Non-breeding territoriality and the effect of territory size on aggression in the weakly electric fish, Gymnotus omarorum

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

Agonistic behavior involves the displays that arise when conspecifics compete for valuable resources such as territory. After conflict resolution, dominants obtain priority access to the resource while subordinates lose it. We aimed to evaluate how agonistic encounters mediate the acquisition of different sized territories in the weakly electric fish, Gymnotus omarorum, a species that displays a well-documented non-breeding agonistic behavior very unusual among teleosts. When tested in intrasexual and intersexual dyads in small arenas, a sex-independent dominant-subordinate status emerged after highly aggressive contests in which subordinates signaled submission by retreating and emitting submissive electric signals. We staged dyadic agonistic encounters in a large arena, in which the initial interindividual distance resembled the one observed in nature. We observed the emergence of a dominant-subordinate status after longer but milder contests with rare electric signaling of submission. We found the persistence of dominance over time with no outcome reversion. We observed how dominants exclude subordinates from their conquered resource during all the recording time. Although the territorial behavior of Gymnotus has been put forth since pioneer reports, this is the first study to show how agonistic behavior depends on the territory size in this genus. Agonistic encounters of G. omarorum in the small arena resemble the characteristics of violent-like behaviors. The ease of shifting from mild to high levels of aggression due to confinement, together with the use of electrical signaling of submission, makes this species an excellent model to explore new perspectives in territoriality assessment.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Adams ES (2001) Approaches to the study of territory size and shape. Annu Rev Ecol Syst 32:277–303

    Article  Google Scholar 

  2. Alexander BK, Roth EM (1971) The effects of acute crowding on aggressive behavior of Japanese monkeys. Behaviour 39:73–90

    Article  CAS  PubMed  Google Scholar 

  3. Armitage KB (1977) Social variety in the yellow-bellied marmot: a population-behavioural system. Anim Behav 25:585–593

    Article  Google Scholar 

  4. Assad C, Rasnow B, Stoddard PK (1999) Electric organ discharges and electric images during electrolocation. J Exp Biol 202:1185–1193

    CAS  PubMed  Google Scholar 

  5. Bakker TCM, Sevenster P (1983) Determinants of dominance in male sticklebacks (Gasterosteus aculeatus L.). Behaviour 86:55–71

    Article  Google Scholar 

  6. Balthazart J, Foidart A, Baillien M, Silverin B (1999) Brain aromatase in laboratory and free-living songbirds: relationships with reproductive behaviour. NJ Adams RH Slotow, pp 1257–1289

  7. Batista G, Zubizarreta L, Perrone R, Silva A (2012) Non-sex-biased dominance in a sexually monomorphic electric fish: fight structure and submissive electric signalling. Ethology 118:398–410

    Article  Google Scholar 

  8. Black-Cleworth P (1970) The role of electrical discharges in the non-reproductive social behaviour of Gymnotus carapo. Anim Behav Monogr 3:1–77

    Article  Google Scholar 

  9. Briffa M, Hardy ICW (2013) Introduction to animal contest. In: ICW H, Briffa M (eds) Animal contest. Cambridge University Press, New York, pp 1–4

    Google Scholar 

  10. Briffa M, Sneddon LU (2010) Contest behavior. In: Westneat DF, Fox CW (eds) Evolutionary behavioral ecology. Oxford University Press, New York, pp 246–265

    Google Scholar 

  11. Brown JL (1964) The evolution of diversity in avian territorial systems. Wilson Bull, pp 160–169

  12. Brown JL (1975) The evolution of behavior. WW Norton, New York

    Google Scholar 

  13. Buchwalder T, Huber-Eicher B (2004) Effect of increased floor space on aggressive behaviour in male turkeys (Meleagris gallopavo). Appl Anim Behav Sci 89:207–214

    Article  Google Scholar 

  14. Caldwell GS, Glickman SE, Smith ER (1984) Seasonal aggression independent of seasonal testosterone in wood rats. Proc Natl Acad Sci 81:5255–5257

    Article  CAS  PubMed  Google Scholar 

  15. Caputi AA, Budelli R (2006) Peripheral electrosensory imaging by weakly electric fish. J Comp Physiol A 192:587–600

    Article  CAS  Google Scholar 

  16. Caputi A, Carlson B, Macadar O (2005) Electric organs and their control. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 410–451

    Google Scholar 

  17. Chiver I, Stutchbury BJM, Morton ES (2014) Seasonal variation in male testosterone levels in a tropical bird with year-round territoriality. J F Ornithol 85:1–9

    Article  Google Scholar 

  18. Ciali S, Gordon J, Moller P (1997) Spectral sensitivity of the weakly discharging electric fish Gnathonemus petersii using its electric organ discharges as the response measure. J Fish Biol 50:1074–1087

    Google Scholar 

  19. Clarke TA (1970) Territorial behavior and population dynamics of a pomacentrid fish, the garibaldi, Hypsypops rubicunda. Ecol Monogr 40:189–212

    Article  Google Scholar 

  20. Crook JH (1965) The adaptive significance of avian social organization. Symp Zool Soc Land 14:181–218

    Google Scholar 

  21. Davies NB (1976) Food, flocking and territorial behaviour of the pied wagtail (Motacilla alba yarrellii Gould) in winter. J Anim Ecol 45:235–253

    Article  Google Scholar 

  22. de Boer SF, Caramaschi D, Natarajan D, Koolhaas JM (2009) The vicious cycle towards violence: focus on the negative feedback mechanisms of brain serotonin neurotransmission. Front Behav Neurosci 3:52. https://doi.org/10.3389/neuro.08.052.2009

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. de Boer SF, Buwalda B, Koolhaas JM (2016) Aggressive behavior and social stress. In: Stress: concepts, cognition, emotion, and behavior. Elsevier, pp 293–303

  24. Desrochers A, Hannon SJ (1989) Site-related dominance and spacing among winter flocks of Black-capped Chickadees. Condor 91:317–323

    Article  Google Scholar 

  25. Fugère V, Ortega H, Krahe R (2011) Electrical signalling of dominance in a wild population of electric fish. Biol Lett 7:197–200. https://doi.org/10.1098/rsbl.2010.0804

    Article  PubMed  Google Scholar 

  26. Gómez-Sena L, Pedraja F, Sanguinetti-Scheck JI, Budelli R (2014) Computational modeling of electric imaging in weakly electric fish: insights for physiology, behavior and evolution. J Physiol Paris 108:112–128

    Article  PubMed  Google Scholar 

  27. Hagedorn M, Carr C (1985) Single electrocytes produce a sexually dimorphic signal in South American electric fish, Hypopomus occidentalis (Gymnotiformes, Hypopomidae). J Comp Physiol A 156:511–523. https://doi.org/10.1007/bf00613975

    Article  Google Scholar 

  28. Hagedorn M, Zelick R (1989) Relative dominance among males is expressed in the electric organ discharge characteristics of a weakly electric fish. Anim Behav 38:520–525

    Article  Google Scholar 

  29. Hau M, Wikelski M, Soma KK, Wingfield JC (2000) Testosterone and year-round territorial aggression in a tropical bird. Gen Comp Endocrinol 117:20–33

    Article  CAS  PubMed  Google Scholar 

  30. Hau M, Stoddard ST, Soma K (2004) Territorial aggression and hormones during the non-breeding season in a tropical bird. Horm Behav 45:40–44

    Article  CAS  PubMed  Google Scholar 

  31. Hazlet BA (1968) Effects of crowding on the agonistic behavior of the hermit crab (Pagurus bernhardus). Ecology 49:573–575

    Article  Google Scholar 

  32. Hopkins CD (1972) Sex differences in electric signaling in an electric fish. Science 176:1035–1037

    Article  CAS  PubMed  Google Scholar 

  33. Hopkins CD (1974) Electric communication: functions in the social behavior of Eigenmannia virescens. Behaviour 50:270–304

    Article  Google Scholar 

  34. Huang W-S, Greene HW, Chang T-J, Shine R (2011) Territorial behavior in Taiwanese kukrisnakes (Oligodon formosanus). Proc Natl Acad Sci 108:7455–7459

    Article  PubMed  Google Scholar 

  35. Hungtinford F, Turner A (1987) Animal conflict. Chapman and Hall Ltd, London

    Google Scholar 

  36. Hupé GJ, Lewis JE (2008) Electrocommunication signals in free swimming brown ghost knifefish, Apteronotus leptorhynchus. J Exp Biol 211:1657–1667

    Article  PubMed  Google Scholar 

  37. Hupé GJ, Lewis JE, Benda J (2008) The effect of difference frequency on electrocommunication: chirp production and encoding in a species of weakly electric fish, Apteronotus leptorhynchus. J Physiol Paris 102:164–172

    Article  PubMed  Google Scholar 

  38. Jalabert C, Quintana L, Pessina P, Silva A (2015) Extra-gonadal steroids modulate non-breeding territorial aggression in weakly electric fish. Horm Behav 72:60–67. https://doi.org/10.1016/j.yhbeh.2015.05.003

    Article  CAS  PubMed  Google Scholar 

  39. Jennions MD, Backwell PRY (1996) Residency and size affect fight duration and outcome in the fiddler crab Uca annulipes. Biol J Linn Soc 57:293–306. https://doi.org/10.1111/j.1095-8312.1996.tb01851.x

    Article  Google Scholar 

  40. Jun JJ, Longtin A, Maler L (2016) Active sensing associated with spatial learning reveals memory-based attention in an electric fish. J Neurophysiol 115:2577–2592. https://doi.org/10.1152/jn.00979.2015

    Article  PubMed  PubMed Central  Google Scholar 

  41. Kaufmann JH (1983) On the definitions and functions of dominance and territoriality. Biol Rev 58:1–20

    Article  Google Scholar 

  42. King JA (1973) The ecology of aggressive behavior. Annu Rev Ecol Syst 4:117–138

    Article  Google Scholar 

  43. Knell RJ (2009) Population density and the evolution of male aggression. J Zool 278:83–90

    Article  Google Scholar 

  44. Kokko H, Rankin DJ (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Phil Trans R Soc B 361:319–334

    Article  PubMed  Google Scholar 

  45. Lissman H (1958) On the function and evolution of electric organs in fish. J Exp Biol 35:156–191

    Google Scholar 

  46. Lorenz K (1963) On aggression. Harcourt, Brace and World, New York

    Google Scholar 

  47. Maciver MA, Sharabash NM, Nelson ME (2001) Prey-capture behavior in gymnotid electric fish: motion analysis and effects of water conductivity. J Exp Biol 204:543–557

    CAS  PubMed  Google Scholar 

  48. Maher CR, Lott DF (1995) Definitions of territoriality used in the study of variation in vertebrate spacing systems. Anim Behav 49:1581–1597

    Article  Google Scholar 

  49. Maynard Smith J, Parker GA (1976) The logic of asymmetric contests. Anim Behav 24:159–175

    Article  Google Scholar 

  50. Miczek KA, de Almeida RMM, Kravitz EA, Rissman EF, de Boer SF, Raine A (2007) Neurobiology of escalated aggression and violence. J Neurosci 27:11803–11806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Morrell LJ, Kokko H (2005) Bridging the gap between mechanistic and adaptive explanations of territory formation. Behav Ecol Sociobiol 57:381–390

    Article  Google Scholar 

  52. Nelson RJ (2006) Biology of aggression. Oxford University Press, New York

    Google Scholar 

  53. Oldfield R (2011) Aggression and welfare in a common aquarium fish, the Midas cichlid. J Appl Anim Welf Sci 14:340–360

    Article  CAS  PubMed  Google Scholar 

  54. Parker GA, Rubenstein DI (1981) Role assessment, reserve strategy, and acquisition of information in asymmetric animal conflicts. Anim Behav 29:221–240

    Article  Google Scholar 

  55. Pedraja F, Aguilera P, Caputi AA, Budelli R (2014) Electric imaging through evolution, a modeling study of commonalities and differences. PLoS Comput Biol 10:e1003722. https://doi.org/10.1371/journal.pcbi.1003722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Pedraja F, Perrone R, Silva A, Budelli R (2016) Passive and active electroreception during agonistic encounters in the weakly electric fish Gymnotus omarorum. Bioinspir Biomim 11(6):065002. https://doi.org/10.1088/1748-3190/11/6/065002

    Article  PubMed  Google Scholar 

  57. Pedraja F, Hofmann V, Lucas KM, Young C, Engelmann J, Lewis JE (2018) Motion parallax in electric sensing. Proc Natl Acad Sci 115:573–577

    Article  CAS  PubMed  Google Scholar 

  58. Perrone R, Silva A (2016) Vasotocin increases dominance in the weakly electric fish Brachyhypopomus gauderio. J Physiol Paris 110:119–126

    Article  PubMed  Google Scholar 

  59. Perrone R, Silva AC (2018) Status-dependent vasotocin modulation of dominance and subordination in the weakly electric fish Gymnotus omarorum. Front Behav Neurosci 12:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Perrone R, Macadar O, Silva A (2009) Social electric signals in freely moving dyads of Brachyhypopomus pinnicaudatus. J Comp Physiol A 195:501–514

    Article  Google Scholar 

  61. Pröhl H (2005) Territorial behavior in dendrobatid frogs. J Herpetol 39:354–365

    Article  Google Scholar 

  62. Quintana L, Zubizarreta L, Jalabert C, Batista G, Perrone R, Silva A (2016) Building the case for a novel teleost model of non-breeding aggression and its neuroendocrine control. J Physiol Paris 110:224–232

    Article  PubMed  Google Scholar 

  63. Randall JA (1984) Territorial defense and advertisement by Footdrumming in Bannertail Kangaroo Rats (Dipodomys spectabilis) at high and low population densities. Behav Ecol Sociobiol 16:11–20

    Article  Google Scholar 

  64. Richer-de-Forges MM, Crampton WGR, Albert JS (2009) A new species of Gymnotus (Gymnotiformes, Gymnotidae) from Uruguay: description of a model species in neurophysiological research. Copeia 2009:538–544

    Article  Google Scholar 

  65. Roth E, Zhuang K, Stamper SA, Fortune ES, Cowan NJ (2011) Stimulus predictability mediates a switch in locomotor smooth pursuit performance for Eigenmannia virescens. J Exp Biol 214:1170–1180

    Article  PubMed  Google Scholar 

  66. Silva A, Quintana L, Galeano M, Errandonea P (2003) Biogeography and breeding in Gymnotiformes from Uruguay. Environ Biol Fish 66:329–338

    Article  Google Scholar 

  67. 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

    Article  CAS  PubMed  Google Scholar 

  68. Silva AC, Perrone R, Zubizarreta L, Batista G, Stoddard PK (2013) Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression. J Exp Biol 216:2412–2420

    Article  PubMed  Google Scholar 

  69. Sogge MK, Koronkiewicz TJ, van Riper C III, Durst S (2007) Willow flycatcher nonbreeding territory defense behavior in Costa Rica. Condor 109:475–480

    Article  Google Scholar 

  70. Stoddard P (2002) The evolutionary origins of electric signal complexity. J Physiol 96:485–491

    Google Scholar 

  71. Summers CH, Winberg S (2006) Interactions between the neural regulation of stress and aggression. J Exp Biol 209:4581–4589

    Article  CAS  PubMed  Google Scholar 

  72. Triefenbach F, Zakon H (2008) Changes in signalling during agonistic interactions between male weakly electric knifefish, Apteronotus leptorhynchus. Anim Behav 75:1263–1272

    Article  Google Scholar 

  73. Turner SP, Ewen M, Rooke JA, Edwards SA (2000) The effect of space allowance on performance, aggression and immune competence of growing pigs housed on straw deep-litter at different group sizes. Livest Sci 66:47–55

    Article  Google Scholar 

  74. Umbers KD, Osborne L, Keogh JS (2012) The effects of residency and body size on contest initiation and outcome in the territorial dragon, Ctenophorus decresii. PLoS One 7:e47143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Westby G (1975a) Further analysis of the individual discharge characteristics predicting social dominance in the electric fish. Anim Behav 23:249–260

    Article  Google Scholar 

  76. Westby GWM (1975b) Comparative studies of the aggressive behaviour of two gymnotid electric fish (Gymnotus carapo and Hypopomus artedi). Anim Behav 23:192–213

    Article  CAS  PubMed  Google Scholar 

  77. Wilson EO (1975) Sociobiology: The New Synthesis. University Press, Harvard

    Google Scholar 

  78. Wingfield JC, Hahn TP (1994) Testosterone and territorial behaviour in sedentary and migratory sparrows. Anim Behav 47:77–89. https://doi.org/10.1006/anbe.1994.1009

    Article  Google Scholar 

  79. Zakon HH, Thomas P, Yan H-Y (1991) Electric organ discharge frequency and plasma sex steroid levels during gonadal recrudescence in a natural population of the weakly electric fish Sternopygus macrurus. J Comp Physiol A 169:493–499. https://doi.org/10.1007/bf00197661

    Article  CAS  PubMed  Google Scholar 

  80. Zubizarreta L, Perrone R, Stoddard PK, Costa G, Silva AC (2012) Differential serotonergic modulation of two types of aggression in weakly electric fish. Front Behav Neurosci 6(77). https://doi.org/10.3389/fnbeh.2012.0007

  81. Zubizarreta L, Stoddard PK, Silva A (2015) Aggression levels affect social interaction in the non-breeding territorial aggression of the weakly electric fish, Gymnotus omarorum. Ethology 121:8–16

    Article  Google Scholar 

Download references

Acknowledgments

We specially thank Laura Quintana and Lucía Zubizarreta for their generous comments and suggestions to our manuscript. We are very grateful to Adriana Migliaro, Carlos Passos, Laura Quintana, Federico Reyes, and Lucía Zubizarreta for their useful discussions during the BERTA Workshop, Cerro del Toro, Piriápolis, Uruguay.

Funding

This work was supported by National Agency for Research and 50 Innovation (ANII), projects FCE 569 and FCE 4272.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ana Silva.

Ethics declarations

Electric fish collection for experimental purposes was authorized by DINARA (National Direction of Aquatic Resources) and MGAP (Ministry of Agriculture and Fisheries), resolution No. 065/2004. All experimental procedures complied with ASAP/ABS Guidelines for the Use of Animals in Research and were approved by our institutional ethical committee (Comisión Bioética, Instituto Clemente Estable, MEC, 007/05/2012).

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Perrone, R., Pedraja, F., Valiño, G. et al. Non-breeding territoriality and the effect of territory size on aggression in the weakly electric fish, Gymnotus omarorum. acta ethol 22, 79–89 (2019). https://doi.org/10.1007/s10211-019-00309-7

Download citation

Keywords

  • Territoriality
  • Agonistic behavior
  • Electric fish
  • Violence