Fish have eyes, but they live in a much more complex sensory world, where even electricity plays a surprising - and convergent - role.

A number of fish possess an active electric sense – they can generate electric fields with an electric organ (EO) and receive electric signals with specialised electroreceptors. Electrogenesis has evolved independently in at least six lineages of teleosts and elasmobranchs, which can be subdivided into strongly and weakly electric fish according to the power of their electric discharge. The electric eel (Electrophorus electricus) is probably the best-known representative of the strongly electric fish that produce electric shocks of up to several hundred volts mainly for stunning prey or predators. Weak electric discharges of no more than a few volts are generated by several hundred species of marine and freshwater fish, but best studied are two speciose freshwater lineages that present remarkable examples of convergence. The African Mormyriformes (which comprise the Mormyridae or elephantfish and the Gymnarchidae with Gymnarchus niloticus as the only species) and the South American Gymnotiformes (or Neotropical knifefish) are only distantly related and have evolved their strikingly similar mechanisms of signal generation and recognition completely separately. Both groups use electric signals for active electrolocation and sophisticated electrocommunication. This dual function could explain why EOs with weak discharges, which have been hypothesised to represent an intermediate stage in the evolution of more powerful EOs, were retained.

Generation and reception of electric signals

The EOs of electric fish consist of modified muscle or nerve cells called electrocytes, the potentials of which are summed and delivered simultaneously to the surrounding water as an electric organ discharge (EOD). Discharge patterns are generated by a hierarchy of control nuclei in different regions of the brain and can be categorised into two types: pulse and wave. Pulse-type EODs are brief, often multi-phasic pulses emitted at irregular intervals, while wave-type EODs are longer lasting, often monophasic (forming a sine wave-like pattern) and delivered constantly within a certain frequency band. EODs show great diversity, due to physiological differences in, for example, the type, density and distribution of ion channels in electrocyte membranes or the mode of EO innervation. Complex pulse and wave discharges have evolved in both the mormyriforms and gymnotiforms and within the latter, pulse-type EODs have probably arisen independently in several families.

The self-generated electric fields as well as those of other fish are perceived with sensitive electroreceptors that convert external electrical stimuli into internal neural responses. They are usually widely distributed over the body surface but more densely clustered around the head. Mormyriforms and gymnotiforms have independently evolved tuberous receptors that consist of a jelly-filled canal covered by an epithelial cell plug and are tuned to the high-frequency components of a species’ EOD. Mormyriforms possess two types of tuberous receptor – so-called Knollenorgans are employed in communication and mormyromasts in electrolocation. In gymnotiforms, one tuberous receptor type is specialised for detecting the amplitude of a stimulus and another for timing, but both are used for electrolocation as well as communication. Similar computational algorithms for the sensory processing of temporal cues have evolved several times, for example at least twice within the mormyriforms. The mechanisms for time coding and time comparison are furthermore reminiscent of those used by barn owls to process auditory stimuli, as both rely on neural delay lines and coincidence detectors.

Electrolocation

Electric fish can detect and identify objects in their surroundings by sensing the minute perturbations these objects make in their self-generated electric field, a process referred to as active electrolocation. It allows them to analyse and distinguish the distance, form and electrical properties of objects and thus to ‘see’ these objects in conditions where vision is impaired (e.g. in murky waters or at night). Weakly electric fish usually swim with a stiff body, as this makes it easier for them to register the distortions of the isopotential lines.

Electrolocation has parallels with echolocation, and like the echolocation calls of bats, the EODs of electric fish are shaped by the environment (as the type of microhabitat is likely to affect the efficiency of different electric signals). Ultra-brief signals, for example, that detect a wider range of impedances from objects have evolved independently in mormyriforms and gymnotiforms. In contrast to echolocation, however, electrolocation only works over short distances, because signal amplitude rapidly decreases with distance. The electric image falling on the receptors is blurred, and resolution depends on electroreceptor density. Some weakly electric fish (e.g. Gnathonemus petersii) evidently possess electric foveae analogous to the auditory fovea of echolocating bats or the fovea of the eye.

Electrocommunication

Electric communication is well developed (and, of course, convergent) in gymnotiforms and mormyriforms. By combining their electrogenic and electroceptive capacities, these fish are able to communicate with electric signals – the EOD of a signaller is sensed by a receiver at a distance. As EODs are complex and diverse, they can convey a great deal of information. EOD waveforms are species-specific and have often been shown to be particularly divergent in sympatric species (e.g. in the genera Campylomormyrus, Marcusenius and Mormyrops). They might act as ‘species markers’, facilitating species recognition during mate choice. Thus, the electrosensory system has probably been a major stimulus (so to speak) in the evolutionary diversification of weakly electric fish, affecting the formation and maintenance of species boundaries within rapidly radiating groups. But EOD waveforms do not only differ between species, but often also between the sexes or age classes; in some species, they are even individually distinct.

The pattern of discharges is involved in signalling aspects of complex social behaviour such as aggression, submission, threat or alarm and might also function in courtship. Not much is known about the use of electric signals in courtship, but a recent study on the mormyrid Brienomyrus brachyistius has shed some light. Males and females of this species performed electrical duetting, where they exchanged ‘rasps’ and ‘bursts’. Potential functions of these duets could be to evaluate the quality of or maintain contact with a potential mate or to indicate mutual interest.

A more unusual example of a communicative function of electric signals involves a piscivorous mormyrid, the Cornish jack (Mormyrops anguilloides). This electric fish preys on rock-dwelling cichlids in Lake Malawi and forms stable predatory associations of 2-10 individuals, reminiscent of the hunting packs observed in socially foraging carnivores and cetaceans. Although no coordinated hunting tactics were obvious, group members produced synchronised EOD bursts that have been interpreted as pack cohesion signals.