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

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

doi:10.1016/j.cub.2018.09.036

Cited by 24 publications

(20 citation statements)

References 40 publications

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“…Although two parameters are not enough to determine the impedance of an object, it has been shown that one can define families of impedance values that, independently of their position, modify reafferent signals in such a way that phase and strength are related by a linear function, defining an electric qualia likened to 'electric color' (Budelli and Caputi, 2000). Recent experimental evidence supports this hypothesis (Gottwald et al, 2018).…”

Section: Introductionmentioning

confidence: 79%

“…In pulse Mormyriformes, electroreceptors have a flat frequency sensitivity within a range of two orders of magnitude (Bell, 1990a, b). Thus, stimulus strength and phase spectrum may be considered the only two dimensions of a manifold where the 'electric color' of species, sex (Hopkins and Bass, 1981;Hopkins, 1986) and object impedance (von der Emde, 1990;von der Emde and Bleckmann, 1992;Gottwald et al, 2018) are represented. The present results show dual encoding of amplitude and phase spectral cues by each receptor type in G. omarorum.…”

Section: Resultsmentioning

confidence: 99%

“…Cues embodied in the changes of the phase spectra of the species-specific allo-and self-generated electric fields are relevant in pulse-emitting Mormyriformes for species and sex identification (Hopkins and Baas, 1981;Hopkins, 1986) and also to discriminate object impedance (von der Emde, f1990; von der Emde and Bleckmann, 1992;Gottwald et al, 2018). These teleosts possess an electrosensory path to sense the discharge of other fish (Bell and Grant, 1989).…”

Section: Introductionmentioning

confidence: 99%

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Encoding phase spectrum for evaluating “electric qualia”

Caputi

Aguilera

2019

Journal of Experimental Biology

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The most broadly expressed and studied aspect of sensory transduction is receptor tuning to the power spectral density of the incoming signals. Temporal cues expressed in the phase spectrum are relevant in African and American pulse-emitting electric fish showing electroreceptors sensing the signals carried by the selfand conspecific-generated electric organ discharges. This article concerns the role of electroreceptor phase sensitivity in American pulse Gymnotiformes. These fish show electroreceptors sharply tuned to narrow frequency bands. This led to the common thought that most electrosensory information is contained in the amplitude spectra of the signals. However, behavioral and modeling studies suggest that in their pulses, Gymnotiformes electroreceptors also encode cues embodied in the phase spectrum of natural stimuli. Here, we show that the two main types of tuberous primary afferents of Gymnotus omarorum differentially respond to cues embodied in the amplitude and phase spectra of self-generated electrosensory signals. One afferent type, pulse markers, is mainly driven by the amplitude spectrum, while the other, burst coders, is predominantly sensitive to the phase spectrum. This dual encoding strategy allows the fish to create a sensory manifold where patterns of 'electric color' generated by object impedance and other potential sources of 'colored' images (such as large nearby objects and other electric fish) can be represented.

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Section: Introductionmentioning

confidence: 79%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Encoding phase spectrum for evaluating “electric qualia”

Caputi

Aguilera

2019

Journal of Experimental Biology

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“…Regarding EOD divergence, the major role of electrolocation in prey recognition is well established, as the natural habitat of Campylomormyrus has extremely low-light conditions due to the high-level of suspended particulate matter and turbidity in the system (Stiassny and Alter 2015), in addition to our species being nocturnal. Recent studies showed that nocturnal weakly electric fish perceive electric colors for fast and reliable prey recognition (Gottwald et al 2018). It has been shown that snout morphology and EOD characteristics are correlated, such that long putatively derived EODs are exhibited by long snouted species (Tiedemann et al 2010).…”

Section: Discussionmentioning

confidence: 99%

Morphological differentiation in African weakly electric fish (genus Campylomormyrus) relates to substrate preferences

et al. 2020

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Under an ecological speciation scenario, the radiation of African weakly electric fish (genus Campylomormyrus) is caused by an adaptation to different food sources, associated with diversification of the electric organ discharge (EOD). This study experimentally investigates a phenotype-environment correlation to further support this scenario. Our behavioural experiments showed that three sympatric Campylomormyrus species with significantly divergent snout morphology differentially react to variation in substrate structure. While the short snout species (C. tamandua) exhibits preference to sandy substrate, the long snout species (C. rhynchophorus) significantly prefers a stone substrate for feeding. A third species with intermediate snout size (C. compressirostris) does not exhibit any substrate preference. This preference is matched with the observation that long-snouted specimens probe deeper into the stone substrate, presumably enabling them to reach prey more distant to the substrate surface. These findings suggest that the diverse feeding apparatus in the genus Campylomormyrus may have evolved in adaptation to specific microhabitats, i.e., substrate structures where these fish forage. Whether the parallel divergence in EOD is functionally related to this adaptation or solely serves as a prezygotic isolation mechanism remains to be elucidated. by Tonio Pieterek. Matlab scripts were inspired by Volker Hofmann.Author's contribution RA participated in the design of the study, carried out the experiments, analysed the data and drafted the manuscript; RN participated in the design of the experiment and critically revised the manuscript; MH carried out the feeding experiments of the C. tamandua individuals under the supervision of RA and RT. RT and FK conceived, participated in the design and coordinated the study. RA and RT revised the manuscript after an initial review. All authors have read and approved the manuscript for publication.

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“…Recent work on mormyrid electrolocation has revealed that animals, plants, and invertebrates all create unique amplitude and waveform modulations referred to “electric colors” that allow these animals to reliably identify and differentiate these items (Gottwald et al. 2018), indicating that different EOD waveforms could therefore differ in their range of “electric color” detections.…”

Section: Discussionmentioning

confidence: 99%

Genetic drift does not sufficiently explain patterns of electric signal variation among populations of the mormyrid electric fishParamormyrops kingsleyae

et al. 2020

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Communication signals serve crucial survival and reproductive functions. In Gabon, the widely distributed mormyrid fishParamormyrops kingsleyae emits an electric organ discharge (EOD) signal with a dual role in communication and electrolocation that exhibits remarkable variation: populations of P. kingsleyae have either biphasic or triphasic EODs, a feature that characterizes interspecific signal diversity among the Paramormyrops genus. We quantified variation in EODs of 327 P. kingsleyae from nine populations and compared it to genetic variation estimated from microsatellite loci. We found no correlation between electric signal and genetic distances, suggesting that EOD divergence cannot be explained by drift alone. An alternative hypothesis is that EOD differences are used for mate discrimination, which would require P. kingsleyae be capable of differentiating between divergent EOD waveforms. Using a habituation-dishabituation assay, we found that P. kingsleyae can discriminate between biphasic and triphasic EOD types. Nonetheless, patterns of genetic and electric organ morphology divergence provide evidence for hybridization between these signal types. Although reproductive isolation with respect to signal type is incomplete, our results suggest that EOD variation in P. kingsleyae could be a cue for assortative mating. K E Y W O R D S : Animal communication, electric organ, electrocytes, genetic drift, signal evolution, weakly electric fish.

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

Cited by 24 publications

References 40 publications

Encoding phase spectrum for evaluating “electric qualia”

Encoding phase spectrum for evaluating “electric qualia”

Morphological differentiation in African weakly electric fish (genus Campylomormyrus) relates to substrate preferences

Genetic drift does not sufficiently explain patterns of electric signal variation among populations of the mormyrid electric fishParamormyrops kingsleyae

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