Electroreception in Weakly Electric Fish

Water’s ability to conduct electricity has made it possible for adaptations that exploit this property to be selected for in aquatic environments, which would not be feasible in terrestrial animals due to air’s poor conductance of electricity. As a result, today there are species of fish that are able to detect the electrical current generated from other organisms and even generate their own electric fields using a specialized electrogenic organ (Crampton). The fields generated from this organ can be used for a number of applications, such as detecting prey, communicating to other conspecific fish, navigating in dark environments, and defending the user. Along with the electric organ, these fish possess electroreceptors which allow them to detect the naturally occurring electric fields from living processes or the feedback from the electric field generated by the electric organ (Crampton). These electric fish can be further categorized by the intensity or strength of their electric field and by the waveform of its current.

Fish with an electric discharge strong enough to stun prey and defend themselves are called strongly electric fish (Crampton). These fish differ from weakly electric fish in that weakly electric fish do not have a strong electric discharge, and instead use their electric organ to generate a weak electric field for communication, navigation and prey detection. Weakly electric fish are found in the order Gymnotiformes and the family Mormyridae (Caputi). The gymnotiform fish in particular generate wave electric organ discharges and are found in Central America and South America, while mormyrid fish generate pulse electric organ discharges and range from the Nile River and central Africa (Caputi).

The electric organ responsible for electrogenesis, or the production of electric fields, is formed by electrocytes which are derived from modified muscle and nerve cells (Crampton). In order to respond to fluctuations in the electric field, weakly electric fish use an array of electroreceptors throughout the skin of the fish. Mormyrid and gymnotiform fish both utilize ampullary electroreceptors and tuberous electroreceptors such as mormyromasts and knollenorgans (Heiligenberg and Bastian). The ampullary electroreceptors respond to low frequency (<40 Hz) stimuli and are used to detect the source of external electric fields (Heiligenberg and Bastian). Being tuberous electroreceptors, mormyromasts and knollenorgans respond to higher frequency stimuli; the mormyromasts, in particular, are used in electrolocation and produce multiple action potentials whose lengths correspond to the intensity of the stimuli, while knollenorgans react to electric organ discharges of other electric fish and produce a single action potential (Heiligenberg and Bastian). Input from the electroreceptors travels through the sensory nervous system to the tectum of the fish’s midbrain, where neurons react to visual and electrosensory input. When given input from both the electrosensory and optic organs, some parts of the tectum will show a greater response (Carr). This overlap of the neurons responsible for the electric sense and vision makes it possible for the fish to spatially orient itself using both senses, however, mormyrid and gymnotiform fish tend to specialize in one sense only and typically use the electric sense for electrolocation at night and in dark, turbid environments (Crampton).

Electrolocation is a key method by which weakly electric fish identify nearby objects and navigate through their environments. By emitting an electric field from the fish’s electric organ, objects inside the field create a disturbance which is registered by the fish’s electroreceptors. This disturbance gives the fish an electric image of the object which can be used to determine its qualities and differentiate it from other objects. Mormyrid fishes, for instance, are able to differentiate from aluminum and plastic objects due to the difference of electrical impedance in both materials (von der Emde). One of the hurdles with the electric sense in these fishes is that they lack a focusing mechanism akin to the lens used in the visual sense. Because of this, the electric image produced is blurred, but shapes of objects can still be determined (von der Emde and Fetz). As a result, the blurring of background objects allows for smaller objects of interest, such as prey (Nelson and Maciver) or navigational markers, to stand out in the electric field.

Because weakly electric fish are generally nocturnal, the use of electrolocation is necessary when navigating in dimly lit environments. In an experiment performed by Peter Cain, William Gerin, and Peter Moller, a selection of mormyrid Peters’s elephantnose fish (Gnathonemus petersii) had some of their senses removed to determine to what extent the fish uses its senses to navigate through environments and ascertain novel environments. This was done by observing how long it took a fish that was intact, blind, electrically silent, or electrically silent and blind to pass through a fixed-size hole placed at various heights in a dimly lit fish tank. Fish that remained intact were able to reliably locate the hole, while fish that had lost their electric sense were not able to. Fish that had only lost their vision were also able to find the hole unless they were electrically silent. From this, the researchers concluded that G. petersii fish rely heavily on the electric sense for navigating and becoming familiar with novel environments, and that other sensory modalities offer little assistance when compared to the electric sense in these situations (Cain et al.).

The performance of electrolocation may also be aided by the presence of other weakly electric fish, where a fish extends the range of its own EOD by using the EOD of the other fish, allowing it to determine the qualities of local objects at distances greater than it could achieve alone. In a study by Federico Pedraja and Nathaniel Sawtell, the sensing range of G. petersii was examined using modeling software, behavioral observations, and recordings of neural responses using electrodes in the fish’s electrosensory lobe. Models of the G. petersii’s EOD suggested that the introduction of a conspecific set perpendicular to the fish would extend the EOD range and improve the intensity of a nearby object’s electric image, and in live experiments this was demonstrated to be the case when observing the increases of EOD rate when the fish was exposed to an artificial EOD. When the artificial EOD was modified to mimic the EOD from a larger fish, the range of the fish’s EOD was shown to have almost tripled in distance. In another experiment, the fish was better able to differentiate between two distant objects when a mimicked EOD was emitted between them. From these results, the researchers determined that G. petersii do exhibit a collective electric sense used for electrolocation, and that this collective sense may be used to silently warn nearby conspecifics of predators in the area or to aid in schooling behavior and prey detection (Pedraja and Sawtell).

The reliance on electrolocation in weakly electric fish may also be evident in their morphology and locomotion. In gymnotiform weakly electric fish, the ventral side is composed of an elongated anal fin. For instance, in the gymnotiform black ghost knifefish (Apteronotus albifrons) this fin allows the fish to move and orient itself in any direction while keeping the trunk of the body rigid, since the bending of the trunk is independent of the control of the anal fin. Because the electric organ of the black ghost knifefish is in its trunk, this form of locomotion allows the fish to influence how it will receive incoming electrosensory signals (Nelson and Maciver). An example of this can be seen in A. albifrons scanning behaviors where the fish will move around an object with its trunk rigid, possibly to determine its position; when the fish arches its trunk during these scans, it is hypothesised that this is done to determine the spatial characteristics of the object (Assad et al.).

Since the electric sense in weakly electric fish is able to differentiate objects based on size or material, this sense is particularly important for detecting prey. The sense is most used for prey detection in dark environments, as shown in a study about the prey capture behavior of A. albifrons by Mark E. Nelson and Malcolm A. MacIver. The experiment in this study recorded the velocities and trajectories of A. albifrons during the capture of Daphnia magna in a dimly lit environment. As a result, it was shown that the A. albifrons fish will swim with its head pitched downwards so that the trunk of the fish forms a leading edge, which enabled the fish to use multiple trunk electroreceptors to aid in the search for prey (Nelson and Maciver).

During prey detection and capture, the electric sense is not the only sensory modality in use; for instance, vision and mechanoreception are both used to enhance the capabilities of the weakly electric fish during prey detection. Neurons in the optic tectum of the electrosensory lateral line lobe in weakly electric fish have been shown to respond to both visual and electrosensory stimuli (Carr). For the brown ghost knifefish, Apteronotus leptorhynchus, the motion of small objects in a blurred electric image and the movement of the weakly electric fish during scanning behaviors can also aid in the detection of prey, however, the blurred electric image is sharpest when detected by electroreceptors in the fish’s midbody; more research is necessary in determining how the electroreceptor dense head region of A. leptorhynchus affects the clarity of the electric image (Babineau et al.).

Because the electric organ requires electroreceptors in order to register distortions in the generated electric field, other fish with electroreceptors but no electric organ are also able to detect the electric field and use this to predate on weakly electric fish. Some clariid catfish, for instance, are electroreceptive, and it is suggested in a study by G.S. Merron that these fish are able to detect the electric organ discharge of mormyrid fish. By analyzing the stomach contents of a sample of 294 Clarias gariepinus and Clarias ngamensis catfish in the shoals of the Okavango Delta in Botswana, Merron found that Marcusenius macrolepidotus mormyrid fish made up 63.7% of their stomach contents. The electric organ discharges from the mormyrid fish when it is disturbed by the pack-hunting behavior of these catfish is likely the way that the catfish are able to prey upon them in such abundance (Merron).

The electric sense is also particularly useful for electrocommunication among conspecific and heterospecific weakly electric fish. Mormyrid and Gymnotiform fishes both have a separate sensory pathway for handling electric organ discharges from other fish. In this pathway, the change in EOD output over time allows the fish to determine the field orientation of a conspecific’s EOD, and also allows the fish to determine the identity of the fish who generated the EOD based on stereotyped timecourses specific to the EODs of different species and sexes (Caputi). Electrocommunication and social interactions between two Mormyrid fish have been examined in a study performed by Peter Moller, Jacques Serrier, and Debora Bowling. In this study, pairs of 12 Brienomyrus niger fish in total were suspended in a fish tank by chambers attached to an air track, which would move the fish closer together or further away. Using electrodes in the container, the researchers found that the outer limit of electrocommunication for this fish is between 101 and 130 cm. They also observed a social-silence response, where the EODs of one fish would cease momentarily while the other fish continued emitting and EOD. This response tended to occur when the fish were 36 to 55 cm apart from one another, and the duration of the silence could last as long as 24.3 to 96.4 seconds, with larger fish generally having shorter durations than smaller fish. In freely swimming fish, the social-silence response typically occurs in the losing fish after a contest between two fish (Moller et al.).

A similar electrocommunication response can be seen when two fish meet with similar EOD frequencies. In situations like this, the similarity of the frequency causes interference that will diminish the performance of each fish’s electric sense, so each fish will alter their EOD frequency to increase the difference and prevent interference. A study by Theodore Bullock, Robert Hamstra, and Henning Scheich examined this response, called the jamming avoidance response (J.A.R.), in the Gymnotiform fishes A. albifrons and Eigenmannia virescens. In this study, the fish were placed in a tank with electrodes that could record the fish’s EOD and mimic an EOD stimulus. It was shown here that A. albifrons will decrease its frequency when presented by a higher frequency EOD stimulus, and will increase its frequency when there is a low frequency stimulus, keeping a ± 4 Hz difference between its own frequency and that of the stimulus. For E. virescens, the fish exhibited a similar J.A.R., but would tend to shift its EOD frequency towards the frequency of the stimulus when it was significantly high, performing what is called a negative J.A.R. The researchers also examined the effects of different external factors on the J.A.R., such as vibrations and sound, anesthesia, temperature, salinity, and light. As a result, it was found that sound and anesthesia have a noticeable affect on the J.A.R., but temperature changed the J.A.R. very little, and darkening light only briefly alters the J.A.R. The researchers suspect that a change in salinity, and the associated changed in water conductivity, would alter the sensitivity of the fish’s electroreceptors, however, this effect was not measured in their study (Bullock et al.).

Electrocommunication among weakly electric fish has also been shown to be sexually dimorphic, where conspecific males and females show differences in EOD rate, frequency, and modulations. For example, males of A. albifrons have lower frequency EODs than the females and do not modulate their EOD frequency, while males of brown ghost knifefish (Apteronotus leptorhynchus and Apteronotus rostratus) have a higher frequency EOD and modulate their EOD frequency more than the females (Zhou and Smith). In order to determine the extent of sexual dimorphism in electrocommunication in gymnotiform species outside of the genus Apteronotus, Muchu Zhou and Troy Smith examined the EODs exhibited by the males and females of Adontosternarchus devenanzii. In this study, electrodes were attached to the head and tail of each fish to measure the frequency of its EOD while electrodes in the tank supplied a stimulus EOD that would appear to be the EOD of another A. devenanzii. As A. devenanzii are not sexually dimorphic in external morphology, the sex of each fish was indentified through laparotomy. As a result of this study, it was found there was no significant difference in EOD duration, rate, frequency, or single-peak modulation among males and females of A. devenanzii, however, the fish did exhibit multi-peaked EOD frequency modulations, where males showed more than 12 times as many multi-peak modulations compared to the females. Other gymnotiform fish, such as those in the genus Apteronotus, do not exhibit a similar multi-peaked EOD frequency modulation. It is then suggested by the researches that the loss of sexual dimorphism in EOD frequency of A. devenanzii is a derived characteristic, as males from ancestral species of gymnotiform such as Sternopygus and Eigenmannia have lower EOD frequencies. The researchers conclude that more studies should be done to investigate the neurology responsible for the differences in EOD modulations among gymnotiforms, as well as to determine the effects of hormones on electrocommunication in Adontosternarchus species (Zhou and Smith).

The electric sense is a unique sensory modality that is found most commonly in fish due to the properties of water, and its use in weakly electric fish aids in the process of navigation, prey detection, and communication. While it is considered to be one of the most well understood vertebrate senses (Carr), there is still much to be learned from this sense and the fishes that use it. Information such as how salinity affects the sensitivity of the electric sense, how electroreceptors in the head of A. leptorhynchus affect its perception of local objects, and how hormones affect electrocommunication in Adontosternarchus fish are still unknown, and more research in these areas would only serve to help broaden our knowledge and deepen our understanding of the electric sense in weakly electric fish.

Works Cited

Assad, Christopher, et al. “Electric organ discharges and Electric Images during electrolocation.” Journal of Experimental Biology, vol. 202, no. 10, 15 May 1999, pp. 1185–1193, https://doi.org/10.1242/jeb.202.10.1185.

Babineau, David, et al. “Spatial acuity and prey detection in weakly electric fish.” PLoS Computational Biology, vol. 3, no. 3, 2 Mar. 2007, https://doi.org/10.1371/journal.pcbi.0030038. Bullock, Theodore H., et al. “The jamming avoidance response of high frequency electric fish.” Journal of Comparative Physiology, vol. 77, no. 1, Mar. 1972, pp. 1–22, https://doi.org/10.1007/bf00696517.

Cain, Peter, et al. “Short‐range navigation of the weakly electric fish, gnathonemus petersii L. (Mormyridae, Teleostei), in novel and Familiar Environments.” Ethology, vol. 96, no. 1, 12 Jan. 1994, pp. 33–45, https://doi.org/10.1111/j.1439-0310.1994.tb00879.x.

Caputi, Ángel A. “Living Life With an Electric Touch.” The Journal of Experimental Biology, vol. 226, no. 23, Nov. 2023, https://doi.org/10.1242/jeb.246060.

Carr, Catherine E. “Neuroethology of Electric Fish.” BioScience, vol. 40, no. 4, Apr. 1990, pp. 259–267, https://doi.org/10.2307/1311262.

Crampton, William G. “Electroreception, electrogenesis and Electric Signal Evolution.” Journal of Fish Biology, vol. 95, no. 1, 18 Mar. 2019, pp. 92–134, https://doi.org/10.1111/jfb.13922.

Heiligenberg, W, and J Bastian. “The electric sense of weakly electric fish.” Annual Review of Physiology, vol. 46, no. 1, Oct. 1984, pp. 561–583, https://doi.org/10.1146/annurev.ph.46.030184.003021.

Merron, G. S. “Pack‐hunting in two species of catfish, clavias gariepinus and C. ngamensis, in the Okavango Delta, Botswana.” Journal of Fish Biology, vol. 43, no. 4, Oct. 1993, pp. 575–584, https://doi.org/10.1111/j.1095-8649.1993.tb00440.x.

Moller, Peter, et al. “Electric organ discharge displays during social encounter in the weakly electric fishbrienomyrus nigerL. (Mormyridae).” Ethology, vol. 82, no. 3, 12 Jan. 1989, pp. 177–191, https://doi.org/10.1111/j.1439-0310.1989.tb00498.x.

Nelson, Mark E., and Malcolm A. Maciver. “Prey capture in the weakly electric fish apteronotus albifrons: Sensory acquisition strategies and electrosensory consequences.” Journal of Experimental Biology, vol. 202, no. 10, 15 May 1999, pp. 1195–1203, https://doi.org/10.1242/jeb.202.10.1195.

Pedraja, Federico, and Nathaniel B. Sawtell. “Collective sensing in Electric Fish.” Nature, vol. 628, no. 8006, 6 Mar. 2024, pp. 139–144, https://doi.org/10.1038/s41586-024-07157-x.

Von der Emde, Gerhard, and Steffen Fetz. “Distance, shape and more: Recognition of object features during active electrolocation in a weakly electric fish.” Journal of Experimental Biology, vol. 210, no. 17, 1 Sept. 2007, pp. 3082–3095, https://doi.org/10.1242/jeb.005694.

Von der Emde, Gerhard. “Active electrolocation of objects in weakly electric fish.” Journal of Experimental Biology, vol. 202, no. 10, 15 May 1999, pp. 1205–1215, https://doi.org/10.1242/jeb.202.10.1205.

Zhou, Muchu, and G. Troy Smith. “Structure and Sexual Dimorphism of the Electrocommunication Signals of the Weakly Electric Fish,Adontosternarchus Devenanzii.” The Journal of Experimental Biology, vol. 209, no. 23, Dec. 2006, pp. 4809–18. https://doi.org/10.1242/jeb.02579.