Reproductive life-history strategies in a species-rich assemblage of Amazonian electric fishes

Autoři: Joseph C. Waddell aff001;  Steve M. Njeru aff001;  Yasmine M. Akhiyat aff001;  Benjamin I. Schachner aff001;  Ericka V. Correa-Roldán aff001;  William G. R. Crampton aff001
Působiště autorů: Department of Biology, University of Central Florida, Orlando, Florida, United States of America aff001;  Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Peru aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0226095


The reproductive biology of only a small fraction of Neotropical freshwater fishes has been described, and detailed comparative studies of reproductive life-history variation in the Neotropical ichthyofauna are lacking. Here we describe interspecific variation in reproductive life history for a multi-species assemblage of the electric knifefish genus Brachyhypopomus (Hypopomidae: Gymnotiformes: Ostariophysi) from Amazonian floodplain and terra firme stream systems. During a year-round quantitative sampling program, we collected and measured key life-history traits from 3,410 individuals. Based on oocyte size distributions, and on circannual variation in gonadosomatic indices, hepatosomatic indices, and capture-per-unit-effort abundance of reproductive adults, we concluded that all species exhibit a single protracted annual breeding season during which females spawn fractionally. We found small clusters of post-larval individuals in one floodplain species and one terra firme stream species, but no signs of parental care. From analyses of body size-frequency distributions and otolith growth increments, we concluded that five species in our study area have approximately one-year (annual) semelparous life history with a single reproductive period followed by death, while two species have a two-year iteroparous life history, with breeding in both year-groups. Despite predictions from life-history theory we found no salient correlations between life history strategy (semelparity or iteroparity) and habitat occupancy (floodplain or terra firme stream). In the iteroparous species B. beebei, we documented evidence for reproductive restraint in the first breeding season relative to the second breeding season and argue that this is consistent with age-regulated terminal investment.

Klíčová slova:

Animal sexual behavior – Flooding – Freshwater fish – Gonads – Lakes – Oocytes – Otolith – Spawning


1. Winemiller KO. Patterns of variation in life history among South American fishes in seasonal environments. Oecologia. 1989;81(2):225–41. doi: 10.1007/BF00379810 28312542

2. Crampton WGR. An ecological perspective on diversity and distributions In: Albert JS, Reis RE, editors. Historical biogeography of neotropical freshwater fishes. Berkeley: University of California Press; 2011. p. 165–89.

3. Reis RE, Albert JS, Di Dario F, Mincarones MM, Petry P, Rocha LA. Fish biodiversity and conservation in South America. Journal of Fish Biology. 2016;89:12–47. doi: 10.1111/jfb.13016 27312713

4. Fricke R, Eschmeyer WN, van der Laan R. Eschmeyer's catalog of fishes: genera, species, references (http://researcharchivecalacademyorg/research/ichthyology/catalog/fishcatmainasp) (Electronic version accessed 01 October 2019). 2019.

5. Loubens G, Aquim JL, Robles E. Primeras observaciones sobre la sexualidad de peces de la region de trinidad, Béni, Bolivia. Informe Cientifico No 1 ORSTOM-UTB-BENI, Trinidad, Bolivia. 1984:34.

6. Lowe-McConnell RH. Ecological studies in tropical fish communities. Cambridge: Cambridge University Press; 1987.

7. Menezes NA, Vazzoler AEAM. Reproductive characteristics of Characiformes. In: Hamlett WC, editor. Reproductive biology of South American vertebrates. New York: Springer; 1992. p. 60–70.

8. Ruffino ML, Isaac VJ. Life cycle and biological parameters of several Brazilian Amazon fish species. NAGA, The ICLARM Quarterly. 1995;18(4):41–5.

9. Nuñez J, Duponchelle F. Towards a universal scale to assess sexual maturation and related life history traits in oviparous teleost fishes. Fish Physiology and Biochemistry. 2009;35:167–80. doi: 10.1007/s10695-008-9241-2 18668334

10. Pires THS, Campos DF, Röpke CP, Sodré J, Amadio S, Zuanon J. Ecology and life-history of Mesonauta festivus: biological traits of a broad ranged and abundant Neotropical cichlid. Environmental Biology of Fishes. 2015;98:789–99.

11. Crampton WGR, de Santana CD, Waddell JC, Lovejoy NR. A taxonomic revision of the Neotropical electric fish genus Brachyhypopomus (Ostariophysi: Gymnotiformes: Hypopomidae), with descriptions of 15 new species. Neotropical Ichthyology. 2016;14(4):639–790.

12. Crampton WGR, De Santana CD, Waddell JC, Lovejoy NR. Phylogenetic systematics, biogeography, and ecology of the electric knifefish genus Brachyhypopomus (Ostariophysi: Gymnotiformes). PLoS One. 2016;11 (e0161680)(10):1–66.

13. Schaan AB, Giora J, Fialho CB. Reproductive biology of the Neotropical electric fish Brachyhypopomus draco (Teleostei: Hypopomidae) from southern Brazil. Neotropical Ichthyology. 2009;7(4):737–44.

14. Giora J, Tarasconi HM, Fialho CB. Reproduction and feeding habits of the highly seasonal Brachyhypopomus bombilla (Gymnotiformes: Hypopomidae) from southern Brazil, with evidence for a domancy period. Environmental Biology of Fishes. 2012;94:649–62.

15. Giora J, Tarasconi HM, Fialho CB. Reproduction and feeding of the electric fish Brachyhypopomus gauderio (Gymnotiformes: Hypopomidae) and the discussion of a life history pattern for gymnotiforms from high latitudes. PLoS One. 2014;9(9):e106515. doi: 10.1371/journal.pone.0106515 25207924

16. Silva A, Quintana L, Galeano M, Errandonea P. Biogeography and breeding in Gymnotiformes from Uruguay. Environmental Biology of Fishes. 2003;66(4):329–38.

17. Miranda M, Silva AC, Stoddard PK. Use of space as an indicator of social behavior and breeding systems in the gymnotiform electric fish Brachyhypopomus pinnicaudatus. Environmental Biology of Fishes. 2008;83:379–89.

18. Gavassa S, Silva AC, Stoddard PK. Tight hormonal phenotypic integration ensures honesty of the electric signal of male and female Brachyhypopomus gauderio. Hormones and Behavior. 2011;60:420–6. doi: 10.1016/j.yhbeh.2011.07.009 21802421

19. Hagedorn M. Ecology and behaviour of a pulse-type electric fish, Hypopomus occidentalis (Gymnotiformes, Hypopomidae), in a fresh-water stream in Panama. Copeia. 1988;1988(3):324–35.

20. Stoddard PK. Electrical signals. In: Breed MD, Moore J, editors. Encyclopedia of Animal Behavior. Cambridge, MA: Academic Press; 2010. p. 601–10.

21. Gavassa S, Goldina A, Silva AC, Stoddard PK. Behavioral ecology, endocrinology and signal reliability of electric communication. Journal of Experimental Biology. 2013;216:2403–11. doi: 10.1242/jeb.082255 23761465

22. Crampton WGR. Electroreception, electrogenesis and signal evolution. Journal of Fish Biology. 2019;95(1):92–134. doi: 10.1111/jfb.13922 30729523

23. Ramalho EE, Macedo J, Vieira TM, Valsecchi J, Marmontel M, Queiroz HL. Ciclo hidrológico nos ambientes de várzea da reserva de desenvolvimento sustentável Mamirauá-médio rio Solimões, período de 1990 a 2008. Uakari. 2010;5(1):61–87.

24. Junk WJ. Investigations on the ecology and production-biology of the "floating meadows" (Paspalo-Echinochloetum) on the middle Amazon. Part I. Amazoniana. 1970;2(4):449–95.

25. Macedo MG, Siqueira-Souza FK, Freitas CEC. Abundance and diversity of predatory fish in the floodplain lakes of the Central Amazon. Revista Colombiana de Ciencia Animal. 2015;7(1):50–7.

26. Affonso AG, de Queiroz HL, Novo EMLM. Limnological characterization of floodplain lakes in Mamirauá Sustainable Development Reserve, central Amazon (Amazonas State, Brazil). Acta Limnologica Brasiliensia. 2011;23(1):95–108.

27. Henderson PA, Hamilton WD, Crampton WGR. Evolution and diversity in Amazonian floodplain communities. In: Newbery DM, Prins HHT, Brown ND, editors. Dynamics of tropical communities. Oxford: Blackwell Science; 1998. p. 385–419.

28. Tomasella J, Hodnett MG, Cuartas LA, Nobre AD, Waterloo MJ, Oliveira SM. The water balance of an Amazonian micro-catchment: the effects of interannual variability of rainfall on hydrological behaviour. Hydrological Processes. 2008;22:2133–47.

29. Espírito-Santo HMV, Zuanon J. Temporary pools provide stability to fish assemblages in Amazon headwater streams. Ecology of Freshwater Fish. 2016;26(3):475–83.

30. Bührnheim CM, Fernandes CC. Low seasonal variation of fish assemblages in Amazonian rain forest streams. Ichthyological Exploration of Freshwaters. 2001;12(1):65–78.

31. Mendonça FP, Magnusson WE, Zuanon J. Relationships between habitat characteristics and fish asemblages in small streams of Central Amazonia. Copeia. 2005;2005(4):750–63.

32. Kirkendall LR, Stenseth NC. On defining 'breeding once'. The American Naturalist. 1985;125:189–204.

33. Roff DA. Life history evolution. Sunderland: Associates, Inc.; 2002. 527 p.

34. Gavassa S, Stoddard PK. Food restriction promotes signaling effort in response to social challenge in a short-lived electric fish. Hormones and Behavior. 2012;62:381–8. doi: 10.1016/j.yhbeh.2012.07.003 22801246

35. Sinnett PM, Markham MR. Food deprivation reduces and leptin increases the amplitude of an active sensory and communication signal in a weakly electric fish. Hormones and Behavior. 2015;71:31–40. doi: 10.1016/j.yhbeh.2015.03.010 25870018

36. Williams GC. Pleiotropy, natural selection and the evolution of senescence. Evolution. 1957;11:398–411.

37. Lee WS, Monaghan P, Metcalfe NB. Experimental demonstration of the growth rate-lifespan trade-off. Proceedings of the Royal Society B: Biological Sciences. 2013;280(1752):20122370. doi: 10.1098/rspb.2012.2370 23235704

38. Wilbur HM, Rudolf VHW. Life-history evolution in uncertain environments: Bet hedging in time. The American Naturalist. 2006;168:398–411. doi: 10.1086/506258 16947114

39. Taylor DR, Aarssen LW, Loehle C. On the relationship between r/k selection and environmental carrying capacity: a new habitat templet for plant life history strategies. Oikos. 1990;58:239–50.

40. Stearns SC. The evolution of life histories. Oxford: Oxford University Press; 1992. 249 p.

41. Pianka ER. On r-and K-selection. The American Naturalist. 1970;104(940):592–7.

42. Reznick D, Bryant MJ, Bashey F. r- and K-selection revisted: the role of population regulation in life-history evolution. Ecology. 2002;83(6):1509–20.

43. Williams GC. Natural selection, the costs of reproduction, and a refinement of Lack's principle. The American Naturalist. 1966;100(916):687–90.

44. Clutton-Brock TH. Reproductive effort and terminal investment in iteroparous animals. The American Naturalist. 1984;123(2):212–29.

45. Jönsson KI. Capital and income breeding as alternative tactics of resource use in reproduction. Oikos. 1997;78(57–77).

46. Waddell JC, Rodríguez-Cattaneo A, Caputi AA, Crampton WGR. Electric organ discharges and near-field spatiotemporal patterns of the electromotive force in a sympatric assemblage of Neotropical electric fish. Journal of Physiology (Paris). 2016;110:164–81.

47. Crampton WGR, Wells JK, Smyth C, Walz SA. Design and construction of an electric fish finder. Neotropical Ichthyology. 2007;5(3):425–8.

48. Brown-Peterson NJ, Wyanski DM, Saborido-Rey F, Macewicz BJ, Lowerre-Barbieri SK. A standardized terminology for describing reproductive development in fishes. Marine and Coastal Fisheries. 2011;3(1):52–70.

49. Waddell JC, Crampton WGR. A simple procedure for assessing sex and gonadal maturation in gymnotiform fish. Aqua, International Journal of Ichthyology. 2018;24(1):1–8.

50. McLachlan G, Peel D. Finite mixture models. Shewhart WA, Wilks SS, editors. New York: John Wiley & Sons; 2000. 419 p.

51. Laslett GM, Eveson JP, Polacheck T. Fitting growth models to length frequency data. International Council for the Exploration of the Sea (ICES) Journal of Marine Science: Journal du Conseil. 2004;61(2):218–30.

52. Sethi SA, Gerken J, Ashline J. Accurate aging of juvenile salmonids using fork lengths. Fisheries Research. 2017;185:161–8.

53. Fraley C, Raferty A, Murphy TB, Scrucca L. mclust Version 4 for R: normal mixture modeling for model-based clustering, classification, and density estimation (Technical Report No. 597). Department of Statistics, University of Washington; 2012. 57 p.

54. Fraser DJ, Weir LK, Bernatchez L, Hansen MM, Taylor EB. Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity. 2011;106:404–20. doi: 10.1038/hdy.2010.167 21224881

55. R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2018.

56. Dempster AP, Laird NM, Rubin DB. Maximum likelihood from incomplete data via the EM algorithm. Journal of the Royal Statistical Society Series B (Methodological). 1977;39(1):1–38.

57. Crampton WGR. Electric signal design and habitat preferences in a species rich assemblage of gymnotiform fishes from the upper Amazon basin. Anais da Academia Brasileira de Ciências. 1998;70(4):805–47.

58. Campana SE. Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. Journal of Fish Biology. 2001;59(2):197–242.

59. Popper AN, Lu Z. Structure-function relationships in fish otolith organs. Fish Research. 2000;46(15–25).

60. Fowler A. Age in years from otoliths of adult tropical fish. In: Green BS, Mapstone BD, Carlos G, Begg GA, editors. Tropical fish otoliths: Information for assessment, management and ecology. Dordrecht: Springer; 2009. p. 55–92.

61. Jepsen DB, Winemiller KO, Taphorn DC, Olarte DC. Age structure and growth of peacock cichlids from rivers and reservoirs of Venezuela. Journal of Fish Biology. 1999;55:433–50.

62. Duponchelle F, Lino F, Hubert N, Panfili J, Renno JF, Baras E, et al. Environment-related life-history trait variations of the red-bellied piranha Pygocentrus nattereri in two river basins of the Bolivian Amazon. Journal of Fish Biology. 2007;71:1113–34.

63. Morison A, Burnett J, McCurdy W, Moksness E. Quality issues in the use of otoliths for fish age estimation. Quality issues in the use of otoliths for fish age estimation. 2005;Marine and Freshwater Research(5):773–82.

64. Platt ER, Ord TJ. Population variation in the life history of a land fish, Alticus arnoldorum, and the effects of predation and density. PLoS One. 2015;10:e0137244. doi: 10.1371/journal.pone.0137244 26398191

65. Lessa R, Santana FM, Duarte-Neto P. A critical appraisal of marginal increment analysis for assessing temporal periodicity in band formation among tropical sharks. Environmental Biology of Fishes. 2006;77:309–15.

66. Lin YJ, Tzeng WN. Validation of annulus in otolith and estimation of growth rate for Japanese eel Anguilla japonica in tropical southern Taiwan. Environmental Biology of Fishes. 2009;84:79–87.

67. Pérez A, Fabre NN. Life-history characteristics of Pseudoplatystoma metaense (Teleostei: Siluriformes: Pimelodidae) from the northwestern Orinoco River Basin. Neotropical Ichthyology. 2018;16(1):10.

68. Bagenal TB. Aspects of fish fecundity. In: Gerking SD, editor. Ecology of freshwater fish production. Oxford: Blackwell Scientific Publications; 1978. p. 75–101.

69. Nunn AD, Harvey JP, Cowx IG. Variations in the spawning periodicity of eight fish species in three English lowland rivers over a 6 year period, inferred from 0+ year fish length distributions. Journal of Fish Biology. 2007;70(4):1254–67.

70. Romagosa E, De Paiva P, Godinho HM. Pattern of oocyte diameter frequency distribution in females of the pacu, Piaractus mesopotamicus (Holmberg 1887) (= Colossoma mitrei Berg 1895), induced to spawn. Aquaculture. 1990;86(1):105–10.

71. Kurita Y, Meier S, Kjesbu OS. Oocyte growth and fecundity regulation by atresia of Atlantic herring (Clupea harengus) in relation to body condition throughout the maturation cycle. Journal of Sea Research. 2003;49(3):203–19.

72. Crampton WGR, Hopkins CD. 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;2005(1):48–60.

73. Gavassa S. Social and environmental regulation of signal plasticity and signal reliability in the electric fish Brachyhypopomus gauderio [PhD]. Miami: Florida International University; 2012.

74. Kirschbaum F, Schugardt C. Reproductive strategies and developmental aspects in mormyrid and gymnotiform fishes. Journal of Physiology-Paris. 2002;96:557–66.

75. Crampton WGR. Gymnotiform fish: an important component of Amazonian floodplain fish communities. Journal of Fish Biology. 1996;48:298–301.

76. Kawasaki M, Heiligenberg W. Distinct mechanisms of modulation in a neuronal oscillator generate different social signals in the electric fish Hypopomus. Journal of Comparative Physiology A. 1989;165:731–41.

77. Perrone R, Macadar O, Silva A. Social electric signals in freely moving dyads of Brachyhypopomus pinnicaudatus. Journal of Comparative Physiology A. 2009;195:501–14.

78. Crampton WGR, Chapman LJ, Bell J. Interspecific variation in gill size is correlated to ambient dissolved oxygen in the Amazonian electric fish Brachyhypopomus (Gymnotiformes: Hypopomidae). Environmental Biology of Fishes. 2008;83(2):223–35.

79. Pazin VFV, Magnusson WE, Zuanon J, Mendonca FP. Fish assemblages in temporary ponds adjacent to 'terra-firme' streams in Central Amazonia. Freshwater Biology. 2006;51(6):1025–37.

80. Allen JRM, Wootton RJ. Effect of food on the growth of carcass, liver, and ovary in female Gasterosteus aculeatus. Journal of Fish Biology. 1982;21:537–47.

81. Bruslé J, Gonzàlez i Anadon G. The structure and function of fish liver. In: Dutta HM, Datta-Mushi JS, editors. Fish morphology: horizons of new research: CRC Press; 1996. p. 77–93.

82. Bakos J. Technology for fish propagation. In: Pillay TVR, editor. Lectures presented at the Aquaculture Development and Coordination Programtraining course in Inland Aquaculture Engineering, Budapest. Rome: United Nations Development Programme Food and Agriculture Organization; 1984. p. 297–323.

83. Kirschbaum F, Schugardt C. Reproductive strategies and developmental aspects in mormyrid and gymnotiform fishes. Journal of Physiology-Paris. 2002;96(5):557–66.

84. Westby GWM. The ecology, discharge diversity and predatory behaviour of gymnotiform electric fish in the coastal streams of French Guiana. Behavioral Ecology and Sociobiology. 1988;22:341–54.

85. Lowe-McConnell RH. The fishes of the Rupununi savanna district of British Guiana. Pt I. Groupings of fish species and effects of the seasonal cycles on the fish. Journal of the Linnean Society, Zoology. 1964;45:103–44.

86. Goulding M. The fishes and the forest. Berkeley: University of California Press; 1980.

87. Junk WJ M. SMG, Saint-Paul U. The fish. In: Junk WJ, editor. The central Amazon floodplain: ecology of a pulsing system. Berlin: Springer; 1997. p. 385–408.

88. Crampton WGR. Ecology and life history of an Amazon floodplain cichlid: the discus fish Symphysodon (Perciformes: Cichlidae). Neotropical Ichthyology. 2008;6(4):599–612.

89. Alkins-Koo M. Reproductive timing of fishes in a tropical intermittent stream. Environmental Biology of Fishes. 2000;57:49–66.

90. Kramer DL. Reproductive seasonality in the fishes of a tropical stream. Ecology. 1978;59(5):976–85.

91. Krekorian CON. Field observations in Guyana on the reproductive biology of the spraying characin Copeina arnoldi Regan. American Midland Naturalist. 1976;96:88–97.

92. Winemiller KO. Seasonality of reproduction by livebearing fishes in tropical rainforest streams. Oecologia. 1993;95(2):266–76. doi: 10.1007/BF00323499 28312951

93. Lowe-McConnell RH. Ecological aspects of seasonality in fishes of tropical waters. Symposia of the Zoological Society of London. 1979;44:219–41.

94. Piedade MTF, Junk W, D'Ângelo SA, Wittmann F, Schöngart J. Aquatic herbaceous plants of the Amazon floodplains: state of the art and research needed. Acta Limnologica Brasiliensia. 2010;22:165–78.

95. dos Anjos MB, de Oliveira RR, Zuanon J. Hypoxic environments as refuge against predatory fish in the Amazonian floodplains. Brazilian Journal of Biology. 2008; 68:45–50.

96. Junk WJ, editor. The Central Amazon floodplain: ecology of a pulsing system. Berlin: Springer; 1997.

97. Espírito-Santo HMV, Magnusson WE, Zuanon J, Mendonça FP, Landeiro VL. Seasonal variation in the composition of fish assemblages in small Amazonian forest streams: evidence for predictable changes. Freshwater Biology. 2009;54:536–48.

98. Saul WG. An ecological study of fishes at a site in upper Amazonian Ecuador. Proceedings Academy of Natural Sciences of Philadelpia. 1975;127:93–134.

99. Beverton RJH, Holt SJ. A review of the lifespans and mortality rates of fish in nature and the relation to growth and other physiological characteristics. The lifespan of animals. London: Churchill (CIBA Foundation: Colloquia on ageing) 1959. p. 142–77.

100. Kirschbaum F. Reproduction of weakly electric teleosts: just another example of convergent development? Environmental Biology of Fishes. 1984;10(1–2):3–14.

101. Ilieş I, Traniello IM, Sirbulescu RF, Zupanc GKH. Determination of relative age using growth increments of scales as a minimally invasive method in the tropical freshwater Apteronotus leptorhynchus. Journal of Fish Biology. 2014;84(1312–1325). doi: 10.1111/jfb.12354 24697593

102. Queiroz HL. Growth and sexual maturation of female Pirarucu (Arapaima gigas): tools for conservation and management of an Amazonian fish (abstract). Journal of Fish Biology. 1998;53 (SupplementA):441–2.

103. Arrantes CC, Castello L, Stewart DJ, M. C, Queiroz HL. Population density, growth and reproduction of Arapaima in an Amazonian river-floodplain. Ecology of Freshwater Fish. 2010;19:455–65.

104. Araujo-Lima C, Goulding M. So fruitful a fish: ecology, conservation and aquaculture of the Amazon's tambaqui. New York: Columbia University Press; 1997.

105. Barthem R, Goulding M. The catfish connection: ecology, migration and conservation of Amazon predators. New York: Columbia University Press; 1997.

106. Pérez A, Fabré NN. Seasonal growth and life history of the catfish Calophysus macropterus (Licthenstein, 1819) (Siluriformes: Pimelodidae) from the Amazon floodplain. Journal of Applied Ichthyology. 2007;25:343–9.

107. Reznick D, Bryant M, Holmes D. The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata). PLoS Biology. 2006;4(1):e7. doi: 10.1371/journal.pbio.0040007 16363919

108. Parenti LR. The phylogeny of Atherinomorphs: Evolution of a novel fish reproductive system. In: Uribe MC, Grier HJ, editors. Viviparous fishes. Homestead, FL: New Life Publications; 2005. p. 13–30.

109. Weitzman SH, Vari RP. Miniaturization in South American freshwater fishes: an overview and discussion. Proceedings of the Biological Society of Washington. 1988;101(2):444–65.

110. Franchina CR. Ontogeny of the electric organ discharge and the electric organ in the weakly electric pulse fish Brachyhypopomus pinnicaudatus (Hypopomidae, Gymnotiformes). Journal of Comparative Physiology A-Neuroethology Sensory Neural and Behavioral Physiology. 1997;181:111–9.

111. Gavassa S, Silva AC, Gonzalez E, Molina J, Stoddard PK. Social competition masculinizes the communication signals of female electric fish. Behavioral Ecology and Sociobiology. 2012;66(7):1057–66.

112. Cognato DdP Fialho CB. Reproductive biology of a population of Gymnotus aff. carapo (Teleostei: Gymnotidae) from southern Brazil. Neotropical Ichthyology. 2006;4(3):339–48.

113. Giora J, Fialho CB. Reproductive biology of weakly electric fish Eigenmannia trilineata Lopez and Castello, 1966 (Teleostei, Sternopygidae). Brazilian Archives of Biology and Technology. 2009;52(3):617–28.

114. Murua H, Kraus G, Saborido-Rey F, Witthames PR, Thorsen A, Junquera S. Procedures to estimate fecundity of marine fish species in relation to their reproductive strategy. Journal of Northwest Atlantic Fishery Science. 2003;33:33–54.

115. Ganias K, Lowerre-Barbieri SK, Cooper W. Understanding the determinate-indeterminate fecundity dichotomy in fish populations using a temperature dependent oocyte growth model. Journal of Sea Research. 2015;96:1–10.

116. Balon EK. Reproductive guilds of fishes: a proposal and definition. Journal of the Fisheries Research Board of Canada. 1975;32(6):821–64.

117. Assunção MIS, Schwassmann HO. Reproduction and larval development of Electrophorus electricus on Marajó Island (Pará, Brazil). Ichthyological Exploration of Freshwaters. 1995;6(2):175–84.

118. Vazzoler AEAM. Biologia de reprodução de peixes teleósteos: teoria e prática. Maringá, Brazil: Editora da Universidade Estadual de Maringá; 1996. 196 p.

119. Reznick DN, Bryant MJ, Roff D, Ghalambor CK, Ghalambor DE. Effect of extrinsic mortality on the evolution of senescence in guppies. Nature. 2004;431:1095–9. doi: 10.1038/nature02936 15510147

120. Gambling SJ, Reimchen TE. Prolonged life span among endemic Gasterosteus populations. Canadian Journal of Zoology. 2012;90:284–90.

121. Affonso AG, de Queiroz HL, Novo EMLM. Abiotic variability among different aquatic systems of the central Amazon floodplain during drought and flood events. Brazilian Journal of Biology. 2015;75(4 (1)):S60–S9.

122. Röpke CP, Amadio S, Zanon J, Ferreira EJG, de Deus CP, Pires THS, et al. Simultaneous abrupt shifts in hydrology and fish assemblage structure in a floodplain lake in the central Amazon. Scientific Reports. 2017;7 (10.1038/srep40170):1–10.

123. Metcalfe NB, Monaghan P. Growth versus lifespan: perspectives from evolutionary ecology. Experimental Gerontology. 2003;38(935–940). doi: 10.1016/s0531-5565(03)00159-1 12954479

124. Goulding M, Carvalho M.L.,and Ferreira E.G. Rio Negro, rich life in poor water. The Hague: SPB Academic Publishing; 1988.

125. Charlesworth B, León JA. The relation of reproductive effort to age. The American Naturalist. 1976;110(973):449–59.

126. Doughty P, Shine R. Detecting life history trade-offs: measuring energy stores in 'capital' breeders reveals costs of reproduction. Oecologia. 1997;110(508–513). doi: 10.1007/s004420050187 28307242

127. Parker GA. The evolution of sexual dimorphism in fish. Journal of Fish Biology. 1992;41:1–20.

128. Trippel EA, Kjesbu OS, Solemdal P. Effects of adult age and size structure on reproductive output in marine fishes. In: Chambers RC, Trippel EA, editors. Early Life History and Recruitment in Fish Populations (Chapman & Hall Fish and Fisheries Series 21). Dordrecht: Springer; 1997. p. 31–62.

129. Basolo AL. Variation between and within the sexes in body size preferences. Animal Behaviour. 2004;68(1):75–82.

130. Curtis CC, Stoddard PK. Mate preference in female electric fish, Brachyhypopomus pinnicaudatus. Animal Behaviour. 2003;66:329–36.

131. Hagedorn M, Zelick R. Relative dominance among males is expressed in the electric organ discharge characteristics of a weakly electric fish. Animal Behaviour. 1989;38:520–5.

132. Salazar VL, Stoddard PK. Social competition affects electric signal plasticity and steroid levels in the gymnotiform fish Brachyhypopomus gauderio. Hormones and Behavior. 2009;56(4):399–409. doi: 10.1016/j.yhbeh.2009.07.009 19647742

133. Gavassa S, Silva AC, Gonzalez E, Stoddard PK. Signal modulation as a mechanism for handicap disposal. Animal Behaviour. 2012;83:935–44. doi: 10.1016/j.anbehav.2012.01.012 22665940

134. Salazar VL, Stoddard PK. Sex differences in energetic costs explain sexual dimorphism in the circadian rhythm modulation of the electrocommunication signal of the gymnotiform fish Brachyhypopomus pinnicaudatus. Journal of Experimental Biology. 2008;211(6):1012–20.

Článok vyšiel v časopise


2019 Číslo 12