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Environmental Biology of Fishes

, Volume 94, Issue 4, pp 649–662 | Cite as

Reproduction and feeding habits of the highly seasonal Brachyhypopomus bombilla (Gymnotiformes: Hypopomidae) from southern Brazil with evidence for a dormancy period

  • Julia GioraEmail author
  • Hellen M. Tarasconi
  • Clarice B. Fialho
Article

Abstract

The reproductive biology and feeding habits of the hypopomid Brachyhypopomus bombilla were studied. The species has seasonal behavior, with breeding and feeding activity occurring mostly during the Southern Hemisphere spring and summer. We defined fractional spawning for the species and a relative fecundity similar to those previously reported for other gymnotiform species. According to the analysis of the food items, B. bombilla was included in the trophic category invertivorous, feeding mainly on autochthonous insects. The reproductive periods of males and females as well as female feeding activity were significantly related to the photoperiod. During a period of 5 months, when the lowest water temperatures and shortest photoperiod were recorded, all the specimens of B. bombilla were found buried in the muddy bottom of the creek, with lower electric organ discharge activity, empty stomachs, and gonads in early stages of the maturation process. This period, herein defined as a dormancy period, is reported here for the first time for a species of the Gymnotiformes order.

Keywords

Diet Breeding Environmental variations Electric fish Rio Grande do Sul 

Notes

Acknowledgements

We are grateful to L. Malabarba for his comments during the development of this study. We also thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—CAPES, and Programa Nacional de Pós Doutorado—PNPD-CAPES (process 2282/09) that has funded the first author, and Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (process 476821/2003–7; 478002/2006–8) that has supported this project.

References

  1. Adebisi AA (1987) The relationships between fecundities, gonadosomatics indices and egg sizes of some fishes of Ogun River, Nigéria. Arch fuer Hydrobiol 111:151–156Google Scholar
  2. Albert JS (2001) Species diversity and phylogenetic systematics of American knifefishes (Gymnotiformes, Teleostei). Miscellan Publ Mus Zool Univ of Mich 190:1–129Google Scholar
  3. Albert JS, Crampton WGR (2003) Family hypopomidae (Bluntnose Knifefishes). In: Reis RE, Kullander SO, Ferraris CJ Jr (eds) Check list of freshwater fishes of South and Central America. Edipucrs, Porto Alegre, pp 494–496Google Scholar
  4. Angermeier PL (1982) Resource seasonality and fish diets in an Illinois stream. Environ Biol Fish 7:251–264. doi: 10.1007/BF00002500 CrossRefGoogle Scholar
  5. Arcifa MS, Froehlich O, Northcote TG (1988) Distribution and feeding ecology of fishes in a tropical Brazilian Reservoir. Socied Cienc Nat La Salle 68:301–326Google Scholar
  6. Ardanaz JL, Silva A, Macadar O (2001) Temperature sensitivity of the electric organ discharge waveform in Gymnotus carapo. J Comp Physiol A 187:853–864. doi: 10.1007/s00359-001-0256-8 CrossRefGoogle Scholar
  7. Arrington AD, Winemiller KO, Loftus WF, Akin S (2002) How often do fishes “run on empty”? Ecology 83:2145–2151Google Scholar
  8. Assunção MIS, Schwassmann HO (1995) Reproduction and larval development of Electrophorus electricus on Marajó Island (Pará, Brazil). Ichth Expl Freshw 6:175–184Google Scholar
  9. Azevedo MA, Malabarba LR, Fialho CB (2000) Reproductive biology of the inseminated Glandulocaudinae Diapoma speculiferum Cope (Actinopterygii: Characidae). Copeia 4:983–989. doi: 10.1643/0045-8511(2000)000[0983:RBOTIG]2.0.CO;2 CrossRefGoogle Scholar
  10. Bastos JR (2002) Biologia alimentar da taxocenose dos peixes do rio Silveira (cabeceira do rio Pelotas), São José dos Ausentes, Rio Grande do Sul, Brasil. Thesis, Universidade Fedral do Rio Grande do SulGoogle Scholar
  11. Barbieri G, Barbieri MC (1982) Fecundidade e tipo de desova de Gymnotus carapo (Linnaeus, 1758), na represa do Lobo, Estado de São Paulo (Pisces, Gymnotidae). Spectr J Bras Ciênc 2:25–29Google Scholar
  12. Burt A, Kramer DL, Nakatsuru K, Spry C (1988) The tempo of reproduction in Hyphessobrycon pulchripinnis (Characidae), with a discussion on the biology of ‘multiple spawning’ in fishes. Environ Biol Fish 22:15–27. doi: 10.1007/bf00000541 CrossRefGoogle Scholar
  13. Campbell HA, Fraser KPP, Bishop CM, Peck LS, Egginton S (2008) Hibernation in an Antarctic fish: on ice for winter. PLoS One. doi: 10.1371/journal.pone.0001743
  14. Carter GS, Beadle LC (1930) Notes on the habits and development of Lepidosiren paradoxa. J Linn Soc Lond (Zool) 27:197–203. doi: 10.1111/j.1096-3642.1930.tb02065.x CrossRefGoogle Scholar
  15. Cognato DP, Fialho CB (2006) Reproductive biology of a population of Gymnotus aff. carapo (Teleostei: Gymnotidae) from southern Brazil. Neotrop Ichth 4:339–348. doi: 10.1590/S1679-62252006000300005 CrossRefGoogle Scholar
  16. Cooke SJ, Grant EC, Schreer JF, Philipp DP, Devries AL (2003) Low temperature cardiac response to exhaustive exercise in fish with different levels of winter quiescence. Comp Biochem Physiol A: 157–165Google Scholar
  17. Costa WJEM, Campos-da-Paz R (1992) Description d’une novelle espèce de poisson eléctrique du genre néotropical Hypopomus (Siluriformes: Gymnotodei: Hypopomidae) du sudest du Brésil. Rev Franç Aquariol 18:117–120Google Scholar
  18. Crampton WGR (1996) Gymnotiform fish: an important component of Amazonian floodplain fish communities. J Fish Biol 48:298–301Google Scholar
  19. Crampton WGR (1998) Efects of anoxia on the distribution, respiratory strategies and electric diversity of gymnotiform fishes. J Fish Biol 53:307–330. doi: 10.1111/j.1095-8649.1998.tb01034.x CrossRefGoogle Scholar
  20. Crampton WGR, Hopkins CD (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 2005:48–60. doi: 10.1643/CI-04-056R1 CrossRefGoogle Scholar
  21. Crampton WGR, Wells JK, Smyth C, Walz SA (2007) Design and construction of an electric fish finder. Neotrop Ichth 5:425–428. doi: 10.1590/S1679-62252007000300022 CrossRefGoogle Scholar
  22. Crawshaw LI (1980) Low-temperature dormancy in fish. Rev Physiol 42:473–491. doi: 10.1146/annurev.ph.42.030180.002353 CrossRefGoogle Scholar
  23. DeLaney RG, Lahiri S, Fishman AP (1974) Aestivation of the African lungfish Protopterus aethiopicus: cardiovascular and respiratory functions. J Expl Biol 61:111–128Google Scholar
  24. Dias TS (2004) Alimentação de Hemipsilichthys hystrix Pereira & Reis, 2002 (Siluriformes, Loricariidae) do rio do Marco, município de Saõ José dos Ausentes, RS, Brasil. Thesis, Universidade Federal do Rio Grande do SulGoogle Scholar
  25. Dufech APS, Azevedo MA, Fialho CB (2003) Comparative dietary analysis of two populations of Mimagoniates rheocharis (Characidae: Glandulocaudinae) from two streams of southern Brazil. Neotrop Ichth 1:67–74. doi: 10.1590/S1679-62252003000100008 CrossRefGoogle Scholar
  26. Fry FEJ (1971) The effect of environmental factors on the physiology of fish. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 6. Academic, New YorkGoogle Scholar
  27. Fryer G, Iles TD (1972) The cichlid fishes of the great lakes of Africa. Oliver & Boyd, EdinburghGoogle Scholar
  28. Giora J, Fialho CB (2003) Biologia alimentar de Steindachnerina brevipinna (Eigenmann & Eigenmann, 1889) do rio Ibicuí Mirim, Rio Grande do Sul, Brasil. Iheringia Ser Zool 93:277–281. doi: 10.1590/S0073-47212003000300007 CrossRefGoogle Scholar
  29. Giora J, Fialho CB (2009) Reproductive biology of weakly electric fish Eigenmannia trilineata López & Castello, 1966 (TELEOSTEI, Sternopygidae). Brazil Arch Biol Techn 52:617–628. doi: 10.1590/S1516-89132009000300014 CrossRefGoogle Scholar
  30. Giora J, Malabarba LR (2009) Brachyhypopomus gauderio, new species, a new example of underestimated species diversity of electric fishes in the southern South America (Gymnotiformes: Hypopomidae). Zootaxa 2093:60–68Google Scholar
  31. Giora J, Fialho CB, Dufech APS (2005) Feeding habit of Eigenmannia trilineata Lopez & Castello, 1996 (Teleostei: Sternopygidae) of Parque Estadual de Itapuã, RS, Brazil. Neotrop Ichth 3:291–298. doi: 10.1590/S1679-62252005000200007 CrossRefGoogle Scholar
  32. Giora J, Malabarba LR, Crampton WGR (2008) Brachyhypopomus draco, a new sexually dimorphic species of Neotropical electric fish from southern South America (Gymnotiformes: Hypopomidae). Neotrop Ichth 6:159–168. doi: 10.1590/S1679-62252008000200002 CrossRefGoogle Scholar
  33. Glass ML (2008) The enigma of aestivation in the African lungfish Protopterus dolloi. Commentary on the paper by Perry et al. Resp Physiol Neurobiol 160:18–20. doi: 10.1016/j.resp.2007.08.001 CrossRefGoogle Scholar
  34. Gonçalves TK, Azevedo MA, Malabarba LR, Fialho CB (2005) Reproductive biology and development of sexually dimorphic structures in Aphyocharax anisitsi (Ostariophysi: Characidae). Neotrop Ichth 3:433–438. doi: 10.1590/S1679-62252005000300012 CrossRefGoogle Scholar
  35. Goulding M (1980) The fishes and the forest: explorations in Amazonian natural history. University of California Press, BerkeleyGoogle Scholar
  36. Granado-Lorencio C, Garcia-Novo F (1986) Feeding habits of the fish community in a eutrophic reservoir in Spain. Ekol Polsk 34:95–110Google Scholar
  37. Greenwood PH (1986) The natural history of African lungfishes. J Morph 1:163–179. doi: 10.1002/jmor.1051900412 CrossRefGoogle Scholar
  38. Greger PD, Deacon JE (1988) Food partitioning among fishes of the Virgin River. Copeia 1988:314–323CrossRefGoogle Scholar
  39. Guillen E, Granado C (1984) Alimentacion de la ictiofauna del embalse de Torrejon (rio Tajo, Caceres). Limn 1:304–310Google Scholar
  40. Hartz SM, Peret AC, Barbieri G (1999) Reproduction of Gymnogeophagus lacustris Reis & Malabarba, 1988, an endemic neotropical cichlid of southern Brazil. Ichth Exp Freshw 10:247–253Google Scholar
  41. Hirano RF, Azevedo MA (2007) Hábito alimentar de Heterocheirodon yatai (Teleostei, Characidae, Cheirodontinae) de dois tributários do rio Ibicuí, Rio Grande do Sul, Brasil. Biociencias 15:207–220Google Scholar
  42. Hynes HBN (1950) The food of freshwater sticklebacks (Gasterosteus aculeatus an Pygosteus pungitius), a review of methods used in studies of the food fishes. J Anim Ecol 19:36–57CrossRefGoogle Scholar
  43. Hyslop EJ (1980) Stomach contents analisys; a review of methods and their application. J Fish Biol 17:411–429. doi: 10.1111/j.1095-8649.1980.tb02775.x CrossRefGoogle Scholar
  44. Kirschbaum F (1995) Taxonomy, Zoogeography and general ecology of South American knifefishes (Gymnotiformes). In: Moller P (ed) Electric fishes, history and behavior. Chapman & Hall, London, pp 446–464Google Scholar
  45. Kirschbaum F, Schugardt C (2002) Reproductive strategies and developmental aspects in mormyrid and gymnotiform fishes. J Physiol 96:557–566Google Scholar
  46. Kramer DL (1978) Reproductive seasonality in the fishes of a tropical stream. Ecology 59:976–985CrossRefGoogle Scholar
  47. Kramer DL, Lindsey CC, Moodie GEE, Stevens ED (1978) The fishes and the aquatic environment of the Central Amazonian basin with particular reference to respiratory patterns. Canad J Zool 56:717–729. doi: 10.1139/z78-101 CrossRefGoogle Scholar
  48. Lampert VR, Azevedo MA, Fialho CB (2004) Reproductive biology of Bryconamericus iheringii (Ostariophysi: Characidae) from rio Vacacaí, RS, Brazil. Neotrop Ichth 2:209–215. doi: 10.1590/S1679-62252004000400003 Google Scholar
  49. Lampert VR, Azevedo MA, Fialho CB (2007) Reproductive biology of Bryconamericus stramineus (Ostariophysi: Characidae) from rio Ibicuí, RS, Brazil. Brazil Arch Biol Technol 50:995–1004. doi: 10.1590/S1516-89132007000700011 CrossRefGoogle Scholar
  50. Link JS, Burnett J (2001) The relation between stomach contents and maturity state for major northwest Atlantic Fishes: new paradigms? J Fish Biol 59:783–794. doi: 10.1111/j.1095-8649.2001.tb00149.x CrossRefGoogle Scholar
  51. Lomholt JP (1993) Breathing in the aestivating African lungfish, Protopterus amphibius. Adv Fish Res 1:17–34Google Scholar
  52. Loureiro M, Silva A (2006) A new species of Brachyhypopomus (Gymnotiformes: Hypopomidae) from Northeast Uruguay. Copeia 2006:665–673. doi: 10.1643/0045-8511(2006)6[665:ANSOBG]2.0.CO;2 CrossRefGoogle Scholar
  53. Lyman CP, Willis JS, Malan A (1982) Hibernation and torpor in mammals and birds. Academic, New YorkGoogle Scholar
  54. Mago-Leccia F (1994) Electric fishes of continental waters of America. Clemente Editores, CaracasGoogle Scholar
  55. McKaye KR (1984) Behavioral aspects of ciclids reproductive strategies: Patterns of territoriality and brood defense in Central American substratum spawners and African mouth brooders. In: Potts GW, Wooton RJ (eds) Fish reproduction: Strategies and tatics. Academic, London, pp 245–273Google Scholar
  56. Mérigoux S, Ponton D (1998) Body shape, diet and onto-genetic diet shifts in young fish of the Sinnamary River, French Guiana, South America. J Fish Biol 52:556–569Google Scholar
  57. Moraes MFPG, Fernandes MN, Höller S, Costa OPF, Glass ML, Perry SF (2005) Morphometric comparison of the respiratory organs of the South American lungfish Lepidosiren paradoxa (Dipnoi). Physiol Bioch Zool 78:546–559CrossRefGoogle Scholar
  58. Motta RL, Uieda VS (2004) Diet and trophic groups of an aquatic insect community in a tropical stream. Brazil J Biol 64:809–817. doi: 10.1590/S1519-69842004000500010 CrossRefGoogle Scholar
  59. Nikolsky GV (1969) Theory of fish population dynamics. Oliver & Boyd Ltda, EdinburghGoogle Scholar
  60. Nunes DM, Hartz SM (2006) Feeding dynamics and ecomorphology of Oligosarcus jenynsii (Gunther, 1864) and Oligosarcus robustus (Menezes, 1969) in Fortaleza Lake, Southern of Brazil. Brazil J Biol 66:121–132. doi: 10.1590/S1519-69842006000100016 CrossRefGoogle Scholar
  61. Oliveira CLC, Fialho CB, Malabarba LR (2010) Reproductive period, fecundity and histology of gonads of two cheirodontines (Ostariophysi: Characidae) with different reproductive strategies—insemination and external fertilization. Neotrop Ichth 8:351–360. doi: 10.1590/S1679-62252010000200014 CrossRefGoogle Scholar
  62. Payne AI (1986) The ecology of tropical lakes and rivers. Wiley, New YorkGoogle Scholar
  63. Provenzano RF (1984) Aspectos de la reproduccion en peces Gymnotiformes del Bajo Llano de Venezuela. Dissertation, Universidade Central de VenezuelaGoogle Scholar
  64. Querol MVM, Querol E, Gomes NNA (2002) Fator de condição gonadal, índice hepatossomático e recrutamento como indicadores do período de reprodução de Loricariichthys platymetopon (Osteichthyes, Loricariidae), bacia do rio Uruguai médio, sul do Brasil. Iheringia Ser Zool 92:79–84CrossRefGoogle Scholar
  65. Quintana L, Silva A, Berois N, Macadar O (2004) Temperature induces gonadal maturation and affects electrophysiological sexual maturity indicators in Brachyhypopomus pinnicaudatus from a temperate climate. J Exper Biol 207:1843–1853. doi: 10.1242/jeb.00954 CrossRefGoogle Scholar
  66. Saccol-Pereira A (2008) Variação sazonal e estrutura trófica da assembléia de peixes do delta do rio Jacuí, RS, Brasil. Dissertation, Universidade Federal do Rio Grande do SulGoogle Scholar
  67. Santos EP (1978) Dinâmica de populações aplicada à pesca e piscicultura. Edusp, São PauloGoogle Scholar
  68. Schaan AB, Giora J, Fialho CB (2009) Reproductive biology of the Neotropical electric fish Brachyhypopomus draco (Teleostei: Hypopomidae) from southern Brazil. Neotrop Ichth 7:737–744. doi: 10.1590/S1679-62252009000400023 CrossRefGoogle Scholar
  69. Schmidt-Nielsen K (1999) Fisiologia Animal, adaptação e meio ambiente. Livraria Santos Editora, São PauloGoogle Scholar
  70. Schwassmann HO (1971) Biological rhythms. In: Hoar WS, Randall DJ (eds) Fish fisiology, vol 6. Academic, New York, pp 371–428Google Scholar
  71. Secor SM, Lignot JH (2010) Aestivation. Springer, BerlinGoogle Scholar
  72. Silva A, Quintana L, Galeano M, Errandonea P, Macadar O (1999) Water temperature sensitivity of EOD waveform in Brachyhypopomus pinnicaudatus. J Comp Physiol A 185:187–197. doi: 10.1007/s003590050377 CrossRefGoogle Scholar
  73. Silva A, Quintana L, Ardanaz JL, Macadar O (2002) Environmental and hormonal influences upon EOD waveform in gymnotiform pulse fish. J Physiol 96:473–484Google Scholar
  74. Silva A, Quintana L, Galeano M, Errandonea P (2003) Biogeography and breeding in Gymnotiformes from Uruguay. Environm Biol Fish 66:329–338. doi: 10.1023/a:1023986600069 CrossRefGoogle Scholar
  75. Silva A, Perrone R, Macadar O (2007) Environmental, seasonal, and social modulations of basal activity in a weakly electric fish. Physiol Behav 90:525–536. doi: 10.1016/j.physbeh.2006.11.003 PubMedCrossRefGoogle Scholar
  76. Silva GSF, Giusti H, Sanchez AP, Carmo JM, Glass ML (2008) Aestivation in the South American lungfish, Lepidosiren paradoxa: effects on cardiovascular function, blood gases, osmolality and leptin levels. Respir Physiol Neurobiol 164:380–385. doi: 10.1016/j.resp.2008.08.009 PubMedCrossRefGoogle Scholar
  77. Soares MGM (1979) Aspectos ecológicos, alimentação e reprodução dos peixes do igarapé do Porto, Aripuanã, MT. Acta Amaz 9:325–352Google Scholar
  78. Storey KB, Storey JM (1990) Metabolic Rate Depression and Biochemical Adaptation in Anaerobiosis, Hibernation and Estivation. Quart Rev Biol 65:145–174PubMedCrossRefGoogle Scholar
  79. Triques ML, Khamis DK (2003) Brachyhypopomus jureiae, a new species of freshwater Neotropical electric fish (Teleostei: Gymnotiformes: Hypopomidae) from a coastal stream of southeastern Brazil. Lundiana 4:61–64Google Scholar
  80. Van Dijk PLM, Staaks G, Hardewig I (2002) The effect of fasting and refeeding on temperature preference, activity and growth of roach, Rutilus rutilus. Oecologia 130:496–504. doi: 10.1007/s00442-001-0830-3 CrossRefGoogle Scholar
  81. Vazzoler AEAM (1996) Biologia da reprodução de peixes teleósteos: Teoria e prática. Editora da Universidade, MaringáGoogle Scholar
  82. Welcomme RL (1979) Fisheries ecology of floodplain rivers. Longman, LondonGoogle Scholar
  83. Zar JH (1999) Biostatistical analisis. Prentice-Hall, New JerseyGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Julia Giora
    • 1
    Email author
  • Hellen M. Tarasconi
    • 1
  • Clarice B. Fialho
    • 1
  1. 1.Laboratório de Ictiologia, Departamento de ZoologiaUniversidade Federal do Rio Grande do SulPorto AlegreBrazil

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