Energetic constraints on electric signalling in wave-type weakly electric fishes

Abstract

SUMMARY Gymnotiform weakly electric fishes generate electric organ discharges (EODs) and sense perturbations of the resulting electric field for purposes of orientation, prey detection and communication. Some species produce oscillatory (‘wave-type’) EODs at very high frequencies (up to 2 kHz) that have been proposed to be energetically expensive. If high-frequency EODs are expensive, then fish may modulate their EOD frequency and/or amplitude in response to low-oxygen (hypoxic) stress and/or compensate for costs of signalling through other adaptations that maximize oxygen uptake efficiency. To test for evidence of an energetic cost of signalling, we recorded EOD in conjunction with metabolic rates, critical oxygen tension and aquatic surface respiration (ASR90) thresholds in Apteronotus leptorhynchus, a species found in high-oxygen habitats, and Eigenmannia virescens, a species more typically found in low-oxygen waters. Eigenmannia virescens had a lower mean ASR90 threshold and critical oxygen tension compared with A. leptorhynchus, consistent with field distributions. Within each species, there was no evidence for a relationship between metabolic rate and either EOD frequency or amplitude under normoxia, suggesting that there is no significant direct metabolic cost associated with producing a higher frequency EOD. However, when exposed to progressive hypoxia, fish generally responded by reducing EOD amplitude, which may reduce energetic costs. The threshold at which fish reduced EOD amplitude tended to be lower in E. virescens, a pattern consistent with higher tolerance to hypoxic stress. The results of this study suggest that wave-type fish reduce their EOD amplitude to reduce direct energetic costs without reducing metabolic rate under hypoxia.

The energetics of electric organ discharge generation in gymnotiform weakly electric fish

“…The axons of the corresponding primary afferent neurons project to the electrosensory lateral line lobe (ELL) Reardon et al, 2011;v Crampton, 1998. of the hindbrain, where each fibre trifurcates to terminate in each of three somatotopic maps ( Fig.2) (Carr et al, 1982;Heiligenberg and Dye, 1982). In addition to the afferent input, the ELL receives a vast amount of feedback from higher areas including the cerebellum.…”

“…2008; Reardon et al, 2011). By making a few assumptions, we can convert oxygen consumption (M O2 ) into the equivalent breakdown of ATP molecules.…”

“…Oxygen consumption varies widely depending on species and body mass (Julian et al, 2003) (see Table1), but here we consider the two species for which we have the most data, the wave-type Eigenmannia cf. virescens (Moorhead, 2010;Reardon et al, 2011) and the pulse-type Brachyhypopomus gauderio (Salazar and Stoddard, 2008 ) for a 14g fish; assuming a 25Hz pulse frequency, the cost would be 1.7×10…”

“…Whereas apteronotids are not known to display circadian rhythms of EOD amplitude or waveform, they are able to increase their EOD frequency by several Hz and maintain this elevated frequency for several hours in response to extended exposure to a conspecific EOD mimic of similar frequency (Oestreich and Zakon, 2002). Accordingly, studies that have examined the energetic cost of electric signals within the context of EOD plasticity have found a significant relationship between EOD-related M O2 or metabolic stress and specific EOD properties (Salazar and Stoddard, 2008;Reardon et al, 2011;Stoddard and Salazar, 2011). Salazar and Stoddard found that the night-time EODs of B. gauderio males are energetically expensive when compared with their daytime counterpart, and with other components of their energy budget (Salazar and Stoddard, 2008).…”

“…Thus, we can hypothesize that only the daytime reduction of the EOD duration seems to be a direct response to predation risk while the daytime reduction of EOD amplitude and frequency may be a response to energetic constraints and, to a lesser extent, predation. Reardon and colleagues used a different strategy to evaluate the relationship between EOD plasticity and EOD-related metabolic demands (Reardon et al, 2011). They measured changes to the EOD amplitude and frequency of individuals from two wave-type species, E. cf.…”