Text: Electroreception in Elasmobranchs Faramarz Samie As a bioengineer I learn to apply mathematical, chemical, and physical concepts to the analysis of biological systems. In the Writing 405 course that I took with Roberta Kirby-Werner, I was given an opportunity to address research issues in my discipline in a formal project. I chose to analyze electroreception, a sensory modality that enables sharks and other animals to perceive electric fields, and wrote a professional-technical paper in which I reported my findings. I studied electroreception because of the insight it gives into the life of animals that perceive the world in a way that we cannot. It also teaches us about identifying and classifying receptors. My objective for this particular paper was to make some of the technical concepts in my discipline accessible to a more general audience which possesses an interest in science. Sharks, rays, and skates make up a scientific grouping of fish called elasmobranchs. Unlike vertebrates, these animals have a cartilaginous skeletal system. The earliest record of this group dates back over 450 million years. In fact, their fossil records date back more than twice that of the dinosaurs. Without question, they are among the most feared animals on earth. Few acts of brutality committed by humans can top the terror that a Great White shark strikes into the hearts of men and women. In keeping with the Hollywood image of sharks (License to Kill, Jaws, Jaws II, and Jaws III), many people see sharks as mindless eating machines that create havoc upon sensing the smallest drop of blood. This image is incorrect. Elasmobranchs are feared because they are misunderstood. Elasmobranchs, through the processes of natural selection, have adapted to live and survive in the earth's oceans and seas. They are one of the most dominant predators in their domain although in comparison to man they are not nearly as dangerous. Their attributes consists of a well-developed sensory network. Their senses include olfactory, tactile, auditory, vision, taste, and electroreception. Electroreception is a remarkable modality1 because it enables the animal to detect electrical fields. The animals use this modality to locate their food and analyze their environment. According to Theodore H. Bullock, a neuroscientist, "the prediction, discovery, and establishment of electroreceptors is of extreme interest not only for the intrinsic insight into the life of some elasmobranchs that see the world through a new sense but also for the lessons it teaches about identifying and classifying receptors by function." As a response to this statement, this article will address electroreception in elasmobranchs by examining the history of electroreception, the morphology2 of electroreceptors, the physiological and behavioral evidence, and, lastly, the ways electroreception influences the behavior of these remarkable animals. History of Electroreceptors It is believed that the "electric" fish evolved from a pre-electric fish without electric organs but sensitive to electric fields. Furthermore, it is suggested that at that primitive stage, the electrosensitivity might have been used to detect the muscular potentials of prey, predators, and members of the same species (Kalmijn, 1971). The first evidence of electrosensitivity in elasmobranchs dates back to 1935 when Dijkgraaf, working on Scyliorhinus canicula, noticed the animal's sensitivity to a rusty steel wire (Dijkgraaf & Kalmijn, 1962). The experimenters approached the head of a blindfolded shark with such a wire. They observed that the animal escaped when the wire was closer than several centimeters from its head. They repeated the experiment with a glass rod, but the animal did not react to it. Dijkgraaf assumed that the shark was stimulated by the galvanic currents produced at the surface of the metal wire, but had no way of proving his assumption. Dijkgraaf's hypothesis largely remained a speculation until Lissmann in 1958 formally suggested, based on behavioral evidence, that a group of receptors and central processes, called the ampullae of Lorenzini, aid in the detection and analysis of electric fields in the marine environment of fish. Later, experimenters verified the existence of the new class of specialized receptors through physiological experiments. They named them "electroreceptors" because their adequate stimuli3 were electric fields (Bullock et al. 1961, Kalmijn, 1966, 1971). The Physical Stimulus for Electroreception In oceans, electric fields are induced by both biological and geological causes. In the latter case electric fields are induced by water flowing or fish swimming through the earth's magnetic field by geomagnetic variations4 and by geophysical events5. The animals use these electric fields for navigation and identification of their environment. Electric fields in the oceans can also be produced by marine animals. The internal and external electrochemical environments of marine animals differs. The difference creates a voltage gradient across the water skin boundary. The potential difference produces current loops which yield a bioelectric field in the surrounding waters. An animal's behavior can produce additional electric fields. For example, when a fish swims, muscles contract. Muscle contraction takes place when chemically-dependent channels, impermeable to sodium and potassium, open. The movement of such ions across the membrane produces an electric field that travels away from the animal in the conducting medium (salt water). The number of muscle contractions affects the magnitude of the electric fields. If more muscles contract, the magnitude of the field is greater and vice versa. Furthermore, the intensity of the electric fields changes in the case of a wounded animal. For example, crustaceans can generate a voltage of 50.0 mV measured with a sensing electrode 1 mm away from the surface of the animal. The same crustacean, if wounded, generates a much higher voltage of 1250.0 mV (Kalmijn, 1974). H. S. Burr in 1947 established the presence of these bioelectric fields in the vicinity of marine animals (Kalmijn, 1974). These gradients can be easily detected by certain members of elasmobranchs. Ampullae of Lorenzini The ampullae of Lorenzini are complicated and extensive specialized skin sense organs characteristic of sharks and rays. The next four subsections of this article address the physical stimulus, the anatomy, and physiological characteristics of electroreceptors. Anatomy The ampullae of Lorenzini are electroreceptive units in sharks. They are jelly-filled canals found on the head of the animal which form a system of sense organs, each of which receives stimuli from the outside environment through the dermis and epidermis. Each canal ends in groups of small bulges lined by the sensory epithelium6. A small bundle of afferent nerve fibers innervates each ampullae7; there are no efferent fibers8 (Murray, 1974). The ampullae are mostly clustered into groups. The lengths of the canals vary from species to species. Even within any one fish, but the pattern of distribution is approximately species specific. An interesting anatomical observation is that the same number of nerve fibers are dedicated to electroreceptors as are dedicated to the eye, ear, and the lateral line (Murray, 1974). The number of nerves that innervate a sensory organ often determine the sensitivity and degree of acuity9 of that sensory organ. They also tell us about the relative importance of that sensory organ for an animal. Consequently, we can conclude that the ampullae of Lorenzini is at least as important to an animal as its eyes, ears, and the lateral line (Murray, 1974). Physiological Characteristics Murray's studies of electrophysiological characteristics in Raja and Scyliorhinus have demonstrated that the ampullae are sensitive to weak electric fields. In fact Scyliorhinus canicula can detect gradients as low as 1-µV/cm while the Raja can detect a 0.01-µV/cm. This means that Raja can detect a 1.5 V gradient (relative to ground) from about 1000 miles away (Kalmijn, 1974). In one experiment Murray recorded the electrical activity from the ampullary nerves under water by stimulating them with electric fields produced by electrodes some distance away. He obtained the best results when the voltage gradient of the field was parallel to the ampullary canals. When the surface openings of the canals were made negative by a DC field, the response was an increase in the frequency of action potentials at the beginning and a decrease in the frequency at the termination of the stimulus. Murray also recorded from the lateral-line organs of the sharks and rays and found them not nearly as sensitive to electric fields as the ampullae of Lorenzini (Murray, 1974). Role of Electroreception in Behavior In 1971 Kalmijn looked at the feeding responses of the shark, Scyliorhinus canicula, and the ray, Raja clavata, toward the flatfish, Pleuronectes platessa. These experiments demonstrated that the animals make significant use of their sensitivity towards electric fields. A synopsis of these experiments follows. First, the flatfish was introduced into a pool where the sharks and rays were maintained, and the flatfish was given enough time to bury itself in the sand. When the sharks and rays swam within 10-15 cm of the flatfish, the researchers observed that the animals attacked the spot where the fish was buried. Subsequently, the animals retrieved and consumed the fish. Then, the fish was placed in an agar chamber to conceal it both mechanically and chemically without affecting the electric field of the animal. The agar chamber did not change the attack pattern of the sharks and rays. To prove that the 1 cm agar10 layer was thick enough to block the chemical scent of the animal, frozen pieces of fish were exchanged for live fish. Following this change, the animals did not attack the chamber. Next, the live flatfish was returned to the agar chamber and a thin electrically-insulating plastic film was placed above the chamber to block the electric field of the flatfish. Once again the sharks made no attempt to attack the flatfish. Finally, to provide direct evidence for the shark's and ray's ability to detect electric fields, two electrodes were buried under the sand, and a current was passed between them. The shark and ray exhibited the same attack pattern as when a live flatfish was buried under the sand. These experiments suggest that detection of electric fields directly influences the feeding response of the animals. The behavioral evidence combined with the ability of the animals to detect electric fields in their natural environment leads to the conclusion that electroreception is a biologically significant modality to the animal. Significance of Research Electroreceptors enable the elasmobranchs to search and locate prey and navigate through the earth's ocean and seas. Electroreception allows these animals to sense the presence of their victims long before the victims have the chance to see their predators. This awesome advantage has made these animals into one of the most threatening predators on earth. By understanding the sensory capabilities of the marine predators and stimuli emanated from their prey we can guard ourselves from hazards by building the proper repellents or shields11. At the same time we protect the animals from the side which effects our technology by taking the necessary precautions. For example when ships or fishing nets are being built, engines could be shielded. Unlike elasmobranchs, humans only possess five sensory modalities. Sometimes humans conclude incorrectly that marine animals use only the same five senses. The type of scientific research described in this article helps to clear up such misunderstandings, but also gives us a better understanding of the world in which we live. References Bullock, T. H. 1982. Electroreception. Annual Review of Neuroscience 5:121-70. Bullock, T. H., Hagiwara, S., Kusano, K., Negishi, K. 1961. Evidence for a category of electroreceptors in the lateral line of gymnotid fishes. Science 134:1426-27. Dijkgraaf, S., Kalmijn, A. J. 1962. Verhaltungsversuche zur Funktion der Lorenzinischen, Ampullen. Naturwissenschaften 49:400. Kalmijn, A. J. 1966. Electro-perception in sharks and rays. Nature 212:1232-33. Kalmijn, A. J. 1971. The Electric Sense of sharks and rays. Journal of Experimental Biology. 55:371-83. Kalmijn, A. J. 1974. The Detection of Electric Fields from animate and Animate Sources Other Than Electric Organs. In: Handbook of Sensory Physiology., A. Fessard, (ed). Springer-Verlag, New York. Murray, R. W. 1974. The Ampullae of Lorenzini. In: Handbook of Sensory Physiology., A. Fessard, (ed). Springer-Verlag, New York. Stevens, W. K. The Odds of a Shark Attack. New York Times, December 8, 1992. Footnotes 1 An avenue of sensation (Webster's Dictionary). 2 Morphology is the study of structure and form in plants and animals (Webster's Dictionary). 3 Adequate stimulus is the form of stimulus to which a sense organ is most sensitive. 4 Geomagnetic variation is the change in the fluctuating strength of earth's magnetic field. 5 An example of a geophysical event is the tectonic processes that cause strain variations in the earth's crust which lead to changes in the magnetization of rocks and local electric fields. 6 The sensory epithelium is a single layer of receptor and supporting cells. 7 Afferent nerve fibers carry information towards the central nervous system (Brain). 8 Efferent nerve fibers carry information towards the peripheral nervous system. 9 Acuity refers to the resolving power of the sensory organ. 10 Agar is a gelatinous colloidal extractive of a red alga (Webster's Dictionary). 11 The chance of being killed by a shark attack is less than the chance of being killed by a bee sting. There are 50 to 70 shark attacks every year worldwide. They result in five to ten deaths according to International Shark Attack file at the Florida Museum of Natural History (Stevens, 1993).

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