Concept: Electric fish
- Proceedings of the National Academy of Sciences of the United States of America
- Published almost 3 years ago
In March 1800, Alexander von Humboldt observed the extraordinary spectacle of native fisherman collecting electric eels (Electrophorus electricus) by “fishing with horses” [von Humboldt A (1807) Ann Phys 25:34-43]. The strategy was to herd horses into a pool containing electric eels, provoking the eels to attack by pressing themselves against the horses while discharging. Once the eels were exhausted, they could be safely collected. This legendary tale of South American adventures helped propel Humboldt to fame and has been recounted and illustrated in many publications, but subsequent investigators have been skeptical, and no similar eel behavior has been reported in more than 200 years. Here I report a defensive eel behavior that supports Humboldt’s account. The behavior consists of an approach and leap out of the water during which the eel presses its chin against a threatening conductor while discharging high-voltage volleys. The effect is to short-circuit the electric organ through the threat, with increasing power diverted to the threat as the eel attains greater height during the leap. Measurement of voltages and current during the behavior, and assessment of the equivalent circuit, reveal the effectiveness of the behavior and the basis for its natural selection.
Interactions among animals can result in complex sensory signals containing a variety of socially relevant information, including the number, identity, and relative motion of conspecifics. How the spatiotemporal properties of such evolving naturalistic signals are encoded is a key question in sensory neuroscience. Here, we present results from experiments and modeling that address this issue in the context of the electric sense, which combines the spatial aspects of vision and touch, with the temporal aspects of audition. Wave-type electric fish, such as the brown ghost knifefish, Apteronotus leptorhynchus, used in this study, are uniquely identified by the frequency of their electric organ discharge (EOD). Multiple beat frequencies arise from the superposition of the EODs of each fish. We record the natural electrical signals near the skin of a “receiving” fish that are produced by stationary and freely swimming conspecifics. Using spectral analysis, we find that the primary beats, and the secondary beats between them (“beats of beats”), can be greatly influenced by fish swimming; the resulting motion produces low-frequency envelopes that broaden all the beat peaks and reshape the “noise floor”. We assess the consequences of this motion on sensory coding using a model electroreceptor. We show that the primary and secondary beats are encoded in the afferent spike train, but that motion acts to degrade this encoding. We also simulate the response of a realistic population of receptors, and find that it can encode the motion envelope well, primarily due to the receptors with lower firing rates. We discuss the implications of our results for the identification of conspecifics through specific beat frequencies and its possible hindrance by active swimming.
Alternative hypotheses had been advanced as to the components forming the elongate fin coursing along the ventral margin of much of the body and tail from behind the abdominal region to the posterior margin of the tail in the Electric Eel, Electrophorus electricus. Although the original species description indicated that this fin was a composite of the caudal fin plus the elongate anal fin characteristic of other genera of the Gymnotiformes, subsequent researchers proposed that the posterior region of the fin was formed by the extension of the anal fin posteriorly to the tip of the tail, thereby forming a “false caudal fin.” Examination of ontogenetic series of the genus reveal that Electrophorus possesses a true caudal fin formed of a terminal centrum, hypural plate and a low number of caudal-fin rays. The confluence of the two fins is proposed as an additional autapomorphy for the genus. Under all alternative proposed hypotheses of relationships within the order Gymnotiformes, the presence of a caudal fin in Electrophorus optimized as being independent of the occurence of the morphologically equivalent structure in the Apteronotidae. Possible functional advantages to the presence of a caudal fin in the genus are discussed.
In order to survive, animals must quickly and accurately locate prey, predators, and conspecifics using the signals they generate. The signal source location can be estimated using multiple detectors and the inverse relationship between the received signal intensity (RSI) and the distance, but difficulty of the source localization increases if there is an additional dependence on the orientation of a signal source. In such cases, the signal source could be approximated as an ideal dipole for simplification. Based on a theoretical model, the RSI can be directly predicted from a known dipole location; but estimating a dipole location from RSIs has no direct analytical solution. Here, we propose an efficient solution to the dipole localization problem by using a lookup table (LUT) to store RSIs predicted by our theoretically derived dipole model at many possible dipole positions and orientations. For a given set of RSIs measured at multiple detectors, our algorithm found a dipole location having the closest matching normalized RSIs from the LUT, and further refined the location at higher resolution. Studying the natural behavior of weakly electric fish (WEF) requires efficiently computing their location and the temporal pattern of their electric signals over extended periods. Our dipole localization method was successfully applied to track single or multiple freely swimming WEF in shallow water in real-time, as each fish could be closely approximated by an ideal current dipole in two dimensions. Our optimized search algorithm found the animal’s positions, orientations, and tail-bending angles quickly and accurately under various conditions, without the need for calibrating individual-specific parameters. Our dipole localization method is directly applicable to studying the role of active sensing during spatial navigation, or social interactions between multiple WEF. Furthermore, our method could be extended to other application areas involving dipole source localization.
Weakly electric fish are unique model systems in neuroethology, that allow experimentalists to non-invasively, access, central nervous system generated spatio-temporal electric patterns of pulses with roles in at least 2 complex and incompletely understood abilities: electrocommunication and electrolocation. Pulse-type electric fish alter their inter pulse intervals (IPIs) according to different behavioral contexts as aggression, hiding and mating. Nevertheless, only a few behavioral studies comparing the influence of different stimuli IPIs in the fish electric response have been conducted. We developed an apparatus that allows real time automatic realistic stimulation and simultaneous recording of electric pulses in freely moving Gymnotus carapo for several days. We detected and recorded pulse timestamps independently of the fish’s position for days. A stimulus fish was mimicked by a dipole electrode that reproduced the voltage time series of real conspecific according to previously recorded timestamp sequences. We characterized fish behavior and the eletrocommunication in 2 conditions: stimulated by IPIs pre-recorded from other fish and random IPI ones. All stimuli pulses had the exact Gymontus carapo waveform. All fish presented a surprisingly long transient exploratory behavior (more than 8 h) when exposed to a new environment in the absence of electrical stimuli. Further, we also show that fish are able to discriminate between real and random stimuli distributions by changing several characteristics of their IPI distribution.
We investigated the ionic mechanisms that allow dynamic regulation of action potential (AP) amplitude as a means of regulating energetic costs of AP signaling. Weakly electric fish generate an electric organ discharge (EOD) by summing the APs of their electric organ cells (electrocytes). Some electric fish increase AP amplitude during active periods or social interactions and decrease AP amplitude when inactive, regulated by melanocortin peptide hormones. This modulates signal amplitude and conserves energy. The gymnotiform Eigenmannia virescens generates EODs at frequencies that can exceed 500 Hz, which is energetically challenging. We examined how E. virescens meets that challenge. E. virescens electrocytes exhibit a voltage-gated Na(+) current with extremely rapid recovery from inactivation (τ(recov) = 0.3 msec) allowing complete recovery of Na(+) current between APs even in fish with the highest EOD frequencies. Electrocytes also possess an inwardly rectifying K(+) current, and a Na(+)-activated K(+) current (I(KNa)) the latter not yet identified in any gymnotiform species. In vitro application of melanocortins increases electrocyte AP amplitude and the magnitudes of all three currents, but increased I(KNa) is a function of enhanced Na(+) influx. Numerical simulations suggest that changing I(Na) magnitude produces corresponding changes in AP amplitude and that K(Na) channels increase AP energy efficiency (10-30% less Na(+) influx/AP) over model cells with only voltage-gated K(+) channels. These findings suggest the possibility that E. virescens reduces the energetic demands of high-frequency APs through rapidly recovering Na(+) channels and the novel use of K(Na) channels to maximize AP amplitude at a given Na(+) conductance.
This study attempts to clarify the controversy regarding the ontogenetic origin of the main organ electrocytes in the electric eel, Electrophorus electricus. The dispute was between an earlier claimed origin from a skeletal muscle precursor [Fritsch, 1881], or from a distinct electrocyte-generating matrix, or germinative zone [Keynes, 1961]. We demonstrate electrocyte formation from a metamerically organized group of pre-electroblasts, splitting off the ventralmost tip of the embryonic trunk mesoderm at the moment of hatching from the egg. We show details of successive stages in the development of rows of electric plates, the electrocytes, by means of conventional histology and electron microscopy. The membrane-bound pre-electroblasts multiply rapidly and then undergo a specific mitosis where they lose their membranes and begin extensive cytoplasm production as electroblasts. Electrical activity, consisting of single and multiple pulses, was noticed in seven-day-old larvae that began to exhibit swimming movements. A separation of discharges into single pulses and trains of higher voltage pulses was seen first in 45-mm-long larvae. A lateralis imus muscle and anal fin ray muscles, implicated by earlier investigators in the formation of electrocytes, begin developing at a time in larval life when eight columns of electrocytes are already present. Axonal innervation is seen very early during electrocyte formation. © 2014 S. Karger AG, Basel.
Electric eels (Electrophorus electricus) are legendary for their ability to incapacitate fish, humans, and horses with hundreds of volts of electricity. The function of this output as a weapon has been obvious for centuries but its potential role for electroreception has been overlooked. Here it is shown that electric eels use high-voltage simultaneously as a weapon and for precise and rapid electrolocation of fast-moving prey and conductors. Their speed, accuracy, and high-frequency pulse rate are reminiscent of bats using a ‘terminal feeding buzz’ to track insects. Eel’s exhibit ‘sensory conflict’ when mechanosensory and electrosensory cues are separated, striking first toward mechanosensory cues and later toward conductors. Strikes initiated in the absence of conductors are aborted. In addition to providing new insights into the evolution of strongly electric fish and showing electric eels to be far more sophisticated than previously described, these findings reveal a trait with markedly dichotomous functions.
Progress towards the integration of technology into living organisms requires electrical power sources that are biocompatible, mechanically flexible, and able to harness the chemical energy available inside biological systems. Conventional batteries were not designed with these criteria in mind. The electric organ of the knifefish Electrophorus electricus (commonly known as the electric eel) is, however, an example of an electrical power source that operates within biological constraints while featuring power characteristics that include peak potential differences of 600 volts and currents of 1 ampere. Here we introduce an electric-eel-inspired power concept that uses gradients of ions between miniature polyacrylamide hydrogel compartments bounded by a repeating sequence of cation- and anion-selective hydrogel membranes. The system uses a scalable stacking or folding geometry that generates 110 volts at open circuit or 27 milliwatts per square metre per gel cell upon simultaneous, self-registered mechanical contact activation of thousands of gel compartments in series while circumventing power dissipation before contact. Unlike typical batteries, these systems are soft, flexible, transparent, and potentially biocompatible. These characteristics suggest that artificial electric organs could be used to power next-generation implant materials such as pacemakers, implantable sensors, or prosthetic devices in hybrids of living and non-living systems.
Nature is replete with predator venoms that immobilize prey by targeting ion channels. Electric eels (Electrophorus electricus) take a different tactic to accomplish the same end. Striking eels emit electricity in volleys of 1 ms, high-voltage pulses. Each pulse is capable of activating prey motor neuron efferents, and hence muscles. In a typical attack, eel discharges cause brief, immobilizing tetanus, allowing eels to swallow small prey almost immediately. Here I show that when eels struggle with large prey or fish held precariously, they commonly curl to bring their own tail to the opposite side of prey, sandwiching it between the two poles of their powerful electric organ. They then deliver volleys of high-voltage pulses. Shortly thereafter, eels juggle prey into a favorable position for swallowing. Recordings from electrodes placed within prey items show that this curling behavior at least doubles the field strength within shocked prey, most likely ensuring reliable activation of the majority of prey motor neurons. Simulated pulse trains, or pulses from an eel-triggered stimulator, applied to a prey muscle preparations result in profound muscle fatigue and loss of contractile force. Consistent with this result, video recordings show that formerly struggling prey are temporarily immobile after this form of attack, allowing the manipulation of prey that might otherwise escape. These results reveal a unique use of electric organs to a unique end; eels superimpose electric fields from two poles, ensuring maximal remote activation of prey efferents that blocks subsequent prey movement by inducing involuntary muscle fatigue.