Neuroethology and life history adaptations of the elasmobranch electric sense

The electric sense of elasmobranch fishes (sharks and rays) is an important sensory modality known to mediate the detection of bioelectric stimuli. Although the best known function for the use of the elasmobranch electric sense is prey detection, relatively few studies have investigated other possible biological functions. Here, we review recent studies that demonstrate the elasmobranch electrosensory system functions in a wide number of behavioral contexts including social, reproductive and anti-predator behaviors. Recent work on non-electrogenic stingrays demonstrates that the electric sense is used during reproduction and courtship for conspecific detection and localization. Electrogenic skates may use their electrosensory encoding capabilities and electric organ discharges for communication during social and reproductive interactions. The electric sense may also be used to detect and avoid predators during early life history stages in many elasmobranch species. Embryonic clearnose skates demonstrate a ventilatory freeze response when a weak low-frequency electric field is imposed upon the egg capsule. Peak frequency sensitivity of the peripheral electrosensory system in embryonic skates matches the low frequencies of phasic electric stimuli produced by natural fish egg-predators. Neurophysiology experiments reveal that electrosensory tuning changes across the life history of a species and also seasonally due to steroid hormone changes during the reproductive season. We argue that the ontogenetic and seasonal variation in electrosensory tuning represent an adaptive electrosensory plasticity that may be common to many elasmobranchs to enhance an individual's fitness throughout its life history.

[1]  J. Meyer Steroid influences upon the discharge frequencies of a weakly electric fish , 1983, Journal of comparative physiology.

[2]  H. Zakon,et al.  Behavioral Actions of Androgens and Androgen Receptor Expression in the Electrocommunication System of an Electric Fish, Eigenmannia virescens , 1998, Hormones and Behavior.

[3]  M. Ferrari,et al.  Individual variation in and androgen-modulation of the sodium current in electric organ , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Albert,et al.  Food , 1917, Nature.

[5]  Harold H. Zakon,et al.  Evidence for a direct effect of androgens upon electroreceptor tuning , 1986, Journal of Comparative Physiology A.

[6]  F. Daiber,et al.  Studies on the Rajid Fishes (Rajidae) Found in the Waters around Japan , 1961 .

[7]  W. Raschi A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces, Rajoidei) , 1986, Journal of morphology.

[8]  P. Belbenoit Fine analysis of predatory and defensive motor events in Torpedo marmorata (Pisces) , 1986 .

[9]  S. Volman,et al.  From behavior to membranes: testosterone-induced changes in action potential duration in electric organs. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Androgens Alter Electric Organ Discharge Pulse Duration despite Stability in Electric Organ Discharge Frequency , 2001, Hormones and Behavior.

[11]  H. Zakon,et al.  Chronic androgen treatment increases action potential duration in the electric organ of Sternopygus , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  T. Tricas,et al.  Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray. , 2000, General and comparative endocrinology.

[13]  M. Bennett,et al.  The Electrophysiology of Electric Organs of Marine Electric Fishes , 1961, The Journal of general physiology.

[14]  R. W. Murray,et al.  The composition of the endolymph, perilymph , 1961 .

[15]  J. New Medullary electrosensory processing in the little skate , 1990, Journal of Comparative Physiology A.

[16]  R. Peters,et al.  FREQUENCY SELECTIVITY IN THE AMPULLARY SYSTEM OF AN ELASMOBRANCH FISH (SCYLIORHINUS CANICULA) , 1985 .

[17]  Daniel J. Miller Miller and Lea's Guide to the Coastal Marine Fishes of California. , 1972, Ichthyology & Herpetology.

[18]  R. W. Murray Electrical sensitivity of the ampullae of Lorenzini. , 1960, Nature.

[19]  C. Lowe,et al.  Feeding and associated electrical behavior of the Pacific electric ray Torpedo californica in the field , 1994, Marine Biology.

[20]  Jelle Atema,et al.  Sensory Biology of Aquatic Animals , 1988, Springer New York.

[21]  M. Hixon,et al.  Night-Shocker: Predatory Behavior of the Pacific Electric Ray (Torpedo californica) , 1978, Science.

[22]  M. Sanders Handbook of Sensory Physiology , 1975 .

[23]  T. Sejnowski,et al.  A freeze-fracture study of the skate electroreceptor. , 1982, Journal of neurocytology.

[24]  J. Sanderson,et al.  On the Electrical Organ of the Skate , 1888, The Journal of physiology.

[25]  W. König,et al.  Bau und Innervation der Lorenzinischen Ampullen und deren Bedeutung als niederes Sinnesorgan , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[26]  T. Taniuchi Aspects of reproduction and food habits of the japanese swellshark Cephaloscyllium umbractile from Choshi, Japan , 1988 .

[27]  D. Ebert Biology of the sevengill shark Notorynchus cepedianus (Peron, 1807) in the temperate coastal waters of southern Africa , 1996 .

[28]  J. New Electric organ discharge and electrosensory reafference in skates. , 1994, The Biological bulletin.

[29]  B. Söderström,et al.  A method for determination of low carbon monoxide concentration in blood. , 1966, Acta physiologica Scandinavica.

[30]  N. Kohler,et al.  Food, Feeding Habits, and Estimates of Daily Ration of the Shortfin Mako (Isurus oxyrinchus) in the Northwest Atlantic , 1982 .

[31]  Timothy C. Tricas Bioelectric-Mediated Predation by Swell Sharks, Cephaloscyllium ventriosum , 1982 .

[32]  A. Bass,et al.  Androgen binding in the brain and electric organ of a mormyrid fish , 1986, Journal of Comparative Physiology A.

[33]  James Stark,et al.  3. On the Existence of an Electrical Apparatus in the Flapper Skate and other Rays. , 1851 .

[34]  A H Bass,et al.  Hormonal control of sexual differentiation: changes in electric organ discharge waveform. , 1983, Science.

[35]  H. Zakon,et al.  Estrogen Modifies an Electrocommunication Signal by Altering the Electrocyte Sodium Current in an Electric Fish,Sternopygus , 1997, The Journal of Neuroscience.

[36]  Ad. J. Kalmijn,et al.  Detection of Weak Electric Fields , 1988 .

[37]  Predation on elasmobranch eggs , 1993 .

[38]  H. Zakon,et al.  Androgens Alter the Tuning of Electroreceptors , 1982, Science.

[39]  J. Musick,et al.  Food division within two sympatric species-pairs of skates (Pisces: Rajidae) , 1976 .

[40]  T. Tricas,et al.  Response properties and biological function of the skate electrosensory system during ontogeny , 1998, Journal of Comparative Physiology A.

[41]  Timothy C. Tricas The neuroecology of the elasmobranch electrosensory world: why peripheral morphology shapes behavior , 2001 .

[42]  T. Tricas,et al.  Periodic gonadal activity and protracted mating in elasmobranch fishes , 1996 .

[43]  R. Keynes,et al.  The discharge of individual electroplates in Raia clavata. , 1953, The Journal of physiology.

[44]  Ad. J. Kalmijn,et al.  The Detection of Electric Fields from Inanimate and Animate Sources Other Than Electric Organs , 1974 .

[45]  D. Ebert Diet of the seven gill shark Notorynchus cepedianus in the temperate coastal waters of southern Africa , 1991 .

[46]  R. W. Murray,et al.  The response of the ampullae of Lorenzini of elasmobranchs to electrical stimulation. , 1962, The Journal of experimental biology.

[47]  A. Bass,et al.  Shifts in frequency tuning of electroreceptors in androgen-treated mormyrid fish , 1984, Journal of Comparative Physiology A.

[48]  A. Kalmijn,et al.  The electric sense of sharks and rays. , 1971, The Journal of experimental biology.

[49]  T. Sejnowski,et al.  A freeze-fracture study of the skate electro receptor , 1982 .

[50]  Joseph A. Sisneros,et al.  Androgen-Induced Changes in the Response Dynamics of Ampullary Electrosensory Primary Afferent Neurons , 2000, The Journal of Neuroscience.

[51]  N. Mikhailenko,et al.  Identification of spinal electromotoneurons in the rayRaja clavata (Rajidae) , 1992, Neuroscience.

[52]  P. Belbenoit Electric organ discharge of Torpedo (Pisces); basic pattern and ontogenetic changes. , 1979, Journal de physiologie.

[53]  J. Sisneros,et al.  Electrosensory optimization to conspecific phasic signals for mating , 1995, Neuroscience Letters.

[54]  B Waltman,et al.  Electrical properties and fine structure of the ampullary canals of Lorenzini. , 1966, Acta physiologica Scandinavica. Supplementum.

[55]  Duncombe Wg The colorimetric micro-determination of long-chain fatty acids. , 1963 .

[56]  J. Ayers,et al.  Observations on the electric organ discharge of two skate species (Chondrichthyes: Rajidae) and its relationship to behaviour , 1987, Environmental Biology of Fishes.

[57]  S. Nordell Observations of the mating behavior and dentition of the round stingray,Urolophus halleri , 1994, Environmental Biology of Fishes.