BIOLOGY CREDIT © 2007 SCIENTIFIC AMERICAN, INC. LEMON SHARK chomps down on an unlucky fish. THE SHARK’S SENSE An astonishingly sensitive detector of electric fields helps sharks zero in on prey By R. Douglas Fields menacing fin pierced the surface such as those animal cells produce when in KEY CONCEPTS and sliced toward us. A great blue contact with seawater. But how they use ■ Sharks and related fish can shark—three meters in length— that unique sense had yet to be proved. We sense the extremely weak homed in on the scent of blood like a torpe- were on that boat to find out. electric fields emitted by animals in the surrounding do. As my wife, Melanie, and I watched sev- Until the 1970s, scientists did not even water, an ability few other eral large sharks circle our seven-meter Bos- suspect that sharks could perceive weak organisms possess. ton Whaler, a silver-blue snout suddenly electric fields. Today we know that such elec- ■ This ability is made possible thrust through a square cutout in the boat troreception helps the fish find food and can by unique electrosensory deck. “Look out!” Melanie shouted. We operate even when environmental condi- structures called ampullae both recoiled instinctively, but we were in tions render the five common senses—sight, of Lorenzini, after the 17th- no real danger. The shark flashed a jagged smell, taste, touch, hearing—all but useless. century anatomist who first smile of ivory saw teeth and then slipped It works in turbid water, total darkness and described them. back into the sea. even when prey hide beneath the sand. ■ The author and his colleagues We had drawn the sharks by ladling My research colleagues and I are now ex- have demonstrated that blood into the ocean, but we were not inter- ploring the molecular basis for this ability, sharks use this “sixth sense” to home in on prey during ested in their well-known attraction to while others pursue such questions as how the final phase of an attack. blood. Rather we were investigating the the sensing organ forms during develop- Other potential uses for hunters’ mysterious “sixth sense.” Labora- ment and whether our own vertebrate an- electroreceptors remain to tory research had demonstrated that sharks cestors once could detect electric fields be- be determined. CREDIT can sense extremely weak electric fields— fore they left the sea. All this work is still —The Editors www.SciAm.com SCIENTIFIC AMERICAN 75 © 2007 SCIENTIFIC AMERICAN, INC. ELECTROSENSORS IN ACTION Pore MAKO SHARK Nerve Brain Sharks and related species sense extremely weak electric fields gener- Ampullae of ated by other animals in seawater thanks Lorenzini to hundreds or even thousands of specialized ●a detectors in their snouts called ampullae of Lorenzini (a). The fields conduct electricity in well- Pore insulated, gel-filled canals (b) that extend from the skin pores to the bulb-shaped ampullae (c) lined with a single layer of sensing cells (d). Those cells, which respond to very slight changes in the electrical charge of the gel in the canal, in turn activate nearby nerves, which inform the brain of the field’s presence. quite preliminary, though. Here I describe how The pores’ purpose started to become clear in investigators first discovered electroreception in the middle of the 19th century, when researchers sharks and how we demonstrated its importance began to glean the function of the so-called lat- to successful hunting—a fascinating, little- eral line, an organ that shares some similarities known tale that spans centuries. with Lorenzini’s pore-and-tube system. The lat- eral line, a stripe extending down the sides of Hidden Sense many fish and amphibians from gills to tail, de- The story begins in 1678, when Italian anatomist tects water displacement. In fish, it consists of a Stefano Lorenzini described pores that speckled specialized row of perforated scales, each of the forward part of the head of sharks and rays, which opens into a tube lying lengthwise just un- ) MILLIONTH endowing them with something resembling a der the skin. At swellings along the length, spe- bad five-o’clock shadow. He noted that the pores cialized sensory cells called hair cells extend slen- OF A VOLT concentrated around a shark’s mouth and found der, brushlike projections (or cilia) into the tube. ACROSS A that if he peeled back the neighboring skin, each Slight water movements, such as those caused by CENTIMETER opening led to a long transparent tube that was fish swimming a few feet away, bend the micro- OF SEAWATER filled with a crystalline gel. Some of the tubes scopic hair masses like wind-driven waves rip- were small and delicate, but others were nearly pling through a field of grain. This reaction ex- photographillustrationsnoutsharkand mako of can be distinguished by a the diameter of a strand of spaghetti and several cites nerves, whose impulses inform the brain shark. This is equivalent to inches in length. Deep within the head, Lorenzi- about the strength and direction of the water dis- a voltage gradient created ni discovered, the tubes congregated in several placement. We retain the descendant of this lat- );AMADEO BACHAR( by a 1.5-volt AA battery large masses of clear jelly. He considered and eral line in our ear cochlea. then rejected the possibility that these pores were By the late 19th century the newly improved with one pole dipped in the source of fish body slime. Later, he speculat- microscope revealed that the pores on a shark’s precedingpages the Long Island Sound and ed that the pores might have another, “more hid- snout and the unusual structures underneath the other pole in waters den function,” but their true purpose remained them, today called ampullae of Lorenzini, must off Jacksonville, Fla. unexplained for hundreds of years afterward. be sensory organs of some kind. Each tube was BRANDON( COLE 76 SCIENTIFIC AMERICAN August 20 07 © 2007 SCIENTIFIC AMERICAN, INC. ELECTROSENSORS IN ACTION A sensing cell reacts when an external electric field produc- es a small electric potential across its membrane, leading channels to allow positively charged calcium ions to rush in. The influx of positive charge causes the cell to release neurotransmitters at synapses, or contact points, with nerves to the brain, stimulating them to fire. The firing rate indicates the strength and polarity of the external field, and the field’s location relative to the shark is thought to be determined by the positions of the activated pores on its body. The cells return to their original electrical state after- TIMELINE: ward by opening a second type of membrane channel that UNDERSTANDING permits positively charged potassium ions to exit. ELECTRORECEPTION 1678: Italian anatomist Stefano Calcium ions Potassium ions Lorenzini describes the structure c ● (Ca++) flow in (K+) flow out of the electroreception system of Cilium sharks and rays. Its function remains a mystery. Late 1800s: Scientists explain the function of fish’s lateral line, an organ that detects water displacement ●d and in some ways resembles the elec- Nerve ●b troreception system. Examination with microscopes delineates the details of what soon become known as ampullae Ampullae of Lorenzini Nerve of Lorenzini. External pore Support cell Gel-filled canal in skin Sensing cell Synapse 1909: G. H. Parker finds that the ampullae respond to touch. He speculates that they might sense seen to end in a bulbous pouch, or ampulla. A haps water pressure, but he could not be sure. Af- water motion. thin nerve emerged from the ampulla and joined ter all, a reflex reaction to a poke in the eye does branches of the anterior lateral line nerve. Scien- not necessarily mean that eyes had evolved to 1938: Alexander Sand records tists traced these nerve fibers to the base of the perceive sudden jabs. nerve impulse output from ampullae of Lorenzini in response to various skull, where they enter the brain through the Just as microscopes had opened up new re- stimuli. He notices that they react to dorsal surface of the medulla, a destination search avenues a century before, the just-devised tiny temperature changes. characteristic of nerves that carry sensory infor- vacuum-tube amplifier advanced the study of mation into the brain. Observers discerned a brain function in the second quarter of the 20th 1950s: H. W. Lissmann and others single tiny hair cell, similar to those of the hu- century. In 1938 Alexander Sand of the Marine describe “tuberous receptors” in weak- man inner ear and of a fish’s lateral line system, Biological Association in Plymouth, England, ly electric fish that sense their own fields. The discovery adds electrorecep- inside each ampulla. The type of stimulus they succeeded in amplifying and recording nerve tion to the list of known animal senses. might detect remained unknown, however. pulses running from ampullae of Lorenzini to the brain. He saw that impulses shot down the Early 1960s: R. W. Murray finds Electroreception Confirmed nerve in a steady stream but that certain stimuli that ampullae of Lorenzini are sensi- Researchers found themselves faced with a caused the rate to increase or decrease suddenly. tive to slight salinity variations and dilemma: How could they determine the function Sand noticed, as Parker had, that the organs re- weak electric fields. of this entirely foreign sense organ? The eventu- sponded to touch or pressure, but he found that 1970s: Adrianus Kalmijn deter- al solution came down to the combination of the firing rate also rose when cooled. Indeed, the mines that in seawater animal bodies good instrumentation and a fertile imagination. ampullae were so sensitive to temperature that produce electric fields.