Elsevier

Journal of Physiology-Paris

Volume 96, Issues 5–6, September–December 2002, Pages 379-389
Journal of Physiology-Paris

Neuroethology and life history adaptations of the elasmobranch electric sense

https://doi.org/10.1016/S0928-4257(03)00016-0Get rights and content

Abstract

The electric sense of elasmobranch fishes (sharks and rays) is an important sensory modality known to mediate the detection of bioelectric stimuli. Although the best known function for the use of the elasmobranch electric sense is prey detection, relatively few studies have investigated other possible biological functions. Here, we review recent studies that demonstrate the elasmobranch electrosensory system functions in a wide number of behavioral contexts including social, reproductive and anti-predator behaviors. Recent work on non-electrogenic stingrays demonstrates that the electric sense is used during reproduction and courtship for conspecific detection and localization. Electrogenic skates may use their electrosensory encoding capabilities and electric organ discharges for communication during social and reproductive interactions. The electric sense may also be used to detect and avoid predators during early life history stages in many elasmobranch species. Embryonic clearnose skates demonstrate a ventilatory freeze response when a weak low-frequency electric field is imposed upon the egg capsule. Peak frequency sensitivity of the peripheral electrosensory system in embryonic skates matches the low frequencies of phasic electric stimuli produced by natural fish egg-predators. Neurophysiology experiments reveal that electrosensory tuning changes across the life history of a species and also seasonally due to steroid hormone changes during the reproductive season. We argue that the ontogenetic and seasonal variation in electrosensory tuning represent an adaptive electrosensory plasticity that may be common to many elasmobranchs to enhance an individual's fitness throughout its life history.

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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