Neuroethology and life history adaptations of the elasmobranch electric sense
Introduction
Sensory neuroethologists seek to understand the neural basis of adaptive behaviors that animals use within their natural environment. Because this requires study of both neural mechanisms and behavior of the animal, multidisciplinary approaches are required. In many cases researchers focus on a single aspect of a neural system that controls behavior and employ a limited set of neurobiology techniques. In addition, behavioral studies are often necessarily limited to a single biological context in which to interpret the sensory system. As a result, it usually takes great time and effort to characterize the adaptive function of a neural system in relation to the natural behavior of the organism.
One example of an incompletely characterized system is the use of the ampullary electrosense by elasmobranch fishes to detect bioelectric stimuli. The ampullary organs were recognized long ago by Stenonis [57] and Lorenzini [34], but its physiological and behavioral functions remained unknown for centuries. The advent of modern neurophysiological techniques first produced evidence for multiple sensory functions until it was convincingly demonstrated to encode weak electric charges external to the animal [43], [44]. A short time later researchers were able to experimentally demonstrate that sharks and rays could use this sense to successfully detect and locate bioelectric stimuli produced by their prey. However, these large fishes are wide ranging, difficult to maintain in the lab or observe in the wild thus there is only limited literature of their natural social, predatory, and anti-predatory behaviors. As a result, most neuroethology research on the ampullary electrosense of sharks and rays has focused on the response dynamics and central neuroanatomy, with relatively few new studies on other possible biological functions. The purpose of this paper is to present recent evidence that the electrosensory system functions in a wide number of behavioral contexts including social, reproductive and anti-predator contexts (Table 1).
Section snippets
The elasmobranch electrosensory system
All elasmobranch fishes (sharks, skates, and rays) possess an elaborate electrosensory system that consists of subdermal groups of electroreceptive organs known as the ampullae of Lorenzini. Single ampullae of Lorenzini consist of a small chamber (the ampulla) and a subdermal canal that projects to a single pore on the surface of the skin (Fig. 1A). The wall of the ampulla is composed of a single-layer sensory epithelium that contains hundreds of sensory receptor and support cells [51], [67]
Electrogenic organs, physiology and behavior
Marine skates of the family Rajidae produce intermittently pulsed, weak electric discharges from spindle-shaped electric organs found bilaterally in the tail [22], [52], [56]. These electrogenic organs consist of disk- or cup-like electrocytes that are arranged within the organ anterioposteriorly in series [16], [23] and are depolarized by spinal electromotoneurons to generate a weak electrical discharge around the animal [3], [10], [33]. The discharges are controlled by descending input from
Courtship and mating behavior of the round stingray
The round stingray, Urolophus halleri, is a relatively small stingray found from Point Conception, California to Panama Bay and is common throughout the Gulf of California [41]. Courtship and mating among many individuals of this species can readily be observed during the winter months (January–March) in the clear shallow waters near Bahia Kino, Mexico [48], [65]. Each day before sunrise during the mating season, reproductively active female rays move into the shallow water habitat along the
Summary and conclusions
Recent studies have experimentally demonstrated new uses of the ampullary electrosense in the natural behavior of sharks and rays that can be classified into four major categories (Fig. 8). The first function demonstrated for the shark electrosense was for the detection of weak bioelectric fields produced by living prey. Most if not all sharks and rays may use the electrosense in this context. The use of the electrosense to detect mates was recently demonstrated for non-electrogenic stingrays,
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