Download Approaches to the Study of the Behavior of

AMER. ZOOL., 17:471-486 (1977).
Approaches to the Study of the Behavior of Sharks
SAMUEL H. GRUBER AND ARTHUR A. MYRBERG.JR.
Division of Biology and Living Resources, Rosenstiel School of Marine and Atmospheric
Science, University of Miami, Miami, Florida 33149
SYNOPSIS Many kinds of sharks are dangerous and apparently unpredictable predators
whose behavior is virtually unknown. This is because they are difficult both to maintain in
captivity and to observe in the field. However, the purpose of this paper is to review the
behavioral information on sharks and, more importantly, to suggest approaches which will
accelerate progress in understanding the activities of these animals. Shark behavior has
been investigated within the methodological frameworks of both comparative psychology
and ethology. Thus the underlying philosophies of these disciplines are briefly discussed.
Six approaches for investigating the activities of sharks are presented. Approach I involved
intuitive studies drawing upon natural history notes and fisheries statistics, and is typified
by Springer (1967). This work set the stage for future quantitative research. Approach II is
also intuitive. Here, as typified by Klausewitz (1962), inferences about behavior and
ecology are drawn from morphologic and taxonomic considerations. Results appear to be
useful in only the broadest of applications. Approach III, an ethological approach we term
"structure of behavior," rests upon direct observation of behavior. The basic rationale
underlying this technique, including examples of field and laboratory studies with sharks,
is given. While we are at a beginning stage in the ethology of sharks, this approach appears
to hold great promise. Approach IV, the study of activity rhythms in sharks, is reviewed.
Little is known about such rhythms, which represent short-term temporal activity.
Practically nothing is known about long-term activity, i.e., behavioral ontogeny. In
Approach V psychological studies of learning are reviewed with emphasis on habituation,
operant and classical conditioning in sharks. It is concluded that learning probably plays an
important role in the lives of sharks and that they are clearly not the stupid, blindly
swimming creatures of folklore. In Approach VI studies of sensory physiology using
behavioral techniques are briefly discussed. Results led to the conclusion that sharks are
well adapted to detect and respond appropriately to a wide variety of environmental
stimuli. Though the difficulties are real and many, the paper ends on an optimistic note,
and it is felt that continued effort will unquestionably lead to a significant increase in our
understanding of these fascinating animals.
INIRODUCI ION
large animals in the sea. In addition,
sharks have, throughout recorded history,
Sharks compose one of the last major interfered with many of man's activities in
groups of living vertebrates whose be- the ocean (and we do not yet know how to
havioral activities remain virtually un- prevent this). The present state of our
known to science. This might well appear relative ignorance rests in large part upon
surprising, since these animals are rela- difficulties which arise when conducting
tively common in most marine, and even in long-term behavioral observations on
certain freshwater habitats throughout the these animals. This, in turn, stems from
world; and it is no mere speculation that the fragility of most species in captivity and
they constitute perhaps the most abundant because facilities for adequate maintenance of adults are virtually non-existent.
Th
Preparation of this paper was entirely supported by
e s e Stumbling blocks a r e actually SO
the Office of Naval Research through contracts formidable that basic questions arising
#N000l4-75-C-0l73 (SHG) and #N000l4-75-C- from biological considerations, such as ap0142 (AAM). We gratefully acknowledge the artistic propriateness of laboratory environments
efforts of Ms. Marie Gruber and the editorial assistj
, seui
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c a n s d d
if
ance of Mrs. Monica Abbott. We thank Ms. Jeanne
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Duke for typing the manuscript. This manuscript was ever, be addressed. Conditions associated
with field studies are often even less favorwritten at 9300 SW 99 St., Miami, Florida 33176.
471
472
SAMUEL H. GRUBER AND ARTHUR A. MYRBERG, JR.
able. Firstly, sharks represent a real threat
to an observer approaching them (Johnson
and Nelson, 1973; Myrberg et al, 1972).
Additionally, logistical and methodological
problems associated with field observations
of swift, far-ranging animals such as
sharks, often combine to make the cost/
effort ratio of data collection untenable.
Thus, progress in describing, let alone
understanding, the behavior of sharks has
been slow indeed.
Several descriptive and empirical approaches to the study of behavior are
briefly reviewed in this paper and possible
ways to accelerate progress in understanding the activities of sharks are suggested.
There have been several conceptual
frameworks upon which the behavior of
sharks has already been investigated.
These have been shaped for the most part
by the methodologies and underlying,
often divergent, philosophies of ethology
and experimental psychology. A simplistic,
but perhaps reasonable, assessment of the
goal of many ethologists is that they hope
to provide an understanding of the role
that adaptive or selective processes play in
molding the behavior of an animal, a
species, a population, or even a community
of interacting species. By appropriate
comparative study of the activities of carefully chosen species, ethologists often seek
insight into the organization of behavioral
"units" through space and time—the latter
being suggested by ontogenetic and/or
phylogenetic series. Thus, analogy and
homology become principles of information as important to the ethologist as they
are to the comparative morphologist
(Lorenz, 1958, 1963, 1974; Wickler, 1961,
1965, 1973). Ethologists as a group appear
rather disinterested in determining, out of
natural context, behavioral structure or
capability per se. However, this has been of
major interest to many experimental and
comparative psychologists since the modifiability of behavior (i.e., its norms and its
limits), especially as it relates to man and
regardless of context, is, by itself, an intriguing subject. Psychological studies
often emphasize the environmental rather
than the genetic contribution to behavior,
although genetics was shown long ago to
play a role even in the maze-learning of
rats (Tryon, 1929). Perhaps the ultimate
goal of most psychologically oriented
studies is the establishment of inclusive
principles, operating especially within the
vertebrate line, that will provide high predictability and control of behavior through
experience. Psychological studies also extend to the functional organization of basic
systems, such as the vertebrate CNS. Here,
investigations are ordinarily confined to a
few intensely studied species. The restriction to "standard species," however, has
been a point of contention by several comparative psychologists (Beach, 1950; Bitterman, 1963, 1975; Gossette, 1968; Gossette and Brown, 1967).
Although it is often difficult for
ethologists and psychologists to view a
given phenomenon or an idea from a
common "vantage point," there has recently been movement toward a more
common synthesis of understanding (see
Demski, this volume) which has been valuable for both disciplines.
DISCUSSION OF THE APPROACHES—
THEIR METHODS AND DATA
Systematic study of the behavior of a
species often begins with accumulation of
information in peripheral areas such as
natural history studies. Carefully recorded
behavioral incidents included in ecological
field notes are also useful. Simple behavioral anecdotes can form the bases of
first hypotheses; however, when there is a
goodly fund of misinformation, as with
sharks, this source of information becomes
exceedingly difficult to evaluate. Still, the
shark biologist has other sources of information. For example, fishery statistics can
provide data on factors such as species
aggregations, i.e., which sharks form
groups, the time of year that such groups
form and their structure. This source of
information, in fact, provided a major
basis for Springer's (1967) paper on the
social organization of shark populations.
He noted that sharks form aggregates
which are segregated almost universally by
size, and often sexually. While many
BEHAVIOR OF SHARKS
sharks were described as indiscriminate
predators on other sharks—a factor leading to size segregation—little intraspecific
aggression was evidenced within groups.
Springer's summary of presumed courtship activities indicated that males cease
feeding well before the mating season
(based on the reduction of liver storage
capacity), while females continue to feed
through that period. By noting the nature
and the distribution of slash wounds on
captured sharks, Springer further speculated that the courtship of carcharhinid
sharks included harassment by males, involving slashing with the teeth, apparently
to induce females to cooperate during
copulation. Such an activity could easily
produce the well-known "mating scars"
commonly seen on mature females and
could set up a rather dangerous situation
for the males, as well. Adult females, being
larger on the average than adult males,
might easily attack their tormentors due to
the absence of any feeding inhibition at the
time. Springer even suggested that killing
of male carcharhinid sharks by females
during courtship might be a factor leading
to a general increase in the size of females
relative to males.
The interesting points made by Springer
in his noteworthy paper were arrived at by
indirect means, and thus a behavioral data
base was lacking. Yet his insight, garnered
over years of experience with sharks,
raised many important questions and
pointed the way to more quantitative observations.
Another approach to the study of shark
behavior stems from strictly anatomical
considerations, whereby inferences about
behavioral and ecological functions are
drawn from the study of morphological
characteristics. This approach is typified
by Klausewitz's (1962) study relating body
form in sharks to habit and habitat. Three
generalized types of sharks were identified
(Fig. 1). Sharks of Group 1 are streamlined
animals with caudal lobes of almost equal
length, the tail forming an angle of about
50° with the body. These sharks also possess conical heads terminating in a pointed
snout and are typified by the family Lamnidae. Its members are said to be pelagic,
473
active, fast-swimming predators, feeding
mainly on swift-moving school fishes.
The sharks of Group 2 are less streamlined, possessing tails with unequal lobes,
the upper forming an angle of about 30°
with the body. The head is dorsoventrally
flattened. This group, typified by the Carcharhinidae, is generally more littoral and
apparently feeds mainly on solitary fishes
and invertebrates. Finally, the animals
represented by Group 3 have massive
heads and tapering, sinuous bodies with
extremely unequal caudal lobes, the lower
being only weakly developed and the
upper approaching an angle of 0° with the
body. This group, typified by the nurse
shark, Ginglymostoma cirratum, and the
other orectolobids, is considered extremely sluggish and wholly benthic, feeding primarily on bottom invertebrates and
fishes.
Klausewitz's appealing scheme unfortunately overlooks numerous obvious and
important exceptions (Budker, 1971). For
example, the basking shark, Cetorhinus
maximus, has a symmetrical tail and a conical head; yet it is a sluggish planctivore.
The reef white tip shark, Triaenodon obesus,
shows few of the characteristics of the
nurse shark; yet it spends much of its time
in caves and feeds on benthic organisms.
Also, the oceanic whitetip, Carcharhinus
longimanus, though a perfect example of
Group 2, occupies the presumed habitat of
the lamnids (Group 1). Thus, it is clear that
the results of such intuitive studies are
perhaps applicable for the broadest of
generalizations but cannot be rigorously
applied to any species without great caution.
A third approach, ethological in nature,
is based upon what might be termed an
analysis of the "structure of behavior."
This approach centers upon direct observation and an analysis of the motor and
action patterns of animals and groups as
they move through space and time. This
approach holds great promise for the future as advances continue to be made in
maintenance of sharks {e.g., Myrberg and
Gruber, 1974) and improved technology
of underwater observations and telemetry
(Myrberg, 1976; Myrberg et al., 1969; Nel-
474
SAMUEL H. GRUBER AND ARTHUR A. MYRBERG, JR.
FIG. 1. Three generalized shark morphotypes as
described in the text. The upper animal representing
group I is the pelagic porbeagle shark (Lamna nasus).
Representing group II in the middle is the more
littoral sandbar shark (Carcharhinus milberti). The
lower shark representing group III is the benthic
nurse shark (Ginglymostoma cirratum). Line drawings
modified from Bigelow and Schroeder (1948) by permission.
BEHAVIOR OF SHARKS
son, 1974; Sciarrotta et al, 1972). The
basic methodology is straightforward — it
requires an initial examination and description of readily identifiable postures
and patterns of movement shown by the
animals concerned. As this so-called descriptive catalogue, or ethogram, develops,
a requirement for accuracy forces the observer^) to analyze the occurrence of such
postures and patterns relative to the occurrence of other similar activities. In addition, the observer attempts to define
those specific situations that appear associated with the elicitation of specific activities described in the ethogram. As this
examination proceeds, hypotheses begin
to be generated about the organization of
the patterns and postures, their functional
interrelationships, their occurrence in
time, and—if more than one species is
being observed—behavioral similarities
and dissimilarities. The next stage often
requires selection of one or more hypotheses, followed by testing with the most
appropriate quantitative methods.
The entire process of unraveling the
"structure of behavior" should ideally
begin with an analysis of locomotion and
its underlying neuroanatomical basis. Actually, this aspect of shark behavior is
relatively well known from the classic
studies by Grey and Sand (1936),
475
Lissmann (1946) and more recently, by
Roberts (1969).
It is often necessary in detailed studies to
select certain postures and motor patterns
from the ethogram that are repeated frequently enough by the animal in specific
situations so that analyses can provide
statistically valid correlations. It is also incumbent upon the observer to analyze a
reasonable number of those situations of
interest. These points have been major
stumbling blocks for ethological studies on
sharks. For example, in a recent review
Gilbert and Heath (1972) stated that mating in sharks had been observed and
figured only four times in the literature
(see also Worms, this volume). While
courtship activities have been inferred
from limited direct observations (e.g.,
Dempster and Herald, 1961; Clark, 1969),
certain indirect evidence appears corroborative. For example, attempts by the
male to grip the pectoral fin of the female
with his teeth could account for the presence of "mating scars" on females
(Springer, 1967) and sexual dimorphism
of teeth in several species (Springer, 1964
and Fig. 2).
Activity patterns during the few cases of
mating that have been observed appear to
be quite varied. Cat sharks, Scyliorhinus
canicula, lie on the bottom entwined, while
FIG. 2. Sexual dimorphism of the teeth in the genus lower teeth (B below), in contrast, are similar to the
Scoliodon. The lower teeth of the male (A above) uppers and appear to be adapted for cutting. Taken
appear to be modified for holding. The female's from V. Springer (1964) by permission.
476
SAMUEL H. GRUBER AND ARTHUR A. MYRBERG, JR.
horn sharks, Heterodontus francisci, lie side
by side. According to Clark (1969), the
lemon shark, Negaprion brevirostris, apparently maintains synchronous swimming
while in copula.
This brief summary covers most of the
published information on courtship and
mating in sharks; and sexual activity is not
the least known area of shark behavior!
Clearly, valid conclusions about the underlying causality of this behavior, based on
such tentative findings, cannot be drawn.
Yet various authors have not hesitated to
ascribe, in the most speculative manner,
behavioral functions {i.e., courtship, dominance or aggression) to one or more activities of sharks which were only casually
observed. It should be evident to even the
most naive observer that only after repetitive and careful observation can such
speculation be considered useful. By ignoring this "rule," misunderstanding, confusion and error often swamp hardearned additions to our knowledge.
The first study that specifically utilized
repetitive observations on the behavior of
sharks was reported by Allee and Dickinson (1954) for members of a captive colony
of smooth dogfish, Mustelus cants. During
their brief investigation, they noted that
smaller individuals within the colony
definitely avoided larger ones if the difference in body length exceeded 7.4%. In
only ten hours of observations, they provided the first direct evidence of social
organization in sharks.
Real progress in understanding shark
behavior will only be made, however, when
investigations of this sort have evolved to
an analytical stage dependent on precise,
accurate description, and a quantitative
data base as described above. Such studies
can be conducted in the field with concomitant natural or induced manipulation
or under the controlled conditions of the
laboratory. The former are exemplified by
the work of Nelson and his colleagues
(Johnson and Nelson, 1973; Nelson,
1974). In one field study on the gray reef
tion appears to be communicative. This
particular display included a specialized
mode of swimming, combined with a
posture that we subsequently termed
HUNCHING (Myrberg and Gruber,
1974, and Fig. 4C). We now know that this
posture is shown by at least five species of
carcharhinid and sphyrnid sharks and all
perform it under similar circumstances.
The specific circumstance mentioned here
was that created by Johnson and Nelson in
their attempt to discover the underlying
cause of this unusual behavior pattern.
The divers positioned themselves on the
reef such that nearby sharks were placed
in an apparent conflict situation of increasing intensity. The authors suggested that
approach:withdrawal represented the
major conflict. As expected, the elements
of the display changed directly with
changes in the situation. The most intense
display occurred when the shark's escape
route was restricted by the body of a diver
and the vertical reef face. Their results not
only suggested the agonistic function of
this behavior but also pointed to the interent danger of this type of field study. It
is understandable that the authors discontinued experiments because of the increasing probability of attack.
An ideal ethological investigation often
combines laboratory study with field observations. This can result in a level of
precision and validity not obtainable in
either alone. Such was our aim in a study
of the bonnethead shark, Sphyrna tiburo
(Myrberg and Gruber, 1974). A major
objective of the investigation, carried out
in a large semi-natural enclosure, was to
provide a basic ethogram for the species.
To that end, about 1,000 man-hours were
spent observing a colony of individually
identifiable bonnetheads. This resulted,
among other things, in a description of 17
separate units of behavior, including three
distinct modes of swimming, and 14 relatively distinct action patterns, eight of
which were performed in a social context.
Figure 4 shows three such patterns. The
shark, Carcharhinus amblyrhincos ( =menisor- uppermost was termed FOLLOW. A shark
rah), these scientists carefully described a performing this pattern copies the movedisplay (Fig. 3), i.e., one or more specific ments of its leader for at least four body
actions closely related in time, whose func- lengths (often much longer). During a
BEHAVIOR OF SHARKS
FIG. 3. Agonistic display of the gray reef shark
477
eral, frontal and dorsal view of the shark in display.
For comparison, right-hand sketches show the same
views of the shark in non-display mode. Modified
from Johnson and Nelson (1973) by permission.
period of 46 hours, following was recorded 153 times, or an average of nearly
once every 20 minutes. Both sex and size
difference was manifested in the distribution of the data. One case was especially
striking: The largest female, when first
introduced to the study colony, was followed nine times more frequently by males
than by other females, and this took place
within the first 90 minutes following her
introduction. Females followed males—
especially large males—more frequently
than they followed other females. CIRCLE
and HUNCH are the other two patterns
shown in Figure 4 and both had clearly
social implications. Another revealing pat-
tern, the GIVEWAY, is shown in Figure 5.
When two sharks were on a collision or
near-collision course, the "subordinate"
shark yielded the right-of-way, while the
"dominant" shark proceeded straight
ahead. Dominant and subordinate, as used
here, are based on strictly operational
definitions. The GIVEWAY was performed frequently enough so that statistical analyses could be applied to the data,
and by this means we found that our study
colony was, indeed, socially organized.
The organization consisted of a straightline, size-dependent, dominance hierarchy
with the sex of the animal also playing a
key role. Figure 6 shows one method of
(Carcharhinus amblyrhincos). Left column shows a lat-
478
SAMUEL H. GRUBER AND ARTHUR A. MYRBERG, JR.
vs
FIG. 4. Three social action patterns of the bonnethead shark (Sphyrna tiburo). Upper sketch (A)
represents the motor pattern termed FOLLOW;
middle sketch (B) represents the CIRCLE; while the
lower drawing (C) is the HUNCH similar in pattern
and context to the agonistic display of Figure 3. See
text for further details. Taken from Myrberg and
Gruber (1974) by permission.
visualizing such an organization. While
size of the animal was clearly important in
the organization, we speculate that the act
of biting by males, which we observed in
contexts suggestive of reproductive activity, might well have affected their dominance relations with females and smaller
males.
Although various behavioral patterns
were described and several analyses performed, this study represents a mere beginning in understanding the activities of a
single species of shark. Clearly, however,
all members of the colony showed a
number of distinct behavioral units that,
when quantified under appropriate conditions, provided meaningful insight into
mechanisms underlying the social interac-
BEHAVIOR OF SHARKS
479
FIG. 5. The action pattern, GIVEWAY, in bonnetheads. Analysis of this behavior formed the basis
of the dominance hierarchy shown in Figure 6. Modified from Myrberg and Gruber (1974) by permission.
tions of sharks. This, hopefully, has set the
stage for continued in-depth studies of
similar activities in the same or other
species. Future investigations could well
involve analyses of specific relationships
between given behavioral events, such as
how they are clustered over time and
space. Also, since completing our 1974
study, we have become aware of still other
distinct motor patterns in several species
and thus, with further study, more comprehensive ethograms can be provided.
The final result of all such investigations,
encompassing a variety of species, can
without question provide meaningful insight into the central problems of ethology: the function, causation, and evolution
of behavior. The ethology of sharks remains virtually unexplored; but the few
small paths, leading to ever-increasing understanding, have shown promise and
could well be widened and extended.
Up to this point, we have been looking at
behavior as if it were relatively fixed over
time. Clearly this is not the case; but little
or no information is presently available on
the temporal modulation of behavior in
sharks either over the long term (ontogenetic) or over shorter periods, such as
annual, lunar or circadian rhythms which
are so universally known in other animals.
The only controlled studies on activity
rhythms in the elasmobranchs are those of
Nelson and Johnson (1970) and Finstad
and Nelson (1975). The former study
demonstrated under appropriate laboratory conditions that two species, the horn
shark, Heterodontus francisci, and the swell
shark, CephaloscyIlium ventriosum, were noc-
turnal and that one, the swell shark, appeared to possess a clear endogenous
component, with light serving as
Zeitgeber. Under constant, dim illumination, Cephaloscyllium had a free-running
period of about 23.6 hours, which gradually drifted out of phase with the local
day-night regime (Fig. 7). Such a phase
drift is considered good evidence for an
endogenously controlled, circadian
rhythm. The horn shark appeared, in the
initial study, to differ with respect to the
controlling mechanism underlying its
locomotor activity. This species showed
low-level aperiodic activity under dim illumination and high-level aperiodic activity in constant darkness. However,
Heterodontus was later subjected to additional scrutiny (Finstad and Nelson, 1975)
and was then found to possess a clearly
endogenous component to its activity, with
a gradual drifting period length between
20 and 23 hours. Field observations by
Nelson and his co-workers also confirmed
that both the horn and swell sharks, as well
as the angel shark, Squatina, and blue
shark, Prionace, are all most active at night.
Further quantitative evidence of diurnal
periodicity in locomotion has been obtained also for the bonnethead, Sphyrna
tiburo (Myrberg and Gruber, 1974), while
additional cases of rhythmicity among various activities have been reported from the
field for the tiger shark, Galeocerdo cuvieri
(Randall, 1967; Springer, 1943,1963), and
480
SAMUEL H. GRUBER AND ARTHUR A. MVRBERG, J R .
April - July
40 Hrs Observations
Upper Tide Channel M. Seaquarium
N = 200 Giveways
33
33
33= % of times that a given
shark gaveway to the shark
to which the arrow points
4 r no. of giveways by one
shark to the shark to
which the arrow points
FIG. 6. Social organization and dominance hierarchy in a colony of 10 bonnetheads. In the diagram,
sharks are ranked in order of descending size. Two
diagonal lines are associated with each shark (except
the largest and smallest). Solid arrows point to the
dominant shark in a GIVEWAY encounter. The
thicker the arrow the more frequently that shark
O6OO
dominated in the encounter. Clearly, larger sharks
dominated in the GIVEWAY situation. Yet sex also
played a role as can be seen for example by noting the
consistently thick arrows pointing to G, SL and SP.
Taken from Myrberg and Gruber (1974) by permis-
1200
1800
2400
1212
DARK |E
FIG. 7. Activity rhythms in the horn shark
(Heterodontus francisct) as a function of light level. On
day 5 the animal was placed in constant illumination
of 2.0 lux (bright) and later in dim illumination of
0.13 lux. The solid bars across the graph represent
motor activity steadily drifting out of phase with the
time reference. Such drift is evidence favoring an
endogenous circadian rhythm. Taken from Finstad
and Nelson (1975) by permission.
481
BEHAVIOR OF SHARKS
gray shark, Carcharhinus sp. (Hobson,
1968).
Since few sharks have been raised in
captivity and long-term studies have never
been carried out, ontogenetic changes in
the behavior of sharks are unknown.
However, changes due to experiential factors, such as learning, have been reasonably well documented. Although learning
processes have been examined by a few
ethologists when they appeared to be
operating in a natural context, the most
reliable evidence for learning in sharks
(e.g., discrimination learning, extinction,
spontaneous recovery) has been gathered
through use of the conventional paradigms of experimental psychologists.
Field experiments, directed at various
aspects of the sensory biology of sharks,
have often shown that these animals readily habituate to irrelevant stimuli, especially if trials are massed (Myrberg et al.,
1969, 1975a,6; Nelson and Johnson,
1972; Nelson et al., 1969). However, control studies for habituation have shown
that responsiveness suddenly reappeared
if certain characteristics of the original
stimuli were changed. Figure 8 illustrates
the results of an experiment in which
sharks, initially attracted to a lowfrequency sound, rapidly reduced their
100
m
"oc
O
50
Z
LU
U
OC
ACQUISITION
•—.DAY I
o— oDAY 2
D - D DAY 3
10
BLOCKS OF TEN TRIALS
FIG. 9. Course of acquisition of a classically conditioned movement of the nictitating membrane of
the lemon shark (Negaprion breviroslris). Training consisted of pairing a flash of light with a low voltage
electric shock 100 times per day (i.e., 10 blocks of 10
trials). Three days of training are shown. Note that
the sharks reached nearly 100% conditioned responses by the 60th trial of the 1st day. Taken from
Gruber and Schneiderman (1975) by permission.
responsiveness in the absence of positive
reinforcement. The figure, unfortunately,
does not show that the sharks reappeared
after the sound was changed by increase of
its pulse characteristics and addition of
lower frequencies.
Standard laboratory studies on learning
have, at times, used sharks as subjects. For
example, Gruber and Schneiderman
(1975) have demonstrated classical (Pavlovian) conditioning in the lemon shark
(Negaprion brevirostris). Figure 9 shows the
acquisition of such a conditioned response
in ten subjects after each had received 100
trials/day over a period of eight days. In
this study each trial consisted of a 500 ms
flash of light, accompanied by a mild electric shock during the last 100 ms of the
A / \
flash. By the third day, the subjects were
reliably responding to the flashes of light
prior to the onset of shock. Still other
studies
that have demonstrated classical
FIG. 8. Attraction of the sharpnose shark (Rhizoprionodon sp.) to acoustic signals consisting of an 80 conditioning in sharks include those by
Hz irregularly pulsed, overdriven tone. Decrease in Banner (1967) and Gruber (1967).
sightings over successive 3-minute test and control
Operant (instrumental) conditioning—a
periods strongly suggested that the sharks were
habituating to the acoustic signals. Taken from Myr- learning situation in which reinforcement
berg et al. (1969) by permission.
is contingent upon the subject's re32 •
TOTAL SIGHTINGS DURING TEST PERIOD
30-
MAXIMUM SIMULTANEOUS SIGHTINGS
28
DURING TEST PERIOD
26-
TOTAL SIGHTINGS DURING CONTROL
PERIOD
2422
t/>20-
wj
TEST PERIODS
olcONTROL PERIODS I
o I
I
2
2
3
3
4
4
5
5
6
6
7
7
8
4§2
SAMUEL H. GRUBER AND ARTHUR A. MYRBERG, JR.
FIG. 10. Underwater photograph ot a lemon shark
at the choice point of a "T-Maze." The shark is
choosing the right-hand door of a pair of doors each
illuminated by an array of optical fibers connected to
a light source. For choosing the brighter of the pair
the shark earns a food reward in the reinforcement
area behind the doors. Photo by C. Bry.
sponse—has also been demonstrated in
various species of sharks (Aronson et ai,
1967; Clark, 1959; Graeber and Ebbesson,
1972; Gruber, in preparation; Tester and
Kato, 1966). Figure 10, taken from
Gruber's unpublished work, shows a
lemon shark under operant training in a
"Y"-maze, the animal being rewarded with
a piece of fish immediately after making
the correct choice—in this case, passing
through the brightly illuminated door.
The results of such training are shown in
Fig. 11. Discrimination levels were about
75% after 10 sessions, consisting of 20
trials per session, with the criterion level of
10% error {i.e., only 2 errors in 20 trials)
reached by the fifteenth session.
Aronson et al. (1967) compared the
learning curves of three unrelated species:
a shark, a teleost and a rodent. The only
difference between the operant situation
was that water had been removed from the
mammal's tank; otherwise trials, responses, and stimuli were very similar.
Each subject was required to choose the
white from a pair of black and white
BEHAVIOR OF SHARKS
NUMBER of
483
SESSIONS
FIG. 11. Learning curve of the lemon shark on the
brightness discrimination task shown in Figure 10.
Open circles represent mean % errors for six animals;
closed circles were calculated from a standard curvefitting procedure. Learning is signaled by reduction
in errors, i.e., choosing the dimmer door. Chance
refers to random choice, i.e., the 50% correct level.
Discr. refers to the 75% correct limit of discrimination
usually allowable in psychophysical testing while
Criterion refers to the arbitrary 90% correct level
chosen in this study (from unpublished studies by S.
H.Gruber).
targets. Positions of those targets were capabilities. Methods utilizing behavior
randomly alternated from trial to trial. As modification and situation analyses have
seen in Fig. 12, sharks certainly do not led to the inescapable conclusion that
appear to be the dumb, blindly swimming sharks are extremely well adapted for decreatures that folklore would have us be- tecting and responding appropriately to a
lieve. Rather, the shark species chosen for wide range of environmental stimuli at
the discrimination task (Ginglymostoma cir- levels which are often astonishing (for a
ratum) had respectable rates of learning general review, see Zahuranec, 1975).
which, in turn, appeared to correlate with Space limitations do not permit elaboratthe complexity and size of their brain (see ing on the experiments or relating the
Northcutt, this volume). These and other considerable evidence affirming this point.
findings thus strongly suggest that be- However, the sensitivity of sharks to elechavior modification through learning trical stimulation is unparalleled in the
plays an important role in the lives of these animal kingdom (Kalmijn, 1971, 1974),
their chemical sensitivity reaches detectapredators.
bility
levels as low as one part per million
Probably our greatest knowledge of
and Mathewson, 1971;
(Hodgson
shark behavior lies in the indirect relation
of specific activities to various sensory Kleerekoper, 1967, 1969), and the low-
484
SAMUEL H. GRUBER AND ARTHUR A. MYRBERG, J R .
morphological data, will unquestionably
lead to a significant reduction in the depth
of ignorance that presently rests below our
shallow behavioral knowledge of this fascinating group of animals.
70
60
cr
§50
SHARK
-MICE
TELEOST
tr.
£ 40
REFERENCES
UJ
o
£30
Q.
20
10
10
15
DAYS
FIG. 12. Learning curves for three vertebrates on a
brightness discrimination problem. While the stimuli
were somewhat similar to those in Figure 10, the
training technique was quite different. Note the similarity in learning between the nurse sharks of this
study and the lemons in Figure 11. Most striking,
however, is the similarity in rate of learning in these
three very different vertebrates. Taken from Aronsonet al. (1967) by permission.
frequency end of their hearing range extends far below ours (Banner, 1967; Myrberg et al., 1975a, 1977; Nelson, 1967;
Wisby et al., (1964). Finally, they rank with
cats in visual sensitivity, exceeding man's
sensitivity by 10-fold (Gruber, 1967).
In summary, various approaches are
available for studying shark behavior. All
require intuition and judgement, the accuracy of which depends upon the direct
experience of the observer involved; most
require an extensive, quantitative data
base. Ever-increasing need for precision
and accuracy, as well as for quantification
(Lorenz, 1973), has often been frustrated
by the inherent difficulties in working with
sharks. In fact, much of our knowledge
about the behavioral biology of these animals derives from investigations of
juveniles simply because we have not been
able to maintain adults under appropriate
conditions. Such difficulties will probably
continue to set limits on the number of
behavioral scientists willing to study these
animals. However, continued investigations of the behavior and physiology of
sharks, supplemented with ecological and
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