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SummaryA complete understanding of animal signal evolution necessitates analyses of both the proximate (e.g. anatomical and physiological) mechanisms of signal generation and reception, and the ultimate (i.e. evolutionary) mechanisms underlying adaptation and diversification. Here we summarize the results of a synthetic study of electric diversity in the species-rich neotropical electric fish genus Gymnotus. Our study integrates two research directions. The first examines the proximate causes of diversity in the electric organ discharge (EOD) – which is the carrier of both the communication and electrolocation signal of electric fishes – via descriptions of the intrinsic properties of electrocytes, electrocyte innervation, electric organ anatomy and the neural coordination of the discharge (among other parameters). The second seeks to understand the ultimate causes of signal diversity – via a continent-wide survey of species diversity, species-level phylogenetic reconstructions and field-recorded head-to-tail EOD (ht-EOD) waveforms (a common procedure for characterizing the communication component of electric fish EODs). At the proximate level, a comparative morpho-functional survey of electric organ anatomy and the electromotive force pattern of the EOD for 11 species (representing most major clades) revealed four distinct groups of species, each corresponding to a discrete area of the phylogeny of the genus and to a distinct type of ht-EOD waveform. At the ultimate level, our analyses (which emphasize the ht-EOD) allowed us to conclude that selective forces from the abiotic environment have had minimal impact on the communication component of the EOD. In contrast, selective forces of a biotic nature – imposed by electroreceptive predators, reproductive interference from heterospecific congeners, and sexual selection – may be important sources of diversifying selection on Gymnotus signals.

SUMMARYElectric fish evaluate the near environment by detecting changes in their self-generated electric organ discharge. To investigate impedance modulation of the self-generated electric field, this field was measured at the electrosensory fovea of Gymnotus carapo in the presence and absence of objects. Changes in local fields provoked by resistive objects were predicted by the change in total energy. Objects with capacitive impedance generated large variations in the relative importance of the different waveform components of the electric organ discharge. We tested the hypothesis that fish discriminate changes in waveform as well as increases in total energy using the novelty response, which is a behavioural response consisting of a transient acceleration of EOD frequency that can follow a change in object impedance. For resistive loads, the amplitude of novelty responses was well predicted by the increase in total energy. For complex loads, the amplitude of novelty responses was correlated not only with increases in total energy but also with waveform changes, consisting of reductions in the early slow negative wave and increases in the late sharp negative wave. The total energy and waveform effects appeared to be additive. These results indicate that G. carapo discriminates complex impedance based on an evaluation of different waveform parameters.

Local electric fields generated by the electric organ discharge of Gymnotus carapo were explored at selected points on the skin of an emitter fish (‘local self-generated fields’) and on the skin of a conspecific (‘local conspecific-generated fields’) using a specially designed probe. Local self-generated fields showed a constant pattern along the body of the fish. At the head, these fields were collimated, much stronger than elsewhere on the fish, and had a time waveform that was site-independent. This waveform consisted of a slow head-negative wave followed by a faster head-positive wave. In contrast, time waveforms in the trunk and tail regions were site-specific, with field vectors that changed direction over time. Local conspecific-generated fields were similar to the head-to-tail field, but their spatio-temporal pattern at the skin depended on the relative orientation between the receiving fish and the emitting fish. Because self-generated fields had a slow early component at the head region, they displayed a low-frequency peak in their power spectral density histograms. In contrast, the conspecific-generated fields had time waveforms with a sharper phase reversal, resulting in a peak at higher frequency than in the self-generated field. Lesions in emitting fish demonstrated that waveform components generated by the trunk and tail regions of the electric organ predominate in conspecific-generated fields, whereas waveform components generated by the abdominal region prevail in self-generated fields. Similar results were obtained from Brachyhypopomus pinnicaudatus. These results suggest that, in pulse-emitting gymnotids, electrolocation and electrocommunication signals may be carried by different field components generated by different regions of the electric organ.

This paper describes the peripheral mechanisms involved in signal processing of self- and conspecific-generated electric fields by the electric fish Gymnotus carapo. The distribution of the different types of tuberous electroreceptor and the occurrence of particular electric field patterns close to the body of the fish were studied. The density of tuberous electroreceptors was found to be maximal on the jaw (foveal region) and very high on the dorsal region of the snout (parafoveal region), decaying caudally. Tuberous type II electroreceptors were much more abundant than type I electroreceptors. Type I electroreceptors occurred exclusively on the head and rostral trunk regions, while type II electroreceptors were found along as much as 90 % of the fish. Electrophysiological data indicated that conspecific- and self-generated electric currents are ‘funnelled’ by the high conductivity and geometry of the body of the fish. These currents are concentrated at the peri-oral zone, where most electroreceptors are located. Moreover, within this region, field vector directions were collimated, constituting the most efficient stimulus for electroreceptors. It can be concluded that the passive properties of the fish tissue represent a pre-receptor device that enhances exafferent and reafferent electrical signals at the fovea–parafoveal region.

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.