"Displacement Reactions" in the Three-Spined Stickleback

Author(s): N. Tinbergen and J. J. A. van Iersel

Source: Behaviour, Vol. 1, No. 1 (1947), pp. 56-63
Published by: BRILL
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"DISPLACEMENT
REACTIONS"
IN THE THREE-SPINED
STICKLEBACK
by
N. TINBERGEN and J. J. A. VAN IERSEL
(Zoological Laboratory, Leiden, Netherlands)
(With 4 textfigures)
(Received

4. VI. 1946)

Several observers of animal behaviour have called attention to the fact

that an animal may, under certain conditions, perform quite "irrelevant"
movements. For instance, fighting domestic cocks go through the motions
of picking up some food; fighting starlings preen their feathers, courting
male birds of paradise wipe their bills, fighting avocets occasionally assume
the sleeping attitude, etc. This phenomenon has been subjected to an analysis
by

KORTLANDT

(I940)

and by

TINBERGEN

(I939, I940).

They showed that

such irrelevant movements occur when the animal is under the influence
of a powerful urge, but at the same time is in ~'ome way prevented from
expressing this urge in the appropriate way. The animal, under such conditions, does not suspend action, but vents its urge in movements belonging
to another drive. The behaviour "sparks over" (MAKKINK, 1936) from one
drive to another. Whereas a good name has been given to it in German which
has been generally accepted ("Ubersprunghandlung" KORTLANDT, "Uberno suitable English term has been found
sprungbewegung" TINBERGEN),
HUXLEY'Sterm "habit preening" for displacement preening in the great
crested grebe (HUXLEY,
19I4) is to be rejected because the phenomenon
has probably nothing to do with habit. Neitner "sparking-over activity", nor
"shamactivity" (CARPENTER, 1934), nor "substitute activity" (KIRKMAN,
1937;

TINBERGEN,

I930)

nor "irrelevant movement"

(RAND,

1943)

seeims

to be entirely satisfactory. The Rev. E. A. ARMSTRONG suggested to one of

us the name "displaced reaction", which was changed by Prof. HUXLEY
during a discussion on the subject into "displacement reaction". This term
is being adopted by Mr. ARMSTRONG in the forthcomningrevised edition of

DISPLACEMENT

REACTIONS

57

his "Bird display" and will be used here. Displacement reactions may
appear under a variety of conditions, most of which are of one of the
following three types:
i. 'he fighting drive cannot express itself by actual fighting because
a conflicting drive (the escape drive) is aroused at the same time. This
situation is of igeneral occurrence during boundary disputes between two
territorial fighters.
2. The mating drive cannot express itself by actual mating because the
required signal movement or releaser is not given by the mate. This is, the
cause of the occurrence of displacement reactions during courtship.
3. When an external stimulus, after having activated a drive, suddenly
stops, the drive may use displacement reactions as an outlet. This situation
seems to give rise to phenomena like post coition ceremonies.
Certain movements, therefore, can be aroused in two ways, viz., either
by activation of its "own" drive, or by activation of another drive, in which
latter case we speak of a displacement reaction. The displacement reaction
gets its impulse from a strange drive, its impulse is "allochthonous"; when
activated by its own drive a movement or rather its impulse is "autochthonous". Often there are differences between the allochthonous movement
and its autochthonous "example". For instance, the displacement reaction
may be very vigorous, in case its allochthonous urge is very strong. The
displacement preening or the displacement wiping-of-the-bill may be very
intensive, very hasty, or/and very much emphasised. Further, the displacement reaction is often less complete than its example: it may consist of
only part of the chain of movements composing the example. Thus a fighting
cock will rarely really eat something; its displacement reaction consists of
the pecking movement only, actual seizing and swallowing of food is not
observed.
Comparative study of displacement reactions has further led to the
following, partly tentative, conclusions:
I. The form of the displacement reaction is characteristic of each species.
For instance, every male starling preens when its fighting drive is obstructed; a cock or a male skylark always makes pecking movements under
the same conditions; a pigeon always preens when the mating urge is
frustrated, and so on. This is based o'n the fact that the displacement reactions are innate. A species may have a number of different displacement
eactions, each belonging to a special situation.
2.
In some cases, displacement reactions have a secondary function,
serving as a social signal for releasing special responses in other individuals
of the same species. Displacement reactions initiated by the fighting drive

58

N. TINBERGEN

AND J. J. A. VAN IERSEL

often have threat function, those by the mating drive may have the power
to release sexual responses in the partner.
3. Those displacement reactions which do have releaser function seem
to differ from such as have no communicative function by what has been
called ritualisation. Instead of being identical, or very nearly so, with the
autochthonous example, they differ from it by showing superposed movements which actually serve to make the movement more conspicuous. Thus
a displacement reaction with threat function may display special weapons
or bright colours.
The above is a sketchy review of the work thus far done. For particulars
we refer

to KORTLANDT (I940)

and to TINBERGEN (I940).

During the spring of I946 we made some more observations on displacement reactions in the three-spined stickleback, on which we shall now
report. We have decided to publish them because we are able to supplement
and to correct former statements made by the senior author and because
we are able to substantiate some of his tentative general conclusions put
forward

in 1940.

Obstruction

of

the

fighting

urge

When a male stickleback in his territory meets another male, he chases

it. Outside his territorv, however, he will not attack but avoids a fight,
and, if attacked, he flees. Where two territories meet,
fierce fighting often ensues on the boundary. In these
combats, actual fighting is interrupted by threatening. A
threatening male stands in a vertical position, head pointing downward, and making the movements of picking
something up from the bottom (fig. i). This movement,
which experiments with dummies have shown to function
as a threat, intimidating other males, is, in origin, a
displacement activity, and can be experimentally aroused
I940). In
by obstructing the fighting drive (TINBERGEN,
previous papers, this movement was interpreted as displaFig. i. Ma'e Gas- cement feeding; new observations have shown that we
terosteus aculeatus have to do with digging, viz., digging a hole for the nest,
L. threatening.
an activity which, when autochthonouslv aroused, precedes
the actual nestbuilding. In most cases the incompleteness of the movement
does not allow us to see whether the animal is going to pick up food or
to remove sand. Occasionally, however, especially when the fighting drive
is very strongly activated, the movement becomes more complete and

DISPLACEMENT

59

REACTIONS

develops into perfect digging. This is very rarely, if ever, seen under
"normal" conditions but we discovered that by putting several males together
into one aquarium (for instance, five males into a tank measuring 200 X 50

A~~~~~~~~~

. ..

. . .

. . . .

.. . .

'
;

Fig.

2.

'

~~~~~~~~~~~~~~~~~~~~~*

*. **'
. ': ,

Male writhnlest inl deep depression made by displacement digging (mnaleI from
fig. 3).

X 50 cm) we coulld evoke complete displacement digginlg at will. IThis was

due to the extremely small size of the individual territories, a condition that,
just as in territorial birds, very strongly activates the fighting drive.
Such males spend their timnein nearly continuous fighting and threatening.
In thfe course of one or two days a male in such a situation would dig one
or more (up till 8) deep holes (see figs 2 and 3). As lonlg as. the tank
remained crowded with territorial males, boundary disputes with threaten-

6o

N. TINBERGEN

AND J. J. A. VAN IERSEL

ing and digging continued, resulting in enormous depressions at or near

the nest. When these males were put apart each in a new tank where they
were allowed to build a new nest alone, they naturally never showed threat
behaviour and no such holes were formed.
These observations show, not only that the threatening movenmentsmust
be interpreted as displacement digging instead of as displacement feeding,
but also that KORTLANDT'S and TINBERGEN's
general conclusion that a

'Vm'

41

,~

..

Fig. 3. Territoriesof two neighbouringmales in "crowded"tank, with holes due to

displacementdigging.Brokenlines: boundarieswherethe ownersare threatening;the
ground between them is no man's land. Crosses indicate Elodea and Batrachium
vegetation.N: nest belongingto inale 2.
displacement reaction is never as complete as its autochthonous example,
aoes not hold good absolutely. When the obstructed urge is exceptionally
strong, the resulting displacement reaction may become complete and
practically identical with its example. The only difference is that the displacement reaction, in this case, is performed in a very "nervous" (hasty or
jerky, intensive and emphasising) way.
In other cases too it has been observed that a displacement reaction may
become as complete as the autochthonous movement. For instance, a lapwing disturbed at its nest will show displacement feeding. Sometimes this
displacement feeding develops into actual catching and swallowing a worm
(VAN SIJN in litt.).

DISPLACEMENT

Obstruction

of

the

mating

61

REACTIONS

drive

When a male has finished its nest, it is ready to mate. It now responds
to any pregnant female arriving in the territory by a series of sideward
"'leaps", each ending"in a flash-like dart in the direction of the female
and a subsequent sudden "dead stop".
This whole ceremony, the "zig-zag dance",
serves to stimulate the female to approach chasn
.5
-,
the male, thereby in her turn inducing him
to lead her towards the nest. When the
female does not follow at once, the male
is unable to lead her, because his leading
i. absolutely dependent on her following
fo00
beha-viour, which acts as a signal. His
mating drive is then discharged in three
different displacement reactions, belong- z!q2ag
ing to the nestbuilding and parental activities: he goes to the nest, pushes his
snout into the roof ("pushing"), makes c4g/bfg
the peculiar ventilating movements, which
normally aerate the eggs ("fanning") and
in addition glues his kidney secretion to pu5h/ng
the nest ("gluing"), an activity normally
serving to stick the algae and other plants
together which are used in the construction
of the nest. Fig. 4 shows the sudden
change in activity provoked by the arrival
*zr~~~nftyg
of a female. Testing of nest material and
zl,
N
digging stop abruptly and zig-zag dance,
pushing, fanning and gluing are per- Fig. 4. Frequency of six activities
of a male in sexual condition
formed instead.
during 30 minutes before and 30
Thus there is a definite connection be- minutes after arrival of a female.
tween digging and the fighting drive on
the one hand, whereas pushing, fanning and gluing are outlets for the
obstructed mating drive.
Comparison
ment fanning

of displacement

digging

and

dissplace-

In several respects the displacement digging differs from its example,

autochthonous digging. A threatening male always takes care to turn its

62

N. TINBERGEN

AND J. J. A. VAN IERSEL

broad lateral side towards the opponent, thus displaying the red parts.
These, as experiment- have shown, act as an intimidating signal. Further,
the ventral spines, or more often one of them, viz., that on the side turned
towards the enemy, is erected. The ventral spines are actually used as
weapons in one of the types of fighting. Lastly, the movement is "emphasised" by brisk shaking motions of the whole body as if the fish made
an attempt to thrust its snout deep into the bottom, yet at the same time
stops; something like "digging on the spot".
These three components have the effect of rendering the displacement
digging more conspicuous, adding colour, movement and the display of an
actual weapon to it. In other words, the activity is ritualised, it is adapted
to its function as a signal. As mentioned above, its releasive function has
actually been proved by experiment.
With displacement fanning the case is different. Only by careful observation one can observe a slight difference between authochthonous fanning
and displacement fanning. We get the impression that in the latter case
the frequency of the rhythmical movements of tail and pectorals is slightly
higher than in autochthonous fanning. This seems to be dependent on the
strength of the mating urge; the stronger the latter is, the faster the fanning
movements seem to be. When fartning is performed as an autochthonous
movement, the strength of the urge definitely increases the frequency, hence
our cautious formulation of the difference between the two types of fanning.
Displacement pushing and displacement gluing cannot be told from their
autochthonous examples at all, as far as our experience goes.
Now, in spite of all attempts, we never found any evidence pointing to
a signal function of these displacement reactions; it does not seem to makethe slightest difference to a female whether the male shows displacementpushing, fanning or gluing, or omits them. 'rhe gluing does have a stimula-ting influence on the male himself, for a male that is not quite ready to
lead a willing female nearly always leads her quite readily immediatelyafter gluing; but we never had any indication of an influence on the female.
These observations, therefore, are striking proof of the correlation be-tween ritualisation and signal function. Displacement reactions with signal
function are ritualised, those without signal function are not.
We are of opinion that this correlation is not accidental and that there
can be little doubt that ritualisation is the outcome of adaptation of the
displacement reaction to its secondary function, viz. that of a signal or
releaser.

DISPLACEMENT

REACTIO-NS

63

LITERATURE
ARMSTRONG,E. A. (I942). Bird display. - Cambridge, Camb. Univ. Press, xvi +
38I p.
CARPENTER,
C. R. (i934). A field study of the behavior and social relations of howling
monkeys. - Comp. psychol. Monogr. X, 2, P. i-i68.
HuxLEY, J. S. (I9I4). The courtship habits of the great crested grebe (Podiceps-

cristatus) with an addition to the theory of sexual selection. -

Proc. zool. Soc..

Lond. XXXV, p. 253,29I.

KIRKMAN,F. B. (I937). Bird behaviour. - London & Edinburg, T. Nelson, xv +
232 P.
KORTLANDT,
A. (ig4o). Wechselwirkung zwischen Instinkten. - Arch. neerl. Zool. IV,
P. 442-520.
MAKKINK,G. F. (i936). An attempt at an ethogram of the European avocet (Recurvirostra avocetta L.) with ethological and psychological remarks. - Ardea XXV,
p. I-6o.
RAND, A. L. (I943). Some irrelevant behavior in birds. - The Auk XL, p. I68-I7I.
TINBERGEN,N. (i93g9).On the analysis of social organization among vertebrates, with
special reference to birds. - Amer. Midl. Nat. XXI, p. 2IO-234.
- Z. Tierpsychol. IV, p. I-40.
, (ig4o). Die tbersprungbewegung.