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...Hypopomid electric fish evolved signal-cloaking strategy that reduces their detectability by predators in the lab (and thus presumably their risk of predation in the field). These fish produce broad-frequency electric fields close to the body, but the heterogeneous local fields merge over space to cancel the low-frequency spectrum at a distance. Mature males dynamically regulate this cloaking mechanism to enhance or suppress low-frequency energy. The mechanism underlying electric-field cloaking involves electrogenic cells that produce two independent action potentials. In a unique twist, these cells orient sodium and potassium currents in the same direction, potentially boosting their capabilities for current generation. Exploration of such evolutionary inventions could aid the design of biogenerators to power implantable medical devices, an ambition that would benefit from the complete genome sequence of a gymnotiform fish.
Keywords: biogenerator, electrogenesis, electroreception, Gymnotiformes, melanocortin
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If you were to fall into the Amazon River, you would find yourself in a world of darkness. The mixture of rainwater, tannins, and suspended minerals known as "whitewater" is virtually opaque. Although the limited penetration of sunlight might be expected to restrict primary productivity, the whitewater rivers of South America are among the world's richest in terms of fish diversity and abundance. The limited visibility in these rivers has shaped the sensory worlds of their inhabitants, favoring the use of electricity and olfaction for navigation, hunting, and communication signaling. Two sister orders of teleost fishes, the catfishes (Siluriformes) and the knifefishes (Gymnotiformes), can detect electric fields. The catfishes use their olfactory whiskers to track the odor trails of prey (Atema 1971, Pohlmann et al. 2001), then rely on their electric sense to zero in on the minute electric stimuli (microvolts per centimeter) generated by the prey's muscle contractions and nervous system activity (Finger 1986). The knifefishes use a specialized electric organ to generate comparatively stronger electric fields, in the range of millivolts per centimeter, and "see" their world within half a body length by analyzing distortions in these electric fields caused by nearby objects with different impedances than the surrounding water. The electrogenic ability of the electric fishes has enabled the secondary evolution of communication. Male electric fish sing electric courtship songs to the females and engage in energetically expensive contests of electric one-upmanship with their rivals (Franchina et al. 2001, Salazar 2003). The same story plays out in the rivers of West Africa, where the Mormyridae, an independent lineage of weakly electric fishes, replace the gymnotiforms.
At the mention of electric fish, people inevitably ask about the electric eel (Electrophorus electricus), the largest and best known of the Gymnotiformes. The electric eel is the only species capable of producing not only weak signals for navigation and communication but also a strong discharge (hundreds of volts) to stun prey and deter would-be predators. The electric eel is itself a formidable predator, and anecdotal evidence suggests that it relies on its electric sense to "eavesdrop" on weakly electric fish (Westby 1988, Stoddard 1999). After locating weakly electric fish by their electric signals, Electrophorus stuns them with its high-voltage discharge and gulps them down before they can recover. Various piscivorous catfish likewise eavesdrop on weakly electric fish. To an electro-receptive predator, the electric fields of a weakly electric fish produce a distinct" eat me" signal. Though we cannot see what goes on below the surface, lab experiments and analysis of stomach contents have borne out the supposition that electro-receptive predators are attuned to the rich foraging opportunities that arise from a shared electric sense and an abundant guild of signaling prey. The stage is set for evolutionary escape from predation, a condition that often precedes adaptive radiation (Ehrlich and Raven 1964), or possibly for an evolutionary arms race if the sensory systems of predators adapt to keep up with the shifting signal strategies of their electrogenic prey.
Escape from predation
Electric fish can reduce predation risk by inhabiting aquatic refugia where predators cannot enter. Some gymnotiforms can breathe air, allowing them to escape the predatory catfish by inhabiting floating meadows where dissolved oxygen concentrations approach zero (Crampton 1998a, Julian et al. 2003). The electric eel, an obligate air breather, does penetrate the floating meadows, as do some of its piscivorous low-voltage kin in the family Gymnotidae (Crampton 1998b). Other gymnotiforms cannot survive in low-oxygen waters and must run the gauntlet of hungry eavesdropping catfish in the river channels. Gymnotiforms constitute 80% of the stomach contents of the piscivorous catfish Pseudoplatystoma tigrinum (Reid 1983), suggesting that there is intense predation pressure on electric fishes in the river channels where these large pimelodid catfish live.
The other key strategy an electric fish can use to lower predation risk is the classic strategy of spectral shifting, or moving the energy in its signals above the sensory range of unwelcome eavesdroppers. Spectral shifting can work only if the signaler already has, or can readily evolve, a sensory range outside that of the eavesdropper. Gymnotiform electric fishes and catfishes share a class of ampullary electroreceptors, similar in physiology to the ampullary electroreceptors of sharks, rays, and other ancient fishes (Zakon 1986). Ampullary receptors detect electric fields in the low-frequency spectral range of to 60 hertz (Hz). Their extreme sensitivity (microvolts per centimeter) allows these receptors to detect the weak electric fields produced by muscle action and by water movements of their prey. A second class of tuberous electroreceptors, derived from the ampullary receptors, is tuned to the higher frequencies of electric signals. Tuberous electroreceptors are less sensitive than ampullary receptors, and are used both for active electrolocation and for communication. As far as we know, tuberous electroreceptors exist only in the electric fishes. One piscivorous Neotropical catfish has been found to have cutaneous receptors on its face whose morphology is similar to that of a tuberous electroreceptor, though the physiology of these receptors has not been confirmed (Andres et al. 1988). Though we should not be surprised to find that some piscivorous catfishes have evolved electroreceptors whose physiology resembles that of the tuberous electroreceptors of the electric fishes on which they prey, the African clarriid catfish that prey on mormyrid electric fishes do appear limited in their electrosensory capabilities to the low-frequency spectrum of the ampullary electroreceptors (Hanika and Kramer 2000).
The electric...
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