Abstract
The banded knife fish Gymnotus carapo is among the most widely distributed, broadly adapted (eurytopic), and phenotypically variable fish species in South America, with a geographic range of about 14 million km2, from the Llanos of Venezuela to the Pampas of northern Argentina. Here we assess the structure of phenotypic variation in G. carapo across this vast range from a study of 486 specimens representing the G. carapo clade, including 175 specimens of G. carapo collected from across the continental platform. We use multivariate statistics to quantify phenotypic differences within and among subspecies and species in aspects of pigmentation, caliper-based morphometrics, geometric morphometrics, meristics, and osteology. Our results demonstrate significant, but not diagnostic, differences among specimens representing seven new subspecies: G. c. australis from the La Plata (Paraná-Paraguay) basin, G. c. caatingaensis from the Parnaíba basin in the Brazilian state of Piauí, G. c. carapo from Suriname and French Guiana, G. c. madeirensis from the upper Madeira basin, G. c. occidentalis from the western Amazon, Negro, and Essequibo basins, G. c. orientalis from the eastern Amazon, Tocantins and Trombetas basins, and G. c. septentrionalis from the Orinoco basin and Trinidad Island. These results support the use of the subspecies, but not the species, rank to recognize and name these regionally delimited taxonomic entities.
References
Albert J.S., de Campos Fernandes-Matioli, F.M. & de Almeida-Toledo L.F. (1999) New Species of Gymnotus (Gymnotiformes, Teleostei) from Southeastern Brazil: Toward the Deconstruction of Gymnotus carapo. Copeia, 1999, 410–421.
https://doi.org/10.2307/1447486Albert, J.S. & Crampton, W.G.R. (2001) Five new species of Gymnotus (Teleostei: Gymnotiformes) from an upper Amazon floodplain, with descriptions of electric organ discharges and ecology. Ichthyological Exploration of Freshwaters, 12, 241–266.
Albert, J.S. & Crampton, W.G.R. (2003) Seven new species of the Neotropical electric fish Gymnotus (Teleostei, Gymnotiformes) with a redescription of G. carapo (Linnaeus). Zootaxa, 287, 1–54.
https://doi.org/10.11646/zootaxa.287.1.1Albert, J.S., Crampton, W.G.R., Thorsen, D.H. & Lovejoy, N.R. (2005) Phylogenetic systematics and historical biogeography of the Neotropical electric fish Gymnotus (Teleostei: Gymnotidae). Systematics and Biodiversity, 2 (4), 375–417.
https://doi.org/10.1017/S1477200004001574Albert, J.S. & Fink, W.L. (1996) Sternopygus xingu, a new species of electric fish from Brazil (Teleostei: Gymnotoidei), with comments on the phylogenetic position of Sternopygus. Copeia, 1996, 85–102.
https://doi.org/10.2307/1446944Albert, J.S. & Miller, R.R. (1995) Gymnotus maculosus: A new species of electric fish from Middle America (Chordata: Teleostei: Gymnotoidei), with a key to the species of Gymnotus. Proceedings Biological Society Washington, 108 (4), 662–678.
Albert, J.S., Petry, P. & Reis, R.E. (2011) Major biogeographic and phylogenetic patterns. In: Albert, J.S. & Reis, R.E. (Eds.), Historical Biogeography of Neotropical Freshwater Fishes. University of California Press, Berkeley, pp. 21–59.
https://doi.org/10.1525/california/9780520268685.003.0002Alexandre, C.V. & Esteves, K.E. (2010) Analysis of fish communities along a rural–urban gradient in a Neotropical stream (Piracicaba River Basin, São Paulo, Brazil). Hydrobiologia, 641 (1), 97–114.
https://doi.org/10.1007/s10750-009-0060-yAllendorf, F.W. & Leary, R.F. (1988) Conservation and distribution of genetic variation in a polytypic species, the cutthroat trout. Conservation Biology, 2 (2), 170–184.
https://doi.org/10.1111/j.1523-1739.1988.tb00168.xAraujo, F.G., Fichberg, I., Pinto, B.C.T. & Peixoto, M.G. (2003) A preliminary index of biotic integrity for monitoring the condition of the Rio Paraíba do Sul, southeast Brazil. Environmental management, 32 (4), 516–526.
https://doi.org/10.1007/s00267-003-3003-9Barbieri G. & Barbieri, M.C. (1982) Fecundidade e tipo de desova de Gymnotus carapo Linnaeus, 1758 na represa do Lobo, estado de São Paulo (Pisces, Gymnotidae). Spectrum: Jornal Brasileiro de Ciência, 2, 25–29.
Barbieri, M.C. & Barbieri, G. (1985) Reprodução de Gymnotus carapo Linnaeus, 1758 na represa do Lobo (SP). Morfologia e histologia de ovário. Variação sazonal. (Teleostei, Gymnotidae). Revista Brasileira de Biologia, 45, 3–12.
Barluenga, M. & Meyer, A. (2004) The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes? Molecular ecology, 13, 2061–2076.
https://doi.org/10.1111/j.1365-294X.2004.02211.xBarrella, W. & Petrere, M. (2003) Fish community alterations due to pollution and damming in Tietê and Paranapanema rivers (Brazil). River Research and Applications, 19 (1), 59–76.
https://doi.org/10.1002/rra.697Bertollo, L.A. C., Born, G.G., Dergam, J.A., Fenocchio, A.S. & Moreira-Filho, O. (2000) A biodiversity approach in the Neotropical Erythrinidae fish, Hoplias malabaricus. Karyotypic survey, geographic distribution of karyomorphs and cytotaxonomic considerations. Chromosome Research, 8, 603–613.
https://doi.org/10.1023/A:1009233907558Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K., Meier, R., Winker, 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.2006.11.004Black-Cleworth, P. (1970) The role of electrical discharges in the non-reproductive social behaviour of Gymnotus carapo (Gymnotidae, Pisces). Animal Behaviour Monographs, 3 (Part 1), 1–77. [IN1]
https://doi.org/10.1016/S0066-1856(70)80001-2Carvalho, T.P. (2013) Systematics and evolution of the toothless knifefishes Rhamphichthyoidea Mago-Leccia (Actinopterygii: Gymnotiformes): diversification in South American freshwaters. University of Louisiana, Lafayette, LA, 488 pp.
Casciotta, J., Almirón, A., Sánchez, S., Iwaszkiw, J. & Bruno, M.C. (2013) The genus Gymnotus (Gymnotiformes: Gymnotidae) in Argentina. How bad taxonomy results in poor regulations and no conservation. Journal of Applied Ichthyology, 29 (1), 208–212.
https://doi.org/10.1111/jai.12028Ciccotto, P.J. (2013) Morphometric Distinctness of an Isolated Population of Percina peltata (Shield Darter) on the Atlantic Coastal Plain of Maryland, USA. Copeia, 2013, 622–626.
https://doi.org/10.1643/CI-12-166Clayton, L.A. (2013) Overview of Brazil’s Legal Structure for Animal Issues. Available from: http://www.animallaw.info (accessed 14 August 2017)
Cognato, D.D.P. & Fialho, C.B. (2006) Reproductive biology of a population of Gymnotus aff. carapo (Teleostei: Gymnotidae) from southern Brazil. Neotropical Ichthyology, 4, 339–348.
https://doi.org/10.1590/S1679-62252006000300005Cognato, D., Richer de Forges, M., Albert, J.S., Crampton & W.G.R. (2007) Gymnotus chimarrao, a new species of electric fish (Gymnotiformes: Gymnotidae) from Southern Brazil. Ichthyological Exploration of Freshwaters, 18, 375–382.
Coyne, J.A. & Orr, H.A. (2004) Speciation. Vol. 37. Sunderland, MA, Sinauer Associates.
Crampton, W.G.R. (1998) Effects of anoxia on the distribution, respiratory strategies and electric signal diversity of gymnotiform fishes. Journal of Fish Biology, 53 (sA), 307–330.
https://doi.org/10.1111/j.1095-8649.1998.tb01034.xCrampton, W.G.R. (2008) Diversity and adaptation in deep channel Neotropical electric fishes. In: Sebart, P., Onyango, D.W. & Kapoor, B. (Eds.), Fish Life in Special Environments. Science Publishers, Enfield, NH, pp. 283–339.
Crampton, W.G.R. (2011) An ecological perspective on diversity and distributions. In: Albert, J.S. & Reis, R.E., (Eds.), Historical Biogeography of Neotropical Freshwater Fishes. University of California Press, Berkeley, pp 165–243.
https://doi.org/10.1525/california/9780520268685.003.0010Crampton, W.G.R. & Albert, J.S. (2003) A redescription of Gymnotus coropinae, an often misidentified species of gymnotid fish, with notes on ecology and electric organ discharge. Zootaxa, 348 (1), 1–20.
https://doi.org/10.11646/zootaxa.348.1.1Crampton, W.G.R. & Albert, J.S. (2004) A redescription of Gymnotus coatesi, with notes on osteology, natural history and electric signals. Copeia, 3, 525–533.
https://doi.org/10.1643/CI-03-246R1Crampton, W.G.R. & Hopkins, C.D. (2005) Nesting and paternal care in the weakly electric fish Gymnotus (Gymnotiformes: Gymnotidae) with descriptions of larval and adult electric organ discharges of two species. Copeia, 2005 (1), 48–60.
https://doi.org/10.1643/CI-04-056R1Crampton, W.G.R., Thorsen, D.H. & Albert, J.S. (2005) Three new species from a diverse assemblage of Gymnotus (Gymnotidae) in the Upper Amazon. Copeia, 2005 (1), 82–99.
https://doi.org/10.1643/CI-03-242R2Crampton, W.G.R., Lovejoy, N.R. & Albert, J.S.(2003) Gymnotus ucamara: a new species of Neotropical electric fish from the Peruvian Amazon (Ostariophysi: Gymnotidae). Zootaxa, 277, 1–18.
https://doi.org/10.11646/zootaxa.277.1.1Crandall, K.A., Bininda-Emonds, O.R., Mace, G.M. & Wayne, R.K. (2000) Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution, 15 (7), 290–295.
https://doi.org/10.1016/S0169-5347(00)01876-0De Queiroz, K. (2005) A unified concept of species and its consequences for the future of taxonomy. Proceedings California Academy of Sciences, 56, 196–215.
de Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56 (6), 879–886.
https://doi.org/10.1080/10635150701701083do Prado, F.D., Fernandez-Cebrián, R., Hashimoto, D.T., Senhorini, J.A., Foresti, F., Martínez, P. & Porto-Foresti, F. (2016) Hybridization and genetic introgression patterns between two South American catfish along their sympatric distribution range. Hydrobiologia, 788 (1), 319–343.
Dobzhansky, T. (1940) Speciation as a stage in evolutionary divergence. The American Naturalist, 74, 312–321.
https://doi.org/10.1086/280899Dubois, A., Minelli, A. & Zhang, Z.Q. (2011) Recommendations about nomenclature for papers submitted to Zootaxa. Zootaxa, 2943, 58–62.
Dumas, F. & Mazzoleni, S. (2017) Neotropical primate evolution and phylogenetic reconstruction using chromosomal data. The European Zoological Journal, 84, 1–18.
https://doi.org/10.1080/11250003.2016.1260655Eldredge, N. (2014) Time frames: The evolution of punctuated equilibria. Princeton University Press, Princeton, 242 pp.
Elliott, J.M. (1994) Quantitative ecology and the brown trout. Oxford University Press, Oxford, 298 pp.
Ellis, M.M. (1913) The gymnotid eels of tropical America. Memoirs of the Carnegie Museum, 6, 109–195.
https://doi.org/10.5962/bhl.title.12969Endangered Species Act of 1973. U.S. Senate Committee on Environment & Public Works. Available from: http://www.epw.senate.gov/esa73.pdf (accessed 11 August 2017)
Eschmeyer, W.N., Fricke, R., Fong, J.D. & Polack, D.A. (2010) Marine fish diversity: history of knowledge and discovery (Pisces). Zootaxa, 2525 (1), 19–50.
Eschmeyer, W.N., Fricke, R. & Van der Laan, R. (2014) Catalog of fishes: genera, species, references. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp (accessed 11 August 2017)
Evans, K.M., Waltz, B.T., Tagliacollo, V.A., Chakrabarty, P. & Albert, J.S. (2017) Why the short face: Developmental covariation between face and braincase skull regions drives convergent evolution in Neotropical electric fishes. Ecology and Evolution, 7 (6), 1783–1801.
https://doi.org/10.1002/ece3.2704Fernandes, F.M.C., Albert, J.S., Daniel-Silva, M.F.Z., Lopes, C.E., Crampton W.G.R. & Almeida-Toledo, L.F. (2005) A new Gymnotus (Teleostei: Gymnotiformes: Gymnotidae) from the Pantanal Matogrossense of Brazil and adjacent drainages; continued documentation of a cryptic fauna. Zootaxa, 933, 1–14.
https://doi.org/10.11646/zootaxa.933.1.1Fernholm, B. & Wheeler, A. (1983) Linnaean fish specimens in the Swedish Museum of Natural History, Stockholm. Zoological Journal of the Linnean Society, 78, 199–286.
https://doi.org/10.1111/j.1096-3642.1983.tb00867.xFerraris, C.J., de Santana, C.D. & Vari, R.P. (2017) Checklist of Gymnotiformes (Osteichthyes: Ostariophysi) and catalogue of primary types. Neotropical Ichthyology, 15 (1), e160067.
https://doi.org/10.1590/1982-0224-20160067Fujita, M.K., Leaché, A.D., Burbrink, F.T., McGuire, J.A. & Moritz, C. (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends in ecology & Evolution, 27 (9), 480–488.
https://doi.org/10.1016/j.tree.2012.04.012Gaither, M.R., Bowen, B.W., Rocha, L.A. & Briggs, J.C. (2016) Fishes that rule the world: circumtropical distributions revisited. Fish and Fisheries, 17 (3), 664–679.
https://doi.org/10.1111/faf.12136Gaston, K.J. & Spicer, J.I. (2013) Biodiversity: An Introduction. John Wiley & Sons, Hoboken, NJ, 208 pp.
Géry, J. & Vu, T.T. (1964) Gymnorhamphichthys hypostomus petiti ssp. nov. un curieux poisson Gymnotoïde Arénicole. Vie et Milieu Supplement, 17, 485–498.
Giuffra, E., Guyomard, R. & Forneris, G. (1996) Phylogenetic relationships and introgression patterns between incipient parapatric species of Italian brown trout (Salmo trutta L. complex). Molecular Ecology, 5, 207–220.
https://doi.org/10.1111/j.1365-294X.1996.tb00308.xGotelli, N.J. & Colwell, R.K. (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters, 4 (4), 379–391.
https://doi.org/10.1046/j.1461-0248.2001.00230.xHaig, S.M., Beever, E.A., Chambers, S.M., Draheim, H.M., Dugger, B.D., Dunham, S. & Lopes, I.F. (2006) Taxonomic considerations in listing subspecies under the US Endangered Species Act. Conservation Biology, 20 (6), 1584–1594.
https://doi.org/10.1111/j.1523-1739.2006.00530.xHarvey, M.G. & Brumfield, R.T. (2015) Genomic variation in a widespread Neotropical bird (Xenops minutus) reveals divergence, population expansion, and gene flow. Molecular Phylogenetics and Evolution, 83, 305–316.
https://doi.org/10.1016/j.ympev.2014.10.023Hulen, K.G., Crampton, W.G. & Albert, J.S. (2005) Phylogenetic systematics and historical biogeography of the Neotropical electric fish Sternopygus (Teleostei: Gymnotiformes). Systematics and Biodiversity, 3 (4), 407–432.
https://doi.org/10.1017/S1477200005001726Huston, M.A. & Huston, M.A. (1994) Biological Diversity: The Coexistence of Species. Cambridge University Press, Cambridge, MA, 681 pp.
Huxley, J. (1940) The New Systematics. Clarendon Press, Oxford, Oxford, 596 pp.
The International Trust for Zoological Nomenclature (1999) International Code of Zoological Nomenclature (ICZN) Fourth Edition. Available from: http://iczn.org/ (accessed 11 August 2017)
Isaac, N.J., Mallet, J. & Mace, G.M. (2004) Taxonomic inflation: its influence on macroecology and conservation. Trends in Ecology & Evolution, 19 (9), 464–469.
https://doi.org/10.1016/j.tree.2004.06.004Jelks, H.L., Walsh, S.J., Burkhead, N.M., Contreras-Balderas, S., Diaz-Pardo, E., Hendrickson, D.A. & Platania, S.P. (2008) Conservation status of imperiled North American freshwater and diadromous fishes. Fisheries, 33 (8), 372–407.
https://doi.org/10.1577/1548-8446-33.8.372Kelch, T.G. (2011) Globalization and animal law: comparative law, international law and international trade. Vol. 32. Kluwer Law International, Alphen aan den Rijn, 696 pp.
Klingenberg, C.P. (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.
https://doi.org/10.1111/j.1755-0998.2010.02924.xLehmberg, E. (2015) Biogeography of the weakly electric knifefish Gymnotus carapo (Teleostei: Gymnotidae) in the Guianas. University of Toronto, Toronto. Available from: https://tspace.library.utoronto.ca/bitstream/1807/69686/3/Lehmberg_Emma_S_201506_MSc_thesis.pdf (accessed 11 August 2017)
Liem, K.F., Eclancher, B. & Fink, W.L. (1984) Aerial respiration in the banded knife fish Gymnotus carapo (Teleostei: Gymnotoidei). Physiological Zoology, 1984, 185–195.
https://doi.org/10.1086/physzool.57.1.30155979Linnaeus, C. (1758) Systema Naturae Per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, Cum Charcteribus, Differentiis, Synonymis, Locis, Editio decima, reformata. Holmiæ. (Salvius), Stockholm, 824 pp.
Lovejoy, N.R., Lester, K., Crampton, W.G.R., Marques, F.P.L. & Albert, J.S. (2010) Phylogeny, biogeography, and electric signal evolution of Neotropical knifefishes of the genus Gymnotus (Osteichthyes: Gymnotidae). Molecular Phylogenetics and Evolution, 54, 278–290.
https://doi.org/10.1016/j.ympev.2009.09.017Lujan, N.K. & Armbruster, J.W. (2011) The Guiana Shield. In: Albert, J.S. & Reis, R.E., (Eds.), Historical Biogeography of Neotropical Freshwater Fishes. University of California Press, Berkeley, pp. 211–222.
https://doi.org/10.1525/california/9780520268685.003.0013Mace, G.M. (2004) The role of taxonomy in species conservation. Philosophical Transactions of the Royal Society B: Biological Sciences, 359 (1444), 711–719.
https://doi.org/10.1098/rstb.2003.1454Mago-Leccia, F. (1994) Electric fishes of the continental waters of America. Biblioteca de la Academia de Ciencias Fisicas, Matematicas y Naturales, Caracas, 206 pp.
Magurran, A.E. (2013) Measuring Biological Diversity. John Wiley & Sons, Hoboken, NJ, 264 pp.
Maldonado-Ocampo, J.A. & Albert, J.S. (2004) Gymnotus ardilai: a new species of Neotropical electric fish (Ostariophysi: Gymnotidae) from the Río Magdalena of Colombia. Zootaxa, 759, 1–10.
Margarido, V.P., Bellafronte, E. & Moreira‐Filho, O. (2007) Cytogenetic analysis of three sympatric Gymnotus (Gymnotiformes, Gymnotidae) species verifies invasive species in the Upper Paraná River basin, Brazil. Journal of Fish Biology, 70 (sb), 155–164.
https://doi.org/10.1111/j.1095-8649.2007.01365.xMaxime, E.L. (2013) Phylogenetic and revisionary taxonomic studies of the banded knifefishes Gymnotus (Teleostei, Ostariophysi, Gymnotiformes) with descriptions of fourteen new species. University of Louisiana, Lafayette, LA, 489 pp.
Maxime, E.L. & Albert, J.S. (2009) A new species of Gymnotus (Gymnotiformes: Gymnotidae) from the Fitzcarrald Arch of southeastern Peru. Neotropical Ichthyology, 7 (4), 579–585.
https://doi.org/10.1590/S1679-62252009000400004Maxime, E.L. & Albert, J.S. (2014) Redescription of the tuvirão, Gymnotus inaequilabiatus Valenciennes, 1839, using high-resolution X-ray computed tomography. Copeia, 2014 (3), 462–472.
https://doi.org/10.1643/CI-13-054Maxime, E.L., Lima, F.C.T. & Albert, J.S. (2011) A new species of Gymnotus (Gymnotiformes, Gymnotidae) from the Rio Tiquié in Northern Brazil. Copeia, 1, 77–81.
https://doi.org/10.1643/CI-10-009Mayr, E. (1942) Systematics and the Origin of Species. Columbia University Press, New York.
Mayr, E. & Ashlock, P.D. (1991) Principles of Systematic Zoology. 2nd Edition, McGraw-Hill, New York, NY, 475 pp.
McClure, M., Elias, M., Ehrlich, P., Raven, P., Janz, N., Nylin, S., Wahlberg, N., Nylin, S., Slove, J., Niklas, J., Janz, N., Nylin, S., Bossart, J., Scriber, J., Ladner, D., Altizer, S., Chew, F., Whinnett, A., Zimmermann, M., Willmott, K., Herrera, N., Mallarino, R., Simpson, F., Joron, M., Lamas, G., Mallet, J., Elias, M., Hill, R., Willmott, K., Dasmahapatra, K., Brower, A., Mallet, J., Jiggins, C., Dasmahapatra, K., Lamas, G., Simpson, F., Mallet, J., Slove, J., Janz, N., Drummond, B., Brown, K., Willmott, K., Mallet, J., Funk, W., Murphy, M., Hoke, K., Muths, E., Amburgey, S., Lemmon, E., Lemmon, A., Gilbert, L., Jiggins, C., McMillan, W., Mallet, J., Vasconcellos-Neto, J., Gratton, C., Welter, S., Jiménez, M.G., Sarmiento, C., Díaz, M., Chautá, A., Peraza, A., Ramírez, A., Murphy, S., Courtney, S., Kibota, T., Kibota, T., Courtney, S., Becerra, J., Venable, D., Matsubayashi, K., Ohshima, I., Nosil, P., Sandoval, C., Nosil, P., Chazot, N., Willmott, K., Endera, P.S., Toporov, A., Hill, R., Jiggins, C., Elias, M., Elias, M., Gompert, Z., Jiggins, C., Willmott, K., Sherratt, T., Nosil, P., Jiggins, C., Naisbit, R., Coe, R., Mallet, J., Naisbit, R., Jiggins, C., Mallet, J., Nylin, S. & Janz, N. (2016) Unravelling the role of host plant expansion in the diversification of a Neotropical butterfly genus. BMC Evolutionary Biology, 16, 128.
https://doi.org/10.1186/s12862-016-0701-5Milhomem, S.S.R., Crampton, W.G.R., Pieczarka, J.C., dos Santos Silva, D., Cardoso, A.L., da Silva, P.C. & Nagamachi, C.Y. (2012a) Chromosomal and electric signal diversity in three sympatric electric knifefish species (Gymnotus, Gymnotidae) from the Central Amazon Floodplain. Reviews in Fish Biology and Fisheries, 22 (2), 485–497.
https://doi.org/10.1007/s11160-011-9239-1Milhomem, S.S.R., Crampton, W.G.R., Pieczarka, J.C., Shetka, G.H., Silva, D.S. & Nagamach, C.Y. (2012b) Gymnotus capanema, a new species of electric knife fish (Gymnotiformes, Gymnotidae) from eastern Amazonia, with comments on an unusual karyotype. Journal of Fish Biology, 80, 802–815.
https://doi.org/10.1111/j.1095-8649.2012.03219.xMilhomem, S.S.R., Pieczarka, J.C., Crampton, W.G.R., De Souza, A.C.P., Carvalho, J.R. & Nagamachi, C.Y. (2007) Differences in karyotype between two sympatric species of Gymnotus (Gymnotiformes: Gymnotidae) from the eastern amazon of Brazil. Zootaxa, 62, 55–62.
Milhomem, S.S.R., Pieczarka, J.C., Crampton, W.G.R., Silva, D.S., De Souza, A.C.P., Carvalho Jr, J.R. & Nagamachi, C.Y. (2008) Chromosomal evidence for a cryptic species in the Gymnotus carapo species-complex (Gymnotiformes, Gymnotidae), BMC Genetics, 9 (75), 1–10.
https://doi.org/10.1186/1471-2156-9-75Milhomem, S.S.R., Scacchetti, P.C., Pieczarka, J.C., Ferguson-Smith, M.A., Pansonato-Alves, J.C., O’Brien, P.C., Foresti, F. & Nagamachi, C.Y. (2013) Are NORs always located on homeologous chromosomes? A FISH investigation with rDNA and whole chromosome probes in Gymnotus fishes (Gymnotiformes). PLoS ONE, 8 (2), e55608.
https://doi.org/10.1371/journal.pone.0055608Moritz, C. (1994) Defining ‘evolutionarily significant units’ for conservation. Trends in Ecology and Evolution, 9 (10), 373–374.
https://doi.org/10.1016/0169-5347(94)90057-4Morris, C.G. (1992) Academic Press dictionary of science and technology. Gulf Professional Publishing, Houston, TX, 2432 pp.
Nagamachi, C.Y., Pieczarka, J.C., Milhomem, S.S., O’Brien, P.C., de Souza, A.C. & Ferguson-Smith, M.A. (2010) Multiple rearrangements in cryptic species of electric knifefish, Gymnotus carapo (Gymnotidae, Gymnotiformes) revealed by chromosome painting. BMC Genetics, 11 (1), 1.
https://doi.org/10.1186/1471-2156-11-28Orr, H.A. (2001) The genetics of species differences. Trends in Ecology & Evolution, 16 (7), 343–350.
https://doi.org/10.1016/S0169-5347(01)02167-XPatten M.A. (2015) Subspecies and the philosophy of science. The Auk, 132, 481–485.
https://doi.org/10.1642/AUK-15-1.1Petchey, O.L. & Gaston, K.J. (2002) Functional diversity (FD), species richness and community composition. Ecology Letters, 5 (3), 402–411.
https://doi.org/10.1046/j.1461-0248.2002.00339.xPianka, E.R. (1967) On lizard species diversity: North American flatland deserts. Ecology, 48 (3), 333–351.
https://doi.org/10.2307/1932670Pires, T.H., Farago, T.B., Campos, D.F., Cardoso, G.M. & Zuanon, J. (2016) Traits of a lineage with extraordinary geographical range: ecology, behavior and life-history of the sailfin tetra Crenuchus spilurus. Environmental Biology of Fishes, 2016, 1–13.
https://doi.org/10.1007/s10641-016-0534-5Pyrcz, T.W., Clavijo, A., Uribe, S., Marin, M.A., Alvarez, C.F. & Zubek, A. (2016) Páramo de Belmira as an important centre of endemism in the northern Colombian Andes: New evidence from Pronophilina butterflies (Lepidoptera: Nymphalidae, Satyrinae, Satyrini). Zootaxa, 4179 (1), 77–102.
https://doi.org/10.11646/zootaxa.4179.1.3Richer-de-Forges, M.M., Crampton, W.G. & Albert, J.S. (2009) A new species of Gymnotus (Gymnotiformes, Gymnotidae) from Uruguay: description of a model species in neurophysiological research. Copeia, 2009 (3), 538–544.
Rohlf, F.J. (2015) The TPS series of software. Hystrix, the Italian Journal of Mammalogy, 26, 1–4.
Ryder, O.A. (1986) Species conservation and systematics: the dilemma of subspecies. Trends in Ecology & Evolution, 1 (1), 9–10.
https://doi.org/10.1016/0169-5347(86)90059-5Rylands, A.B., Mittermeier, R.A. & Silva, J.S. (2012) Neotropical primates: taxonomy and recently described species and subspecies. International Zoo Yearbook, 46, 11–24.
https://doi.org/10.1111/j.1748-1090.2011.00152.xSaul, W.G. (1975) An ecological study of fishes at a site in upper Amazonian Ecuador. Proceedings of Academy of Natural Sciences of Philadelphia, 127, 93–134.
Scacchetti, P.C., Pansonato-Alves, J.C., Utsunomia, R., Oliveira, C. & Foresti, F. (2011) Karyotypic diversity in four species of the genus Gymnotus Linnaeus, 1758 (Teleostei, Gymnotiformes, Gymnotidae): Physical mapping of ribosomal genes and telomeric sequences. Comparative Cytogenetics, 5, 223–235.
https://doi.org/10.3897/compcytogen.v5i3.1375Sexton, J.P., McIntyre, P.J., Angert, A.L. & Rice, K.J. (2009) Evolution and ecology of species range limits. Annual Review of Ecololgical and Evolutionary Systematcs, 40, 415–436.
https://doi.org/10.1146/annurev.ecolsys.110308.120317Shaffer, H.B. & McKnight, M.L. (1996) The polytypic species revisited: genetic differentiation and molecular phylogenetics of the tiger salamander Ambystoma tigrinum (Amphibia: Caudata) complex. Evolution, 417–433.
https://doi.org/10.1111/j.1558-5646.1996.tb04503.xSlatkin, M. (1987) Gene flow and the geographic structure of natural populations. Science, 236 (4803), 787–792.
https://doi.org/10.1126/science.3576198Stefánsson, M.O., Sigurdsson, T., Pampoulie, C., Daníelsdóttir, A.K., Thorgilsson, B., Ragnarsdóttir, A., Gíslason, D., Coughlan, J., Cross, T.F. & Bernatchez, L. (2009) Pleistocene genetic legacy suggests incipient species of Sebastes mentella in the Irminger Sea. Heredity, 102, 514–524.
https://doi.org/10.1038/hdy.2009.10Taeger, A., Blank, S.M. & Liston, A.D. (2010) World Catalog of Symphyta (Hymenoptera). Zootaxa, 2580, 1–1064.
Tagliacollo, V., Bernt, M.J., Craig, J.M., Oliviera, C. & Albert, J.S. (2016) Model-based Total Evidence phylogeny of Neotropical electric knifefishes (Ostariophysi, Gymnotiformes). Molecular Phylogenetics and Evolution, 95, 20–33.
https://doi.org/10.1016/j.ympev.2015.11.007Taylor, 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, 107–119.
Templeton, A.R. (1989) The meaning of species and speciation: a genetic perspective. The Units of Evolution: Essays on the Nature of Species, 1989, 159–183.
Terai, Y., Seehausen, O., Sasaki, T., Takahashi, K., Mizoiri, S., Sugawara, T., Sato T., Watanabe, M., Konijnendijk, N., Mrosso, H.D.J., Tachida, H., Imai, H., Shichida, Y. & Okada, N. (2006) Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. PLoS Biology, 4, 2244–2251.
https://doi.org/10.1371/journal.pbio.0040433Tilman, D. & Downing, J.A. (1996) Biodiversity and stability in grasslands. In: Tilman, D. & Downing, J.A. (Eds.), Ecosystem Management. Springer, New York, pp. 3–7.
https://doi.org/10.1007/978-1-4612-4018-1_1Tobias, J.A., Cornwallis, C.K., Derryberry, E.P., Claramunt, S., Brumfield, R.T. & Seddon, N. (2013) Species coexistence and the dynamics of phenotypic evolution in adaptive radiation. Nature, 506, 359–363.
https://doi.org/10.1038/nature12874Torres, R.A., Roper, J.J., Foresti, F. & Oliveira, C. (2005) Surprising genomic diversity in the Neotropical fish Synbranchus marmoratus (Teleostei: Synbranchidae): how many species? Neotropical Ichthyology, 3 (2), 277–284.
https://doi.org/10.1590/S1679-62252005000200005Torstrom, S.M., Pangle, K.L. & Swanson, B.J. (2014) Shedding subspecies: The influence of genetics on reptile subspecies taxonomy. Molecular Phylogenetics and Evolution, 76, 134–143.
https://doi.org/10.1016/j.ympev.2014.03.011Voje, K.L., Hansen, T.F., Egset, C.K., Bolstad, G.H. & Pélabon, C. (2014) Allometric constraints and the evolution of allometry. Evolution, 68, 866–885.
https://doi.org/10.1111/evo.12312Wagner, G.P. & Schwenk, K. (2000) Evolutionarily stable configurations: functional integration and the evolution of phenotypic stability. In: Wagner, G.P. & Schwenk, K. (Eds.), Evolutionary Biology. Springer, New York, pp. 155–217.
https://doi.org/10.1007/978-1-4615-4185-1_4Waples, R.S. (1991) Pacific salmon, Oncorhynchus spp., and the definition of “species” under the Endangered Species Act. Marine Fisheries Review, 53 (3), 11–22.
Wheeler, A. (1991) The Linnaean fish collection in the Zoological Museum of the University of Uppsala. Zoological Journal of the Linnean Society, 103, 145–195.
https://doi.org/10.1111/j.1096-3642.1991.tb00901.xWiens, J.J. & Donoghue, M.J. (2004) Historical biogeography, ecology and species richness. Trends in Ecology & Evolution, 19 (12), 639–644.
https://doi.org/10.1016/j.tree.2004.09.011Wiley, E.O. & Mayden, R.L. (1985) Species and speciation in phylogenetic systematics, with examples from the North American fish fauna. Annals of the Missouri botanical Garden, 72 (4), 596–635.
https://doi.org/10.2307/2399217Willis, S.C., Macrander, J., Farias, I.P. & Ortí, G. (2012) Simultaneous delimitation of species and quantification of interspecific hybridization in Amazonian peacock cichlids (genus Cichla) using multi-locus data. BMC Evolutionary Biology, 12 (1), 1.
https://doi.org/10.1186/1471-2148-12-96Worm, B., Barbier, E.B., Beaumont, N., Duffy, J.E., Folke, C., Halpern, B.S. & Sala, E. (2006) Impacts of biodiversity loss on ocean ecosystem services. Science, 314 (5800), 787–790.
https://doi.org/10.1126/science.1132294Xiao, D. (2014) Phylogeny and molecular evolution of the voltage-gated sodium channel gene scn4aa in the electric fish genus Gymnotus. University of Toronto, Toronto. Available from: https://tspace.library.utoronto.ca/handle/1807/44073 (accessed 11 August 2017)
Zachos, F.E. (2015) Taxonomic inflation, the phylogenetic species concept and lineages in the tree of life–A cautionary comment on species splitting. Journal of Zoological Systematics and Evolutionary Research, 53 (2), 180–184.
https://doi.org/10.1111/jzs.12088Zachos, F.E. (2016) An Annotated List of Species Concepts. In: Zachos, F.E. (Ed.), Species Concepts in Biology, Springer International Publishing, Gewerbestrasse, pp. 77–96.
https://doi.org/10.1007/978-3-319-44966-1_4Zubizarreta, L., Stoddard, P.K. & Silva, A. (2015) Aggression levels affect social interaction in the non‐breeding territorial aggression of the weakly electric fish, Gymnotus omarorum. Ethology, 121 (1), 8–16.
https://doi.org/10.1111/eth.12299