Electroreception

Electroreception, the ability to detect weak naturally occurring electrostatic fields in the environment. Electroreception is found in a number of vertebrate species, including the members of two distinct lineages of teleosts (a group of ray-finned fishes) and monotremes (egg-laying mammals). Bumblebees also are able to detect weak electric fields. In vertebrates electroreception is made possible through the existence of sensitive electroreceptor organs in the skin.

Electroreception facilitates the detection of prey or other food sources and objects and is used by some species as a means of social communication. In general, terrestrial animals have little use for electroreception, because the high resistance of air limits the flow of electric current. Thus, humans lack electroreceptors; however, through the indiscriminant stimulation of sensory and motor nerve fibres, humans are able to detect strong electric currents (e.g., from batteries or static generators) resulting from either direct contact with an electric source or indirect contact with a conducting medium such as water.

Discovery of electroreceptors

Electroreceptor organs were first identified physiologically in the early 1960s from weakly electric fish by American neuroscientist Theodore H. Bullock and colleagues and by French scientists Thomas Szabo and Alfred Fessard. The existence of electroreceptors had been anticipated in the 1950s by British zoologist Hans W. Lissmann, who was the first to discover continuous weak electric discharges from an electric organ in the tail of a species of African freshwater fish (Gymnarchus niloticus). By 1958 he had demonstrated the reason for the discharge by showing that the fish could detect the presence of glass and metal rods or other conducting or nonconducting objects at distances of 10 cm (about 4 inches) or more, even in the absence of visual, mechanical, or chemical cues. Lissmann postulated that the fish was sensing the distortions of its own electric organ discharges as electrical shadows on its skin. He correctly surmised that there were dermal electroreceptors in the fish. He called their behaviour “electrolocation,” after the well-known ability of bats to echolocate objects by detecting returning ultrasonic echoes from their calls.

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In the 1960s Dutch scientists Sven Dijkgraaf and Adrianus J. Kalmijn established that sharks and rays, which have dermal sense organs called ampullae of Lorenzini, could sense weak electric currents from their prey organisms such as flatfishes even when the organisms were buried under sand. Dijkgraaf and Kalmijn showed that the ampullae of Lorenzini were essential to this behaviour, which was entirely based on electrosensory cues, and that prey had weak direct current (DC) electric fields surrounding their gills, gut, and skin wounds that gave away their presence to the sharks. When given a choice between a prey fish covered with plastic wrap and a pair of wire electrodes connected to a prey fish in another tank, the shark preferred to dig up the wires. Kalmijn and colleagues called this ability passive electrolocation, in contrast to the active electrolocation ability of G. niloticus discovered by Lissmann.

Evolution and anatomy of electroreception

Electroreception first appeared in jawless craniates (animals with skulls) such as lampreys that possess an epidermal “end-bud” organ innervated by the lateral line nerve. The end-bud receptors are sensitive to weak low-frequency (DC to 50 hertz [Hz]) electric fields. Among the earliest jawed vertebrates, the first ampullary electroreceptors were embedded in the skin or at the base of a long conducting canal leading from the skin surface to a specialized patch of modified sensory epithelial cells (in the case of ampullae of Lorenzini). The sensory epithelial cells resemble hair cells of the lateral line or inner ear, and the nerve fibres connecting them to the brain travel in the same nerve bundles with the lateral line nerves. The cells lining the ampullary canals are packed tightly to make a high-resistance insulator around the low-resistance canal lumen, which is composed of a salty gelatinous matrix. Similar to an insulated wire, this arrangement is ideal for conducting electric currents to the sensory cell membranes. All vertebrate electroreceptors follow this basic design.

Electroreception is shared by all the primitive aquatic vertebrates, including some aquatic amphibians, but it was lost in the amniotes as they made the transition to a terrestrial existence. In those monotreme mammals in which the sense reappeared, electroreception is derived from modified mucous glands on the bill or the snout. The mucous glands have low-resistance canals that conduct current from the environment to bare nerve endings of the trigeminal nerve. Electroreception is absent in most modern fishes, with the exception of two independently evolved lineages of teleosts, which include the catfishes and the notopterid knifefishes of Africa. In those groups, electroreceptors evolved independently as ampullary receptors. Tuberous, or alternating current– (AC-) sensitive, electroreceptors also appeared in both of those lineages as subgroups of electric fishes. Those subgroups are the South American knifefishes (Gymnotiformes), which include the electric eel (Electrophorus electricus), and the unrelated freshwater mormyrid fishes (Mormyroidea) from Africa. Members of both groups use their tuberous organs for active electrolocation of objects and for electrical communication.

Investigations of electroreception among invertebrates have indicated the existence of high behavioral thresholds; for example, the worm Caenorhabditis elegans responds to currents that are greater than three volts per centimetre. By comparison, sharks and rays, which have the most-sensitive ampullary receptors, have thresholds as low as 0.02 microvolts per centimetre. Bumblebees detect weak electric fields produced by flowers, though the mechanism and function of electroreception in this case is unknown. The phenomenon was first reported for the species Bombus terrestris.

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Functions of electroreception

Electroreceptors provide a low-resistance pathway for current to flow from the external environment to a sensory epithelium containing cells with voltage-sensitive proteins known as ion channels in their membranes. As a sensory cell takes in positive ions as a result of voltage-induced ion channel stimulation, its polarization state shifts and briefly reverses, resulting in the generation of an action potential. The action potential produces a nerve impulse that travels to the brain, causing a behavioral response in the animal. The specific behaviour produced is related to the type of electroreceptor involved.

Ampullary electroreceptors are used for passive electrolocation of the DC electric fields from prey organisms, predators, or conspecifics. The ability to sense other animals presumably gave electroreceptive fishes an advantage in navigating through dark or turbid water. Tuberous electroreceptors, which are found only in electroreceptive species of teleosts, are used for sensing the AC electric fields from electric organs, either for active electrolocation of objects or for social communication. Electric communication signals from electric organs can be quite elaborate and varied. A rich repertoire of electric signals is used for signaling threats, submission, alarm, and courtship, and some of electroreceptive fish have electric signals for sex, species, and individual recognition.