Spooky Interaction at a Distance in Cave and Surface Dwelling Electric Fishes.

Eric S Fortune, Nicole Andanar, Manu Madhav, Ravikrishnan P Jayakumar, Noah J Cowan, Maria Elina Bichuette, Daphne Soares
Author Information
  1. Eric S Fortune: Biological Sciences, New Jersey Institute of Technology, Newark, NJ, United States.
  2. Nicole Andanar: Biological Sciences, New Jersey Institute of Technology, Newark, NJ, United States.
  3. Manu Madhav: Department of Mechanical Engineering, Johns Hopkins University, Baltimore, MD, United States.
  4. Ravikrishnan P Jayakumar: Department of Mechanical Engineering, Johns Hopkins University, Baltimore, MD, United States.
  5. Noah J Cowan: Department of Mechanical Engineering, Johns Hopkins University, Baltimore, MD, United States.
  6. Maria Elina Bichuette: Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de São Carlos, São Carlos, Brazil.
  7. Daphne Soares: Biological Sciences, New Jersey Institute of Technology, Newark, NJ, United States.

Abstract

Glass knifefish () are a group of weakly electric fishes found throughout the Amazon basin. Their electric organ discharges (EODs) are energetically costly adaptations used in social communication and for localizing conspecifics and other objects including prey at night and in turbid water. Interestingly, a troglobitic population of blind cavefish survives in complete darkness in a cave system in central Brazil. We examined the effects of troglobitic conditions, which includes a complete loss of visual cues and potentially reduced food sources, by comparing the behavior and movement of freely behaving cavefish to a nearby epigean (surface) population (). We found that the strengths of electric discharges in cavefish were greater than in surface fish, which may result from increased reliance on electrosensory perception, larger size, and sufficient food resources. Surface fish were recorded while feeding at night and did not show evidence of territoriality, whereas cavefish appeared to maintain territories. Surprisingly, we routinely found both surface and cavefish with sustained differences in EOD frequencies that were below 10 Hz despite being within close proximity of about 50 cm. A half century of analysis of electrosocial interactions in laboratory tanks suggest that these small differences in EOD frequencies should have triggered the "jamming avoidance response," a behavior in which fish change their EOD frequencies to increase the difference between individuals. Pairs of fish also showed significant interactions between EOD frequencies and relative movements at large distances, over 1.5 m, and at high differences in frequencies, often >50 Hz. These interactions are likely "envelope" responses in which fish alter their EOD frequency in relation to higher order features, specifically changes in the depth of modulation, of electrosocial signals.

Keywords

References

  1. J Exp Biol. 2013 Jul 1;216(Pt 13):2451-8 [PMID: 23761470]
  2. J Exp Biol. 2012 Dec 1;215(Pt 23):4196-207 [PMID: 23136154]
  3. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005 Sep;191(9):865-72 [PMID: 16001182]
  4. An Acad Bras Cienc. 2017 Jul-Sep;89(3):1615-1628 [PMID: 28876384]
  5. Front Integr Neurosci. 2019 Jul 05;13:21 [PMID: 31333424]
  6. Horm Behav. 2015 May;71:31-40 [PMID: 25870018]
  7. J Neurosci. 2002 Sep 15;22(18):8287-96 [PMID: 12223583]
  8. Science. 1972 Jun 2;176(4038):1035-7 [PMID: 17778429]
  9. J Neurosci. 2018 Jun 13;38(24):5456-5465 [PMID: 29735558]
  10. ILAR J. 2009;50(4):361-72 [PMID: 19949252]
  11. J Comp Physiol A. 1998 Oct;183(4):419-32 [PMID: 9809452]
  12. Behav Brain Res. 2010 Mar 5;207(2):368-76 [PMID: 19874855]
  13. J Comp Physiol A. 1997 Nov;181(5):532-44 [PMID: 9373958]
  14. Proc Natl Acad Sci U S A. 2013 Mar 26;110(13):5263-8 [PMID: 23440218]
  15. Science. 1982 Nov 26;218(4575):916-8 [PMID: 7134985]
  16. Integr Comp Biol. 2016 Nov;56(5):889-900 [PMID: 27549201]
  17. J Fish Biol. 2019 Jul;95(1):92-134 [PMID: 30729523]
  18. PLoS Biol. 2009 Sep;7(9):e1000203 [PMID: 19787026]
  19. J Exp Biol. 2013 Nov 15;216(Pt 22):4272-84 [PMID: 23997196]
  20. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005 Sep;191(9):845-56 [PMID: 16007457]
  21. Behav Brain Res. 2005 Oct 14;164(1):83-92 [PMID: 16099058]
  22. eNeuro. 2019 Mar 19;6(2): [PMID: 30899777]
  23. Proc Natl Acad Sci U S A. 2018 Jan 16;115(3):573-577 [PMID: 29295924]
  24. Annu Rev Genet. 2009;43:25-47 [PMID: 19640230]
  25. Horm Behav. 1998 Aug;34(1):30-8 [PMID: 9735226]
  26. PLoS One. 2018 May 2;13(5):e0195991 [PMID: 29718938]
  27. J Exp Biol. 1971 Oct;55(2):371-83 [PMID: 5114029]
  28. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2006 Jun;192(6):613-24 [PMID: 16437223]
  29. J Exp Biol. 2008 May;211(Pt 10):1657-67 [PMID: 18456893]
  30. Front Psychol. 2017 Aug 31;8:1497 [PMID: 28912746]
  31. J Neurosci. 2006 Apr 19;26(16):4370-82 [PMID: 16624957]
  32. J Physiol Paris. 2013 Jan-Apr;107(1-2):13-25 [PMID: 22981958]
  33. J Exp Biol. 2020 Feb 10;223(Pt 3): [PMID: 31937524]
  34. J Exp Biol. 1999 May;202(Pt 10):1195-203 [PMID: 10210661]
  35. Biol Lett. 2011 Apr 23;7(2):197-200 [PMID: 20980295]
  36. J Exp Biol. 2013 Jul 1;216(Pt 13):2459-68 [PMID: 23761471]
  37. J Exp Biol. 2013 Jul 1;216(Pt 13):2393-402 [PMID: 23761464]
  38. Biol Open. 2018 Nov 29;7(12): [PMID: 30341102]
  39. Front Integr Neurosci. 2020 Oct 22;14:561524 [PMID: 33192352]
  40. J Neurosci. 2016 Sep 21;36(38):9859-72 [PMID: 27656024]
  41. J Exp Biol. 2014 Apr 15;217(Pt 8):1381-91 [PMID: 24363423]
  42. Front Integr Neurosci. 2019 Aug 20;13:39 [PMID: 31481882]
  43. PLoS One. 2020 Jun 15;15(6):e0228976 [PMID: 32542049]
  44. Front Integr Neurosci. 2019 Jul 31;13:36 [PMID: 31417374]
  45. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2002 Sep;188(8):649-57 [PMID: 12355241]
  46. J Exp Biol. 2018 Aug 13;221(Pt 15): [PMID: 29954835]
  47. Sci Rep. 2018 Apr 11;8(1):5830 [PMID: 29643472]

Word Cloud

Created with Highcharts 10.0.0cavefishfishEODfrequencieselectricfoundtroglobiticsurfacedifferencesinteractionsweaklydischargesnightpopulationcompletefoodbehaviorepigeanSurfaceHzelectrosocialavoidanceresponseGlassknifefishgroupfishesthroughoutAmazonbasinorganEODsenergeticallycostlyadaptationsusedsocialcommunicationlocalizingconspecificsobjectsincludingpreyturbidwaterInterestinglyblindsurvivesdarknesscavesystemcentralBrazilexaminedeffectsconditionsincludeslossvisualcuespotentiallyreducedsourcescomparingmovementfreelybehavingnearbystrengthsgreatermayresultincreasedrelianceelectrosensoryperceptionlargersizesufficientresourcesrecordedfeedingshowevidenceterritorialitywhereasappearedmaintainterritoriesSurprisinglyroutinelysustained10despitewithincloseproximity50cmhalfcenturyanalysislaboratorytankssuggestsmalltriggered"jamming"changeincreasedifferenceindividualsPairsalsoshowedsignificantrelativemovementslargedistances15mhighoften>50likely"envelope"responsesalterfrequencyrelationhigherorderfeaturesspecificallychangesdepthmodulationsignalsSpookyInteractionDistanceCaveDwellingElectricFishesdiceCTenvelopegymnotiformesjamming

Similar Articles

Cited By