Abstract
Sharks and rays have a long evolutionary history as major predators in marine ecosystems, but the biological functions and selective pressures that shape the evolution of their ampullary electrosensory system are poorly known. The ampulla of Lorenzini is the functional electrosensory unit that consists of a small subdermal ampulla and a canal that projects to a surface pore on the head or pectoral fins. The sensory epithelium of the ampulla wall detects differences between the potential at the skin pore and internal potential of the animal, and stimulates neural transmission of information about the physical features of an external field to the brain. Natural weak electric stimuli include polar fields from bioelectric sources and induced fields from physical sources in the environment. Neurophysiological studies show that the ampullary electrosense responds to electric field gradients as low as 20 nV/cm, and behav- ioral studies show responses to gradients of 1-5 nV/cm. Elasmobranch fishes show behavioral responses to bioelectric stimuli produced by natural prey, mates, consexuals and potential predators. Numerous models exist for electrosensory navigation, but they remain to be rigorously tested. Recent work shows age-dependent changes in the response properties of the electrosense among embryo, juvenile and adult stages and are proposed to reflect ontogenetic adaptations to their changing environments. In addition, the electrosense response properties are seasonally modified by the periodic expression of gonadal steroids and may serve important modulation of sensory function during reproductive behaviors. Future work should continue to investigate different biological contexts in which the electrosense is used by elasmobranch fishes, and to test the selective forces that may have shaped the evolution of this remark- able sensory system.
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References
Andrianov G.N., Broun G.R., Ilyinsky O.B., Muraveiko V.M. (1984) Frequency characteristics of skate electroreceptive central neurons responding to electric and magnetic stimulation, Neurophysiology 16: 365–376.
Arnold A.E, Gorski R.A. (1984) Gonadal steroid induction of structural sex differences in the central nervous system, Annual Rev. Neuroci. 7: 413–442.
Bennett, M.V.L, Clussin W.T. (1977) Physiology of the ampulla of Lorenzini, the electroreceptor of elasmobranchs, in: Sensory biology of sharks, skates and rays, Hodgson E.S., Mathewson R.R. (Eds.) Office of Naval Research, Arlington, Virginia, pp. 483–506.
Blonder B.I., Alevizon W.S. (1988) Prey discrimination and electroreception in the stingray Dasyatis sabina, Copeia 1988: 33–36.
Bratton B.O., Ayers J.L. (1987) Observations on the electric discharge of two skate species (Chondrichthyes: Rajidae) and its relationship to behavior, Environ. Biol. Fishes 20: 241–254.
Bullock T.H., Heligenberg W. (1986) Electroreception, John Wiley and Sons, New York.
Cox D.L., Koob T.J. (1993) Prédation on elasmobranch eggs, Environ. Biol. Fishes 38: 117–125.
Haine O.S., Ridd P.V., Rowe R.J. (2001) Range of electrosensory detection of prey by Carcharhinus melanopterus and Himantura granulata, Mar. Freswater Res. 52: 291–296.
Kajiura S.M., Holland K.N. (2002) Electroreception in juvenile scalloped hammerhead and sandbar sharks, J. Exp. Biol. 205: 3609–3621.
Kajiura S.M., Sebastian, A., Tricas T.C. (2000) Dermal bite wounds as indicators of reproductive seasonality and behaviour in the Atlantic stingray, Dasyatis sabina, Environ. Biol. Fishes: 58: 23–31.
Kalmijn A.J. (1971) The electric sense of sharks and rays, J. Exp. Biol. 55: 371–383.
Kalmijn A.J. (1974) The detection of electric fields from inanimate and animate sources other than electric organs, in: Handbook of Sensory Physiology (Vol. 3), Fessard A. (Ed.) Springer-Verlag, New York, pp. 147–200.
Kalmijn A.J. (1981) Biophysics of geomagnetic field detection, IEEE Trans. Magnetics MAG 17: 1113–1124.
Kalmijn A.J. (1982) Electric and magnetic field detection in elasmobranch fishes, Science 218: 916–918.
Kalmijn A.J. (1984) Theory of electromagnetic orientation: a further analysis, in: Comparative Physiology of Sensory Systems, Bolis A., Keynes R.D., Madrell S.H.P. (Eds.) Cambridge University Press, Cambridge, pp. 525–559.
Kalmijn A.J. (1988) Detection of weak electric fields, in: Sensory Biology of Aquatic Animals. Atema J., Fay R.R., Popper A.N., Tavolga W.N. (Eds.) Springer-Verlag, New York, pp. 151–186.
Kelly M.J. (1982) Electrical effects of steroids in neurons, in: Hormonally active brain peptides, McKerns K.W., Pantic B. (Eds.) Plenum Press, New York, pp. 253–265.
Klimley A.P. (1993) Highly directional swimming by scalloped hammerhead sharks, Sphyrna leweni and subsurface irradiance, temperature, bathymetry, and geomagnetic field, Mar. Biol. 117: 1–22.
Lowe C.G., Bray R.N., Nelson D.R. (1994) Feeding and associated electrical behavior of the Pacific electric ray Torpedo californica in the field, Mar. Biol. 120: 161–169.
Luer C.A., Gilbert PW. (1985) Mating behavior, egg deposition, incubation period, and hatching in the clearnose skate, Raja eglanteria, Environ. Biol. Fishes 13: 161–171.
Maruska K.P, Cowie E.G., Tricas T.C. (1996) Periodic gonadal activity and protracted mating in elasmobranch fishes, J. Exp. Zool. 276: 219–232.
Mikhailenko N.A. (1971) Biological significance and dynamics of electrical discharges in weak electric fishes of the Black Sea (in Russian), Zool. Zh. 50: 1347–1352.
Montgomery J.C. (1984) Frequency response characteristics of primary and secondary neurons in the electrosensory neurons in the electrosensory system of the thornback ray, Comp. Biochem. Physiol. 79A: 189–195.
Montgomery J.C, Bodznick D. (1993) Hindbrain circuitry mediating common-mode suppression of ventilatory reafference in the electrosensory system of the little skate, Raja erinacea, J. Exp. Biol. 183: 203–315.
Mortenson J., Whitaker R.H. (1973) Electrical discharges in free swimming female winter skates (Raja ocellata), Am Zool. 13: 1266.
Murray R.W., Potts T.W. (1961) The composition of the endolymph and other fluids of elasmobranchs, Comp. Biochem. Physio. 2: 65–75.
Murray R.W. (1962) The response of the ampullae of Lorenzini in elasmobranchs to electrical stimulation, J. Exp. Biol. 39: 119–128.
New J.G. (1990) Medullary electrosensory processing in the little skate. I. Response characteristics of neurons in the dorsal octavolateralis nucleus, J. Comp. Physiol. A 167: 285–294.
New J.G. (1994) Electric organ discharge and electrosensory reafference in skates, Biol. Bull. 187: 64–75.
New J.G., Tricas T.C. (1998) Electroreceptors and Magnetoreceptors: Morphology and Function, in: Cell Physiology Source Book, Sperlakis N. (Ed.) 2nd ed., Academic Press, San Diego, pp. 741–758.
Obara S., Benett M.V.L. (1972) Mode of operation of ampullae of Lorenzini of the skate, Raja, J. Gen. Physiol. 60: 534–557.
Pals N., Valentijn P., Verwey D. (1982a) Orientation reactions of the dogfish, Scyliorhinus canicula, to local electric fields, Neth. J. Zool. 32: 495–512.
Pals N., Peters R.C., Schoenhage A.A.C. (1982b) Local geo-electric fields at the bottom of the sea and their relevance for electrosensitive fish, Neth. J. Zool. 32: 479–494.
Paulin M.G. (1995) Electroreception and the compass sense of sharks, J. Theor. Biol. 174: 325–339.
Peters R.C., Evers H.P. (1985) Frequency selectivity in the ampullary system of an elasmobranch fish (Scyliorhinus canicula), J. Exp. Biol. 118: 99–109.
Raschi W. (1986) A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces, Rajoidei), J. Morph. 189: 225–247.
Roberts B.L., Meredith G.E. (1989) The efferent system, in: The Mechanosensory Lateral Line, Coombs S., Görner P., Münz H., (Eds.) Springer-Verlag, New York, pp. 445–459.
Sisneros J.A., Tricas T.C. (2000) Androgen-induced changes in the response dynamics of ampullary electrosensory primary afferent neurons, J. Neurosci. 20: 8586–8595.
Sisneros J.A., Tricas T.C. (2002a) Ontogenetic changes in the response properties of the peripheral electrosensory system in the Atlantic stingray (Dasyatis sabina), Brain, Behav. Evol. 59: 130–140.
Sisneros J.A., Tricas T.C. (2002b) Neuroethology and life history adaptations of the elasmobranch electric sense, J. Physiol. (Paris), 96: 379–389.
Sisneros J.A., Tricas T.C., Luer C.A. (1998) Response properties and biological function of the skate electrosensory system during ontogeny, J. Comp. Physiol. A 183: 87–99.
Tricas T.C. (1982) Bioelectric-mediated predation by swell sharks, Cephaloscyllium ventriosum, Copeia 1982: 948–952.
Tricas T.C. (2001) The neuroecology of the elasmobranch electrosensory world: why peripheral morphology shapes behavior, Environ. Biol. Fishes 60: 77–92.
Tricas T.C., New J.G. (1998) Sensitivity and response dynamics of electrosensory primary afferent neurons to near threshold fields in the round stingray, J. Comp. Physiol. A 182: 89–101.
Tricas T.C., Maruska K.P, Rasmussen L.E.L. (2000) Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray, Gen. Comp. Endocrinol. 118: 209–225.
Tricas T.C., Michael S.W., Sisneros J.A. (1995) Electrosensory optimization to conspecific phasic signals for mating, Neurosci. Lett. 202: 29–131.
Waltman B. (1966) Electrical properties and fine structure of the ampullary canals of Lorenzini, Acta Physiol. Scand. 66, Suppl. 264: 1–60.
Wilkens L.A., Russell D.F., Pei, X., Gurgens C. (1997) The paddlefish rostrum functions as an electrosensory antenna in plankton feeding, Proc. R. Soc. Lond. B Biol. Sci. 264: 1723–1729.
Zakon H.H.(1988) The electroreceptors: diversity in structure and function, in: Sensory Biology of Aquatic Animals, Atema, J., Fay R.R., Popper A.N., Tavolga W.N. (Eds.) Springer-Verlag, New York, pp. 151–186.
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Tricas, T.C., Sisneros, J.A. (2004). Ecological Functions and Adaptations of the Elasmobranch Electrosense. In: von der Emde, G., Mogdans, J., Kapoor, B.G. (eds) The Senses of Fish. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1060-3_14
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DOI: https://doi.org/10.1007/978-94-007-1060-3_14
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