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

2018; Elsevier BV; Volume: 28; Issue: 22 Linguagem: Inglês

10.1016/j.cub.2018.09.036

1879-0445

Martin Gottwald, Neha Singh, André N Haubrich, Sophia Regett, Gerhard von der Emde,

Ichthyology and Marine Biology

Many sighted animals use color as a salient and reliable cue [1Kelber A. Jacobs G.H. Evolution of Color Vision.in: Kremers J. Baraas R.C. Marshall N.J. Human Color Vision. Springer, Switzerland2016: 317-354Crossref Google Scholar] to identify conspecifics [2Detto T. The fiddler crab Uca mjoebergi uses colour vision in mate choice.Proc. Biol. Sci. 2007; 274: 2785-2790Crossref PubMed Scopus (65) Google Scholar, 3Couldridge V. Alexander G.J. Color patterns and species recognition in four closely related species of Lake Malawi cichlid.Behav. Ecol. 2002; 13: 59-64Crossref Scopus (106) Google Scholar, 4Tamura N. Fujii Y. Boonkhaw P. Prayoon U. Kanschanasaka B. Colour vision in Finlayson’s squirrel (Callosciurus finlaysonii): is conspicuous pelage colour useful for species recognition?.Trop. Zool. 2017; 30: 1-15Crossref Scopus (4) Google Scholar], predators, or food [5Lunau K. Maier E.J. Innate colour preferences of flower visitors.J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1995; 177: 1-19Crossref Scopus (220) Google Scholar, 6Kawamura G. Bagarinao T.U. Bin Asmad M.F. Lim L.-S. Food colour preference of hatchery-reared juveniles of African catfish Clarias gariepinus.Appl. Anim. Behav. Sci. 2017; 196: 119-122Abstract Full Text Full Text PDF Scopus (9) Google Scholar, 7Taylor L.A. Maier E.B. Byrne K.J. Amin Z. Morehouse N.I. Colour use by tiny predators: jumping spiders show colour biases during foraging.Anim. Behav. 2014; 90: 149-157Crossref Scopus (39) Google Scholar]. Similarly, nocturnal, weakly electric fish Gnathonemus petersii might rely on “electric colors” [8Budelli R. Caputi A.A. The electric image in weakly electric fish: perception of objects of complex impedance.J. Exp. Biol. 2000; 203: 481-492PubMed Google Scholar] 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) [9von der Emde G. Ruhl T. Matched Filtering in African Weakly Electric Fish: Two Senses with Complementary Filters.in: von der Emde G. Warrant E. The Ecology of Animal Senses. Springer, Switzerland2015: 237-263Google Scholar, 10von der Emde G. Bleckmann H. Differential responses of two types of electroreceptive afferents to signal distortions may permit capacitance measurement in a weakly electric fish, Gnathonemus petersii.J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1992; 171: 683-694Crossref Scopus (52) Google Scholar, 11von der Emde G. Ronacher B. Perception of electric properties of objects in electrolocating weakly electric fish: two-dimensional similarity scaling reveals a City-Block metric.J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1994; 175: 801-812Crossref Scopus (48) Google Scholar, 12von der Emde G. Schwarz S. Imaging of objects through active electrolocation in Gnathonemus petersii.J. Physiol. Paris. 2002; 96: 431-444Crossref PubMed Scopus (56) Google Scholar]. Electrical capacitive objects (animals, plants) modulate both parameters; resistive targets (e.g., rocks) modulate only the signal’s amplitude [11von der Emde G. Ronacher B. Perception of electric properties of objects in electrolocating weakly electric fish: two-dimensional similarity scaling reveals a City-Block metric.J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1994; 175: 801-812Crossref Scopus (48) Google Scholar, 12von der Emde G. Schwarz S. Imaging of objects through active electrolocation in Gnathonemus petersii.J. Physiol. Paris. 2002; 96: 431-444Crossref PubMed Scopus (56) Google Scholar]. 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 [8Budelli R. Caputi A.A. The electric image in weakly electric fish: perception of objects of complex impedance.J. Exp. Biol. 2000; 203: 481-492PubMed Google Scholar, 13Caputi A.A. Budelli R. Peripheral electrosensory imaging by weakly electric fish.J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2006; 192: 587-600Crossref PubMed Scopus (91) Google Scholar, 14Gottwald M. Bott R.A. von der Emde G. Estimation of distance and electric impedance of capacitive objects in the weakly electric fish Gnathonemus petersii.J. Exp. Biol. 2017; 220: 3142-3153Crossref PubMed Scopus (5) Google Scholar], 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 [15Stevens K.A. The vision of David Marr.Perception. 2012; 41: 1061-1072Crossref PubMed Scopus (8) Google Scholar], reliability, and use of which resemble those of color in vision. This suggests “color” perception as a sensory concept beyond vision and passive sensing.