Oecologia

, Volume 137, Issue 4, pp 502–511 | Cite as

Oxygen consumption in weakly electric Neotropical fishes

  • David Julian
  • William G. R. Crampton
  • Stephanie E. Wohlgemuth
  • James S. Albert
Ecophysiology

Abstract

Weakly electric gymnotiform fishes with wave-type electric organ discharge (EOD) are less hypoxia-tolerant and are less likely to be found in hypoxic habitats than weakly electric gymnotiforms with pulse-type EOD, suggesting that differences in metabolism resulting from EOD type affects habitat choice. Although gymnotiform fishes are common in most Neotropical freshwaters and represent the dominant vertebrates in some habitats, the metabolic rates of these unique fishes have never been determined. In this study, O2 consumption rates during EOD generation are reported for 34 gymnotiforms representing 23 species, all five families and 17 (59%) of the 28 genera. Over the size range sampled (0.4 g to 125 g), O2 consumption of gymnotiform fishes was dependent on body mass, as expected, fitting a power function with a scaling exponent of 0.74, but the O2 consumption rate was generally about 50% of that expected by extrapolation of temperate teleost metabolic rates to a similar ambient temperature (26°C). O2 consumption rate was not dependent on EOD type, but maintenance of “scan swimming” (continuous forwards and backwards swimming), which is characteristic only of gymnotiforms with wave-type EODs, increased O2 consumption 2.83±0.49-fold (mean±SD). This suggests that the increased metabolic cost of scan swimming could restrict gymnotiforms with wave-type EODs from hypoxic habitats.

Keywords

Gymnotiforms Electric fish Electric organ discharge Metabolism Amazon Scan swimming 

Notes

Acknowledgements

The authors would like to thank Hernan Ortega and Lorgio Verdi for helping to arrange permits to work in the Peruvian Amazon, Katty Miche for field assistance, Victoriano Panduro of the Red Tail Cat Aquarium in Iquitos, Peru for providing space to perform experiments, and Lauren J. Chapman, David H. Evans, Brian K. McNab, and Ashley W. Seifert for valuable insights and discussions. The final manuscript was greatly improved by comments from Philip Stoddard and an anonymous reviewer. All studies were approved by the University of Florida Institutional Animal Care and Use Committee, and by the Peruvian National Ministry of the Environment under permit 13 S/C-2000 INRENA-DGANPFS-DANP to J.S. Albert.

References

  1. Albert JS (2001) Species diversity and phylogenetic systematics of American knifefishes (Gymnotiformes, Teleostei). Miscellaneous Publications of the Museum of Zoology, University of Michigan 190, pp1–127Google Scholar
  2. Albert JS (2003a) Family Apterontoidae. In: Reis RE, Kullander SO, Ferraris CJ Jr (eds) Checklist of the freshwater fishes of South and Central America. EDIPUCRS, Porto Alegre, pp493–497Google Scholar
  3. Albert JS (2003b) Family Sternopygidae. In: Reis RE, Kullander SO, Ferraris CJ Jr (eds) Checklist of the freshwater fishes of South and Central America. EDIPUCRS, Porto Alegre, pp503–508Google Scholar
  4. Albert JS, Crampton WGR (2003) Family Hypopomidae. In: Reis RE, Kullander SO, Ferraris CJ Jr (eds) Checklist of the freshwater fishes of South and Central America. EDIPUCRS, Porto Alegre, pp500–502Google Scholar
  5. Albert JS, Lannoo MJ, Yuri T (1998) Testing hypotheses of neural evolution in gymnotiform electric fishes using phylogenetic character data. Evolution 52:1760–1780Google Scholar
  6. Albert JS, Froese R, Bauchot R, Ito H (1999) Diversity of brain size in fishes: preliminary analysis of a database including 1174 species in 45 orders. In: Seret B, Sire JY (eds) 5th Indo-Pacific Fish Conference Proceedings. Societe Francaise d’Ichtyologie, Paris pp647–656Google Scholar
  7. Albert JS, Froese R, Paulay D (2000) The brains table. In: Froese R, Paulay D (eds) FishBase 2000, concepts, design and data sources. ICLARM, Manila, pp234–237Google Scholar
  8. Assad C, Rasnow B, Stoddard PK, Bower JM (1998) The electric organ discharges of the gymnotiform fishes: II. Eigenmannia. J Comp Physiol A 183:419–432Google Scholar
  9. Assad C, Rasnow B, Stoddard PK (1999) Electric organ discharges and electric images during electrolocation. J Exp Biol 202:1185–1193PubMedGoogle Scholar
  10. Bass AH (1986) Electric organs revisited: evolution of a vertebrate communication and orientation organ. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp13–70Google Scholar
  11. Bastian J (1986) Electrolocation: behavior, anatomy and physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp577–612Google Scholar
  12. Bell CC, Hopkins CD, Grant K (1993) Contributions of electrosensory systems to neurobiology and neuroethology. J Comp Physiol A 173:657–763Google Scholar
  13. Bennett MVL (1971) Electric organs. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 5. Academic Press, New York, pp346–491Google Scholar
  14. Black-Cleworth P (1970) The role of electrical discharges in the non-reproductive social behavior of Gymnotus carapo (Gymnotidae, Pisces). Anim Behav Monogr 3:1–77Google Scholar
  15. Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8. Academic Press, New York, pp280–352Google Scholar
  16. Bullock TH, Heiligenberg W (1986) Electroreception. Wiley-Interscience, New YorkGoogle Scholar
  17. Campos-da-Paz RC (2003) Family Gymnotidae. In: Reis RE, Kullander SO, Ferraris CJ Jr (eds) Checklist of the freshwater fishes of South and Central America. EDIPUCRS, Porto Alegre, pp483–486Google Scholar
  18. Caputi AA, Silva AC, Macadar O (1998) The electric organ discharge of Brachyhypopomus pinnicaudatus. Brain Behav Evol 52:148–158CrossRefPubMedGoogle Scholar
  19. Carter GS, Beadle LC (1931) The fauna of the swamps of the Paraguayan chao in relation to its environment. II. Respiratory adaptations in the fishes. Zool J Linn Soc Lond 37:327–366Google Scholar
  20. Chapman LJ, Chapman CA (1998) Hypoxia tolerance of the mormyrid Petrocephalus catostoma: Implications for persistence in swamp refugia. Copeia 1998:762–768Google Scholar
  21. Chapman LJ, Hulen KG (2001) Implications of hypoxia for the brain size and gill morphometry of mormyrid fishes. J Zool 254:461–472CrossRefGoogle Scholar
  22. Chapman LJ, Chapman CA, Nordlie FG, Rosenberger AE (2002) Physiological refugia: swamps, hypoxia tolerance and maintenance of fish diversity in the Lake Victoria region. Comp Biochem Physiol A 133:421–437Google Scholar
  23. Clarke A, Johnston N (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905CrossRefGoogle Scholar
  24. Crampton WGR (1996) Gymnotiform fish: an important component of Amazonian floodplain fish communities. J Fish Biol 48:298–301CrossRefGoogle Scholar
  25. Crampton WGR (1998a) Electric signal design and habitat preferences in a species rich assemblage of gymnotiform fishes from the Upper Amazon basin. An Acad Bras Cienc 70:805–847Google Scholar
  26. Crampton WGR (1998b) Effects of anoxia on the distribution, respiratory strategies and electric signal diversity of gymnotiform fishes. J Fish Biol 53 (Supp 1):307–330CrossRefGoogle Scholar
  27. Crampton WGR, Hulen KH, Albert JS (2003) Sternopygus branco, a new species of Neotropical electric fish (Gymnotiformes: Sternopygidae) from the lowland Amazon Basin, with descriptions of ecology and electric organ discharges. Copeia (in press)Google Scholar
  28. Emde G von der (1997) Electroreception. In: Evans DH (ed) The physiology of fishes. CRC Press, Boca Raton, Fla., pp313–343Google Scholar
  29. Ferraris CJ Jr (2003) Family Rhamphichthyidae. In: Reis RE, Kullander SO, Ferraris Jr CJ (eds) Checklist of the freshwater fishes of South and Central America. EDIPUCRS, Porto Alegre, pp492–493Google Scholar
  30. Franchina CR, Stoddard PK (1998) Plasticity of the electric organ discharge waveform of the electric fish Brachyhypopomus pinnicaudatus. I. Quantification of day-night changes. J Comp Physiol A 183:759–768CrossRefPubMedGoogle Scholar
  31. Franchina CR, Salazar VL, Volmar CH, Stoddard PK (2001) Plasticity of the electric organ discharge waveform of male Brachyhypopomus pinnicaudatus. II. Social effects. J Comp Physiol A 187:45–52Google Scholar
  32. Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotoid fish. Anim Behav 33:254–265Google Scholar
  33. Heiligenberg W (1987) Central processing of sensory information in electric fish. J Comp Physiol A 161:621–631PubMedGoogle Scholar
  34. Heiligenberg W (1991) Neural nets in electric fish. MIT, CambridgeGoogle Scholar
  35. Heiligenberg W, Bastian J (1984) The electric sense of weakly electric fish. Annu Rev Physiol 46:561–583CrossRefPubMedGoogle Scholar
  36. Hopkins CD (1974) Electric communication: functions in the social behaviour of Eigenmannia virescens. Behaviour 50:270–305Google Scholar
  37. Hopkins CD (1976) Stimulus filtering and electroreception: tuberous electroreceptors in three species of gymnotoid fish. J Comp Physiol A 111:171–208Google Scholar
  38. Hopkins CD (1988) Neuroethology of electric communication. Annu Rev Neurosci 11:497–535CrossRefPubMedGoogle Scholar
  39. Hopkins CD (1999) Design features for electric communication. J Exp Biol 202:1217–1228PubMedGoogle Scholar
  40. Hopkins CD, Comfort NC, Bastian J, Bass AH (1990) Functional analysis of sexual dimorphism in an electric fish, Hypopomus pinnicaudatus, order Gymnotiformes. Brain Behav Evol 35:350–367Google Scholar
  41. Kramer B (1995) Electroreception and communication in fishes. George Fischer, StuttgartGoogle Scholar
  42. Lannoo MJ, Lannoo SJ (1993) Why do electric fish swim backwards? An hypothesis based on gymnotiform foraging behavior interpreted through sensory constraints. Environ Biol Fish 36:157–165Google Scholar
  43. Lopez-Rojas H, Lundberg JL, Marsh E (1984) Design and operation of a small trawling apparatus for use with dugout canoes. N Am J Fish Manage 4:331–334Google Scholar
  44. Lundberg JG, Lewis WM, Saunders JF, Mago-Leccia F (1987) A major food web component in the Orinoco river channel: evidence from planktivorous electric fish. Science 237:81–83Google Scholar
  45. MacIver MA, Sharabash NM, Nelson ME (2001) Prey-capture behavior in gymnotid electric fish: Motion analysis and effects of water conductivity. J Exp Biol 204:543–557PubMedGoogle Scholar
  46. McAnelly L, Silva A, Zakon HH (2003) Cyclic AMP modulates electrical signaling in a weakly electric fish. J Comp Physiol A 189:273–82Google Scholar
  47. McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press, New YorkGoogle Scholar
  48. Moortgat KT, Keller CH, Bullock TH, Sejnowski TJ (1998) Submicrosecond pacemaker precision is behaviorally modulated: The gymnotiform electromotor pathway. Proc Natl Acad Sci USA 95:4684–4689CrossRefPubMedGoogle Scholar
  49. Nanjappa P, Brand L, Lannoo M J (2000) Swimming patterns associated with foraging in phylogenetically and ecologically diverse American weakly electric teleosts (Gymnotiformes). Environ Biol Fish 58:97–104CrossRefGoogle Scholar
  50. Nillson G (1996) Brain and body oxygen requirements of Gnathonemus petersii, a fish with an exceptionally large brain. J Exp Biol 199:603–607PubMedGoogle Scholar
  51. Rasnow B, Bower JM (1996) The electric organ discharges of the electric fish. 1. Apteronotus leptorhynchus. J Comp Physiol A 178:453–462Google Scholar
  52. Rosenberger AE (1997) Potential of wetland tributaries as refugia for endangered fishes from nonnative predators: a case study of Lake Nabugabo, Uganda. MS Thesis, University of Florida, Gainesville, FloridaGoogle Scholar
  53. Schofield PJ, Chapman LJ (2000) Hypoxia tolerance of introduced Nile perch: implications for survival of indigenous fishes in the Lake Victoria basin. Afr Zool 35:35–42Google Scholar
  54. Stoddard PK (1999) Predation enhances complexity in the evolution of electric fish signals. Nature 400:254–256CrossRefPubMedGoogle Scholar
  55. Stoddard PK (2002) Electric signals: predation, sex, and environmental constraints. Adv Study Behav 31:201–241Google Scholar
  56. Stoddard PK, Rasnow B, Assad C (1999) Electric organ discharges of the gymnotiform fishes: III Brachyhypopomus. J Comp Physiol A 184:609–630CrossRefPubMedGoogle Scholar
  57. Sullivan JP (1997) A phylogenetic study of the Neotropical hypopomid electric fishes (Gymnotiformes: Rhamphichthyoidea). PhD Thesis, Duke University, Durham, North CarolinaGoogle Scholar
  58. Val AL, Silva MNP, Almeida-Val VMF (1998) Hypoxia adaptation in fish of the Amazon: a never-ending task. S Afr J Zool 33:107–114Google Scholar
  59. Westby GWM (1975) Comparative studies of the aggressive behavior of two gymnotid electric fish (Gymnotus carapo and Hypopomus artedi). Anim Behav 23:192–213Google Scholar
  60. Winberg GG (1961) New information on metabolic rate in fishes (Original in Russian). Translation Series No. 362, Fisheries Research Board of Canada, Nanaimo, BCGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • David Julian
    • 1
  • William G. R. Crampton
    • 1
  • Stephanie E. Wohlgemuth
    • 1
  • James S. Albert
    • 1
    • 2
  1. 1.Department of ZoologyUniversity of FloridaGainesvilleUSA
  2. 2.Florida Museum of Natural HistoryUniversity of Florida

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