Proceedings of the Royal Society B: Biological Sciences
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Electroreception in the Guiana dolphin (Sotalia guianensis)

Nicole U. Czech-Damal

Nicole U. Czech-Damal

Biocenter Grindel and Zoological Museum, University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany

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Alexander Liebschner

Alexander Liebschner

German Federal Agency for Nature Conservation, Marine and Coastal Nature Conservation Unit, Isle of Vilm–Branch Office, 18581 Putbus, Rügen, Germany

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,
Lars Miersch

Lars Miersch

Institute for Biosciences, University of Rostock, Albert-Einstein-Strasse 3, 18059 Rostock, Germany

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Gertrud Klauer

Gertrud Klauer

Department of Cellular and Molecular Anatomy (Anatomy III), J.W. Goethe-University, Theodor-Stern-Kai 7, 60590 Frankfurt, Germany

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Frederike D. Hanke

Frederike D. Hanke

Institute for Biosciences, University of Rostock, Albert-Einstein-Strasse 3, 18059 Rostock, Germany

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Christopher Marshall

Christopher Marshall

Department of Marine Biology, Texas A&M University, 5007 Avenue U, Galveston, TX 77551-5923, USA

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Guido Dehnhardt

Guido Dehnhardt

Institute for Biosciences, University of Rostock, Albert-Einstein-Strasse 3, 18059 Rostock, Germany

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Wolf Hanke

Wolf Hanke

Institute for Biosciences, University of Rostock, Albert-Einstein-Strasse 3, 18059 Rostock, Germany

[email protected]

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    Passive electroreception is a widespread sense in fishes and amphibians, but in mammals this sensory ability has previously only been shown in monotremes. While the electroreceptors in fish and amphibians evolved from mechanosensory lateral line organs, those of monotremes are based on cutaneous glands innervated by trigeminal nerves. Electroreceptors evolved from other structures or in other taxa were unknown to date. Here we show that the hairless vibrissal crypts on the rostrum of the Guiana dolphin (Sotalia guianensis), structures originally associated with the mammalian whiskers, serve as electroreceptors. Histological investigations revealed that the vibrissal crypts possess a well-innervated ampullary structure reminiscent of ampullary electroreceptors in other species. Psychophysical experiments with a male Guiana dolphin determined a sensory detection threshold for weak electric fields of 4.6 µV cm−1, which is comparable to the sensitivity of electroreceptors in platypuses. Our results show that electroreceptors can evolve from a mechanosensory organ that nearly all mammals possess and suggest the discovery of this kind of electroreception in more species, especially those with an aquatic or semi-aquatic lifestyle.

    References

    • 1
      Thewissen J. G. M.& Nummela S.. 2008 Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. Berkeley, CA: University of California Press. CrossrefGoogle Scholar
    • 2
      Collin S. P.& Marshall N. J.. 2003 Sensory processing in aquatic environments. New York, NY: Springer. CrossrefGoogle Scholar
    • 3
      Lissmann H. W.. 1951 Continuous electrical signals from the tail of a fish, Gymnarchus niloticus. Nature 167, 201–202.doi:10.1038/167201a0 (doi:10.1038/167201a0). Crossref, PubMed, ISIGoogle Scholar
    • 4
      von der Emde G.. 2006 Non-visual environmental imaging and object detection through active electrolocation in weakly electric fish. J. Comp. Physiol. A 192, 601–612.doi:10.1007/s00359-006-0096-7 (doi:10.1007/s00359-006-0096-7). Crossref, ISIGoogle Scholar
    • 5
      Collin S. P.& Whitehead D.. 2004 The functional roles of passive electroreception in non-electric fishes. Anim. Biol. 54, 1–25.doi:10.1163/157075604323010024 (doi:10.1163/157075604323010024). Crossref, ISIGoogle Scholar
    • 6
      Fritzsch B., Wahnschaffe U., Decaprona M. D. C.& Himstedt W.. 1985 Anatomical evidence for electroreception in larval Ichthyophis kohtaoensis. Naturwissenschaften 72, 102–104.doi:10.1007/BF00508148 (doi:10.1007/BF00508148). Crossref, ISIGoogle Scholar
    • 7
      Münz H., Claas B.& Fritzsch B.. 1982 Electro-physiological evidence of electroreception in the axolotl Siredon mexicanum. Neurosci. Lett. 28, 107–111.doi:10.1016/0304-3940(82)90216-6 (doi:10.1016/0304-3940(82)90216-6). Crossref, PubMed, ISIGoogle Scholar
    • 8
      Proske U., Gregory J. E.& Iggo A.. 1998 Sensory receptors in monotremes. Phil. Trans. R. Soc. Lond. B 353, 1187–1198.doi:10.1098/rstb.1998.0275 (doi:10.1098/rstb.1998.0275). Link, ISIGoogle Scholar
    • 9
      Scheich H., Langner G., Tidemann C., Coles R. B.& Guppy A.. 1986 Electroreception and electrolocation in platypus. Nature 319, 401–402.doi:10.1038/319401a0 (doi:10.1038/319401a0). Crossref, PubMed, ISIGoogle Scholar
    • 10
      Gregory J. E., Iggo A., McIntyre A. K.& Proske U.. 1989 Responses of electroreceptors in the snout of the echidna. J. Physiol. Lond. 414, 521–538. CrossrefGoogle Scholar
    • 11
      Dehnhardt G., Mauck B.& Bleckmann H.. 1998 Seal whiskers detect water movements. Nature 394, 235–236.doi:10.1038/28303 (doi:10.1038/28303). Crossref, ISIGoogle Scholar
    • 12
      Dehnhardt G., Mauck B., Hanke W.& Bleckmann H.. 2001 Hydrodynamic trail following in harbor seals (Phoca vitulina). Science 293, 102–104.doi:10.1126/science.1060514 (doi:10.1126/science.1060514). Crossref, PubMed, ISIGoogle Scholar
    • 13
      Rice F. L., Mance A.& Munger B. L.. 1986 A comparative light microscopical analysis of the sensory innervation of the mysticial pad. 1. Innervation of vibrissal follicle-sinus complexes. J. Comp. Neurol. 252, 154–174.doi:10.1002/cne.902520203 (doi:10.1002/cne.902520203). Crossref, PubMed, ISIGoogle Scholar
    • 14
      Hyvärinen H., Palviainen A., Strandberg U.& Holopainen I. J.. 2009 Aquatic environment and differentiation of vibrissae: comparison of sinus hair systems of ringed seal, otter and pole cat. Brain Behav. Evol. 74, 268–279.doi:10.1159/000264662 (doi:10.1159/000264662). Crossref, PubMed, ISIGoogle Scholar
    • 15
      Ling J. K.. 1977 Vibrissae of marine mammals. Functional anatomy of marine mammals (ed. & Harrison R. J.), pp. 387–415. London, UK: Academic Press. Google Scholar
    • 16
      Yablokov A. V.& Klezeval G. A.. 1969 Whiskers of whales and seals and their distribution, structure and significance. Morphological characteristics of aquatic mammals (ed. & Kleinenberg S. E.), pp. 48–81. Moscow, Russia: Izdatel'stvo Nauka. Google Scholar
    • 17
      Mauck B., Eysel U.& Dehnhardt G.. 2000 Selective heating of vibrissal follicles in seals (Phoca vitulina) and dolphins (Sotalia fluviatilis guianensis). J. Exp. Biol. 203, 2125–2131. Crossref, PubMed, ISIGoogle Scholar
    • 18
      Goldner J.. 1938 A modification of the Masson trichrome technique for routine laboratory purpose. Am. J. Pathol. 14, 237–243. PubMedGoogle Scholar
    • 19
      Spaethe A.. 1984 Eine Modifikation der Silbermethode nach Richardson für die Axonfärbung von Paraffinschnitten. Verhandlungen der Anatomischen Gesellschaft 78, 101–102. Google Scholar
    • 20
      Borobia M.& Barros N. B.. 1989 Notes on the diet of marine Sotalia fluviatilis. Mar. Mamm. Sci. 5, 395–399.doi:10.1111/j.1748-7692.1989.tb00353.x (doi:10.1111/j.1748-7692.1989.tb00353.x). Crossref, ISIGoogle Scholar
    • 21
      Araujo Pansard K. C., de Castro Bezerra Gurgel H., de Araujo Andrade L. C.& Yamamoto M. E. In press. Feeding ecology of the estuarine dolphin (Sotalia guianensis) on the coast of Rio Grande do Norte, Brazil. Mar. Mamm. Sci. (doi:10.1111/j.1748-7692.2010.00436.x). ISIGoogle Scholar
    • 22
      Gescheider G. A.. 1976 Psychophysics: method and theory. Hillsdale, NJ: Lawrence Erlbaum Associates. Google Scholar
    • 23
      Manger P. R.& Pettigrew J. D.. 1995 Electroreception and the feeding behavior of platypus (Ornithorhynchus anatinus, Monotremata, Mammalia). Phil. Trans. R. Soc. Lond. B 347, 359–381.doi:10.1098/rstb.1995.0030 (doi:10.1098/rstb.1995.0030). Link, ISIGoogle Scholar
    • 24
      Hyvärinen H.& Katajisto H.. 1984 Functional structure of the vibrissae of the ringed seal (Phoca hispida). Acta Zool. Fennica 171, 27–30. Google Scholar
    • 25
      Hyvärinen H.. 1995 Structure and function of the vibrissae of the ringed seal (Phoca hispida). Sensory systems of aquatic mammals (eds , Kastelein R. A., Thomas J. A.& Nachtigall P. E.), pp. 429–445. Woerden, The Netherlands: De Spil Publishers. Google Scholar
    • 26
      Marshall C. D., Amin H., Kovacs K. M.& Lydersen C.. 2006 Microstructure and innervation of the mystacial vibrissal follicle-sinus complex in bearded seals, Erignathus barbatus (Pinnipedia: Phocidae). Anat. Rec. A 288A, 13–25.doi:10.1002/ar.a.20273 (doi:10.1002/ar.a.20273). CrossrefGoogle Scholar
    • 27
      Halata Z.& Munger B. L.. 1980 Sensory nerve-endings in rhesus-monkey sinus hairs. J. Comp. Neurol. 192, 645–663.doi:10.1002/cne.901920403 (doi:10.1002/cne.901920403). Crossref, PubMed, ISIGoogle Scholar
    • 28
      Halata Z.. 1975 The mechanoreceptors of the mammalian skin: ultrastructure and morphological classification. Adv. Anat. Embryol. Cell Biol. 50, 3–77. PubMedGoogle Scholar
    • 29
      Rice F. L., Fundin B. T., Arvidsson J., Aldskogius H.& Johansson O.. 1997 Comprehensive immunofluorescence and lectin binding analysis of vibrissal follicle sinus complex innervation in the mystacial pad of the rat. J. Comp. Neurol. 385, 149–184.doi:10.1002/(SICI)1096-9861(19970825)385:2<149::AID-CNE1>3.0.CO;2-1 (doi:10.1002/(SICI)1096-9861(19970825)385:2<149::AID-CNE1>3.0.CO;2-1). Crossref, PubMed, ISIGoogle Scholar
    • 30
      Andres K. H.& von Düring M.. 1988 Comparative anatomy of vertebrate electroreceptors. Prog. Brain Res. 74, 113–131.doi:10.1016/S0079-6123(08)63006-X (doi:10.1016/S0079-6123(08)63006-X). Crossref, PubMedGoogle Scholar
    • 31
      Andres K. H.& von Düring M.. 1984 The platypus bill. A structural and functional model of a pattern-like arrangement of different cutaneous sensory receptors. Sensory receptor mechanisms (eds , Hamann W.& Iggo A.), pp. 81–89. Singapore: World Scientific Publishing Co. Google Scholar
    • 32
      New J. G.. 1997 The evolution of vertebrate electrosensory systems. Brain Behav. Evol. 50, 244–252.doi:10.1159/000113338 (doi:10.1159/000113338). Crossref, PubMed, ISIGoogle Scholar
    • 33
      von der Emde G.. 1998 Electroreception. The physiology of fishes (ed. & Evans D. H.), pp. 313–343. Boca Raton, FL: CRC Press. Google Scholar
    • 34
      Bullock T. H.. 1999 The future of research on electroreception and electrocommunication. J. Exp. Biol. 202, 1455–1458. Crossref, PubMed, ISIGoogle Scholar
    • 35
      Alves-Gomes J. A.. 2001 The evolution of electroreception and bioelectrogenesis in teleost fish: a phylogenetic perspective. J. Fish. Biol. 58, 1489–1511.doi:10.1006/jfbi.2001.1625 (doi:10.1006/jfbi.2001.1625). Crossref, ISIGoogle Scholar
    • 36
      Brown B. R., Hutchison J. C., Hughes M. E., Kellogg D. R.& Murray R. W.. 2002 Electrical characterization of gel collected from shark electrosensors. Phys. Rev. E 65, 061903.doi:10.1103/PhysRevE.65.061903 (doi:10.1103/PhysRevE.65.061903). Crossref, ISIGoogle Scholar
    • 37
      Manger P. R., Pettigrew J. D., Keast J. R.& Bauer A.. 1995 Nerve terminals of mucous gland electroreceptors in the platypus. Proc. R. Soc. Lond. B 260, 13–19.doi:10.1098/rspb.1995.0053 (doi:10.1098/rspb.1995.0053). Link, ISIGoogle Scholar
    • 38
      Baum C., Meyer W., Roessner D., Siebers D.& Fleischer L.-G.. 2001 A zymogel enhances the self-cleaning abilities of the skin of the pilot whale (Globicephala melas). Comp. Biochem. Physiol. A-Mol. Integr. Physiol. 130, 835–847.doi:10.1016/S1095-6433(01)00445-7 (doi:10.1016/S1095-6433(01)00445-7). Crossref, PubMed, ISIGoogle Scholar
    • 39
      Baum C., Stelzer R., Meyer W., Siebers D.& Fleischer L.-G.. 2000 A cryo-scanning microscopy study of the skin surface of the pilot whale Globicephala melas. Aquat. Mamm. 26, 7–16. Google Scholar
    • 40
      Gregory J. E., Iggo A., McIntyre A. K.& Proske U.. 1987 Electroreceptors in the platypus. Nature 326, 386–387.doi:10.1038/326386a0 (doi:10.1038/326386a0). Crossref, PubMed, ISIGoogle Scholar
    • 41
      Peters R. C., Eeuwes L. B. M.& Bretschneider F.. 2007 On the electrodetection threshold of aquatic vertebrates with ampullary or mucous gland electroreceptor organs. Biol. Rev. 82, 361–373.doi:10.1111/j.1469-185X.2007.00015.x (doi:10.1111/j.1469-185X.2007.00015.x). Crossref, PubMed, ISIGoogle Scholar
    • 42
      Taylor N. G., Manger P. R., Pettigrew J. D.& Hall L. S.. 1992 Electromyogenic potentials of a variety of platypus prey items: an amplitude and frequency analysis. Platypus and echidnas (ed. & Augee M. L.), pp. 216–224. Mosman, Australia: The Royal Zoological Society of New South Wales. Google Scholar
    • 43
      Kalmijn A. J.. 1966 Electro-perception in sharks and rays. Nature 212, 1232–1234.doi:10.1038/2121232b0 (doi:10.1038/2121232b0). Crossref, ISIGoogle Scholar
    • 44
      Manger P. R.& Pettigrew J. D.. 1996 Ultrastructure, number, distribution and innervation of electroreceptors and mechanoreceptors in the bill skin of the platypus, Ornithorhynchus anatinus. Brain Behav. Evol. 48, 27–54.doi:10.1159/000113185 (doi:10.1159/000113185). Crossref, PubMed, ISIGoogle Scholar
    • 45
      Rossi-Santos M. R.& Wedekin L. L.. 2006 Evidence of bottom contact behavior by estuarine dolphins (Sotalia guianensis) on the eastern coast of Brazil. Aquat. Mamm. 32, 140–144.doi:10.1578/AM.32.2.2006.140 (doi:10.1578/AM.32.2.2006.140). CrossrefGoogle Scholar
    • 46
      de Gurjao L. M., de Antrade Furtado Neto M. A., dos Santos R. A.& Cascon P. Feeding habits of marine tucuxi, Sotalia fluviatilis, at Ceara State, northeastern Brasil. Lat. Am. J. Aquat. Mamm. 2, 117–122. Google Scholar
    • 47
      Di Beneditto A. P. M.& Ramos R. M. A.. 2004 Biology of the marine tucuxi dolphin (Sotalia fluviatilis) in south-eastern Brazil. J. Mar. Biol. Assoc. UK 84, 1245–1250.doi:10.1017/S0025315404010744h (doi:10.1017/S0025315404010744h). Crossref, ISIGoogle Scholar
    • 48
      Di Beneditto A. P. M.& Siciliano S.. 2007 Stomach contents of the marine tucuxi dolphin (Sotalia guianensis) from Rio de Janeiro, south-eastern Brazil. J. Mar. Biol. Assoc. UK 87, 253–254.doi:10.1017/S0025315407053647 (doi:10.1017/S0025315407053647). Crossref, ISIGoogle Scholar
    • 49
      Silva F. J. D., Porpino K. D., Firmino A. S. L., de Oliveira I. T. G.& Simoes-Lopes P. C.. 2010 Bone alterations caused by a sting ray spine in the vertebra of Sotalia guianensis (Cetacea, Delphinidae). Mar. Mamm. Sci. 26, 234–238.doi:10.1111/j.1748-7692.2009.00312.x (doi:10.1111/j.1748-7692.2009.00312.x). Crossref, ISIGoogle Scholar
    • 50
      Rossbach K. A.& Herzing D. L.. 1997 Underwater observations of benthic-feeding bottlenose dolphins (Tursiops truncatus) near Grand Bahama Island, Bahamas. Mar. Mamm. Sci. 13, 498–504.doi:10.1111/j.1748-7692.1997.tb00658.x (doi:10.1111/j.1748-7692.1997.tb00658.x). Crossref, ISIGoogle Scholar
    • 51
      de Moura J. F., Sholl T. G. C., da Silva Rodrigues E., Hacon S.& Siciliano S.. 2009 Marine tucuxi dolphin (Sotalia guianensis) and its interaction with passive gill-net fisheries along the northern coast of the Rio de Janeiro State, Brazil. Mar. Biodivers. Rec. 2, 1–4.doi:10.1017/S1755267208000018 (doi:10.1017/S1755267208000018). CrossrefGoogle Scholar