Anatomical, taxonomic, and phylogenetic reappraisal of a poorly known ghost knifefish, Tembeassu marauna (Ostariophysi: Gymnotiformes), using X-ray microcomputed tomography

Autoři: Luiz A. W. Peixoto aff001;  Aléssio Datovo aff001;  Ricardo Campos-da-Paz aff002;  Carlos D. de Santana aff003;  Naércio A. Menezes aff001
Působiště autorů: Museu de Zoologia da Universidade de São Paulo, Seção de peixes, São Paulo, SP, Brazil aff001;  Universidade Federal do Estado do Rio de Janeiro, Centro de Ciências Biológicas e da Saúde, Instituto de Biociências, Rio de Janeiro, RJ, Brazil aff002;  National Museum of Natural History, Smithsonian Institution, Division of Fishes, Department of Vertebrate Zoology, Washington, DC, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225342


A detailed osteological study of the poorly known and critical endangered ghost knifefish, Tembeassu marauna, from the rio Paraná, Brazil, was conducted using X-ray microcomputed tomography (μCT scan). A redescription of the external anatomy was performed, including the unusual presence of a rostral patch of extra teeth on the region of the upper lip anterior to the premaxilla and the prominent anterior fleshy expansions in both upper and lower lips. The newly surveyed characters were included and analyzed in light of a recent morphological data matrix for Gymnotiformes. In spite of some uncertainties that remains as to phylogenetic allocation of the genus, the most probable hypothesis is that Tembeassu is the sister group of a clade that includes Megadontognathus and Apteronotus sensu stricto. The phylogenetic analysis also supports that Tembeassu is considered a valid genus of Apteronotidae. An amended diagnosis for the genus is also provided.

Klíčová slova:

Computed axial tomography – Dentition – Jaw – Ossification – Osteology – Phylogenetic analysis – Teeth – Vertebrae


1. Fricke R, Eschemeyer WN, van der Lann R. 2019. Eschmeyer’s catalog of fishes: genera, species, and references. Available from:

2. Mago-Leccia F. Electric fishes of the continental water of America: classification and catalogue of the electric fishes of the order Gymnotiformes (Teleostei: Ostariophysi), with descriptions of new genera and species. Fund Desar Cien Fis Mat Nat. 1994;29: 1–206.

3. Franchina RC, Hopkins CD. The dorsal filament of the weakly electric Apteronotidae (Gymnotiformes; Teleostei) is specialized for electroreception. Brain Behav. Evol. 1996;47: 165–178. doi: 10.1159/000113236 9156779

4. Albert JS. Species diversity and phylogenetic systematics of American knifefishes (Gymnotiformes, Teleostei). Misc Public Mus Zool Univ Mich. 2001;190: 1–127.

5. de Santana CD, Vari RP, Wosiacki WB. The untold story of the caudal skeleton in the electric eel (Ostariophysi: Gymnotiformes: Electrophorus). PLoS One. 2013;8(7): e68719. doi: 10.1371/journal.pone.0068719 23894337

6. Cox Fernandes C, Podos J, Lundberg JG. Amazonian ecology: tributaries enhance the diversity of electric fishes. Science. 2004;305: 1960–1962. doi: 10.1126/science.1101240 15448270

7. Crampton WGR. Diversity and adaptation in deep channel Neotropical electric fishes. In: Sebert P, Onyango DW, Kapoor BG (eds.). Fish Life in Special Environments. Science Publishers Inc., Enfield, New Hampshire, 2007. pp. 283–339.

8. de Santana CD, Vari RP. Electric fishes of the genus Sternarchorhynchus (Teleostei, Ostariophysi, Gymnotiformes): phylogenetic and revisionary studies. Zool J Linn Soc. 2010;159: 223–371.

9. de Santana CD, Vari RP. Brown ghost electric fishes of the Apteronotus leptorhynchus species-group (Ostariophysi, Gymnotiformes); monophyly, major clades, and revision. Zool J Linn Soc. 2013;168: 564–596.

10. Lopez-Rojas H, Lundberg JG, Marsh E. Design and operation of a small trawling apparatus for use with dugout canoes. N Am J Fish Manag. 1984;4: 331–334.

11. Marrero C, Taphorn DC. Notas sobre la historia natural y la distribuicion de los peces Gymnotiformes em la cuenca del Rio Apure y otros rios de la Orinoquia. Biollania. 1991;8: 123–142.

12. Kirschbaum F. Taxonomy, zoogeography and general ecology of South American knifefishes (Gymnotiformes). In: Moller P, editor. Electric Fishes: History and Behavior; 1995. pp. 446–464.

13. Moller P. Electric Fishes: History and Behavior. New York: Chapman & Hall; 1995.

14. Crampton WGR, Albert JS. Evolution of electric signal diversity in gymnotiform fishes. In: Ladich F, Collin SP, Moller P, Kapoor BG. (eds). Communication in fishes. Enfeld: Science Publishers, 2006. pp 647–731.

15. Crampton WGR. Electric signals, design and habitat preference in a rich assemblage of gymnotiform fishes from the upper Amazon basin. An Acad Bra Cienc. 2019;70: 805–847.

16. Lundberg JG, Cox-Fernandes C, Albert JS, Garcia M. Magosternarchus, a new genus with two new species of electric fishes (Gymnotiformes: Apteronotidae) from the Amazon River Basin, South America. Copeia. 1996;3: 65–670.

17. Marrero C. Notas preliminaries acerca de la historia natural de los peces del Bajo Llano. I. Comparacion de los hábitos alimentarios de tres espécies de peces Gymnotiformes em el Rio Apure (Edo Apure, Venezuel). Rev. Hydrobiol. Trop. 1987;20: 57–63.

18. Marrero C, Winemiller KO. Tube snouted gymnotiform and mormyriform fishes: Convergence of a specialized foraging mode in teleosts. Env. Biol. Fish. 1993;38: 299–309.

19. Mago-Leccia F, Lundberg, Baskin N. Systematics of the South American freshwater fish genus Adontosternarchus (Gymnotiformes, Apteronotidae). Contrib. sci. 1985;358: 1–19.

20. Py-Daniel LHR, Cox-Fernandes C. Dimorfismo sexual em Siluriformes e Gymnotiformes (Ostariophysi) da Amazônia. Acta Amazon, 2005;35: 97–110.

21. Cox Fernandes C, Lundberg JG, Riginos C. Largest of all electric-fish snouts: hypermorphic facial growth in male Apteronotus hasemani and the identity of Apteronotus anas (Gymnotiformes: Apteronotidae). Copeia, 2002;1: 52–61.

22. Hilton EJ, Cox Fernandes C. Sexual dimorphism in Apteronotus bonapartii (Gymnotiformes: Apteronotidae). Copeia, 2006;4: 826–833.

23. Albert JS, Crampton WGR. A new species of electric knifefish, genus Compsaraia (Gymnotiformes: Apteronotidae) from the Amazon River, with extreme sexual dimorphism in snout and jaw length. Syst Biodivers. 2009;7: 81–92.

24. Keeffe R, Hilton E, Souza M, Cox Fernandes. Cranial morphology and osteology of the sexually dimorphic electric fish, Compsaraia samueli Albert & Crampton (Apteronotidae, Gymnotiformes), with comparasions to C. compsa (Mago-Leccia). Zootaxa, 2019;1: 101–112.

25. Triques ML. Tembeassu marauna, new genus and species of electrogenic neotropical fish (Ostariophysi: Gymnotiformes: Apteronotidae). Revue française d'Aquariologie Herpétologie, 1998;25: 5–10.

26. Albert J. Gymnotiformes. In: Reis RE, Kullander SO, Ferraris CJ, editors. Check list of the freshwater fishes of South and Central America. Porto Alegre: EDIPUCRS; 2003. pp. 1–729.

27. Triques ML. Análise cladística dos caracteres de anatomia externa e esquelética de Apteronotidae (Teleostei: Gymnotiformes). Lundiana, 2005;6: 121–149.

28. Campos-da-Paz R. Previously undescribed dental arrangement among electric knifefishes, with comments on the taxonomic and conservation status of Tembeassu marauna Triques (Otophysi: Gymnotiformes: Apteronotidae). Neotrop Ichthyol, 2005;3: 395–400.

29. ICMBIO/MMA. Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Brasília: 2018.

30. Ferraris CJ, de Santana CD, Vari RP. Checklist of Gymnotiformes (Osteichthyes: Ostariophysi) and catalogue of primary types. Neotrop Ichthyol 2017;15: 1–44.

31. Tagliacollo VA, Bernt MJ, Craig JM, Oliveira C, Albert JS. Model-based total evidence phylogeny of Neotropical electric knifefishes (Teleostei, Gymnotiformes). Mol Phylogenetic Evo. 2016a;95: 20–33.

32. Bernt MJ, Tagliacollo VA, Albert JS. Molecular Phylogeny of the ghost knifefishes (Gymnotiformes: Apteronotidae). Mol Phylogenetic Evo. 2019;135: 297–307.

33. Peixoto LAW, Dutra GM, Wosiacki WB. The Electric Glass Knifefishes from the Eigenmannia trilineata species-group (Gymnotiformes: Sternopygidae): monophyly and description of seven new species. Zool J Linn Soc. 2015;175: 384–414.

34. Fink S, Fink W. Interrelationships of the ostariophysan fishes (Teleostei). Zool J Linn Soc. 1981;72: 297–353.

35. Fink S, Fink W. 1996. Interrelationships of Ostariophysan. In: Stiassny ML, Parenti LR and Johnson D, editors. Interrelationships of fishes. San Diego: Academic Press; 1996. pp. 209.

36. Hilton EJ, Cox-Fernandes C, Sullivan JP, Lundberg JG, Campos-da-Paz R. Redescription of Orthosternarchus tamandua (Boulenger, 1898) (Gymnotiformes, Apteronotidae), with reviews of its ecology, electric organ discharges, external morphology, osteology, and phylogenetic affinities. Proc Acad Nat Sci Phila. 2007;156: 1–25.

37. Hopkins CD. Hypopomus pinnicaudatus (Hypopomidae), a new species of gymnotiform fish from French Guiana. Copeia. 1991;2: 151–161.

38. Campos-da-Paz RC. New species of Megadontognathus from the Amazon Basin, with phylogenetic and taxonomic discussions on the genus. Copeia. 1999;4: 1041–1049.

39. Carr CE, Maler L, Sas E. Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish. J Comp Neurol. 1982;211: 139–153. doi: 10.1002/cne.902110204 7174886

40. Vischer HA, Lannoo MJ, Heiligenberg W. Development of the electrosensory nervous system in Eigenmannia (Gymnotiformes): I. The peripheral nervous system. J Comp Neurol. 1989;290: 16–40. doi: 10.1002/cne.902900103 2592608

41. Winterbottom RA. Descriptive synonymy of the striated muscles of the Teleostei. Proc Acad Nat Sci Phila. 1974;125: 225–317.

42. Datovo A, Vari RP. The jaw adductor muscle complex in teleostean fishes: evolution, homologies and revised nomenclature (Osteichthyes: Actinopterygii). PLoS One. 2013;8(4): e60846. doi: 10.1371/journal.pone.0060846 23565279

43. Goloboff PA, Farris JS, Nixon KC. TNT, a free program for phylogenetic analysis. Cladistics. 2008;24: 774–786.

44. Goloboff PA, Catalano SA. TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics. 2016;32: 221–238.

45. Albert JS, Petry P, Reis RE. Major biogeographic and phylogenetic patterns. In: Albert JS, Reis RE, editors. Historical biogeography of Neotropical freshwater fishes. London: University of California Press; 2011. pp. 21–58.

46. Albert JS and Crampton WGR. Pariosternarchus amazonensis: a new genus and species of Neotropical electric fish (Gymnotiformes: Apteronotidae) from the Amazon River. Ichthyol. Explor. Freshw. 2006;17: 267–274.

47. Crampton WGR. Diversity and adaptation in deep channel Neotropical electric fishes. In: Sebert P, Onyango DW and Kapoor BG, editors. Fish life in special environments. Science Publishers: Enfield, NH, 2007. pp. 283–339.

48. de Santana CD, Vari RP. The South American electric fish genus Platyurosternarchus (Gymnotiformes: Apteronotidae). Copeia, 2009;2: 233–244.

49. Crampton WGR. An ecological perspective on diversity and distributions. In: Albert JS, Reis RE, editors. Historical biogeography of Neotropical freshwater fishes. Los Angeles. University of California Press, 2011. pp.165–89.

50. Triques ML. Apteronotus acidops, new species of long snouted electric fish (Teleostei: Gymnotiformes: Apteronotidae) from the upper rio Paraná basin in Brazil, with a key to the apteronotid species from the area. Vertebr zoology. 2011;61: 299–306.

51. Reis R. E., Albert J. S., Di Dario F., Mincarone M. M., Petry P. and Rocha L. A. 2016. Fish biodiversity and conservation in South America. J Fish Biol. 2016; 1–36.

52. Crampton WG, Ribeiro AC. Apteronotidae. In: Queiroz LJ, Torrente-Vilara G, Ohara WM, Pires TH, Zuanon J, Doria CR. Peixes do Rio Madeira, vol. III. São Paulo: Dialeto Latin American Documentary; 2013. pp. 257–258.

53. Tagliacollo VA, Bernt MJ, Craig JM, Oliveira C, Albert JS. Model-based total evidence phylogeny of Neotropical electric knifefishes (Teleostei, Gymnotiformes)- Data supporting phylogenetic recostructions of he Neotropical calde Gymnotiformes. Mol Phylogenetic Evo. 2016b;95: 23–59.

54. Triques ML. Filogenia dos gêneros de Gymnotiformes (Actinopterygii, Ostariophysi), com base em caracteres esqueléticos. Comun Mus Cien PUCRS, Ser Zool. 1993;6: 85–130.

55. Ivanyisky SJ, Albert JS. Systematics and biogeography of Sternarchellini (Gymnotiformes: Apteronotidae): Diversification of electric fishes in large Amazonian rivers. Neotrop Ichthyol. 2014;3: 565–584.

56. Turner CR, Derylo M, de Santana CD, Alves-Gomes JA, Smith GT. Phylogenetic comparative analysis of electric communication signals in ghost knifefishes (Gymnotiformes: Apteronotidae). J Exp Biol. 2007;23: 4104–4122.

57. Vari RP, de Santana CD, Wosiacki WB. South American electric knifefishes of the genus Archolaemus (Ostariophysi, Gymnotiformes): undetected diversity in a clade of rheophiles. Zool J Linn Soci. 2012;165: 670–699.

Článek vyšel v časopise


2019 Číslo 11