Electric-Color Sensing in Weakly Electric Fish Suggests Color Perception as a Sensory Concept beyond Vision

Many sighted animals use color as a salient and reliable cue [1] to identify conspecifics [2-4], predators, or food [5-7]. Similarly, nocturnal, weakly electric fish Gnathonemus petersii might rely on "electric colors" [8] for unambiguous, critical object recognitions. These fish identify nearby targets by emitting electric signals and by sensing the object-evoked signal modulations in amplitude and waveform with two types of epidermal electroreceptors (active electrolocation) [9-12]. Electrical capacitive objects (animals, plants) modulate both parameters; resistive targets (e.g., rocks) modulate only the signal's amplitude [11, 12]. Ambiguities of electrosensory inputs arise when object size, distance, or position vary. While previous reports suggest electrosensory disambiguations when both modulations are combined as electric colors [8, 13, 14], this concept has never been demonstrated in a natural, behaviorally relevant context. Here, we assessed electric-color perception (1) by recording object-evoked signal modulations and (2) by testing the fishes' behavioral responses to these objects during foraging. We found that modulations caused by aquatic animals or plants provided electric colors when combined as a ratio. Individual electric colors designated crucial targets (electric fish, prey insect larvae, or others) irrespective of their size, distance, or position. In behavioral tests, electrolocating fish reliably identified prey insect larvae of varying sizes from different distances and did not differentiate between artificial prey items generating similar electric colors. Our results indicate a color-like perceptual cue during active electrolocation, the computation [15], reliability, and use of which resemble those of color in vision. This suggests "color" perception as a sensory concept beyond vision and passive sensing.