The Electric and Magnetic Sense of Sharks, SkaS, andRays - by Adrianus J. Kalmijn
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A shark swimming through the earth’s magnetic field
induces electric fields giving the animal’s compass
heading (the horizontal component of the earth’s
magnetic field and the induced electrical currents are
indicated). (From Kalmijn, 1974)
The Electric and Magnetic Sense
of Sharks, SkaS, andRays
by Adrianus J. Kalmijn
Scientists must know the sensory world of an that the elasmobranchs also detect the electric
animal if they are to understand its behavior. fields they induce when swimming through
Certainly most aquatic vertebrates have good the earth’s magnetic field, and thus sense their
eyesight, hear well, and are endowed with a compass heading. Obviously, the electric
sharp sense of smell and taste. Yet the physical sense of these ancient fishes has reached a
characteristics of underwater light, sound, and high degree of sophistication.
odor fields are quite different from those on Last year, the author and his student
land. Moreover, animals use the sensory collaborators initiated field experiments in
information in a variety of ways, depending on Vineyard Sound off Cape Cod, Massachusetts,
the particular interest of the species. to verify the results of earlier laboratory
Therefore, scientists cannot infer from man’s studies on the electrical aspects of predation.
own sensory experience how an animal After chumming with chopped herring, we
perceives its environment but have to learn observed the smooth dogfish Mu&e/us canis
through behavioral tests and field search the bottom and viciously attack a
observations. This point is dramatically current source simulating the bioelectric fields
emphasized by animals that have sensory of the shark’s prey. Although attracted and
capabilities that stretch man’s imagination. motivated by odor, the predators made their
One of the most interesting examples of this is final approach exclusively relying on their
the electromagnetic sensory performance of electric sense. Coming in with the sharks, the
marine sharks, skates, and rays, commonly American eel Anguilla rostrata paid no
referred to as elasmobranch fishes. attention to the fields, whereas in comparative
In predation, sharks, skates, and rays tests the catfish lctalurus nebulosus repeatedly
cunningly cue in on the weak, bioelectric dug at a current source hidden in the mud
fields of their prey, even though it may be along the banks of a local freshwater pond.
hiding under sand. These well-aimed feeding The magnetic orientation studies have
responses clearly demonstrate the remarkable been conducted on the stingray Urolophus
acuity of the elasmobranchs’ electric sense halleri at our land facilities, set up in the woods
and testify to its biological significance in the of the quiet Quissett Campus of the Woods
animals’ daily life. Recent research indicates Hole Oceanographic Institution. The stingrays
45were trained to seek reward and avoid decelerations when applying electric fields of
punishment by orienting to the earth’s voltage gradients as low as 0.01 microvolt per
magnetic field. Between trials, the horizontal centimeter, which represents the highest
component of the magnetic field was reversed electrical sensitivity known in the animal
in a random order to eliminate the use of kingdom. In later behavioral tests, the
alternative orientational cues. These frequency range of the animals’ response
experiments have conclusively demonstrated appeared to extend from direct current (DC) up
the elasmobranchs’ magnetic sensory abilities, to about 8 hertz. Reception of these
which the author predicted on the basis of low-frequency, low-level electric fields was *_
their acute electric sense. shown to take place by means of the ampullae
of Lorenzini, delicate sensory structures in the ,,
Previous Studies protruding snout of the elasmobranch fishes
(Figure 1).
In 1917, G. H. Parker and A. P. Van Heusen
published a historic paper on the curious
behavior of Ictalurus, the common brown
bullhead, with regard to metallic and
non-metallic objects. They noticed that
blindfolded specimens responded to the
approach of metallic rods at distances of
several centimeters, whereas a glass rod did
not elicit a reaction until it actually touched the
skin of the animals. In a series of simple but
convincing experiments, Parker and Van
Heusen demonstrated that these distant
responses were due to galvanic currents Figure 1. Ampullae offorenziniandmechanicallateral-line
system in head region of the shark Scyliorhinus canicula.
generated at the interface between metal and
(Solid dots: skin pores of electroreceptors. Small circles:
aquarium water. Though very close to openings of lateral-line canals) (From Dijkgraafand
discovering the catfish’s electric sense, these Kalmijn, 7963)
scientists did not realize the biological
implications of their remarkable results. By measuring the electric fields in the
In 1934, the Dutch biologist S. Dijkgraaf laboratory habitat of the sharks and skates, it
also observed a great sensitivity to metallic was found that aquatic animals produce
objects in the small shark Scyliorhinus direct-current and low-frequency electric
canicula. A quarter of a century later, he fields in the water, which stem mainly from
suggested that the author, then his student in potential differences at the skin/water
the Netherlands, investigate the possibility of interface. In fish, for example, the mucous
electrical stimulation, as in the case of the membranes lining the mouth and the gill
catfish, and evaluate the biological epithelia in the pharynx give rise to steady DC
significance of the response. A few years fields, usually modulated by ventilatory
earlier, H. W. Lissmann in England had movements. Externally, the bioelectric fields
discovered that certain knife-fishes produce are of distributed dipole* configuration and,
weak electrical discharges to probe their accordingly, fall off steeply with increasing
environment. Sharks, however, lack distance. Yet the DC voltage gradients
electrogenic organs; therefore, the main emanating from small fish and wounded crabs
questions were: what might be the fields in often measured over 0.01 microvolt per
nature that the sharks detect, and what could centimeter at distances up to 25 centimeters,
be the role of these fields in the animals’ daily which suggested the role of the
life? elasmobranchs’ electric sense in predation.
Subsequent research soon revealed To elucidate the electrical aspects of
that marine sharks, skates, and rays are indeed predation, the author decided to analyze the
extremely sensitive to weak electric fields. By feeding responses of the shark Scyliorhinus
recording the heartbeat of free-swimming
specimens with implanted electrodes, the *A field produced by equal but opposite electrical p’oles,
author established transient cardiac usually separated by a small distance.
46(a)
(b)
Figure 2. Feeding
responses of the shark
Scvliorhinus caniculato:
(a)’ flounder under sand,
ib) flounder .~ in.._an --‘.,
.C
C.__.._L ..N.-
electrically transparent
agarchamber, (c)pieces of ,.--
--.-
whiting in an agar
chamber, (d) flounder in
an agar chamber covered
with an electrically
insulating plastic film, and
flounder. Agar chamber
not to scale. Solidarrows:
responses of shark;
dashed arrows: flow of
seawater through agar
chamber. (From Kalmijn,
1971)
canicula and the skate Raja clavata to small purpose of the agar chamber was to conceal
specimens of the flounder Pleuronectes the flounder visually, chemically, and
platessa. The prey was cautiously introduced mechanically without impeding the animal’s
into the seawater habitat, and after it had bioelectric field. Again, after odor motivation,
hidden itself in the sand, a few drops of the sharks and skates made their well-aimed
liquified whiting were diffusely spread feeding attacks from the same distance and in
throughout the water. Motivated by the odor, the same frenzied manner, as if the prey were
the sharks and skates began randomly not screened by agar at all (Figure 2b).
searching the bottom of the pool. When To prove that the l-centimeter-thick
coming within a distance of IO to 15 roof of the agar chamber was really effective in
centimeters from the flounder, they made attenuating odor stimuli, the live flounder was
well-aimed dives at their prey, uncovered it exchanged for pieces of whiting that had been
from under the sand, and devoured it frozen for several days (whiting was the regular
voraciously (Figure2a). Subsequently, the food for the experimental animals). In this
flounder was placed in a flat chamber made case, the predators did not show the slightest
out of 3 percent agar in seawater, and response to the food when swimming over the
positioned under the sand on the bottom of agar chamber, although they-were strongly
the pool. The chamber was aerated by a steady motivated by the odor of the seawater flow
flow of seawater to keep the prey alive. The ventilating the chamber (Figure2c). Whether
47the agar was adequate to mechanically shield During the summer of 1976, we learned
the live flounder was indirectly tested by from longline fishing off Cape Cod that the
repeating the original experiment, this time, smooth dogfish Mustelus regularly frequents
however, with a thin, electrically insulating the shallow, inshore waters of Vineyard Sound
polyethylene film covering the agar chamber. on its nightly feeding excursions. This
Now, the sharks and skates no longer predatory shark is a warm-season visitor,
responded to the prey, although they eagerly arriving at Woods Hole in May and leaving for
searched about and often passed directly over the South again in late October or shortly
it (Figure 2d). This drastic effect could not thereafter. It is an active bottom hunter,
conceivably be due to the mechaniical preying on small fish as well as crustaceans and
properties of the thin (IO micrometer) and other invertebrate animals. The females reach
extremely pliable polyethylene film, since an average length of 115 centimeters; the
even the stiff, l-centimeter-thick agar roof to males are slightly smaller. The smooth dogfish
which the film was added did not nioticeably is truly live-bearing; the new-born measure 29
weaken the feeding responses. Hence, the to 37 centimeters.
sharks and skates evidently were able to attack To observe the sharks’ feeding
a flounder hiding in the sand without the aid of behavior, we worked from an inflatable rubber
visual, chemical, or mechanical cues.
raft (Zodiac Mark II) free of any metal under
The results of these behavioral tests the waterline. On station in 2.5 to
suggested that the sharks and skates 3.0-meter-deep water over a sand patch devoid
electrically located the agar-screened prey. of seaweed, we attracted the sharks by
This would also explain the all-or-none effect squeezing liquified herring through a long
of the polyethylene film, which offered Tygon tube that ran from the raft to the bottom
an extremely high electrical resistamce,
of the sea. The Tygon chumming tube was
whereas the agar layer did not distort the
attached to a polypropylene line, suspended
bioelectric field of the flounder to any extent. from a Styrofoam float and stretched over the
To provide direct evidence for the electrical
ocean floor between two polyvinyl pipes
hypothesis, the presence of the flounder was anchored in low-profile cinder blocks (Figure
simulated by passing electrical current
3). Starting after dark, we illuminated the area
between two salt-bridge electrodes’ buried in
with a loo-watt, battery-operated underwater
the sand. After odor motivation, the predators
light. To break the water surface, we used a
displayed the same characteristic feeding
glass-bottom viewing box secured behind the
responses to the electrodes (whether or not
stern of the raft.
covered with agar) as they did to the actual
prey (Figure 2e). They dug tenaciously at the Two pairs of agar-filled, salt-bridge
source of the field, responding again and again electrodeswere tied to the polypropylene line
when coming across the electrodes. These and positioned on the sand, one on either side
results proved that the electric sense of sharks of the odor source and 30 centimeters from it.
and skates plays an important role in the Mekka underwater plugs with stainless steel
animals’ lives. pins and integral cables connected the thin, 30
to 90-centimeter-long Silastic salt-bridge tubes
to the electrical equipment set up in the
rubber raft. The use of a constant-current
Field Observations on Cape Cod Sharks source virtually eliminated the adverse effects
Following the studies on captive shalrks, we of polarization at the stainless steel/seawater
have sought to verify the results in tests on wild interfaces. From the raft, we could
specimens, roaming freely in their natural conveniently vary the strength of the field and
habitat. The main problem, however, has been select the pair of electrodes to be energized,
approaching the animals without introducing the other pair functioning as the control. The
galvanic fields or other perturbations into the applied direct-current dipole moments ranged
environment that might interfere with the from 1 to 8 microamperes x 5 centimeters
fishes’ normal behavior. Remember that the (dipole current x distance between
electrical sensitivity of catfish and sharks first electrodes), roughly corresponding to the
revealed itself through the animals’ Iunusual bioelectric fields of small prey at a seawater
responses to metallic objects. resistivity of 20.0 to 20.5 ohm.centimeters and
48f
.
Figure 3. Field setup for
observing the feeding
responses of sharks to
electrically stimulated
prey. Though attracted by
fish extract exuding from
chumming tube, the shark
Mustelus caniszeroes in
on electricaldipole fieldin
Vineyard Sound.
a temperature of 19 to 22 degrees Celsius. attracted the sharks from a distance. Since the
After entering the area, the smooth odor of wounded prey lingers long after the
dogfish began frantically searching over the animal is gone, the sharks obviously need
sand, apparently trying to locate the odor more precise directional cues to locate their
source. Both young and mature sharks were prey accurately, enabling them to seize it with
observed, sometimes alone, sometimes in one quick move.
groups of two to five. Neither the raft nor the Behaviorally, elasmobranchs readily
underwater light appeared to bother them. respond to direct-current fields.
Most interestingly, when nearing the odor Electrophysiologically, however, the ampullae
source, the animals did not bite at the opening of Lorenzini are not true DC receptors,
of the chumming tube but from distances up to although they do detect frequencies as low als
25 centimeters turned sharply to the 0.1 hertz. That is, to sense a prey’s DC field,
current-electrodes, viciously attacking the elasmobranch fishes have to move relative to
electrically simulated prey. After snapping the their prey, or vice versa. Alternatively, they
line with their teeth right at the position of the may detect the low-frequency components
electrodes, the sharks usually attempted to rip that accompany the prey’s ventilatory and
them apart-and one night they succeeded. body movements. Odor-motivated sharks and
When the current was switched to the other skates do zero in on DC, as well as
pair of electrodes, the animals let go, circled low-frequency dipole fields of biological
around for awhile, and attacked again, but at strengths. In their final approach, they aim
the electrodes on the other side of the odor directly at their prey, deriving its location frorn
source. At the lower current levels, the sharks the spatial configuration of the animal’s
kept responding, though from increasingly bioelectric field.
shorter distances. The American eels that visited our test
These observations convincingly area often nibbled at the opening of the
demonstrate that odor-motivated sharks are chumming tube, but theydidnot pay any
capable of detecting and taking prey by the attention to the current-passing electrodes.
exclusive use of their electric sense, not only The eels’ behavior was particularly noteworthy
under well-controlled laboratory conditions, because the fish had been reported to exhibit
but also in their electrically more noisy, ocean similar cardiac decelerations when subjected
habitat. Of course, other sense organs, in to weak electric fields, as previously observed
particular the fish’s lateral-line in elasmobranch fishes. The eels’ responses,
mechanoreceptors, also can play an important however, have not been independently
part in predation. At short range, the electric confirmed, nor are these fish known to have
fields appear to dominate in our experiments specific electroreceptors. In predation at least,
over the much vaguer odor cues that initially they evidently are more chemically inclined.
49Toward the end of the season, we author has endeavored to collect hard
conducted comparative tests on the common experimental evidence of the elasmobranchs’
brown bullhead, which is endemic to the magnetic abilities predicted from the animals’
Cape’s freshwater ponds. With small pieces of known electric sense and the theory of
beef liver, we lured the fish into shallow water, electromagnetic induction.
and offered them direct-current dipole fields Our first, most simple magnetic tests
of 0.5 to 4.0 microamperes passed between were performed on the leopard shark, Triakis
two salt-bridge electrodes with openings I semifasciata, in outdoor, all-fiberglass pools
centimeter apart buried in the mud. Along the on the bluffs of Scripps Institution of
banks of the pond, the resistivity of the water Oceanography’s campus at La Jolla, California.
measured 19 kiloohm-centimeters at a With the fish swimming steadily along the
temperature of 20 degrees Celsius. As with the circumference of their circular habitat, we
sharks, the catfish repeatedly dug at the source introduced a local magnetic field by passing an
of the field in apparent attempts to devour the electrical current through a small induction
electrically simulated prey. coil (20 centimeters in diameter) held external
Although we primarily conceived this to the tank. The field was switched on when
field work with the undisturbed bioelectric the sharks were at the far side of the pool.
sensory world of the sharks in mind, the Then, seconds later, upon completing their lap
results of our tests also indicated that attacks and swimming into the imposed field, the
on humans and underwater gear may be sharks suddenly veered off to the center of the
elicited and guided by electric fields tank, although the coil current did not distort
resembling those of regular prey. The human the earth’s ambient magnetic field by more
body, especially when the skin is damaged, than 25 percent.
creates DC bioelectric fields that sharks in the
Next, we noticed that the leopard
ocean may detect from distances up to 1 or 2 sharks each morning before dawn gathered in
meters. The galvanic fields of metallic objects the northern area of the tank. To eliminate the
on the body may be even stronger. In this possibility of visual orientation, we covered
connection, we expect that the U.S. Navy’s their pool with a large sheet of black plastic.
polyvinyl anti-shark bag, which is suspended We also took all objects out of the water and
from an inflatable floatation collar and even rotated the whole tank. Surprisingly, this
designed to visually and olfactorily conceal a did not change the sharks’ early-morning
mariner in distress, electrically screens the orientation. However, when we roughly
person as well. Sidetracking the sharks to neutralized the earth’s ambient magnetic field
alternative sources of electricity that
by passing electrical current through two large
secondarily release a discouraging agent may,
induction coils diametrically attached to the
under certain circumstances, be another outside of the tank, the animals lost their
means of warding off electrically evoked shark positional preference and distributed
bites. It should be emphasized here that the randomly.
electrical aspects of the animals’ environment
Although the outcome of these
should be taken into account in all behavioral
preliminary tests was consistent with the idea
studies on elasmobranchs and, if possible, left
of geomagnetic orientation, none were fully
undisturbed.
conclusive. The avoidance reactions nroved
the sharks’ sensitivity to fields of geomagnetic
Evidence of Geomagnetic Orientation strength but were not of obvious biological
When cruising through the earth’s magnetic significance. The spontaneous orientation was
field, marine sharks, skates, and rays induce biologically more interesting, but at that time
electric fields that are well within the dynamic we were not technically prepared to reverse
range of their highly-sensitive electroreceptor the field in order to verify the magnetic nature
system. As the induced voltage gradients of the response.
depend on the direction in which the animals In the meantime, the author moved to
are heading, they may form the physical basis Massachusetts to pursue his magnetic studies
of an electromagnetic compass sense in these at the Woods Hole Oceanographic Institution.
fishes. To substantiate the biological feasibility To scale down the technical problems of
of this novel orientation mechanism, the controlling the ambient magnetic field, we
50(4
lb)
Figure 4. Magnetic test
facility on the Quissett
campus of the Woods
Hole Oceanographic
institution (a). The round
stingray Urolophus halleri,
swimming toward the east S
enclosure to secure food,
undernormalandreversed
field conditions (b). Norma I Reversed
looked for a good experimental animal of coils, each 5 meters in diameter, were
smaller size, which one of the students found mounted along the north-south axis to control
in the round stingray Urolophus halleri. The the horizontal component of the earth’s
round stingray is a hardy, very alert and active magnetic field in the tank (Figure 4a). We
elasmobranch of subtropical and tropical seas, chose for our tests a magnetic induction of 0.34
reaching an average span of 25 centimeters. To gauss, corresponding to the horizontal
fit our tanks, we selected five specimens component of the Southern California region
measuring only 15 to 20 centimeters. from where the animals were taken.
The stingrays were tested in a circular, During the 1 to 2-hour training sessions,
fiberglass pool, 1.8 meters in diameter, which twelve concealed lights illuminated the ceiling
rested on Teflon blocks to insulate it from over the tank to produce an even, low-level
ground. The pool was filled with natural light distribution. For the rest of the day, the
seawater to a depth of 15 centimeters. Coarse lights were programmed to simulate the
sand covered the bottom, and two airlifts sunshift and daily variation in brightness of the
maintained a slow, internal circulation. We sky in accordance with the direction of the
surrounded the pool with a lighttight, ambient magnetic field. Lights, heaters, and
twelve-sided hut devoid of any ferromagnetic coils were DC-powered from distantly located
materials. The seawater was kept at 20 degrees voltage and current sources. The wiring was
Celsius by regulating the air temperature in the tightly twisted and judiciously installed to
hut. Outside the hut, two large Helmholtz prevent unwanted electric and magnetic fields
51from straying into the animals’ habitat. a follow-up series, we changed the direction of
Each morning, two observers ran a the field again on a daily basis, but this time in
series of 15 to 20 trials after first turning on the random order. Under this regime, our most
lights, shutting off the airlifts, and checking active stingray, without further training, made
the direction of the horizontal component of 120 correct choices out of 184 trials (PYou can also read
