82. Lilly, John C. 1963."DistressCall of the BottlenoseDolphin:Stimuliand
Evoked Behavioral Responses." Science. Vol. 139. P. 116-118
Reprinled
from
Science.
lanuuiy
11,1963,
Voi.139,
No.3550,
pages
116-118
Copyright
O 1963 by the American
Association
for the Advancement
from
DistrPssCallof the Bottlenose
Dolphin:Stimuliand
by
the
East
Coast
of
the
Florida
The instances in which the call was
Abstract. Analysis of the Innlzy different vocal prodnction.r of pairs of bolrlenose dolphins (Tursiops truncatus Montngrc) antl the related behavior patterns
shows that one pair Of specific sIIort (0.2 to 0.6 second) M,histles was consli,nulnted
x··-
Keys.
Evoked Behavioral Responses
si.~tenrly
~
of Science
physicnl
rlirlress.
observed
are
specific
stimuli
related
to
seem
distress.
The
to be the
result
of real or potential
physical
damage.
The
situations
which
or prevents
surfac-
most
frequent
This call stii~~rtlnrerl
nearby aniinals elicitedthis call were: (i) somecondi-
to PLIsh the head of the distressed nni,nal to the surface to breathe.
arnOl?nl breathed, a vocal exchange preceded other forms of aid,
After tAe
tion which
impedes
ing to breathe; (ii) removal of a young
The bottlenose dolphin (TLlrisops
truncatlts Montagil) emits specific
sounds under well-defined conditions
(1-3). A special pair of whistles and
fundamental frequency (8 to 20 kcy/ (4 to 6 feet long) dolphin from the
sec) and falls to a relatively low funda- water; (iii) son~e painful stimulus to
mental frequency (3 to 5 key/sec). the body; (iv) a condition, in the case
This pair is emitted repeatedly with a of infants, that isolates it from its moth-
the behavior
associated with these
whistles was first observed in 1955 and
delay of only a few tenths of a second
between pairs for several seconds.or
er; (v) excessively forceful contacts
(with teeth or ramming or striking)
briefly described in 1958 (3). This
several hours and stops when appro-
by another anima'l: and (vi) electri-
account presents further
priate relief is obtained.
cal stimuli
this pair
(2-4).
of whistles
evidence that
is a "distress
call"
This call is one of many unique
The call is emitted
air depending
underwater
on the
or in
circumstances.
inforcing)
in specific
brain
(negatively
areas
(4,
cally, the first response
1O).
re-
Typi-
of the other
short whistle patterns (1, 2, 4) and is
The intensity (measured at the dolphin's
individuals within hearing of the call
not to be confused with general "alarm
whistling" (5-7); the latter is apparentry the same as some of the more
prolonged "vocal exchanges" between
dolphins (2, 5) and similar to the secondary exchanges which occur as consequences of rescue actions.
Distress calls of animals other than
the dolpi~in have been described in the
head) of the underwater call can be
as low as the noise level of the electronic apparatus or up to 100 decibels
higher. In the usual cases during underwater emissions the blowhole slit can
either emit air or not emit air (6).
Young, small (5 to 6 feet long) dolphins usually emit air; older ones may
or may not,
was to stop the emission of all sounds
and to start a search for the dolphin
emitting the call. When the animal in
stress was found, the finder pushed the
head to the surface by placing its
own head under that of the animal in
distress. The rescued animal then took
one or several deep breaths and sank
again.
literature (8). In the case of the dol-
In air the call was heard faintly,
phin, the responses of nearby animals
accompanied
of the same species may resemble, in
general effects, those described in the
lips of the blowhole or heard loudly
at the open blowhole from structures
literature
at the outer
After this "first-aid" maneu\·cr !primary tactics),
an eschange
of whistler;
(2) took place between the distressLi:
dolphin and the rescuer(s). After such
deeper in the airways. The sounds in
an
but they differ from those described for
air can be of such low intensity that
changed tactics from pushing Lip under
some birds and some fish.
they can be barely audible even near
the head
Behavior was visually and sonically
recorded with motion pictures and tape
the head (closed or open blowhole) action (secondary tactics) (4). A
or they can be piercingly loud a few mother rescued its infant directly in
recordings
for some terrestrial mammals
by bubbles,
(1,
2).
The
underwater
feet away from the head (open blow-
eschange,
the
rescuer
Llsunlly
to more singly appropriate
an appropriate
fashion, thus abolishin~
whistles were recorded by means of a
hydrophone and the whistles in air by
hole): the range from the lowest to the distress call (prinlary tactics only)
the highest intensity is about 80 deci- by steering it out of a corner, and
means of an air microphone
bels. The animals vary individually
The observations
(1, 2).
were made from
1955
their
abilities
to whistle
a distress
in
call
driving off other animals, for example.
SLIPPort
Of the
infant
by the
n~other
into 1962 under a variety of environmental situations on 23 different animals captured from three regions of the
shoal waters of Florida (the St. Au-
in air with high intensity. However,
each animal was able to make quite
loud whistles under water. While a
dolphin was whistling under water we
may continue even after the death of
the infant (II).
Tn several cases an animal fell over
to one side for one reason or another,
gustine inlet to Jupiter inlet, the middle
Florida Keys near Marathon, and~ at
manually felt, over the skull, the vesti- and was unable to reach the surface
bular sacs partici~ating in the vocal in order to breathe without inhaling
Naples on the west coast of Florida).
The call itself is similar to other
whistles in the "vocal exchange" group
of sounds (2). It is repeated many times
process as these sacs filled and emptied during whistling.
There were individual differences in
the voices of the animals (2, S);trained
water. These secondary
lowed: the aiding dolphin
held still) on the proper
distressed dolphin in order
tactics folswam (or
side of the
to prop it
until an appropriateresponseis elicited humanlistenerscoulddistinguishemis- up ~hese tactics allow the blowhole
either from the other dolphins in the
neighborhood or from a human. The
call consists of a group of two whistles
(Fig. i). The first whistle starts at a
relatively low fundamental frequency
(3 to 5 key/sec) and rises to a relatively high fundamental frequency (8 to
20 key/sec).
The second whistle of
sions from individual dolphins. Such
differences did not affect the rescue
responses of animals meeting for the
first time. For example, the calls of an
injured large female (8 feet 3 inches),
newly captured from the Gulf of Mex··
ico near Naples, Florida, elicited a rescue response at first meeting by a
to be raised to the surface either while
both dolphins are stationary or in motion. This seems to be a common secondary;maneuver
for correction of
asymmetrical propulsion and buoyancy
problems, which may result from bloating of the rumen (two cases, gas expelled later), breaking of ribs, tone
the
young
case
pair
starts
at
a
relatively
high
(6 feet 9 inches)
male captured
at
autopsy),
injuries
to
flippers
(six cases), and malfunctions of' the
One of them propped her upright. She head with tightly closed blowhole, in-
central nervous system (two cases of
stopped distress calls and a rapid vocal side head with open blowhole, and at
prolonged anoxia).
exchange took place among the three. biowhole slit) suggests that these ani-
The secondary correcting maneuvers
are preceded by vocal exchanges. Re-
Immediately, one animal held her up mals can use each of several parts of
and the other one stayed nearby. From the nose for these whistles, rather than
cently, we were given a opportunity then on, the two animals took turns just a single area (4, 6, 7, 9, IS, 14).
for continuous observations over a period of several days. A newly caught
female began distress whistling after
propping the injured female against the
JOHNC. LILLY
wall of the tank to keep her from Co~l2n?LlnicntionResearch InstitLlte,
tipping her blowhole over to the left Min,~li 33, Floridn
being alone for a few hours. She fell
side, or they would holdher
over to her side and water
water
entered
her
blowhole with each breath. Two other
animals were allowed to enter her tank.
between
them
in the
in the
center
of
the tank (12). Other appropriate maneuvers maintained
the animal upright.
One rescuing dolphin, for example,
pressed the flukes of the sick dolphin
A
v
;·
8
,~B
other
effective
tacticthe rescuer put
his head just behind the dorsal fin on
ii i sec
key/sec
Ibl·''
Were a variety of ways of keeping the
animal
upright
in the
shallow
These tactics continued
b=r
-
water.
day and night
for four days and were intermittent for
2 weeks
I,.,,.,,
-----"jSec
B'
~'''
·...
,*
key/sec
·~r
until
the
distressed
animal
re-
covered.
cases
a sick animal
isolated
case
was
found
dead
in the
isolation tank in the morning. Seven
·Plo--·-as----e
n
for injections
of antibiotics
vitamins and returned
and
to the group. Tn
sonicspectrographic
records(A and A': "II but two caseswhen a healthydolB and t3') are shown for each of two calls
phin was allowed to care for the sick
(two inverted
dolphin,
V's). In a typical sequence
of such calls, A is separated from B by an
to 1.0 secconsists
of
to 50 or more calls. The variations between the patterns of the two above calls
are within the normally occurring range
of variation.
The amplittlde
varies somewhat during
each whistle of each call: it
reaches
a maximum
early
in the rising
the
ill animal
survived.
The meanings of each half of the
distress call are still obscure; eventually
nlea"ines may be assignable to each
half. A healthy dolphin in solitude may
emit the first portion of the distress call
repeatedly.
This seems
to be an "atten-
frequency phase, falls somewhat as the frequency reaches peak, and rises again as
the frequency falls. From one individual
tion" call
"~e""t to
be within
of other
to the next the highest
and lowest
quencies
of the first partial vary from
20 and from 3 to 5 key/sec
(A' a,ld
water of the isolation
tank,
was emitted by the solitaire.
fre8 to
B').
The average rate of change of frequency
with respect to time is typical (4 to 10
key/sec")
The
duration
for the first partials
of
each
half
of
(A and B).
the
call
is
(without expressing distress)
reach any animals who may
hearing distance. After spoor
animals was released in the
this
call
Very rarely have we heard the falling
tone pattern of the last half of the call
without first hearing the preceding ris-
usuallyequalto the otherhalfand ran~es ing O"e.Dolphinsemit manydifferent
from 0.2 to 0.6 second.
With minor
ex-
ceptions (at onset or offset A'), the
kinds
of complex
whistles
and
whistle
patterns in their vocal exchanges (1, 2)
first partials contributemore energy but this pure fallingpattern is rarely
and are usually more continuous tMan
the
higher
partials
(A'
and
B').
With
minor exceptions,the higher partials are
1958);
W.
Univ. Press, Cambridge, Mass.,
E.
EdS.. nni,nnl
(Alnerican
Lanyon
and
W.
N. Tavolga,
Sounn+ n,~d Co,~l,,ll~,lico~io,~
Institute
of
Biological
Sciences,
Washington,
D.C. 1960).
9. B. Lawrence and W. E. Schevill. UI~II.MIIto.
sel~m Comp. Zool. Han.,
114 (1956).
J.
Miller,
c.
Lilly
and
A.
M.
J.
Co,,~p.
P''''"'o'.PS''C"O'.;
55,73 (1962).
11. C. L. Hubbs, J. Mnnlrnnl. 34, 498 (1953);
J· C· Moore, ihii(.. 36, 466 (1955).
'3· J· C· L"'y, Proc. Am. Phil. Sec. 11i6, 520
(1962).
the
Office
of
found within such exchanges. The fol-
lowi"6 phase (coupled to the rising
integral multiples (2, 3, and so on) of the
one) seems to be reserved for real or
frequency of the first partial (A' and B')
potential physical distress.
at a given instant. The frequency scale in
kilocpcles per second is given at the right
side of the figure; the time scale for A and
whistle
The mechanism of production
as well as other
whistles
of this
is still
B is tinder A and that for A' and B' is bC3- under investigation, The npnnber of the
tween A' and B',
observed areas of production finside
Naval
Research.
Current
sup-
port is from tl,e National Institutes of Health
~~,~he Air ForceOfficeof Scientific
Re-
ditt'erent sick animals were isolated 310ctober1962
briefly
Llnderwater
distress
calls
dolphin.
Two
samples
of
interval
of silence
lasting
0.5
end.
A representative
group
,,lnls (Harvard
from a nonsick one sent out immediate 14.The early portionsof this work were supdistress calls. The isolated sick aninlal
po''ed by NationalInstitutesof Healthand
in each
Fig. I. Typical
of bottlenose
ChicagoPress, Chicago,Ill., 1961).
8· W· H· Thorpe. Lmming o,ld Instinct ir2nni-
12.:S6Bil9S~e6~enaler
""dD·Caldwell,
ibid..37,
In three
~'''
p~---~-~----a
~*~';~'~^~"""
"'"~"~
the left side, and elevated the biowhole
above the surface of the water. There
.·Or·rwH4luw*r·~·-
A'
··
city, N.Y., 1961).
key/sec flat against the bottom in the shallow 5. F. E. ErS"p'"",
Nnl.Hisr.Mnp.62 (1953).
water, thus straighteningher up. In an- 7. W.
F,I?·si·~·
PsJ·chol.
41,111(1948).
N. Kellopg, Porpoises
nnd Sonnr (Univ. of
1
Ir······· ·u.-l·~c~s,
References and Notes
1· J· C· L"ly and A. M. Miller,Scie,lce133,
2. 1689(1961).
~ihid~134, 1873(1961).
3·
J·
C·
L"'y.
Anl.J. Pr)chinr.
115,498Garden
(1958).
4. --,
Mnn nnd Dolpltin
(Doubleday,