On a remarkable sexual dimorphic trait in the Characiformes related to the olfactory organ and description of a new miniature species of Tyttobrycon Géry (Characiformes: Characidae)

Autoři: Vitor Pimenta Abrahão aff001;  Murilo Pastana aff001;  Manoela Marinho aff001
Působiště autorů: Museu de Zoologia da Universidade de São Paulo, São Paulo, SP, Brazil aff001;  Programa de Pós-Graduação em Biodiversidade e Evolução, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Geremoabo, Ondina, Salvador, BA, Brazil aff002;  Laboratório de Sistemática e Morfologia de Peixes, Departamento de Sistemática e Ecologia/CCEN, Universidade Federal da Paraíba, Campus I, João Pessoa, PB, Brazil aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226130


Among the order Characiformes, secondary sexual dimorphism is commonly associated to the occurrence of bony hooks on fins, shape and length of the dorsal and anal fins, and sexual dichromatism. The analysis of a new miniature Characidae species of the genus Tyttobrycon, described herein, yielded to the discovery of a sexually dimorphic trait related to nostril aperture and number of olfactory lamellae. In this type of dimorphism, mature males present larger nostril aperture and higher number of olfactory lamella than females. A dimorphic olfactory organ is for the first time recorded and described for a member of the Characiformes. Gross morphology and development of brain and peripheral olfactory organ of Tyttobrycon sp. n. are described and compared to other species of Characidae. It is hypothesized that such dimorphic trait is related to male-male detection during cohort competition in small characids. The new species of Tyttobrycon is diagnosed from its congeners by the number of branched anal-fin rays (19–21) and the absence of a caudal-peduncle blotch. It occurs in a small tributary of Rio Madeira basin, near to the limit between Brazil and Bolivia, Acre State, Brazil.

Klíčová slova:

Brazil – Cartilage – New species reports – Teeth – Olfactory organs – Sexual dimorphism – Melanophores


1. Moore AJ. The evolution of sexual dimorphism by sexual selection: the separate effects of intrasexual selection and intersexual selection. Evolution. 1990; 44: 315–331 doi: 10.1111/j.1558-5646.1990.tb05201.x 28564385

2. Wiley ML, Collette BB. Breeding tubercles and contact organs in fishes: their occurrence, structure, and significance. Bull AMNH. 1970; 143.

3. Fink WL, Weitzman SH. The so-called cheirodontin fishes of Central America with descriptions of two new species (Pisces: Characidae). Smithsonian Contrib Zool. 1974; 172: 1–27. https://doi.org/10.5479/si.00810282.172

4. Weitzman SH, Fink SV. Xenurobryconin phylogeny and putative pheromone pumps in glandulocaudine fishes (Teleostei, Characidae). Smithsonian Contrib Zool. 1985; 1–121. https://doi.org/10.5479/si.00810282.421

5. Weitzman SH, Fink SV, Machado-Allison A, Royero R. A new genus and species of Glandulocaudinae (Teleostei: Characidae) from southern Venezuela. Ichthyol Explor Fresh. 1994; 5: 45–64.

6. Malabarba LR, Weitzman SH. A new genus and species of South American fishes (Teleostei: Characidae: Cheirodontinae) with a derived caudal fin, including comments about inseminating cheirodontines. Proc Biol Soc Was. 1999; 112: 410–432.

7. Malabarba LR, Weitzman SH. A new genus and species of inseminating fish (Teleostei: Characidae: Cherirodontidae: Compsurini) from South America with uniquely derived caudal-fin dermal papillae. Proc Biol Soc Was. 2000; 113: 269–283.

8. Malabarba LR, Weitzman SH. Descriptions of a new genus from southern Brazil, Uruguay and Argentina, with a discussion of a putative characid clade (Teleostei: Characiformes: Characidae). Com Mus Cienc Tecn PUCRS. 2003; 16: 67–151.

9. Lima FC, Sousa LM. A new species of Hemigrammus from the upper rio Negro basin, Brazil, with comments on the presence and arrangement of anal-fin hooks in Hemigrammus and related genera (Ostariophysi: Characiformes: Characidae). aqua: International Journal of Ichthyology. 2009; 15: 153–169.

10. Camelier P, Zanata AM. A new species of Astyanax Baird & Girard (Characiformes: Characidae) from the Rio Paraguaçu basin, Chapada Diamantina, Bahia, Brazil, with comments on bony hooks on all fins. J Fish Biol. 2014; 84: 475–490. doi: 10.1111/jfb.12295 24446730

11. Bührnheim CM, Malabarba LR. Redescription of Odontostilbe pulchra (Gill, 1858) (Teleostei: Characidae: Cheirodontinae), and description of two new species from the río Orinoco basin. Neotrop Ichthyol. 2007; 5: 1–20.

12. Chuctaya J, Bührnheim CM, Malabarba LR. Two new species of Odontostilbe historically hidden under O. microcephala (Characiformes: Cheirodontinae). Neotrop Ichthyol. 2018; 16: el70047.

13. Costa WJEM, Géry J. Two new species of the genus Hyphessobrycon (Characiformes: Characidae) from the rio Xingú basin, central Brazil. Rev Franç D'Aqua. 1993; 20: 71–76.

14. Weitzman SH, Palmer L. A new species of Hyphessobrycon (Teleostei: Characidae) from the Neblina region of Venezuela and Brazil, with comments on the putative ‘rosy tetra clade'. Ichthyol Explor Fresh. 1997; 7: 209–242.

15. Moreira CR, Landim MI, Costa WJEM. Hyphessobrycon heliacus: a new characid fish (Ostariophysi: Characiformes) from the upper rio Tapajós basin, Central Brazil. Copeia. 2002; 2: 428–432. https://doi.org/10.1643/00458511(2002)002[0428:HHANCF]2.0.CO;2

16. Teixeira TF, Lima FC, Zuanon J. A new Hyphessobrycon Durbin from the Rio Teles Pires, Rio Tapajós Basin, Mato Grosso State, Brazil (Characiformes: Characidae). Copeia, 2013; 4: 612–621. https://doi.org/10.1643/CI-13-026

17. Ingenito LF, Lima FC, Buckup PA. A new species of Hyphessobrycon Durbin (Characiformes: Characidae) from the rio Juruena basin, Central Brazil, with notes on H. loweae Costa & Géry. Neotrop Ichthyol. 2013; 11: 33–44. http://dx.doi.org/10.1590/S1679-62252013000100004

18. Dagosta FC, Marinho MM, Camelier P. A new species of Hyphessobrycon Durbin (Characiformes: Characidae) from the middle rio São Francisco and upper and middle rio Tocantins basins, Brazil, with comments on its biogeographic history. Neotrop Ichthyol. 2014; 12: 365–375. http://dx.doi.org/10.1590/1982-0224-20130179

19. Marinho MM, Dagosta FC, Birindelli JL. Hemigrammus ataktos: a new species from the rio Tocantins basin, central Brazil (Characiformes: Characidae). Neotrop Ichthyol. 2014; 12: 257–264.

20. Pastana MN, Ohara WM. A new species of Hyphessobrycon Durbin (Characiformes: Characidae) from rio Aripuanã, rio Madeira basin, Brazil. Zootaxa. 2016; 4161: 386–398. doi: 10.11646/zootaxa.4161.3.6 27615938

21. Ohara WM, Abrahão VP, Espíndola VC. Hyphessobrycon platyodus (Teleostei: Characiformes), a new species from the Rio Madeira basin, Brazil, with comments on how multicuspid teeth relate to feeding habits in Characidae. J Fish Biol. 2017; 91: 835–850. doi: 10.1111/jfb.13383 28744927

22. Pastana MNL, Dagosta FCP, Esguícero ALH. A new sexually dichromatic miniature Hyphessobrycon (Teleostei: Characiformes: Characidae) from the Rio Formiga, upper Rio Juruena basin, Mato Grosso, Brazil, with a review of sexual dichromatism in Characiformes. J Fish Biol. 2017; 91: 1301–1318. doi: 10.1111/jfb.13449 28905382

23. Camelier P, Dagosta FCP, Marinho MMF. New remarkable sexually dimorphic miniature species of Hyphessobrycon (Characiformes: Characidae) from the upper Rio Tapajós basin. J Fish Biol. 2018; 92: 1149–1162. doi: 10.1111/jfb.13579 29498044

24. Weitzman SH, Vari RP. Miniaturization in South American freshwater fishes; an overview and discussion. Proc Biol Soc Was. 1998; 101: 444–465.

25. Géry J. New and little‐known Aphyoditeina (Pisces, Characoidei) from the Amazon basin. Stud Neotrop Fauna Environ. 1973; 8: 81–137. https://doi.org/10.1080/01650527309360455

26. Marinho MM, Bastos DA, Menezes NA. New species of miniature fish from Marajó Island, Pará, Brazil, with comments on its relationships (Characiformes: Characidae). Neotrop Ichthyol. 2013; 11: 739–746. http://dx.doi.org/10.1590/S1679-62252013000400002

27. Menezes NA, Weitzman SH. Two species of Mimagoniates (Teleostei: Characidae), their phylogeny and biogeography and a key to the glandulocaudin fishes of brazil and paraguay. Proc Biol Soc Was. 1990; 103: 380–426.

28. Dingerkus G, Uhler LD. Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilage. Stain technol. 1977; 52: 229–232. doi: 10.3109/10520297709116780 71769

29. Taylor WR, Van Dyke GC. Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium. 1985; 9: 107–109.

30. Weitzman SH. The osteology of Brycon meeki, a generalized characid fish, with an osteological definition of the family. Stanford Ichthyol. Bull. 1962; 8: 1–77.

31. Meek J, Nieuwenhuys R. Holosteans and teleosts. In Nieuwenhuys R, Donkelaar HJ, Nicholson C, org. The central nervous system of vertebrates. Berlin: Springer. 1998. pp. 759–937.

32. Zeiske E, Theisen B, Breucker H. Structure, development, and evolutionary aspects of the peripheral olfactory system. In Hara TJ, ed. Fish chemoreception. Springer, Dordrecht. 1982. pp. 13–39.

33. Datovo A, Bockmann FA. Dorsolateral head muscles of the catfish families Nematogenyidae and Trichomycteridae (Siluriformes: Loricarioidei): comparative anatomy and phylogenetic analysis. Neotrop Ichthyol. 2010; 8: 193–246. http://dx.doi.org/10.1590/S1679-62252010000200001

34. Lima FCT de, Malabarba LR, Buckup PA, Silva JFP da, Vari RP, Benine R et al. Genera Incertae sedis in Characidae. In: Reis RE, Kullander SO, Ferraris CA, org. Check list of the freshwater fishes of South and Central America. Porto Alegre: EDIPUCRS; 2003. pp. 104–169.

35. Johnson DG, Brothers EB. Schindleria: A Paedomorphic Goby (Teleostei: Aobioidei). Bulletin of Marine Science. 1993; 52: 441–471.

36. Britz R, Kottelat M. Descriptive osteology of the family Chaudhuriidae (Teleostei, Synbranchiformes, Mastacembeloidei), with a discussion of its relationships. Amer Mus Nov. 2003; 3418: 1–62. https://doi.org/10.1206/00030082(2003)418<0001:DOOTFC>2.0.CO;2

37. Pastana MNL, Bockmann FA, Datovo A. The laterosensory system of Characiformes (Teleostei; Ostariophysi): anatomy and phylogenetic information. Zool J Lin Soc. In press; 10.1093/zoolinnean/zlz105.

38. Mattox GM, Britz R, Toledo-Piza M, Marinho MM. Cyanogaster noctivaga, a remarkable new genus and species of miniature fish from the Rio Negro, Amazon basin (Ostariophysi: Characidae). Ichthyol Explor Fresh. 2013; 23: 297–318.

39. Marinho MM, Menezes NA. Taxonomic review of Copella (Characiformes: Lebiasinidae) with an identification key for the species. PloS one. 2017; 12: e0183069. doi: 10.1371/journal.pone.0183069 28817598

40. Géry J. Characoids of the world. 1st ed. Neptune City: T.F.H. Publications; 1977.

41. Mirande JM. Phylogeny of the family Characidae (Teleostei: Characiformes): from characters to taxonomy. Neotrop Ichthyol. 2010; 8: 385–568. http://dx.doi.org/10.1590/S1679-62252010000300001

42. Mirande JM. Morphology, molecules and the phylogeny of Characidae (Teleostei, Characiformes). Cladistics. 2018; 35: 282–300. https://doi.org/10.1111/cla.12345

43. Pereira TNA. Anatomia encefálica comparada de Characiformes (Teleostei: Ostariophysi). PhD Thesis Universidade de São Paulo. 2014. Available from: http://www.teses.usp.br/teses/disponiveis/59/59139/tde-18122014-143500/en.php

44. Bertelsen E. The ceratioid fishes. Ontogeny, taxonomy, distribution and biology. Dana Rep. 1951; 39: 1–276.

45. Marshall NB. The olfactory organs of bathypelagic fishes. In Symposia of the Zoological Society of London. 1967; 19: pp. 57–70.

46. Caruso JH. Sexual dimorphism of the olfactory organs of lophiids. Copeia; 1975: 380–381. https://doi.org/10.2307/1442897

47. Bertelsen F. Lithostratigraphy and depositional history of the Danish Triassic. Danska Geol Undersogelse, ser. B. 1980; 4: 1–59.

48. Bertelsen E. The deep sea eel family Monognathidae (Pisces, Anguilliformes). Steenstrupia. 1987; 13: 141–198.

49. Nielsen JG, Bertelsen F. The gulper-eel family Saccopharyngidae (Pisces, Anguilliformes). Steenstrupia. 1985; 11: 157–206.

50. Martins FO, Andrade BN, Rosa AC, Langeani F. Chauliocheilos saxatilis, a new genus and species of Hypoptopomatinae from rio Jequitinhonha basin, with a unique labial appendix (Teleostei: Loricariidae). Ichthyol Explor Fresh. 2014; 25: 193–204

51. Martins FDO, Langeani F. Microlepidogaster dimorpha, a new species of Hypoptopomatinae (Siluriformes: Loricariidae) from the upper Rio Paraná system. Neotrop Ichthyol. 2011; 9: 79–86. http://dx.doi.org/10.1590/S1679-62252011000100005

52. Roxo FF, Melo BF, Silva GS, Oliveira C. New species of Parotocinclus (Siluriformes: Loricariidae) from coastal drainages of Rio de Janeiro, southeastern Brazil. Zootaxa. 2017; 4232:260–270. http://dx.doi.org/10.11646/zootaxa.4232.2.9

53. Gamarra SP, Calegari BB, Reis RE. A new species of Curculionichthys (Siluriformes: Loricariidae) from the north edge of the Brazilian Shield, lower Amazon basin. Neotrop Ichthyol. 2019; 17: el 190001. http://dx.doi.org/10.1590/1982-0224-20190001

54. Hansen A, Zeiske E. Development of the olfactory organ in the zebrafish, Brachydanio rerio. J. Comp. Neurol. 1993; 333: 289–300. doi: 10.1002/cne.903330213 8345108

55. Hansen A, Zielinski BS. Diversity in the olfactory epithelium of bony fishes: development, lamellar arrangement, sensory neuron cell types and transduction components. J Neurocytol. 2005; 34: 183–208. doi: 10.1007/s11068-005-8353-1 16841163

56. Angulo A, Langeani F. Gross brain morphology of the armoured catfish Rineloricaria heteroptera, Isbrücker and Nijssen (1976), (Siluriformes: Loricariidae: Loricariinae): A descriptive and quantitative approach. J Morph. 2017; 278: 1689–1705. doi: 10.1002/jmor.20742 28914457

57. Herring PJ. Species abundance, sexual encounter and bioluminescent signalling in the deep sea. Philo Trans Royal Soc London. Series B: Biological Sciences. 2000; 355: 1273–1276. http://dx.doi.org/10.1098/rstb.2000.0682

58. Regan T. Pediculate fishes of the suborder Ceratioidea. Leiden: Brill. 1926.

59. Regan CT, Trewavas E. Deep-sea angler-fishes (Ceratioidea) (No. 2). Oxford University Press. 1932.

60. Sazima I. Similarities in feeding behaviour between some marine and freshwater fishes in two tropical communities. Journal of Fish Biology. 1986; 29: 53–65. https://doi.org/10.1111/j.1095-8649.1986.tb04926.x

61. Menezes NA, Vazzoler AEADM. Reproductive characteristics of Characiformes. In Hamlett WC, ed. Reproductive biology of South American vertebrates. New York, Springer 1992. pp. 60–70.

62. Gomiero LM, Garuana L, Braga FMDS. Reproduction of Oligosarcus hepsetus (Cuvier, 1829) (Characiforms) in the Serra do Mar State Park, São Paulo, Brazil. Braz J Biol. 2008; 68: 187–192. doi: 10.1590/s1519-69842008000100027 18470396

63. Bisazza A, Marconato A, Marin G. Male competition and female choice in Padogobius martensi (Pisces, Gobiidae). Anim Behav. 1989; 38: 406–413. https://doi.org/10.1016/S0003-3472(89)80033-8

64. Bisazza A. Male competition, female mate choice and sexual size dimorphism in poeciliid fishes. Mar Fresh Behav Phy. 1993; 23; 257–286. https://doi.org/10.1080/10236249309378869

65. Taborsky M. Sperm competition in fish: bourgeois' males and parasitic spawning. Trends Eco Evol. 1998; 13: 222–227.

66. Seehausen O, Schluter D. Male–male competition and nuptial–colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proc Royal Soc London. Series B: Biol Sci. 2004; 271: 1345–1353. https://doi.org/10.1098/rspb.2004.2737

67. Constantz GD. Sperm competition in poeciliid fishes. In: Smith RL, editor. Sperm competition and the evolution of animal mating systems. London: Academic Press, Inc. 1984. Pp. 465–485.

68. Liley NR. Chemical communication in fish. Canad J Fish Aqua Sci. 1982; 39: 22–35. https://doi.org/10.1139/f82-005

69. Liley NR, Stacey NE. Hormones, Pheromones, and Reproductive Behavior in Fish. In Hoar WS, Randall DJ, Donaldson EM, org. Fish physiology. London: Academic Press. 1983. pp. 1–63. https://doi.org/10.1016/S1546-5098(08)60301-5

70. Atkins DL, Fink WL. Morphology and histochemistry of the caudal gland of Corynopoma riisei Gill. J Fish Biol. 1979; 14: 465–469. https://doi.org/10.1111/j.1095-8649.1979.tb03543.x

71. Weitzman SH, Menezes NA. Relationships of the tribes and genera of the Glandulocaudinae (Ostariophysi: Characiformes: Characidae) with a description of a new genus, Chrysobrycon. In: Malabarba LR, Reis RE, Vari RP, Lucena ZMS, Lucena CAS, eds. Phylogeny and classification of Neotropical fishes. Porto Alegre: Edipucrs. 1998. pp. 171–192.

72. Weitzman SH, Menezes NA, Evers HG, Burns JR. Putative relationships among inseminating and externally fertilizing characids, with a description of a new genus and species of Brazilian inseminating fish bearing an anal-fin gland in males (Characiformes: Characidae). Neotrop Ichthyol. 2005; 3: 329–360. http://dx.doi.org/10.1590/S1679-62252005000300002

73. Stacey NE, Sorensen PW. 17α, 20β-dihydroxy-4-pregnen-3-one: a steroidal primer pheromone increasing milt volume in the goldfish, Carassius auratus. Canad J Zool. 1986; 64: 2412–2417. https://doi.org/10.1139/z86-360

74. Stacey NE. Teleost sex pheromones: recent studies on identity and function. In Proceedings of the third international symposium on reproductive physiology of fish. Memorial University Press. 1987. pp. 150–153.

75. Resink JW, Voorthuis PK, Van Den Hurk R, Peters RC, Van Oordt PGWJ. Steroid glucuronides of the seminal vesicle as olfactory stimuli in African catfish, Clarias gariepinus. Aquaculture. 1989; 83: 153–166. https://doi.org/10.1016/0044-8486(89)90068-9

76. Sorensen PW, Hara TJ, Stacey NE. Extreme olfactory sensitivity of mature and gonadally-regressed goldfish to a potent steroidal pheromone, 17α, 20β-dihydroxy-4-pregnen-3-one. J Comp Phys A. 1987; 160: 305–313.

77. Sorensen PW, Hara TJ, Stacey NE, Dulka JG. Extreme olfactory specificity of male goldfish to the preovulatory steroidal pheromone 17α, 20β-dihydroxy-4-pregnen-3-one. J Comp Phys A. 1990; 166: 373–383.

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