scholarly journals Derived loss of signal complexity and plasticity in a genus of weakly electric fish

2021 ◽  
Author(s):  
David E. Saenz ◽  
Tingting Gu ◽  
Yue Ban ◽  
Kirk O. Winemiller ◽  
Michael R. Markham

AbstractSignal plasticity can maximize the usefulness of costly animal signals such as the electric organ discharges (EODs) of weakly electric fishes. Some species of the order Gymnotiformes rapidly alter their EOD amplitude and duration in response to circadian cues and social stimuli. How this plasticity is maintained across related species with different degrees of signal complexity is poorly understood. In one genus of weakly electric gymnotiform fish (Brachyhypopomus) only one species, B. bennetti, produces a monophasic signal while all other species emit complex biphasic or multiphasic EOD waveforms produced by two overlapping but asynchronous action potentials in each electric organ cell (electrocyte). One consequence of this signal complexity is the suppression of low-frequency signal content that is detectable by electroreceptive predators. In complex EODs, reduction of the EOD amplitude and duration during daytime inactivity can decrease both predation risk and the metabolic cost of EOD generation. We compared EOD plasticity and its underlying physiology in Brachyhypopomus focusing on B. bennetti. We found that B. bennetti exhibits minimal EOD plasticity, but that its electrocytes retained vestigial mechanisms of biphasic signaling and vestigial mechanisms for modulating the EOD amplitude. These results suggest that this species represents a transitional phenotypic state within a clade where signal complexity and plasticity were initially gained and then lost. We discuss potential the roles of signal mimicry, species recognition, and sexual selection in maintaining the monophasic EOD phenotype in the face of detection by electroreceptive predators.

Author(s):  
David E. Saenz ◽  
Tingting Gu ◽  
Yue Ban ◽  
Kirk O. Winemiller ◽  
Michael R. Markham

Signal plasticity can maximize the usefulness of costly animal signals such as the electric organ discharges (EODs) of weakly electric fishes. Some species of the order Gymnotiformes rapidly alter their EOD amplitude and duration in response to circadian cues and social stimuli. How this plasticity is maintained across related species with different degrees of signal complexity is poorly understood. In one genus of weakly electric gymnotiform fish (Brachyhypopomus) only one species, B. bennetti, produces a monophasic signal while all other species emit complex biphasic or multiphasic EOD waveforms produced by two overlapping but asynchronous action potentials in each electric organ cell (electrocyte). One consequence of this signal complexity is the suppression of low-frequency signal content that is detectable by electroreceptive predators. In complex EODs, reduction of the EOD amplitude and duration during daytime inactivity can decrease both predation risk and the metabolic cost of EOD generation. We compared EOD plasticity and its underlying physiology in Brachyhypopomus focusing on B. bennetti. We found that B. bennetti exhibits minimal EOD plasticity, but that its electrocytes retained vestigial mechanisms of biphasic signaling and vestigial mechanisms for modulating the EOD amplitude. These results suggest that this species represents a transitional phenotypic state within a clade where signal complexity and plasticity were initially gained and then lost. Signal mimicry, mate recognition, and sexual selection are potential factors maintaining the monophasic EOD phenotype in the face of detection by electroreceptive predators.


Author(s):  
Stefan Mucha ◽  
Lauren J. Chapman ◽  
Rüdiger Krahe

AbstractAnthropogenic environmental degradation has led to an increase in the frequency and prevalence of aquatic hypoxia (low dissolved oxygen concentration, DO), which may affect habitat quality for water-breathing fishes. The weakly electric black ghost knifefish, Apteronotus albifrons, is typically found in well-oxygenated freshwater habitats in South America. Using a shuttle-box design, we exposed juvenile A. albifrons to a stepwise decline in DO from normoxia (> 95% air saturation) to extreme hypoxia (10% air saturation) in one compartment and chronic normoxia in the other. On average, A. albifrons actively avoided the hypoxic compartment below 22% air saturation. Hypoxia avoidance was correlated with upregulated swimming activity. Following avoidance, fish regularly ventured back briefly into deep hypoxia. Hypoxia did not affect the frequency of their electric organ discharges. Our results show that A. albifrons is able to sense hypoxia at non-lethal levels and uses active avoidance to mitigate its adverse effects.


1999 ◽  
Vol 202 (10) ◽  
pp. 1205-1215 ◽  
Author(s):  
G. von der Emde

Weakly electric fish produce electric signals (electric organ discharges, EODs) with a specialised electric organ creating an electric field around their body. Objects within this field alter the EOD-induced current at epidermal electroreceptor organs, which are distributed over almost the entire body surface. The detection, localisation and analysis of objects performed by monitoring self-produced electric signals is called active electrolocation. Electric fish employ active electrolocation to detect objects that are less than 12 cm away and have electric properties that are different from those of the surrounding water. Within this range, the mormyrid Gnathonemus petersii can also perceive the distance of objects. Depth perception is independent of object parameters such as size, shape and material. The mechanism for distance determination through electrolocation involves calculating the ratio between two parameters of the electric image that the object projects onto the fish's skin. Electric fish can not only locate objects but can also analyse their electrical properties. Fish are informed about object impedance by measuring local amplitude changes at their receptor organs evoked by an object. In addition, all electric fish studied so far can independently determine the capacitative and resistive components of objects that possess complex impedances. This ability allows the fish to discriminate between living and non-living matter, because capacitance is a property of living organisms. African mormyrids and South American gymnotiforms use different mechanisms for capacitance detection. Mormyrids detect capacitance-evoked EOD waveform distortions, whereas gymnotiforms perform time measurements. Gymnotiforms measure the temporal phase shift of their EODs induced at body parts close to the object relative to unaffected body parts further away.


2002 ◽  
Vol 205 (16) ◽  
pp. 2525-2533 ◽  
Author(s):  
Stefan Schuster

SUMMARYGymnotiform weakly electric fish find their way in the dark using a continuously operating active sensory system. An electric organ generates a continuous train of discharges (electric organ discharges, EODs), and tuberous high-frequency electroreceptors monitor the pattern of transcutaneous current flow associated with each EOD. Here, I report that a prior interruption to the continuous train of EODs dramatically affects a response shown by many pulse-type gymnotids. In this so-called novelty response, fish normally raise their electrosensory sampling rate in response to novel sensory stimuli. The gymnotid Gymnotus carapo was induced to pause its EODs briefly, and the novelty response to sensory stimuli given post-pause was analyzed. Mechanosensory stimuli given as early as 20 EODs after a pause elicited clear novelty responses, but strong high-frequency electrical stimuli were ineffective at this time. Moreover, high-frequency electrical stimuli remained less efficient in eliciting normal-sized responses until approximately 2000 EODs, or 40s, after a pause. The post-pause inefficiency of high-frequency stimuli was not due to an inappropriate choice of intensity or their temporal patterning and did not result from the stimulation that caused the pausing. Low-frequency stimuli that also recruited ampullary electroreceptors were more efficient than high-frequency stimuli in eliciting post-pause responses. These findings show that continuous activity is required either to maintain sensitivity to high-frequency electrical stimuli or to ensure that such stimuli are able to modulate efficiently the pacemaker that sets the discharge frequency.


1993 ◽  
Vol 71 (11) ◽  
pp. 2301-2310 ◽  
Author(s):  
Günther K. H. Zupanc ◽  
Leonard Maler

Apteronotus leptorhynchus, a gymnotiform fish, produces highly regular electric organ discharges of 600–1000 Hz. Short-term modulations of the electric organ discharge ("chirps") were elicited by imitating the discharges of neighboring fish. Chirps displayed an increase in frequency of approximately 100 Hz, a duration of about 15 ms, and an absolute amplitude of 0.5–2 mV. Since, similar to natural conditions, chirps summated with the beat caused by interference of the fish's own electric organ discharge and the imitating discharge, the size and shape of the chirp's amplitude envelope varied greatly according to its phase relative to the beat cycle; however, the frequency of the chirp amplitude modulation was always 50–100 Hz. All 21 males examined chirped, but their rate of chirping varied considerably (range 2–59 chirps/30 s; mean 22 chirps/30 s). In contrast, only one out of nine females chirped (mean 0.25 chirps/30 s). The latency between stimulus onset and first chirp was variable and often long (range 1.0–25.0 s; median 3.3 s). We propose that chirps are not a sensory reflex but a communicatory behavior regulated by hypothalamic peptidergic input.


2010 ◽  
Vol 7 (2) ◽  
pp. 197-200 ◽  
Author(s):  
Vincent Fugère ◽  
Hernán Ortega ◽  
Rüdiger Krahe

Animals often use signals to communicate their dominance status and avoid the costs of combat. We investigated whether the frequency of the electric organ discharge (EOD) of the weakly electric fish, Sternarchorhynchus sp., signals the dominance status of individuals. We correlated EOD frequency with body size and found a strong positive relationship. We then performed a competition experiment in which we found that higher frequency individuals were dominant over lower frequency ones. Finally, we conducted an electrical playback experiment and found that subjects more readily approached and attacked the stimulus electrodes when they played low-frequency signals than high-frequency ones. We propose that EOD frequency communicates dominance status in this gymnotiform species.


2000 ◽  
Vol 203 (9) ◽  
pp. 1433-1446 ◽  
Author(s):  
S. Schuster

During their entire lives, weakly electric fish produce an uninterrupted train of discharges to electrolocate objects and to communicate. In an attempt to learn about activity-dependent processes that might be involved in this ability, the continuous train of discharges of intact Gymnotus carapo was experimentally interrupted to investigate how this pausing affects post-pause electric organ discharges. In particular, an analysis was conducted of how the amplitude and relative timing of the three major deflections of the complex discharge change over the course of the first 1000 post-pause discharges. The dependence of these variables on the duration of the preceding pause and on water temperature is analysed. In addition, pause-induced small reverberations at the end of the discharge are described. Common to all amplitude changes is a fast initial decrease in amplitude with a slow recovery phase; amplitude changes scale with the duration of the preceding pause and are independent of the interdischarge interval. The absence of changes in the postsynaptic-potential-derived first phase of the discharge together with changes in the amplitude ratio of the third and fourth deflections suggest that the amplitude changes are mainly due to pause-induced changes in the inner resistance of the electric organ. A model is formulated that approximates the pattern of amplitude changes. The post-pause changes described here may provide a new way to test current models of complex discharge generation in Gymnotus carapo and illustrate the speed at which changes of an electric organ discharge can take place.


2018 ◽  
Vol 5 (2) ◽  
pp. 170443 ◽  
Author(s):  
Rebecca Nagel ◽  
Frank Kirschbaum ◽  
Jacob Engelmann ◽  
Volker Hofmann ◽  
Felix Pawelzik ◽  
...  

Effective communication among sympatric species is often instrumental for behavioural isolation, where the failure to successfully discriminate between potential mates could lead to less fit hybrid offspring. Discrimination between con- and heterospecifics tends to occur more often in the sex that invests more in offspring production, i.e. females, but males may also mediate reproductive isolation. In this study, we show that among two Campylomormyrus African weakly electric fish species, males preferentially associate with conspecific females during choice tests using live fish as stimuli, i.e. when all sensory modalities potentially used for communication were present. We then conducted playback experiments to determine whether the species-specific electric organ discharge (EOD) used for electrocommunication serves as the cue for this conspecific association preference. Interestingly, only C. compressirostris males associated significantly more with the conspecific EOD waveform when playback stimuli were provided, while no such association preference was observed in C. tamandua males. Given our results, the EOD appears to serve, in part, as a male-mediated pre-zygotic isolation mechanism among sympatric species. However, the failure of C. tamandua males to discriminate between con- and heterospecific playback discharges suggests that multiple modalities may be necessary for species recognition in some African weakly electric fish species.


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