Abstract
Banded Knifefishes (Gymnotus, Gymnotidae) comprise the most species-rich genus of Neotropical electric fishes, with 41 species currently described from throughout the humid Neotropics, from Mexico to Argentina. Despite substantial alpha-taxonomic work in recent years, the diversity of Gymnotus in some regions remains poorly understood. Here we describe the Gymnotus fauna of the Upper Madeira basin of Bolivia and Peru from examination of more than 240 adult specimens. Species are delimited and described using body proportions (traditional morphometrics), fin-ray, squamation and laterosensory-pore counts (meristics), quantitative shape differences (geometric morphometrics), osteological traits, and color patterns. Comparisons of standardized linear measures as well as multivariate statistical methods validate the presence in the Upper Madeira basin of three previously described species, two with wide-spread geographic distributions throughout Greater Amazonia (G. carapo and G. coropinae), and one (G. chaviro) endemic to southwestern Amazonia. We also diagnose and describe two new species that are endemic to the Upper Madeira basin: G. eyra n. sp., morphologically most similar to G. mamiraua from lowland Amazonia, and G. riberalta n. sp., morphologically most similar to G. pantanal from the Paraguay-Paraná basin. The five Gymnotus species from the Upper Madeira basin are not monophyletic, each species being more closely related to a different species from another region; i.e. the Gymnotus species from the Upper Madeira represents a polyphyletic assemblage. These descriptions to 43 the number of valid Gymnotus species.
References
Abell, R., Thieme, M.L., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Balderas, S.C., Bussing, W., Stiassny, M.L.J., Skelton, P., Allen, G.R., Unmack, P., Naseka, A., Ng, R., Sindorf, N., Robertson, J., Armijo, E., Higgins, J.V., Heibel, T.J., Wikramanayake, E., Olson, D., Lopez, H.L., Reis, R.E., Lundberg, J.G., Perez, M.H.S. & Petry, P. (2008) Freshwater ecoregions of the world: A new map of biogeographic units for freshwater biodiversity conservation. Bioscience, 58, 403–414.
https://doi.org/10.1641/B580507Albert, J.S. (2001) Species Diversity and Phylogenetic Systematics of American Knifefishes (Gymnotiformes, Teleosti). Miscellaneous Publications, Museum of Zoology, University of Michigan, 190, 1–140.
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., Carvalho, T.P., Petry, P., Holder, M.A., Maxime, E.L., Espino, J., Corahua, I., Quispe, R., Rengifo, B., Ortega, H. & Reis, R.E. (2011a) Aquatic biodiversity in the amazon: Habitat specialization and geographic isolation promote species richness. Animals, 1, 205–241.
https://doi.org/10.3390/ani1020205Albert, 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, 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.
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, C.A., pp. 21–58.
https://doi.org/10.1525/california/9780520268685.003.0002Craig, J.M., Crampton, W.G.R. & Albert, J.S. (2017) Revision of the polytypic electric fish Gymnotus carapo (Gymnotiformes, Teleostei), with descriptions of seven subspecies. Zootaxa, 4318 (3), 401–438.
https://doi.org/10.11646/zootaxa.4318.3.1Crampton, W.G.R. & Albert, J.S. (2003) Redescription of Gymnotus coropinae (Gymnotiformes, Gymnotidae), an often misidentified species of Neotropical electric fish, with notes on natural history and electric signals. Zootaxa, 348 (1), 1–20.
https://doi.org/10.11646/zootaxa.348.1.1Crampton, W.G.R. & Albert, J.S. (2004) Redescription of Gymnotus coatesi (Gymnotiformes, Gymnotidae): A Rare Species of Electric Fish from the Lowland Amazon Basin, with Descriptions of Osteology, Electric Signals, and Ecology. Copeia, 2004, 525–533.
https://doi.org/10.1643/CI-03-246R1Crampton, 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), with notes on ecology and electric organ. Zootaxa, 277 (1), 1–18.
https://doi.org/10.11646/zootaxa.277.1.1Crampton, W.G.R., Lovejoy, N.R. & Waddell, J.C. (2011) Reproductive character displacement and signal ontogeny in a sympatric assemblage of electric fish. Evolution, 65, 1650–1666.
https://doi.org/10.1111/j.1558-5646.2011.01245.xCrampton, W.G.R., Rodríguez-Cattáneo, A., Lovejoy, N.R. & Caputi, A.A. (2013) Proximate and ultimate causes of signal diversity in the electric fish Gymnotus. The Journal of Experimental Biology, 216, 2523–2541.
https://doi.org/10.1242/jeb.083261Crampton, W.G.R., Thorsen, D.H. & Albert, J.S. (2005) Three New Species from a Diverse, Sympatric Assemblage of the Electric Fish Gymnotus (Gymnotiformes: Gymnotidae) in the Lowland Amazon Basin, with Notes on Ecology. Copeia, 2005, 82–99.
https://doi.org/10.1643/CI-03-242R2Espinoza Villar, R., Martinez, J.M., Le Texier, M., Guyot, J.L., Fraizy, P., Meneses, P.R. & Oliveira, E. de (2013) A study of sediment transport in the Madeira River, Brazil, using MODIS remote-sensing images. Journal of South American Earth Sciences, 44, 45–54.
https://doi.org/10.1016/j.jsames.2012.11.006Fearnside, P.M. (2014) Impacts of Brazil’s Madeira River Dams: Unlearned lessons for hydroelectric development in Amazonia. Environmental Science & Policy, 38, 164–172.
https://doi.org/10.1016/j.envsci.2013.11.004Fernandes, F.M., 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), 1–14.
https://doi.org/10.11646/zootaxa.933.1.1Goulding, M., Barthem, R. & Ferreira, E. (2003) The Smithsonian Atlas of the Amazon. Smithsonian Books, Washington D.C., 254 pp.
Hoedeman, J.J. (1962) Notes on the ichthyology of Surinam and other Guianas. 9. New records of gymnotid fishes. Bulletin of Aquatic Biology, 3, 53–60.
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.xLévêque, C., Oberdorff, T., Paugy, D., Stiassny, M.L.J. & Tedesco, P. a. (2008) Global diversity of fish (Pisces) in freshwater. Hydrobiologia, 595, 545–567.
https://doi.org/10.1007/s10750-007-9034-0Maxime, E.L. & Albert, J.S. (2009) A new species of Gymnotus (Gymnotiformes: Gymnotidae) from the Fitzcarrald Arch of southeastern Peru. Neotropical Ichthyology, 7, 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, 14, 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 Rio Tiquié in Northern Brazil. Copeia, 1, 77–81.
https://doi.org/10.1643/CI-10-009Nijssen, H. & Isbrücker, I.J.H. (1968) Gymnotus carapo and G. anguillaris (syn.: G. coropinae), two often confused species of gymnotid fishes (Pisces, Cypriniformes). Beaufortia, 15, 161–168.
Ortega, H. & Hidalgo, M. (2008) Freshwater fishes and aquatic habitats in Peru: Current knowledge and conservation. Aquatic Ecosystem Health and Management, 11, 257–271.
https://doi.org/10.1080/14634980802319135Ortega, H., Hidalgo, M., Correa, E., Espino, J., Chocano, L., Trevejo, G., Meza, V., Cortijo, A.M. & Quispe, R. (2010) Lista anotada de los peces de auguas continentales del Perú. National History Museum, National University of San Marcos (UNMSM), Lima, 58 pp.
Pfeiffer, W.C., Malm, O., Souza, C.M.M. & Reuther, R. (1990) Mercury pollution due to gold mining in the Madeira River basin, Brazil. Ambio, 19, 11–15.
de Queiroz, L.J., Torrente-Vilara, G., Ohara, W.M., Pires, T.H. da S., Zuanon, J. & Doria, C.R. da C. (2013a) Peixes do Rio Madeira. Vol.1. Biblioteca UNIR Ji-Paraná, São Paulo, Brazil, 402 pp.
de Queiroz, L.J., Torrente-Vilara, G., Vieira, F.G., Ohara, W.M., Zuanon, J. & Doria, C.R.C. (2013b) Fishes of Cuniã Lake, Madeira River Basin, Brazil. Check List, 9, 540–548.
https://doi.org/10.15560/9.3.540Rohlf, F.J. (2015) The tps series of software. Hystrix, the Italian Journal of Mammalogy, 26, 1–4.
Rosenzweig, M.L. (2004) Applying Species-area Relationships to the Conservation of Species Diversity. In: Rosenzweig, M.L. (Ed.), Frontiers of biogeography: new directions in the geography of nature, Sinauer Associates, Inc., Sunderland, M.A., pp. 325–343.
Sabaj, M.H. (2016) Standard symbolic codes for institutional resource collections in herpetology and ichthyology: an Online Reference. Version 6.5 (16 august 2016). Available from: http://www.asih.org/resources (accessed 7 March 2018)
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.
Trancoso, R., Carniero Filho, A., Tomasella, J., Schiette, J., Forsberg, B.R., Miller, R. & Pritchard, R. (2009) Deforestation and conservation in major watersheds of the Brazilian Amazon. Environmental Conservation, 36, 277–288.
https://doi.org/10.1017/S0376892909990373Waddell, J.C., Rodríguez-Cattáneo, A., Caputi, A.A. & Crampton, W.G.R. (2016) Electric organ discharges and near-field spatiotemporal patterns of the electromotive force in a sympatric assemblage of Neotropical electric knifefish. Journal of Physiology Paris, 110, 164–181.
https://doi.org/10.1016/j.jphysparis.2016.10.004