For citation:
Olshanskiy V. M., Baron V. D., MacMahon E., Zlenko D. V. Electric fish as an object of fundamental research. Izvestiya VUZ. Applied Nonlinear Dynamics, 2023, vol. 31, iss. 6, pp. 776-812. DOI: 10.18500/0869-6632-003075, EDN: VORGFP
This is an open access article distributed under the terms of Creative Commons Attribution 4.0 International License (CC-BY 4.0).
Full text PDF(Ru):
(downloads: 0)
Full text PDF(En):
(downloads: 41)
Language:
Russian
Heading:
Article type:
Review
UDC:
530.182
EDN:
Electric fish as an object of fundamental research
Autors:
Olshanskiy Vladimir Mendelevich, A. N. Severtsov Institute of Ecology and Evolution of the RAS
Baron Vladimir Davidovich, A. N. Severtsov Institute of Ecology and Evolution of the RAS
MacMahon Eoin, Biosphere Environmental Ltd
Zlenko Dmitry Vladimirovich, Lomonosov Moscow State University
Abstract:
The aim of this work is to show the role of research on electric fish and their role in fundamental problems’ solvation. We are trying to involve additional specialists in our studies.
Methods. We have developed a setup allowing simultaneous multielectrode registration and visualization of electric fields around fish, which is a novel tool in electric fish studies.
Results. The article is a review. We tried to show the history of electric fish research and the peculiarities of the Russian school of electroecology.
Reference:
- Maxwell JC. A Treatise on Electricity and Magnetism. Vol. 1. Oxford, UK: Clarendon Press; 1873. 425 p.
- Finger S, Piccolino M. The Shocking History of Electric Fishes: From Ancient Epochs to the Birth of Modern Neurophysiology. Oxford: Oxford University Press; 2011. 496 p. DOI: 10.1093/acprof: oso/9780195366723.001.0001.
- Lissmann HW. On the function and evolution of electric organs in fish. Journal of Experimental Biology. 1958;35(1):156–191. DOI: 10.1242/jeb.35.1.156.
- Baron VD. Possible role of electroreception in the behavior of marine weakly electric rays Raja clavata (Rajidae). Sensory Systems. 1994;8(3–4):147–161 (in Russian).
- Orlov AA, Golubtsov AS, Baron VD, Pavlov DS. Bioelectric fields of the African marbled lungfish Protopterus aethiopicus (Sarcopterygii: Protopteridae), African (Heterotis niloticus) and South American silver (Osteoglossum bicirrhosum) arowanas (Actinopterygii: Osteoglossidae): Primitive electrogenesis? Journal of Ichthyology. 2015;55(6):874–879. DOI: 10.1134/S0032945215060120.
- Soh Z, Matsuno M, Yoshida M, Tsuji T. Real-time cameraless measurement system based on bioelectrical ventilatory signals to evaluate fear and anxiety. Zebrafish. 2018;15(2):133–144. DOI: 10.1089/zeb.2017.1491.
- Asano M, Hanyu I. Sensitivity to electricity in the catfish, Parasilurus asotus. Comparative Biochemistry and Physiology Part A: Physiology. 1987;86(3):485–489. DOI: 10.1016/0300- 9629(87)90530-5.
- Griffin DR. Listening in the Dark: The Acoustic Orientation of Bats and Men. New Haven CT: Yale University Press; 1958. 413 p.
- Lissmann HW. Continuous electrical signals from the tail of a fish, Gymnarchus niloticus Cuv. Nature. 1951;167(4240):201–202. DOI: 10.1038/167201a0.
- Olshanskiy VM, Zlenko DV, Orlov AA, Kasumyan AO, Moller P, MacMahon E, Xue W. Multielectrode registration of episodic discharges generated by weakly electric fishes. Izvestiya VUZ. Applied Nonlinear Dynamics. 2022;30(2):239–252. DOI: 10.18500/0869-6632-2022-30-2- 239-252.
- Zlenko DV, Olshanskiy VM, Orlov AA, Kasumyan AO, MacMahon E, Wei X, Moller P. Visualization of electric fields and associated behavior in fish and other aquatic animals. Behavior Research Methods. 2023. DOI: 10.3758/s13428-023-02175-5.
- Kuhn ТS. The Structure of Scientific Revolutions. Chicago: University of Chicago Press; 1962. 264 p.
- Maxwell JC. A Treatise On Electricity And Magnetism. Vol. 2. Oxford, UK: Clarendon Press; 1873. 444 p.
- Rosenberger F. Die geschichte der physik in grundzugen. Bd. 3. Braunschweig: F. Vieweg und Sohn; 1890. 300 s. (in German).
- Faraday M. On the character and direction of the electric force of the Gymnotus. In: Experimental Researches in Electricity. Vol. 2. London: Richard and John Edward Taylor; 1844.
- Piccolino M. The Taming of the Ray: Electric Fish Research in the Enlightenment from John Walsh to Alessandro Volta. Firence: Olschki; 2003. 221 p.
- Walsh J. Of the electric property of the torpedo. In a letter from John Walsh, Esq; F. R. S. to Benjamin Franklin, Esq; LL. D., F. R. S., Ac. R. Par. Soc. Ext., &c. Phil. Trans. R. Soc. 1773;63:461–480. DOI: 10.1098/rstl.1773.0039.
- Cavendish H. An account of some attempts to imitate the effects of the torpedo by electricity. Phil. Trans. R. Soc. 1776;66:196–225. DOI: 10.1098/rstl.1776.0013.
- Feynman R. The Character of Physical Law. United States: BBC; 1965. 173 p.
- Maxwell JC. The Electrical Researches of the Honourable Henry Cavendish. London: Frank Cass & Co.; 1879. 534 p.
- Galvani L. De Viribus Electricatitis in Motu Musculari Commentarius. Bononiae: Ex Typographia Instituti Scientiarium; 1791. 80 p. (in Latin).
- Lebedinsky AB. The role of Galvani and Volta in the history of physiology. In: Galvani A, Volta A. Selected Works on Animal Electricity. Moscow, Leningrad: Biomedgiz; 1937. P. 7–63 (in Russian).
- Piccolino M, Bresadola M. Shocking Frogs: Galvani, Volta, and the Electric Origins of Neuroscience. Oxford: Oxford University Press; 2013. 400 p. DOI: 10.1093/acprof:oso/9780199782161. 001.0001.
- Matteucci C. Electro-physiological researches – third memoir. On Induced contractions. Phil. Trans. R. Soc. 1845;135:303–317. DOI: 10.1098/rstl.1845.0013.
- Volta A. On the electricity excited by the mere contact of conducting substances of different kinds. In a letter from Mr. Alexander Volta, F. R. S. Professor of Natural Philosophy in the University of Pavia, to the Rt. Hon. Sir Joseph Banks, Bart. K.B. P. R. S. Phil. Trans. R. Soc. 1800;90:403–431. DOI: 10.1098/rstl.1800.0018.
- Faraday M. On the source of power in the voltaic pile. In: Experimental Researches in Electricity. Vol. 2. London: Richard and John Edward Taylor; 1844.
- Piccolino M. Electric fishes research in the nineteenth century, following the steps of Carlo Matteucci and Giuseppe Moruzzi. Archives Italiennes de Biologie. 2011;149(4):10–17.
- Piccolino M, Wade NJ. Carlo Matteucci (1811–1868), the “frogs pile”, and the Risorgimento of electrophysiology. Cortex. 2012;48(6):645–646. DOI: 10.1016/j.cortex.2011.08.002.
- Moruzzi G. The electrophysiological work of Carlo Matteucci. Brain Research Bulletin. 1996;40(2): 69–91. DOI: 10.1016/0361-9230(96)00036-6.
- Matteucci C. Electro-physiological researches – first memoir. The muscular current. Phil. Trans. R. Soc. 1845;135:283–295. DOI: 10.1098/rstl.1845.0011.
- Matteucci C. Electro-physiological researches – second memoir. On the proper current of the frog. Phil. Trans. R. Soc. 1845;135:297–301. DOI: 10.1098/rstl.1845.0012.
- Matteucci C. Electro-physiological researches - Fifth series. Part I. Upon induced contractions. Phil. Trans. R. Soc. 1847;137:231–237. DOI: 10.1098/rstl.1847.0013.
- Catania KC. An optimized biological taser: Electric eels remotely induce or arrest movement in nearby prey. Brain Behav. Evol. 2015;86(1):38–47. DOI: 10.1159/000435945.
- Darwin C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. 6th edition. London: Murray; 1872. 502 p.
- Robin C. Memoir sur la demonstration experimentale de la production d’electricite par un appareilpropre aux poisons du genre des raies. J. Anat. Physiol. 1865;23:577–645 (in French).
- Bennett MVL. Electric organs. Fish Physiology. 1971;5:347–491. DOI: 10.1016/S1546-5098(08) 60051-5.
- Lissmann HW, Machin KE. The mechanism of object location in Gymnarchus Niloticus and similar fish. Journal of Experimental Biology. 1958;35(2):451–486. DOI: 10.1242/jeb.35.2.451.
- Olshanskiy VM. Body-sized electric eye. Science and Life. 2005;11:94–104 (in Russian).
- Lissmann HW, Machin KE. Electric receptors in a non-electric fish (Clarias). Nature. 1963;199: 88–89. DOI: 10.1038/199088a0.
- Bullock TH, Bodznick DA, Northcutt RG. The phylogenetic distribution of electroreception: Evidence for convergent evolution of a primitive vertebrate sense modality. Brain Research Reviews. 1983;6(1):25–46. DOI: 10.1016/0165-0173(83)90003-6.
- Protasov VR, Bondarchuk AI, Olshanskiy VM. Introduction to Electroecology. Moscow: Nauka; 1982. 336 p. (in Russian).
- Lissmann HW. Electric location by fishes. Scientific American. 1963;208(3):50–59.
- Chagas C, Paes de Carvalho A, editors. Bioelectrogenesis. Amsterdam: Elsevier; 1961. 413 p.
- Bass AH. Electric organs revisited: Evolution of a vertebrate communication and orientation organ. In: Bullock TH, Heiligenberg W, editors. Electroreception. New York: Wiley; 1986. P. 13–70.
- Hagedorn M, Womble M, Finger TE. Synodontid catfish: A new group of weakly electric fish: Behavior and anatomy. Brain Behav. Evol. 1990;35(5):268–277. DOI: 10.1159/000115873.
- Boyle KS, Colleye O, Parmentier E. Sound production to electric discharge: sonic muscle evolution in progress in Synodontis spp. catfishes (Mochokidae). Proc. R. Soc. B. 2014;281(1791):20141197. DOI: 10.1098/rspb.2014.1197.
- Kever L, Parmentier E, Bass AH, Chagnaud BP. Morphological diversity of acoustic and electric communication systems of mochokid catfish. The Journal of Comparative Neurology. 2021;529(8):1787–1809. DOI: 10.1002/cne.25057.
- Baron VD. Electric Power Generating Systems of Fish: Evolution and Adaptation Mechanisms. Moscow: Nauka; 1982. 112 p. (in Russian).
- Baron VD. Electric discharges of two species of stargazers from the South China Sea (Urano-scopidae, Perciformes). Journal of Ichthyology. 2009;49(11):1065–1072. DOI: 10.1134/S0032945 209110058.
- Bullock TH. General introduction. In: Fessard A, editor. Electroreceptors and Other Specialized Receptors in Lower Vertrebrates. Vol. 3/3 of Handbook of Sensory Physiology. Berlin, Heidelberg: Springer; 1974. P. 1–12. DOI: 10.1007/978-3-642-65926-3_1.
- Hopkins CD. Evolution of electric communication channels of mormyrids. Behav. Ecol. Sociobiol. 1980;7(1):1–13. DOI: 10.1007/BF00302513.
- Hopkins CD. The neuroethology of electric communication. Trends Neurosci. 1981;4:4–6. DOI: 10.1016/0166-2236(81)90003-5.
- Hopkins CD. On the diversity of electric signals in a community of mormyrid electric fish in West Africa. American Zoologist. 1981;21(1):211–222. DOI: 10.1093/icb/21.1.211.
- Hopkins CD. Behavior of mormyridae. In: Bullock TH, Heiligenberg W, editors. Electroreception. New York: Wiley; 1986. P. 527–576.
- Hopkins CD, Bass AH. Temporal coding of species recognition signals in an electric fish. Science. 1981;212(4490):85–87. DOI: 10.1126/science.7209524.
- Heiligenberg W, Bastian J. The electric sense of weakly electric fish. Annu. Rev. Physiol. 1984;46:561–583. DOI: 10.1146/annurev.ph.46.030184.003021.
- Russel CJ, Meyers JP, Bell CC. The echo response in Gnathonemus petersii (Mormyridae). J. Comp. Physiol. 1974;92(2):181–200. DOI: 10.1007/BF00694505.
- Dye JS, Meyer JH. Central control of the electric organ discharge in weakly electric fish. In: Bullock TH, Heiligenberg W, editors. Electroreception. New York: Wiley; 1986. P. 71–102.
- Kalmijn AJ. The detection of electric fields from inanimate and animate sources other than electric organs. In: Fessard A, editor. Electroreceptors and Other Specialized Receptors in Lower Vertrebrates. Vol. 3/3 of Handbook of Sensory Physiology. Berlin, Heidelberg: Springer; 1974. P. 147–200. DOI: 10.1007/978-3-642-65926-3_5.
- Kalmijn AJ. Electric and magnetic field detection in elasmobranch fishes. Science. 1982;218(4575): 916–918. DOI: 10.1126/science.7134985.
- Zakon HH. The electroreceptive periphery. In: Bullock TH, Heiligenberg W, editors. Electroreception. New York: Wiley; 1986. P. 103–156.
- Brown GR, Ilyinsky OB. Physiology of Electroreceptors. Leningrad: Nauka; 1984. 248 p. (in Russian).
- Moller P. Electric Fishes: History and Behavior. Dordrecht: Springer; 1995. 584 p.
- Baron VD. In memory of W. Heiligenberg. Russian Journal of Physiology. 2014;100:891–895 (in Russian).
- Bullock TH, Heiligenberg W. Electroreception. New York: Wiley; 1986. 722 p.
- Srivastava CBL, Prasad MS. Tuberous organs in a non-eletric teleosts Rita rita (Ham.). Proc. Natl. Acad. Sci. India B. 1984;54(3):187–188.
- Heiligenberg W. Electrolocation of objects in the electric fish Eigenmannia (Rhamphichthyidae, Gymnotoidei). J. Comp. Physiol. 1973;87(2):137–164. DOI: 10.1007/BF01352158.
- Heiligenberg W. Electrolocation and jamming avoidance in a Hypopygus (Rhamphichthyidae, Gymnotoidei), an electric fish with pulse-type discharges. J. Comp. Physiol. 1974;91(3):223–240. DOI: 10.1007/BF00698054.
- Heiligenberg W. Electrolocation and jamming avoidance in the electric fish Gymnarchus niloticus (Gymnarchidae, Mormyriformes). J. Comp. Physiol. 1975;103(1):55–67. DOI: 10.1007/BF013 80044.
- Heiligenberg W. Electrolocation and jamming avoidance in the mormyrid fish Brienomyrus. J. Comp. Physiol. 1976;109(3):357–372. DOI: 10.1007/BF00663615.
- Scheich H, Bullock TH. The detection of electric fields from electric organs. In: Fessard A, editor. Electroreceptors and Other Specialized Receptors in Lower Vertrebrates. Vol. 3/3 of Handbook of Sensory Physiology. Berlin, Heidelberg: Springer; 1974. P. 201–256. DOI: 10.1007/978-3-642- 65926-3_6.
- Heiligenberg W. Principles of Electrolocation and Jamming Avoidance in Electric Fish: A Neuroethological Approach. Berlin, Heidelberg: Springer; 1977. 88 p. DOI: 10.1007/978-3-642-81161-6.
- Heiligenberg W. Jamming avoidance responses: model systems for neuroethology. In: Bullock TH, Heiligenberg W, editors. Electroreception. New York: Wiley; 1986. P. 613–650.
- Olshanskiy VM. Bionic Modeling of Electrical Systems of Weakly Electric Fish. Moscow: Nauka; 1990. 208 p. (in Russian).
- Westby GWM. Electric communication in fish and the problem of recognizing very brief waveforms. Journal of Biological Education. 1987;21(3):190–196. DOI: 10.1080/00219266.1987. 9654895.
- Schumacher EL, Carlson BA. Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes. eLife. 2022;11:e74159. DOI: 10.7554/eLife.74159.
- Huang CG, Metzen MG, Chacron MJ. Descending pathways mediate adaptive optimized coding of natural stimuli in weakly electric fish. Sci. Adv. 2019;5(10):eaax2211. DOI: 10.1126/sciadv.aax2211.
- Nelson ME. Electric fish. Curr. Biol. 2011;21(14):R528–R529. DOI: 10.1016/j.cub.2011.03.045.
- Mikhailenko NA. On the biological significance of electrical discharges in weakly electric fish species of the Black Sea. Zoological Journal. 1971;50:1347–1356 (in Russian).
- Baron VD, Mikhailenko NA. Uranoscopus scaber: Transitional form in the evolution of electrical organs in fish. Proceedings of the Academy of Sciences of the USSR. 1976;229(4):983–986 (in Russian).
- Baron VD, Mikhailenko NA. Electrical discharge structure of the sea-fox. Biophysics. 1974;22(2): 369–371.
- Orlov AA, Baron VD, Olshanskiy VM. Electric generating activity of Synodontis and its changes under the action of weak electric fields. Proceedings of the Russian Academy of Sciences. 1993;332(1):110–113 (in Russian).
- Baron VD, Morshnev KS, Olshansky VM, Orlov AA. Electric organ discharges of two species of African catfish (Synodontis) during social behaviour. Anim. Behav. 1994;48(6):1472–1475. DOI: 10.1006/anbe.1994.1387.
- Baron VD, Orlov AA, Golubtsov AS. African Clarias catfish elicits long-lasting weak electric pulses. Experientia. 1994;50(7):664–647. DOI: 10.1007/BF01952864.
- Olshanskii VM, Soldatova OA, Nguyen TN. Episodic electric discharges in the course of social interactions: An example of Asian clariid catfish. Biology Bulletin Reviews. 2011;72(3):220–235 (in Russian).
- Olshanskiy VM, Kasumyan AO, Moller P. On mating and function of associated electric pulses in Clarias macrocephalus (Gunther 1864): probing an old puzzle, first posed by Charles Darwin. Environmental Biology of Fishes. 2020;103(1):99–114. DOI: 10.1007/s10641-019-00936-w.
- Olshansky VM. Elaboration of equipment and methods of continuous recording of electric activity of clariid catfish (Clariidae, Siluriformes) in social and reproductive behavior. Journal of Ichthyology. 2010;50(11):1077–1091. DOI: 10.1134/S0032945210110147.
- Orlov AA, Baron VD, Golubtsov AS. Electric discharges of two African catfishes of the genus Auchenoglanis (Claroteidae, Siluriformes). Doklady Biological Sciences. 2015;462(1):138–140. DOI: 10.1134/S0012496615030059.
- Baron VD, Pavlov DS. Discovery of specialized electrogenerating activity in two species of Polypterus (Polypteriformes, Osteichthyes). Journal of Ichthyology. 2003;43(Suppl. 2):S259–S261.
- Morshnev KS, Olshanskiy VM. Electrical discharges of Asian catfish Ompok bimaculatus (Siluridae). Proceedings of the Russian Academy of Sciences. 1997;354(3):419–422 (in Russian).
- Baron VD, Olshansky VM. Monopolar electric discharges of the catfish Parasilurus asotus (Siluridae, Siluriformes). Journal of Ichthyology. 2009;49(5):403–408. DOI: 10.1134/S003294 5209050063.
- Olshanskii VM, Baron VD, Wei X. Electrical discharges in Chinese salamander Andrias davidianus. Doklady Biochemistry and Biophysics. 2016;471(1):447–449. DOI: 10.1134/S1607672916060193.
- Dunlap KD, Koukos HM, Chagnaud BP, Zakon HH, Bass AH. Vocal and electric fish: Revisiting a comparison of two teleost models in the neuroethology of social behavior. Frontiers in Neural Circuits. 2021;15:713105. DOI: 10.3389/fncir.2021.713105.
- Mashkin PV, Olshansky VM, Volkov SV, Uteshev VK, Wei X. Continuous biological monitoring of water quality in rivers and seas using biosensors: Bivalve mollusks. In: Topical Issues of Zoology, Ecology and Nature Conservation. Vol. 5. Moscow: «Sel’skohozyajstvennye Tekhnologii»; 2023. P. 133–138 (in Russian).
- Tomasello DL, Sive H. Noninvasive multielectrode array for brain and spinal cord local field potential recordings from live zebrafish larvae. Zebrafish. 2020;17(4):271–277. DOI: 10.1089/zeb. 2020.1874.
Received:
31.07.2023
Accepted:
13.09.2023
Available online:
13.11.2023
Published:
30.11.2023
Journal issue:
- 697 reads