EODf and chirping

EODf was 138.6±23.7 Hz (mean±s.e.m.; Table 1). Fish often responded to playbacks by rapidly modulating their EOD, which is characteristic of electric fish responding to a social stimulus. We use the term ‘chirp’ here to describe these modulations, based on their relatively short duration and associated abrupt increases and decreases in EODf (after Hagedorn and Heiligenberg, 1985). Across individuals, chirp rate ranged from 0.48 to 2.12 chirps min⁻¹. Fish chirped primarily when playback stimuli were presented, although one fish also chirped spontaneously during the baseline recording. Spontaneous chirping has been reported in other gymnotiform species, although as in the current study, chirping occurs most often during social interactions or in response to playbacks (Zupanc et al., 2001; Kolodziejski et al., 2007; Dunlap et al., 2010). There was no relationship between chirp rate and the difference frequency of the playback (F_10,30=1.24, P=0.31). A typical D. conirostris chirp began with a small (approximately 10–30 Hz) increase in EODf followed by a brief cessation of the EOD that lasted approximately 20–25 ms. The EOD resumed at a slightly lower frequency but then increased quickly to baseline (Fig. 1A,B). However, some chirps consisted of only an increase or decrease in frequency, not both. A small subset of chirps (<10%) had short durations (∼25 ms) that created a phase shift of a single EOD cycle rather than interrupting multiple EOD cycles. These shorter chirps tended to occur in brief bursts of 3–7 chirps (Fig. 1C). Across all fish and all chirps, chirp duration averaged 90.8±5.8 ms.

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Fig. 1.

Representative Distocyclus conirostris chirps. (A,B) Electric organ discharge frequency (EODf) (top traces) and head–tail EOD voltage (bottom traces) during chirps of two different D. conirostris individuals. EODf transiently increased then decreased before returning to baseline. These chirps interrupted the EOD. The frequency undershoot lasts several EOD cycles, which indicates that this frequency increase and decrease is not an artifact of the missed EOD cycles. Durations of the chirps were 89 ms (A) and 104 ms (B). (C) A small subset of chirps (11 of 169) were substantially shorter in duration than other chirps (26–27 ms). These chirps tended to occur in small clusters. The shorter duration chirps were not accompanied by an interruption of the EOD but instead caused a phase advance of a single EOD cycle.

The D. conirostris chirps were similar in structure to Eigenmannia chirps, which have a rapid increase and decrease in EODf, last 20–100 ms, and vary in duration based on social context (Hopkins, 1974b; Hagedorn and Heiligenberg, 1985). However, we did not observe the long interruptions that have been found in Eigenmannia during live courtship interactions (Hagedorn and Heiligenberg, 1985; Hopkins, 1974b). It is possible that D. conirostris can produce longer interruptions, but that our experimental paradigm (i.e. chirp chamber recordings in response to one playback stimulus at a time) was not sufficient to elicit them. That is, as D. conirostris are social like Eigenmannia, and are typically exposed simultaneously to signals of many individuals, they might not produce their full repertoire of signals in response to the signal of a single fish or in the absence of multiple live conspecifics (Stöckl et al., 2014). Moreover, because the fish were collected at the end of the rainy season and their gonads had largely regressed, they might not have produced signals used only during spawning. Because we were able to record signals from only four D. conirostris, we are unable to assess individual variation in chirping or the JAR or whether chirps or EODf are sexually dimorphic, as they are in other gymnotiform species (Smith, 2013). The D. conirostris chirps recorded in this study were similar to – although shorter than – the short (∼800 ms) interruptions of Sternopygus (Hopkins, 1974a). Like those interruptions, D. conirostris chirps often began with a frequency increase and ended with a frequency undershoot below baseline. Thus, it appears that the general patterns in EOD modulations are largely conserved across these three genera.

JAR

Distocyclus conirostris shifted EODf at the onset of a conspecific signal mimic (Fig. 2). When fish were presented with a stimulus frequency higher than their own EODf, they consistently decreased EODf for the duration of the playback and then increased EODf back to baseline after playback cessation (Fig. 2A). However, when fish were presented with stimuli lower in frequency than their own EOD, the direction of the JAR varied: fish increased EODf in eight of 20 trials with stimulus frequencies lower than their EODf (40%, jamming avoidance; Fig. 2B), but decreased EODf in 12 trials (60%, anti-jamming avoidance; Fig. 2C). Specifically, all four fish raised EODf in response to the −3 Hz playback, two fish raised EODf in response to the −5 Hz playback, and two fish raised EODf in response to the −40 Hz playback (Fig. 2D). None of the fish raised EODf in response to the −10 Hz or −20 Hz playback. In two cases, the fish first raised and then lowered its EODf in response to higher-frequency stimuli. The difference frequency of the playback and the EODf change during the JAR were not linearly correlated across the entire range of playback difference frequencies (R²=0.02, P=0.40). However, examining the positive and negative playback differences separately revealed a significant linear correlation for positive playback difference frequencies (playback frequency >EODf; R²=0.31, P=0.01) but no correlation for negative playback difference frequencies (R²=0.05, P=0.32). The same pattern of jamming and anti-jamming responses to positive and negative difference frequencies was observed when the magnitude of the JAR was plotted versus the steady-state difference frequency (i.e. the difference between the stimulus frequency and the fishes' EODf near the end of the playback stimulus; Fig. 2E).

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Fig. 2.

Anomalous jamming avoidance response in D. conirostris. Fish shifted EODf (blue line) when presented with a stimulus of a similar frequency (red line). Distocyclus conirostris (A) decreased or (B) increased EODf to shift EODf away from that of the stimulus (i.e. jamming avoidance). (C) In response to playbacks below the fish's own EODf, fish often performed anomalous, ‘anti-jamming’ responses that decreased rather than increased the difference between the fishes' EODf and playback frequency. In this example, a stimulus 10 Hz below the fishes' EODf elicited a decrease, rather than an increase, in EODf. EODf gradually returned to baseline after stimulus offset. Arrowhead indicates a chirp. (D) Fish responded differently to higher- versus lower-frequency playbacks. The difference frequency (DF) of the stimulus relative to the fishes' baseline EODf is plotted versus the change in EODf in response to the playback stimulus. For stimuli higher in frequency than the fish's EOD (i.e. positive playback DFs), all fish lowered EODf, with the most robust responses to the DFs closest to zero. For stimuli lower in frequency than the fish's EOD (negative playback DFs), the direction of the frequency shift was less consistent. Individual fish are shown with different colored squares; open black circles  are means (±s.e.m.). (E) Same data as in D, with the x-axis showing the steady-state DF (i.e. the difference between the stimulus frequency and the fish's EODf after its response to the stimulus reached steady state).

Like Eigenmannia, but unlike Sternopygus, D. conirostris shifted EODf at the onset of a playback stimulus. Sternopygus is largely solitary and territorial, but Eigenmannia forms large social aggregations (Hopkins, 1974a; Stamper et al., 2010; Tan et al., 2005). We strongly suspect that D. conirostris is gregarious like Eigenmannia, as D. conirostris are typically found in groups clustered around floating vegetation when they are collected (J.A.A.-G., personal observation). Both Eigenmannia and D. conirostris demonstrate the physiological capability for a bi-directional JAR, but Sternopygus does not. This could suggest that the JAR is critical for species that regularly co-exist with nearby conspecifics producing interfering signals but less important for species that live solitary lifestyles. However, the situation may be more complicated for several reasons. First, Sternopygus does not show impaired electrolocation from signals with similar frequencies presented at ecologically relevant amplitudes, which obviates the need for a neural strategy to avoid jamming (Matsubara, 1981; Matsubara and Heiligenberg, 1978). Thus, Sternopygus is less impaired by jamming stimuli from conspecifics and simultaneously less likely to encounter it. It is possible that Sternopygus' lack of a JAR is linked to its very low EODf. However, we have shown that D. conirostris has similarly low EODfs but produces a JAR. Additionally, there may be other neural mechanisms for fish to avoid jamming from nearby EODs with similar frequencies, such as comparing local and global distortions of the EOD (Chacron et al., 2003).

The JAR has also been postulated to have functions other than jamming avoidance. Kramer (1987) observed anomalous JARs in Eigenmannia that mirror the asymmetrical response reported here in D. conirostris. That is, some female Eigenmannia responded consistently to higher-frequency stimuli by lowering EODf, but responded weakly or not at all to lower-frequency stimuli. Juvenile Eigenmannia showed somewhat more robust JARs, but males did not robustly change EODf when presented with stimuli at frequencies near their EODf. Based on these observations, Kramer (1987) proposed a social function for the JAR in addition to (or in place of) its purported function of minimizing deleterious interference. Thus, if the JAR were used in preventing intra-specific aggression or for mediating and maintaining dominance hierarchies within social groups, the JAR might be more highly developed in gregarious species than in territorial species. A communication function would also explain why the fish we recorded here showed small but consistent responses to playback stimuli that were 20 Hz and 40 Hz above their own EODfs, well outside the usual range of frequencies shown to impair electrolocation (Heiligenberg, 1973; Behrend, 1977; Matsubara and Heiligenberg, 1978). Similar asymmetric JAR-like or anti-jamming responses to EODfs outside of the range known to cause jamming have also been found in some apteronotid electric fish species (Dye, 1987; Ho et al., 2010). These anomalous JARs in apteronotids may result in part from the fact that the electric fields generated by apteronotid EODs, unlike those of Eigenmannia, are spatially complex. This complexity may degrade sensory information required to unambiguously discriminate between stimuli above versus below a fish's own EODf (Shifman and Lewis, 2018).

A comparative characterization of the JAR among other species of wave-type electric fish could provide more insight into how the JAR is shaped by both social context and the risk of impairment to electrolocation. For example, examining the JAR in two other sternopygid genera that likely vary in sociality and EODf – Rhabdolichops and Archolaemus – could further elucidate when the JAR evolved and whether it functions as a communication signal and/or is related to social organization. An additional area for future study involves comparing diversity in the mechanisms underlying JARs and chirping across species. For example, differences in the JAR between Eigenmannia (bidirectional JARs that can raise or lower EODf) and Apteronotus (unidirectional JARs that can only increase EODf) are linked to species differences in brain circuits that control the sign and magnitude of the JAR (Heiligenberg et al., 1996). Investigating how these brain regions control the anomalous JAR in Distocyclus may lead to a better understanding of how sensorimotor circuits evolve to produce behavioral diversity across species.