Energetics of Sensing and Communication in Electric Fish: A Blessing and a Curse in the Anthropocene?

Abstract

Weakly electric freshwater fish use self-generated electric fields to image their worlds and communicate in the darkness of night and turbid waters. This active sensory/communication modality evolved independently in the freshwaters of South America and Africa, where hundreds of electric fish species are broadly and abundantly distributed. The adaptive advantages of the sensory capacity to forage and communicate in visually-unfavorable environments and outside the detection of visually-guided predators likely contributed to the broad success of these clades across a variety of Afrotropical and neotropical habitats. Here we consider the potentially high and limiting metabolic costs of the active sensory and communication signals that define the gymnotiform weakly electric fish of South America. Recent evidence from two well-studied species suggests that the metabolic costs of electrogenesis can be quite high, sometimes exceeding one-fourth of these fishes' daily energy budget. Supporting such an energetically expensive system has shaped a number of cellular, endocrine, and behavioral adaptations to restrain the metabolic costs of electrogenesis in general or in response to metabolic stress. Despite a suite of adaptations supporting electrogenesis, these weakly electric fish are vulnerable to metabolic stresses such as hypoxia and food restriction. In these conditions, fish reduce signal amplitude presumably as a function of absolute energy shortfall or as a proactive means to conserve energy. In either case, reducing signal amplitude compromises both sensory and communication performance. Such outcomes suggest that the higher metabolic cost of active sensing and communication in weakly electric fish compared with the sensory and communication systems in other neotropical fish might mean that weakly electric fish are disproportionately susceptible to harm from anthropogenic disturbances of neotropical aquatic habitats. Fully evaluating this possibility, however, will require broad comparative studies of metabolic energetics across the diverse clades of gymnotiform electric fish and in comparison to other nonelectric neotropical fishes.