Anim . Eehav .
, 1967, 8, 574-585
CHANGES IN THE BEHAVIOUR OF LEBISTES RETICULATUS UPON A
REPEATED SHADOW STIMULUS
BY ELEANOR M . RUSSELL
Department of Zoology, Cambridge University*
Some observations (Lorenz, 1939 ; Nice & ter
Pelkwyk, 1941 ; Schleidt, 1961) demonstrate the
great resistance to extinction of the innate re-
sponse to a predator pattern . Other work (Hinde,
1954, 1960 ; Andrew, 1961 ; Melzack et al., 1959)
gives evidence of habituation to predators, to a
degree which can only appear to be harmful .
Schleidt (1961) found that when moving pre-
dator-models are shown to turkeys, the models
which were rarely shown caused more and
stronger reactions than those presented more
frequently. He suggests that too frequent or too
lengthy presentations of a model can cause rapid
waning of a response . On the other hand, Hinde
(1960) demonstrated that a significant response
decrement remains 24 hr after a 2-min initial
presentation . He found that the inter-relations
between response characteristics were different
on second presentations after a long rest inter-
val from those found for initial responses .
Eikmans (1955) has observed that the decre-
ment which takes place in the prey-seizing be-
haviour of Bufo occurs at different rates for
different measures of the response . These results
and the demonstration that the interaction of
long-term incremental and decremental effects
produce waning of the owl-mobbing response of
the chaffinch (Fringilla coelebs) have led Hinde
(1954, 1960) to suggest that habituation, although
a useful term, should not be taken to imply a
unitary process .
The present study deals with the changes
in behaviour to a novel stimulus of the small
tropical cyprinodont Lebistes reticulatus . Fear
responses involving fleeing and freezing have
been described in several teleost fishes (Hoar,
1958 ; Morris, 1958 ; Russell, 1931 ; Brawn,
1961 ; Barlow, 1962) . A recent study (Rodgers
et al., 1963) of response decrement in the gold-
fish (Carassius sp .) took little account of the
normal behaviour of the fish, or of its fear
responses, and found no incremental effects .
Fear responses involving • fleeing and freezing
have been observed in Lebistes reticulatus, and
present an excellent opportunity for a detailed
*Present address : Department of Zoology, University of
New South Wales, Kensington, Sydney, Australia 2033 .
574
study of the course of response changes, and of
changes in the relationship between the fleeing
and freezing components of the response .
Method
Lebistes reticulatus (Peters) was obtained from
a mixed stock maintained by the Department of
Zoology, Cambridge . They were kept at 25 ° C
in large earthenware tanks surrounded on all
sides by a wall extending to 60 cm above the
top of the tanks, to eliminate passing shadows .
Constant light was maintained by a 15 W .
tungsten filament lamp suspended 50 cm above
the water surface .
Apparatus
Figure 1 shows the experimental arrange-
ment and the apparatus used to produce a
shadow moving over a fish in a 10 x 10 x 25
CM 3 Perspex dish . To prevent a drop in temper-
ature during experiments, the dishes were placed
on a rack above a water bath at 25 ° C . All this
was covered by a 65 x 80 x 100 cm3 enclosure
with wooden frame and roof, and black cloth
sides . The enclosures was divided into two
compartments, each of which had a peephole
of one-way cellophane in the front wall . A third
compartment in which the observer sat extended
from the front wall .
The shadow was produced by the piece of
card attached to an L-shaped metal rod (A),
rotating under the lamp in the roof of the en-
closure . This rod passed through the roof of the
enclosure, and connected at right angles via 1 :1
bevel gears to the shaft (B), which was turned by
a belt driven by an electric motor at 60 r .p .m.
The belt from the motor passed round a pulley
on the shaft which rotated only when the cog
wheel fixed on the shaft was engaged with that
fixed onto the rear surface of the pulley . This
simple clutch (C) mechanism was manually
operated .
The card attached to the rod (A) was tri-
angular, of base 7 .5 cm and height 15 cm . A
hardboard screen just below the card, with a
7 . 5 x 7 .5 CM 2 hole directly below a lamp,
 RUSSELL : LEBISTES RETICULATUS AND REPEATED SHADOW STIMULUS 575

LAMP 6 A
PULLEY TO
MOTOR

W N
O W
U bD
n n n
K 3 3

DISH

V V V

- --------------------------------

. 1 . Apparatus for producing a shadow moving over a fish in a dish .

A, L-shaped rod bearing a card which produces a shadow . B, shaft con-
nected to rod A at right angles by bevel gears and driven by an electric
motor . C, clutch mechanism .
576 ANIMAL BEHAVIOUR, 15, 4
limited the space lit. A line on this screen in-
dicated the starting point for one revolution of
the rod .
All parts of the apparatus were mounted on
rubber to reduce vibration. When the L-shaped
rod was replaced by a straight rod so that no
shadow should be cast, no change in behaviour
of fish was seen during operation of the motor .
From Walls' (1942) account of the working
of the teleost eye, it is clear that images of the
card moving across the lamp at 48 cm per sec
and the shadow moving across the dish at 190
cm per sec (calculated for the mid-point of the
leading edge) must fall on the retina . The time
for the passage of the shadow is 0 .29 sec . The
velocity of the shadow and of the card is of the
order of values quoted for the swimming of
fish of a size to prey on Lebistes (Bainbridge,
1960) . The fastest swimming speed measured for
Lebistes (roughly, against a squared back-
ground) was 4 cm per sec .
Procedure
Fish were transferred to `observation' dishes,
with water and sand but no weed, 48 hr before
an experiment . The dishes were placed in the
shadow apparatus on the evening before an
experiment.
The behaviour of the fish was observed for
10 -min before the first stimulus was given . A
series of forty stimuli were given at fixed in-
tervals . In some cases an interval for recovery
was allowed, and a second and third series of
stimuli given . Immediately after the end of the
second series, ten stimuli were given for which
the shadow mechanism was operated by hand
at a lower velocity.
Table I shows the intervals allowed between
stimuli and between series ; the number of fish
to which each treatment was given and the
response measures were recorded .
Recording and Analysis
The Perspex dishes were marked with a 5 cm
grid from which distances moved were estimated.
The initial response of Lebistes to a moving
shadow was some kind of movement, generally
one or more tail-beats . This response was called
a jerk response . When the first response was
given the following details were recorded
(1) Type of initial response .
(2) Distance travelled during jerk response
(called distance of jerk response) and of swim-
ming subsequent to jerk response
(3) Number of tail-beats in one jerk response .
Table I. Summary of Stimulus Presentations
Time between Time between No . of
stimuli series 1 & 2 fish
2 min 15 min 6
30 min 6
2 hr 4
24 hr 5
48 hr 7
4 min 10
15 sec 10
2 min 15 min 12
(altered
stim .) 30 min 12
A stop clock was started at the beginning of
the experiment . When the fish began to move or
stopped moving, the time from the start of the
experiment was recorded . The distance moved
and other behaviour (e .g. feeding and various
fin movements) were also recorded .
From these records, three main response
measures were calculated :
(1) Distance of the jerk response (J 1 , J2, etc.)
(2) Time spent immobile between two success-
ive stimuli (T1, T2, etc .)
(3) Swimming speed (Sw l, Sw2, etc .) calcu-
lated from the distance swum in the time spent
moving between two successive stimuli .
To test the significance of changes in these
measures, the Wilcoxon Matched Pairs, Signed
Ranks test (Siegel, 1956) was used with the
`before and after' results for individual fish.
Correlations between measures were calculated
by the Spearman Rank Correlation r, . Values of
Student's t associated with values of r, were
calculated, and used to find the probability that
rs so calculated is not significantly different
from zero. Two-tailed tests of significance were
used throughout .
Results
Response of Lebistes to a Moving Shadow
When Lebistes is disturbed, its response is
clearly divisible into two parts : initiation of
movement, and cessation of movement . When a
fish is frightened by a shadow, it makes a rapid,
disorganized dash about its living area, gener-
ally towards the bottom or a corner, and there it
freezes for a time. This occurs for the first or
 RUSSELL : LEBISTES RETIC'ULATUS AND REPEATED SHADOW STIMULUS 5 77

first few stimuli of any type, but later, variations
of the response appear . Four types of move-
ment response were recognized .
(1) Jerk response-a rapid dash about the
dish involving several tail-beats, and movement
farther than 5 cm .
(2) Single jerk-a single beat of the tail, which
moves the fish less than 5 cm .
(3) Drifting-the fish does not beat its tail,
although the caudal fin is bent as it is pre-
paratory to swimming . The fish moves a very
small distance up or down, backwards or
forwards .
(4) Fin and tail movements-no change of
position at all, but fin and tail movements occur
-generally flickering, or an increase in the rate
of flickering .
(1), (2) and (3) occur when the fish is moving or
stationary . (4) occurs only when the fish is
stationary .
Each of these four responses is followed by a
period of `freezing' or suppression of movement,
e .g . if the stimulus is followed only by an in-
crease in the rate of flickering of the fins, there
follows a period when the fins are not moved
at all .
It is possible for a moving fish to freeze,
with no preceding movement response, and for a
stationary fish to show no other response than
to remain still .
Changes in the Type of Response During a
Stimulus Series
As a shadow stimulus was repeated, there
was a change in the type of response which
occurred, shown in Table II and Fig . 2 . The
series of forty stimuli, 2 min apart, is divided
into four groups of ten . Figure 2 shows the
decrease in the number of jerk responses and the
increase in the ratio of non jerk to jerk responses .
There is a significant increase in the ratio non-
jerk/jerk, from 0 . 23 to 0 . 53, from the first ten
to the fourth ten stimuli (X 2 =25 . 5, P<0 . 001) .
Table It shows a decline in jerk responses of I
(i .e . 5 cm) or greater, which are replaced by
lesser responses . The changes in single jerk, and
drifting are not significant, but the increase in
fin and tail movements is significant .
Changes in the Jerk Response
The decline from the number of jerk responses
given to stimuli 1 to 5 to the number given to
stimuli 35 to 40 is significant (z=2 . 68, P<0 . 01) .
There is a significant decrease in the mean num-
ber of tail-beats per jerk (z>4 . 00, P<0 . 0001)
over forty trials . Figure 3 shows the change in
mean distance of jerk, when the results for forty-
three fish are added together . Table III shows the
significance of changes in distance of jerk, based
on changes in response for individual fish .
Changes in `Freezing' Responses
Figure 4 shows the mean time still (T) in the
2 min between stimuli . Table IV gives the sig-
nificance of changes in T . The difference be-
tween T 1 and T 40 is not significant, but there is a
significant decrease from T 1 _ 5 to T 3 5-40 .
Changes in Swimming Speed
Figure 5 shows the mean swimming speed
during the time swimming in 2 min between

Table II. The Succession of Types of Response to a Shadow. A Series of Forty Stimuli, Divided
into Four Groups of Ten. P Represents the Probability that the Change from the First to the
Fourth Stimulus Group Is Significant . N=forty-three fish

Type of response
Stimulus No moves fin drifting single jerk jerk jerk
group response and tail jerk .. 5 cm 10 cm > 10 cm
1-10 1 26 54 79 104 106 70
11-20 3 56 64 85 127 74 20
21-30 5 69 60 90 121 59 22
31-40 6 79 52 97 82 60 15
Total 15 240 230 342 454 299 127
P - <0 . 001 >0 . 05 >0 .05 <0 .01 <0 .001 <0 . 001
578 ANIMAL BEHAVIOUR, 15, 4

400 -8

Jerk

300 -6

0
d
200 -4
0

E
Z

100 -2

0
10 20 30 40
Number of trials (groups of 10)

Fig . 2. Changes in the type of response from first ten trials to last ten trials .
Number of jerk and non jerk responses are shown, and the increase in the
proportion of non jerk to jerk responses (1687 observations on forty-three
fish) .

14

12

10
EU
Y
d
0
d
C 6
0
U7

0 4

2
N=43
r
10 20 30 40
Trial

Fig. 3 . Change in distance of jerk response per fish in the course of forty
shadow presentations (N=43) .
RUSSELL : LEBISTES RETICULATUS AND REPEATED SHADOW STIMULUS 579

Table III . Changes in Distance of Jerk Response During Forty

Shadow Stimuli . Probability Calculated by Wilcoxon Test from
Changes for Individual Fish . N=Forty-three Fish

Changes and direction

of change z Probability
J 1 /J 2 < 1 .4 ns

Jt/J5 (-) >4 .00 <0 .001

Jt/J4o (-) >4 .00 <0 .001

Sum JI_5/SumJ35-4o( -) >4 . 00 <0 . 001

Table IV . Changes in `Freezing' (Time Still) Response During Forty

Shadow Stimuli . Probability Calculated from Wilcoxon Test from
Changes for Individual Fish

Change and direction z Probability

of change

To/TI (+) >4 . 00 <0 .001

TI/T2 (+) 1 . 76 <0 . 05

TI/T5 (+) 1 . 76 <0 .05

Ti/Tao (-) 1 . 13 n .s .
Sum T1_ 5/Sum T35-4o (-) 3 . 81 <0 . 001
To/T40 (+) 2 .09 <0 . 05

60

6
N'
40

20

0 10 20 30 40
Trial

Fig . 4 . Changes in `freezing' in the course of forty shadow stimuli, meas-

ured by the change in time still in the 2 min between shadows. N=43 . X is
level of time still in 2 min before the first stimulus .
580 ANIMAL BEHAVIOUR, 15, 4

stimuli . Table V gives the significance of changes
in swimming speed .
Relation Between Measures
Table VI shows values of correlation co-
efficients and of P for all relationships described
in this section.
There is some correlation of T o with T 1 :
less active fish freeze for longer .
As one would expect, the distance of J is
strongly correlated with the number of single
tail-flips in one J response .
It is not possible to predict values for J from
any measure of behaviour taken before trial 1 .
There is no significant correlation between J 1
and T 0 or Sw 0 .
There is no correlation between any measures
of J and Sw but swimming speed and time still
for any trial are generally negatively correlated
since time moving in 2 min is used in calculating
swimming speed and time moving plus time
still is constant .
Recovery
The degree of recovery of the jerk response
in the time allowed after the first series of 40
stimuli was measured by the ratio
Sum J 1_ 10, series 1
series 2, expressed as a percentage,
Sum J - 10,
and the difference from 100 per cent tested by a
t-test . Table VII shows percentage recovery of
the J response after various intervals. There is a

Table V. Changes in Swimming Speed in the 2 Min After a Shadow

Stimuli in the Course of Forty Stimuli . Probability Calculated by
Wilcoxon Test from Changes for Individual Fish. N=43

Change and direction

of change z Probability
Swo/Swi (-) 1 .98 <0 . 05

Swl/Sw2 (-) 2 . 52 <0 . 01

SW t/Sw15 (-) 2 .77 <0 . 01

Sum SW1-5/sum SW35-40 1 .6 n .s.

1 .2

v
a)
a
3 06
0
0

N=43

' - 0--- 10 20 30 40
Trial
Fig . 5. Changes in swimming speed in the course of forty shadow presenta-
tions, calculated for each fish from the distance moved in the time spent
moving. N=43. X is the level of swimming speed in the 2 min before the
first stimulus.
 RUSSELL : LEBISTES RETICULATUS AND REPEATED SHADOW STIMULUS 581

Table VI . Values of ro and Associated Probabilities (t test) for

Relations Between Measures . Abbreviations as Above

Probability
Correlation between ra (2-tailed)

Sum J1_5 and Sum J 36-40 +0 . 19 ns

Sum J3-7 Sum J36-40 +0 . 47 <0 . 01

No . tail flips Dist. J 1 +0 .90 <0 . 001

J1 To +0 . 17 ns

J1 T1 +0 .29 ns

J1-2 T1-2 +023 ns

J1 T1-To +0 .29 ns

J3-7 T3-7 +0 . 30 <0 . 05

J30-40 T30-40 +0-12 ns

J1 Dist . Sw o -0 .22 ns

J1 Swo -0 . 23 ns
J1 Dist . Sw 1 -0 . 22 ns
SumJi_5 Swo -0 . 07 Us

TO T1 +0 . 51 <0 .001
T1 Swl -0 . 70 <0 .001
To Swo -0 . 59 <0 .001

rapid increase to around 60 per cent of the initial
level, and then a slow increase to the initial
level .
Changes in time spent still follow a similar
pattern of recovery . After 24 hr, time spent still
remains significantly below its initial value
(Wilcoxon, T=O, P= 0 . 01), and after 48 hr,
time spent still is not significantly different
from its initial value (Wilcoxon, T=3,) .
Response to an Altered Stimulus
Experiments were done with twelve fish, in
which the characteristics of the stimulus were
altered during a series of stimuli immediately
after the second series of thirty standard stimuli
had been completed .
The velocity of the shadow decreased to
about half its original value, i .e . to about 95
cm/sec, and the time for the shadow to pass over
the dish increased from 0 . 29 to about 0 . 58 sec .
The velocity of the second stimulus shadow could
not be held exactly constant . Table VIII shows
the results of observations on twelve fish .
The change in stimulus results in a significant
increase in the jerk response measured by J 1_ 5
for series 3, over the response at the end of
series 2 (Wilcoxon test, T=5, P<0 .01) . The
response to the changed stimulus is still sig-
nificantly different from the response to J1-5
of series 1 .
Differences in Response to Stimuli at Intervals of
15 Sec, 2 Min and 4 Min
Table IX summarizes the direction and sig-
nificance of changes in response calculated from
changes in response of individual fish . These . are
comparable with results in Table III and IV
from the main experiment for a 2 min interval .
Table X gives the significance .of differences _in
the measures of rate of change of jerk response
and time still . The overall rate of change is
J30-40
measured by These simple measures are
J1-10
preferred to the calculation of regression lines
for ten very variable individuals .
582 ANIMAL BEHAVIOUR, 15, 4

Table VII . Percentage Recovery of Jerk Response during Various Intervals with No Stimulus ;
Difference from 100 per cent Tested by `t' test

Time since Percentage recovery :

end of previous Sum J 1_ 10 Series 1 N t P
stimulus series x 100
(hr) Sum J1_ 10 Series 2
0 . 25 0 . 52 5 5 . 64 <0 .01
0 . 50 0 . 46 6 4 .26 <0 .01
2 . 00 0 . 67 8 3 . 88 <0 .02
24 . 00 0 . 68 12 2 .46 >0 .05
48 . 00 0 . 91 8 1 .06 >0 .05

Table VIII. Response to an Altered Stimulus

Change and direction of change T P

(Wilcoxon test)

J1_ 5 Series I/J1.-5 Series 2 (-) 3 <0 .01

J1_ 5 Series 2/J26-30 Ser. 2 (-) 12 ns

J26-30 Series 3/J1_5 Series I (-~-) 5 <0 . 01

J 1_ 5 Series 3/J 1_ 5 Series I (-I-) 5 <0 . 05

The stimulus was changed before the third series of stimuli . (N=12)

From Tables IX and X it is clear that there is
little difference in the effects on jerk response
and time spent still of stimulus intervals of 2 and
4 min . The only real difference is that for a 4 min
interval, the differences between J 1 and J 5 ,
and T 1 and T 5 are not significant, whereas for a
2-min interval, J decreases and T increases . The
increase from T 1 is significant for both 2- and
4-min intervals .
The jerk response decreases further and more
rapidly with stimuli at 15-sec intervals . The
pattern of changes in time still is quite different .
With a 2-min stimulus interval, time still in-
creases and then decreases, to be not significantly
different from its initial value after forty trials .
The time still after stimuli 15 sec apart shows a
significant increase after forty stimuli and de-
creases after this to be not significantly different
from T 1 after a hundred stimuli .
Discussion
It was obvious that when stimuli were given
very close together (e .g . at 15-sec intervals) the
jerk response waned far more rapidly than when
the stimuli were 2 min apart . This tends to re-
inforce the view that it is the relative frequency
with which animals encounter possible predators
which determines their responses to them
(Schleidt, 1961 ; Verheiken, quoted by Thorpe,
1963) .
There is little earlier work on fish on the
waning of a response to a repeated stimulus, but
scattered observations in the literature (e .g .
Breder & Halpern, 1946 ; Keenleyside, 1955 ;
Barlow, 1962 ; Rodgers, Melzack & Segal, 1963)
suggest that responses similar to the jerk
response tend to wane . The significance of changes
in `freezing' and swimming speed have not
previously been noted . The only other detailed
study of response decrement in fish (Rodgers et
al., 1963) involved only the 'tail-flip' responses
of goldfish (probably Carassius) and some orien-
tation responses . It is not clear how this reflex
tail-flip response is related to ordinary swim-
ming or to the complex avoidance responses
shown by Carassius, Lebistes and many other
fish . There is no doubt that a decrement does
occur in the rapid escape response of both
Carassius and Lebistes . This escape response
does not by itself give a clear picture of the be-
haviour changes . In Lebistes, the jerk response
could be produced by a variety of disturbing
 RUSSELL : LEBISTES RETICULATUS AND REPEATED SHADOW STIMULUS 583

Table IX . Significance of Changes in Response to Stimuli it is not possible to say for Lebistes, as do Rodgers
at 14 Sec and 4 Min Intervals et al. for Carassius, that there was `no observable
response', because of the still persisting changes
Stimulus Direction which occur in the `freezing' responses and in
interval Response of change P
swimming speed .
15 sec J102 (-) <0 .01 In view of the fear responses of Lebistes
and other fish (Russell, 1931 ; Hoar, 1958 ;
J1/Js (-) <0 . 05 Morris, 1958 ; Brawn, 1961 ; Barlow, 1962 ;
(-) <0 . 01 Miller, 1963), direct comparison by Rodgers
Ji/J40
et al . of the 'tail-flip' response of the goldfish
Ji-036-40 (-) <0 . 01 with the mobbing of owls by chaffinches or the
fear responses of Mallards to predator models
To/Ti (+) <0 .01
(Melzack et al ., 1958) seems too simple . The fear
T1/T5 ns responses described for Lebistes can perhaps be
compared with the fear responses of Mallards
Ti/T40 (+) <0 . 01 described by Melzack et al. (1958), in that in
ns both cases, fleeing and freezing occur . Melzack
Ti/Tioo
et al. lump these together as `fear responses'
4 min J1/J2 ns and do not differentiate changes in each type of
fear response, although Melzack (1958) notes
Ji/Js (-) ns
the continuance of orientating responses after
J1/J40 (-) <0 .05 the disappearance of overt fear responses . In
Lebistes, similar orientating responses continue
Jl-5036-40 (-) <0 .05 after the disappearance of an actual jerk re-
To/Ti (+) <0 . 01 sponse .
Waning of the response certainly occurs .
Ti/Ts (+) ns After a series of forty stimuli, the jerk response
ns has recovered to two-thirds of its initial level
TI-5/T36-40 (-)
after 2 hr, and has recovered fully after 48 hr ;
P calculated from Wilcoxon test (2-tailed) recovery f t e ree ng response so s n t
complete until 48 hr after the initial series .
Complete disappearance of the response is not
Table X. Significance of Difference in Rate of Change of J caused by the series of forty stimuli, and it is
and T for Stimulus Intervals of 15 see,, 2 min and 4 min
(Wilcoxon Matched Pairs, Signed Ranks Test) therefore not possible to make direct com-
parisons of these experiments with, for example,
Stimulus Rate of those of Hinde (1954, 1960) or Rodgers et al.
interval change P (1963) . But it is clear that at least two different
0 .07 <0 .0001 rates of change are involved .
15 sec J30-a0
In Lebistes, it has been shown that freezing
Ji-io follows fleeing, and that the changes in fleeing
and freezing do not occur together . In spite of
2 min 0 .66 ns
this, the two different responses need not be
4 min 0 . 68 completely independent of each other . As
Wiepkema (1962) has pointed out, the incom-
15 sec T30-40 1 .90 patibility of two motor patterns does not mean
<0 0001
the incompatability of corresponding major (i .e .
Ti-10 causal) tendencies . There is no reason why
2 min 0 . 94 ns fleeing and freezing should not both be con-
sidered as manifestation of fear . Eikmans (1955)
4 min 0 . 83
has observed that the changes which occur in
the prey-seizing behaviour of Bufo occur at
stimuli . It was gradually replaced by the 'orien- different rates for different measures of the re-
tation' and alert responses described by Rodgers sponse . Hinde (1960) says that the inter-relation-
et al. (1963) . Although both jerk responses and ships between the response characteristics were
orientation responses disappeared on occasion, different on second presentation after a long rest
584 ANIMAL BEHAVIOUR, 15, 4
interval from those found for initial responses .
In Lebistes, more than one response is involved,
but the two measures of inhibition of move-
ment (time still and swimming speed) do change
at different rates .
Sokolov (1960) has suggested that the waning
of the orientating reflex (orienting reaction) is
due to the `elaboration of an inhibitory con-
ditioned reflex regulating the transmission of
impulses to the reticular formation' . The orien-
tation reaction is normally evoked when the
properties of the stimulus do not correspond with
a `neuronal model' set up in the brain by pre-
vious repeated stimulation . Drever (1964) has
suggested that Sokolov's explanation of the
habituation of the orientation reaction applies
to all habituation . Experiments such as these
with Lebistes, which show differential changes in
response measures, make less acceptable an
explanation of habituation in terms of a block of
impulses to the reticular formation .
Andrew (1961) ascribes the waning of mobbing
of owls by the blackbird Turdus merula to
changes in the perceptual organization involved
in mobbing such that the effect of the owl de-
creases . The changes in perceptual organization
must be concerned with the recognition of
frightening objects and with the control of fear
responses . The different changes in parts of the
fear responses of Lebistes suggest an effect on
the motivational control of fear responses . The
comparison between the response of Lebistes to
stimuli at 15-sec and 2-min intervals is of
interest here . The jerk response decreases more
rapidly with more frequent stimuli, but the
changes in time still have a similar course for
both intervals . Freezing is a common mani-
festation of fear, and it seems that although the
jerk response wanes quickly, the level of fear
remains high ; perhaps the response is under
hormonal control .
One may consider that for the first few stimuli
of a series, or during the initial phases of a long
presentation, the stimulus is strange, undiffer-
entiated from the surroundings, and because it is
strange, it is frightening (Hebb, 1946) . For some
time the state of fear may render the animal
incapable of beginning to differentiate and
classify the stimulus, and the effects of arousal
may serve to increase this fear response . As the
stimulus is repeated or protracted and nothing
occurs to harm the animal, it can begin to differ-
entiate and recognize the stimulus, the state of
fear diminishes, and the response wanes . Where
only deeremental changes occur, if this is ever
really so, the initial response may be far less
intense, and therefore interfere less with the
learning process . The `learning process' may be
considered either as the discrimination of stimuli,
or as the incorporation of the repeated stimulus
into the animal's perceptual framework .
To determine the validity of this way of con-
sidering response waning, it will be necessary
to show not only that an animal with perceptual
experience of a stimulus is better able to dis-
criminate between that stimulus and another
than between two unfamiliar stimuli (Gibson
et al ., 1958), but also that perceptual experience
of a stimulus is followed by more rapid re-
sponse waning. This may prove difficult to test .
Even the suggestion that an animal shows
fear responses to something strange implies the
presence of `perceptual knowledge', and the
disappearance of such fear responses - with
repeated stimulations shows that some changes
in this perceptual knowledge must occur .
The interval between stimuli in these experi-
ments was probably too small to resemble natur-
al conditions . One of the major criticisms made
by Schleidt (1961) of many of the experiments
which show habituation to predators is that
`predator stimuli' are presented too close to-
gether-he suggests that habituation does not
occur to a predator at its natural frequency of
occurrence . The emphasis in these experiments
has been not on response to predators, but on
the decrement of a response, and a `predator'
stimulus was the most convenient . The results
certainly cannot be taken as showing that
habituation to predators does occur . It could
occur if the predator appeared very frequently
and caused no harm to the animal . In other
animals it can certainly be produced experi-
mentally under conditions which suggest that it
could occur naturally (Hinde, 1954, 1960) .
Why this should be so remains a problem .
Summary
1 . A shadow was passed repeatedly across
dishes containing the small fish Lebistes reticu-
latus .
2 . The fear responses shown by Lebistes to
disturbing stimuli are described ; fleeing was
followed by freezing .
3 . With frequent repetition of the shadow (at
2-min intervals), the intense multiple tail-beat
of the early responses (`jerk response') gave way
to less intense responses, and then to orientation
responses (fin movements) . Freezing persisted
for longer,
 RUSSELL : LEBISTES RETICULATUS AND REPEATED SHADOW STIMULUS
4 . There was a significant decrease in number
and intensity of jerk responses during forty
stimuli .
5 . `Freezing', measured by the time a fish
spent in moving, is a real phenomenon . The
time `frozen' increased and then decreased,
and after forty stimuli had returned to the level
of the first presentation .
6 . The response declined during forty stimuli
to about two-thirds of its initial level, and had
recovered to about 60 per cent after 2 hr .
After 48 hr, the recovery was practically com-
plete .
7 . A change in the stimulus resulted in an
increase in response .
8 . The jerk response decreased further and
more rapidly with more frequent stimuli . The
time course of the freezing response was relative-
ly independent of stimulus frequency, although
the response was more intense at higher stimulus
frequencies .
Acknowledgements
The author is grateful to the late Professor
C . F . A . Pantin for permission to work at the
Department of Zoology, Cambridge ; to the
University of Queensland for the University of
Queensland Research Scholarship which made
this work possible ; to Drs R . Bainbridge and
C . C . Hemmings and Professor R. A . Hinde for
much helpful discussion in the course of this
work, and to Dr R . H . J . Brown for advice
on the construction of apparatus .
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