Variations in electrosensory system morphology in teleost and elasmobranch fishes

Suppression of Ventilatory Reafference in the Elasmobranch Electrosensory System: Medullary Neuron Receptive Fields Support a Common Mode Ejection Mechanism

Journal of Experimental Biology ◽

10.1242/jeb.171.1.127 ◽

1992 ◽

Vol 171 (1) ◽

pp. 127-137 ◽

Cited By ~ 2

Author(s):

DAVID BODZNICK ◽

JOHN C. MONTGOMERY

Keyword(s):

Receptive Fields ◽

Strong Support ◽

Projection Neurons ◽

Common Mode ◽

Electrosensory System ◽

Ejection Mechanism ◽

Inhibitory Components ◽

Field Organization ◽

Elasmobranch Fishes ◽

Receptive Field Organization

Elasmobranch fishes have an electroreceptive system which they use for prey detection and orientation. Sensory inputs in this system are corrupted by a form of reafference generated by the animal's own ventilation. However, we show here that in the carpet shark, Cephaloscylium isabella, as in two previously studied batoid species, this ventilatory ‘noise’ is reduced by sensory processing within the medullary nucleus of the electrosensory system. It has been proposed that the noise cancellation is achieved by a common mode rejection mechanism. One prediction of this hypothesis is that secondary neurons within the medullary nucleus should have both excitatory and inhibitory components to their receptive fields. This prediction is experimentally verified here. Projection neurons of the medullary nucleus in the carpet shark typically have a focal excitatory, and a diffuse inhibitory, receptive field organization including a component of contralateral inhibition. This result provides strong support for the hypothesis that ventilatory suppression in the elasmobranch electrosensory system is achieved by a common mode mechanism. Note: Department of Biology, Wesleyan University, Middletown, CT 06457, USA. Present address: Department of Zoology, University of Auckland, Auckland, New Zealand.

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Electroreception in the obligate freshwater stingray, Potamotrygon motoro

Marine and Freshwater Research ◽

10.1071/mf14354 ◽

2015 ◽

Vol 66 (11) ◽

pp. 1027 ◽

Cited By ~ 4

Author(s):

Lindsay L. Harris ◽

Christine N. Bedore ◽

Stephen M. Kajiura

Keyword(s):

Electric Fields ◽

Sensory System ◽

Voltage Gradient ◽

Single Family ◽

Potential Prey ◽

Freshwater Environment ◽

Electrosensory System ◽

High Impedance ◽

Morphological Adaptations ◽

Elasmobranch Fishes

Elasmobranch fishes use electroreception to detect electric fields in the environment, particularly minute bioelectric fields of potential prey. A single family of obligate freshwater stingrays, Potamotrygonidae, endemic to the Amazon River, demonstrates morphological adaptations of their electrosensory system due to characteristics of a high impedance freshwater environment. Little work has investigated whether the reduced morphology translates to reduced sensitivity because of the electrical properties of freshwater, or because of a marine-tuned sensory system attempting to function in freshwater. The objective of the present study was to measure electric potential from prey of Potamotrygon motoro and replicate the measurements in a behavioural assay to quantify P. motoro electrosensitivity. Median orientation distance to prey-simulating electric fields was 2.73cm, and the median voltage gradient detected was 0.20mVcm–1. This sensitivity is greatly reduced compared with marine batoids. A euryhaline species with marine-type ampullary morphology was previously tested in freshwater and demonstrated reduced sensitivity compared with when it was tested in seawater (0.2μVcm–1 v. 0.6nVcm–1). When the data were adjusted with a modified ideal dipole equation, sensitivity was comparable to P. motoro. This suggests that the conductivity of the medium, more so than ampullary morphology, dictates the sensitivity of elasmobranch electroreception.

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Electrosensory-driven feeding behaviours of the Port Jackson shark (Heterodontus portusjacksoni) and western shovelnose ray (Aptychotrema vincentiana)

Marine and Freshwater Research ◽

10.1071/mf14245 ◽

2016 ◽

Vol 67 (2) ◽

pp. 187 ◽

Cited By ~ 4

Author(s):

R. M. Kempster ◽

C. A. Egeberg ◽

N. S. Hart ◽

S. P. Collin

Keyword(s):

Electric Fields ◽

Interspecific Variation ◽

Electrosensory System ◽

Field Gradients ◽

Highly Sensitive ◽

Elasmobranch Species ◽

Elasmobranch Fishes ◽

Species Specific ◽

Port Jackson ◽

Abundance And Distribution

Elasmobranch fishes (sharks, skates and rays) possess a highly sensitive electrosensory system that enables them to detect weak electric fields, such as those produced by potential prey organisms. Despite several comparative anatomical studies, the functional significance of interspecific variation in electrosensory system morphology remains poorly understood. In the present study, we directly tested the electrosensitivity of two benthic elasmobranchs that share a similar habitat and feed on similarly sized prey items (Port Jackson sharks, Heterodontus portusjacksoni, and western shovelnose rays, Aptychotrema vincentiana), but differ significantly in their electrosensory system morphology. Aptychotrema vincentiana possesses almost five times the number of electrosensory pores of H. portusjacksoni (~1190 and ~239 respectively), yet both species are able to initiate feeding responses to electric-field gradients below 1 nV cm–1, similar to other elasmobranch species tested. However, A. vincentiana showed a greater ability to resolve the specific location of electrosensory stimuli, because H. portusjacksoni would more often overshoot the target and have to turn around to locate it. These results suggested that differences in abundance and distribution of electrosensory pores have little to no effect on the absolute electrical sensitivity in elasmobranchs, and instead, may reflect species-specific differences in the spatial resolution and directionality of electroreception.

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Navigation by Induction-Based Magnetoreception in Elasmobranch Fishes

Journal of Biophysics ◽

10.1155/2009/380976 ◽

2009 ◽

Vol 2009 ◽

pp. 1-6 ◽

Cited By ~ 6

Author(s):

T. C. A. Molteno ◽

W. L. Kennedy

Keyword(s):

Frequency Domain ◽

Geomagnetic Field ◽

Domain Model ◽

Relative Movement ◽

Behavioral Experiments ◽

Synchronous Detection ◽

Electrosensory System ◽

Elasmobranch Fishes

A quantitative frequency-domain model of induction-based magnetoreception is presented for elasmobranch fishes. We show that orientation with respect to the geomagnetic field can be determined by synchronous detection of electrosensory signals at harmonics of the vestibular frequency. The sensitivity required for this compass-sense mechanism is shown to be less than that known from behavioral experiments. Recent attached-magnet experiments have called into doubt the induction-based mechanism for magnetoreception. We show that the use of attached magnets would interfere with an induction-based mechanism unless relative movement between the electrosensory system and the attached magnet is less than 100 m. This suggests that further experiments may be required to eliminate induction as a basis for magnetoreception.

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Absorption and excretion of water and salts by the elasmobranch fishes. IV. The secretion of exogenous creatining by the dogfish, Squalus acanthias

Journal of Cellular and Comparative Physiology ◽

10.1002/jcp.1030040205 ◽

1934 ◽

Vol 4 (2) ◽

pp. 211-220 ◽

Cited By ~ 10

Author(s):

James A. Shannon

Keyword(s):

Squalus Acanthias ◽

Elasmobranch Fishes

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Elevated carbon dioxide alters the plasma composition and behaviour of a shark

Biology Letters ◽

10.1098/rsbl.2014.0538 ◽

2014 ◽

Vol 10 (9) ◽

pp. 20140538 ◽

Cited By ~ 59

Author(s):

Leon Green ◽

Fredrik Jutfelt

Keyword(s):

Ocean Acidification ◽

Fossil Fuels ◽

Resting Metabolic Rate ◽

Blood Chemistry ◽

Teleost Fishes ◽

Behavioural Effects ◽

Swimming Pattern ◽

Acclimation Period ◽

Elevated Water ◽

Elasmobranch Fishes

Increased carbon emissions from fossil fuels are increasing the p CO 2 of the ocean surface waters in a process called ocean acidification. Elevated water p CO 2 can induce physiological and behavioural effects in teleost fishes, although there appear to be large differences in sensitivity between species. There is currently no information available on the possible responses to future ocean acidification in elasmobranch fishes. We exposed small-spotted catsharks ( Scyliorhinus canicula ) to either control conditions or a year 2100 scenario of 990 μatm p CO 2 for four weeks. We did not detect treatment effects on growth, resting metabolic rate, aerobic scope, skin denticle ultrastructure or skin denticle morphology. However, we found that the elevated p CO 2 group buffered internal acidosis via accumulation with an associated increase in Na + , indicating that the blood chemistry remained altered despite the long acclimation period. The elevated p CO 2 group also exhibited a shift in their nocturnal swimming pattern from a pattern of many starts and stops to more continuous swimming. Although CO 2 -exposed teleost fishes can display reduced behavioural asymmetry (lateralization), the CO 2 -exposed sharks showed increased lateralization. These behavioural effects may suggest that elasmobranch neurophysiology is affected by CO 2 , as in some teleosts, or that the sharks detect CO 2 as a constant stressor, which leads to altered behaviour. The potential direct effects of ocean acidification should henceforth be considered when assessing future anthropogenic effects on sharks.

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