo, P. Eggleton, T. G. Barraclough & A. P. Vogler, 2009. Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58: 298–311.CrossRefPubMedGoogle Scholar
  53. Musilová, Z., O. Říčan, Š. Říčanová, P. Janšta, O. Gahura & J. Novák, 2015. Phylogeny and historical biogeography of trans-Andean cichlid fishes (Teleostei: Cichlidae). Vertebrate Zoology 65: 333–350.Google Scholar
  54. Myers, N., R. A. Mittermeier, C. G. Mittermeier, G. A. B. da Fonseca & J. Kent, 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–858.CrossRefPubMedGoogle Scholar
  55. Nylander, J. A. A., 2004. MrModeltest 2.2. Evolutionary Biology Centre, Uppsala University, Sweden. Available on internet at: http://www.abc.se/~nylander.
  56. Paíz, L. M., L. Baumgärtner, W. J. da Graça, V. P. Margarido & C. S. Pavanelli, 2017. Cytogenetics of Gymnogeophagus setequedas (Cichlidae: Geophaginae), with comments on its geographical distribution. Neotropical Ichthyology 15: e160035.CrossRefGoogle Scholar
  57. Pereyra, S. & G. García. 2008. Patterns of genetic differentiation in the Gymnogeophagus gymnogenys species complex, a neotropical cichlid from South American basins. Environmental Biology of Fishes 83: 245–257.CrossRefGoogle Scholar
  58. Piálek, L., O. Říčan, J. Casciotta, A. Almirón & J. Zrzavý, 2012. Multilocus phylogeny of Crenicichla (Teleostei: Cichlidae), with biogeography of the C. lacustris group: species flocks as a model for sympatric speciation in rivers. Molecular Phylogenetics and Evolution 62: 46–61.CrossRefPubMedGoogle Scholar
  59. Piálek, L., K. Dragová, J. Casciotta, A. Almirón & O. Říčan, 2015. Description of two new species of Crenicichla (Teleostei: Cichlidae) from the lower Iguazú river with a taxonomic reappraisal of C. iguassuensis, C. tesay and C. yaha. Historia Natural 5: 5–27.Google Scholar
  60. Pons, J., T. G. Barraclough, J. Gomez-Zurita, A. Cardoso, D. P. Duran, S. Hazell, S. Kamoun, W. D. Sumlin & A. P. Vogler, 2006. Sequence based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55: 595–609.CrossRefPubMedGoogle Scholar
  61. Powell, J. R., 2012. Accounting for uncertainty in species delineation during the analysis of environmental DNA sequence data. Methods in Ecology and Evolution 3: 1–11.CrossRefGoogle Scholar
  62. Rambaut, A. & A. J. Drummond, 2007. Tracer 1.5.0. [Available on internet at: http://beast.bio.ed.ac.uk/Tracer].
  63. Reis, R. E. & L. R. Malabarba, 1988. Revision of the Neotropical cichlid genus Gymnogeophagus Ribeiro, 1918, with descriptions of two new species (Pisces, Perciformes). Revista Brasileira de Zoologia 4: 259–305.CrossRefGoogle Scholar
  64. Reis, R. E., L. R. Malabarba & C. S. Pavanelli, 1992. Gymnogeophagus setequedas, a new cichlid species (Teleostei: Labroidei) from middle rio Paraná system, Brazil and Paraguay. Ichthyological Exploration of Freshwaters 3: 265–267.Google Scholar
  65. Resende, E. K., 2003. Migratory fishes of the Paraguay-Paraná basin excluding the Upper Paraná basin. In: Carolsfeld, J., B. Harvey, C. Ross & A. Baer (eds), Migratory Fishes of South America: Biology, Fisheries and Conservation Status. International Development Research Center: 99–155.Google Scholar
  66. Říčan, O. & S. O. Kullander, 2006. Character- and tree-based delimitation of species in the ‘Cichlasoma’ facetum group (Teleostei, Cichlidae) with the description of a new genus. Journal of Zoological Systematics and Evolutionary Research 44: 136–152.CrossRefGoogle Scholar
  67. Říčan, O. & Š. Říčanová, 2017. Live coloration, habitat, biogeography and phylogenetic position of Australoheros guarani Říčan & Kullander, 2008 (Teleostei: Cichlidae). Ichthyological Contributions of PecesCriollos 57: 1–6.Google Scholar
  68. Říčan, O., R. Zardoya & I. Doadrio, 2008. Phylogenetic relationships of Middle American cichlids (Teleostei, Cichlidae, Heroini) based on combined evidence from nuclear genes, mtDNA, and morphology. Molecular Phylogenetics and Evolution 49: 941–958.CrossRefPubMedGoogle Scholar
  69. Říčan, O., L. Piálek, A. Almirón & J. Casciotta, 2011. Two new species of Australoheros (Teleostei: Cichlidae), with notes on diversity of the genus and biogeography of the Río de la Plata basin. Zootaxa 2982: 1–26.Google Scholar
  70. Říčan, O., L. Piálek, R. Zardoya, I. Doadrio & J. Zrzavý, 2013. Biogeography of the Mesoamerican Cichlidae (Teleostei: Heroini): colonization through the GAARlandia land bridge and early diversification. Journal of Biogeography 40: 579–593.CrossRefGoogle Scholar
  71. Říčan, O., L. Piálek, K. Dragová & J. Novák, 2016. Diversity and evolution of the Middle American cichlid fishes (Teleostei: Cichlidae) with revised classification. Vertebrate Zoology 66: 1–102.Google Scholar
  72. Říčan, O., A. Almirón & J. Casciotta, 2017a. Rediscovery of Crenicichla yaha (Teleostei: cichlidae). Ichthyological Contributions of PecesCriollos 50: 1–8.Google Scholar
  73. Říčan, O., L. Piálek, Š. Říčanová, K. Dragová, A. Almirón & J. Casciotta, 2017b. First record of Gymnogeophagus constellatus Malabarba, Malabarba & Reis, 2015 (Teleostei: cichliformes) from Argentina. Ichthyological Contributions of PecesCriollos 56: 1–3.Google Scholar
  74. Ronquist, F. & J. P. Huelsenbeck, 2003. MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.CrossRefPubMedGoogle Scholar
  75. Souza-Shibatta, L., T. Kotelok-Diniz, D. G. Ferreira, O. A. Shibatta, S. H. Sofia, L. de Assumpção, S. F. R. Pini, S. Makrakis & M. C. Makrakis, 2018. Genetic Diversity of the Endangered Neotropical Cichlid Fish (Gymnogeophagus setequedas) in Brazil. Frontiers in Genetics 9: 13.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Swofford, D. L., 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates, Sunderland, MA.Google Scholar
  77. Terán, G. E., J. Ferrer, M. Benitez, F. Alonso, G. Aguilera & J. M. Mirande, 2017. Living in the waterfalls: a new species of Trichomycterus (Siluriformes: Trichomycteridae) from Tabay stream, Misiones. Argentina. PLoS ONE 12: e0179594.CrossRefPubMedGoogle Scholar
  78. Varella, H. R., 2011. Revisão taxonômica das espécies de Crenicichla Heckel das bacias dos rios Paraná e Paraguai (Teleostei: Cichlidae). Instituto de Biociências da Universidade de São Paulo, Dissertação de mestrado: 194.Google Scholar
  79. Vuataz, L., M. Sartori, A. Wagner & M. T. Monaghan, 2011. Toward a DNA taxonomy of Alpine Rhithrogena (Ephemeroptera: Heptageniidae) using a mixed Yule-coalescent analysis of mitochondrial and nuclear DNA. PloS One 6: e19728.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Wesselingh, F. P. & C. Hoorn, 2011. Geological Development of Amazon and Orinoco Basins. In Albert, J. S. & R. E. Reis (eds), Historical Biogeography of Neotropical Freshwater Fishes. University of California Press, Berkeley CA: 59–67.Google Scholar
  81. Zhang, J., P. Kapli, P. Pavlidis & A. Stamatakis, 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Zoology, Faculty of ScienceUniversity of South BohemiaCeské BudějoviceCzech Republic
  2. 2.División Zoología Vertebrados, Facultad de Ciencias Naturales y MuseoUNLPLa PlataArgentina
  3. 3.CIC, Comisión de Investigaciones Científicas de la Provincia de Buenos AiresLa PlataArgentina

Personalised recommendations