An analysis of locomotor behaviour of goldfish (Carassius auratus)

Anim. Behav.,1970,18 317-330

AN ANALYSIS OF LOCOMOTOR BEHAVIOUR OF GOLDFISH

( CARASSIUS AURA TUS ) By H. KLEEREKOPER, A. M. TIMMS, G. F. WESTLAKE, F. B. DAVY, T. MALAR & V. M. ANDERSON Institute of Life Science, Texas A & M University, College Station, Texas 77843 The hydrodynamics and the mechanics of locomotion in fishes have received considerable and careful attention in the literature (Breder 1926; Harris, 1936, 1938; Gray 1957; Nursall 1958, 1962; Bainbridge 1958, 1960, 1961, 1962; Watts 1961; Walters 1962), but general locomotor behaviour has been little analysed on a quantitative basis. The available information refers almost exclusively to special aspects of locomotion as functions of environmental and physiological variables, such as response to currents (Lyon 1904, 1905, 1909; Steinmann 1914a, b; Davidson 1949), and swimming speeds under natural (Ellis 1966) and various laboratory conditions (Fry & Hart 1948; Brett, Hollands & Alderdice 1958; Blaxter & Dickson 1959; Bainbridge 1961 ; Brett, 1965). Studies of general locomotor activity per se, through an analysis of one or more of its parameters, were made by Schuett (1934), Breder (1926), Breder & Nigrelli (1938), Welker &Welker (1958), Russell (1967), Brawn (1961), Herter (1930, 1953), Escobar, Minahan & Shaw (1936), and recently by Kleerekoper (1967a, b) and Kapoor (1968). The above studies provided limited data on only some of the parameters required to describe quantitatively locomotor behaviour in all its aspects. Furthermore, no evaluations could be made in these studies of the restraining effects of the walls of the tanks and the bias introduced by them into the data, while, in the earlier work, the recording techniques did not allow for observations during extended periods, so that little attention could be given to the problems of variability, periodic or otherwise, of the data collected. With the development of the monitor and data processing system specifically designed for the analysis of locomotor behaviour in fish in the horizontal plane (Kleerekoper 1967a, b; Kleerekoper & Malar 1968; Kleerekoper et al. 1969), it became possible to record and compute all the required information in statistically reliable ways for extended periods. This paper presents an analysis of general locomotor activity in naive goldfish recorded by

that monitor system in environmental conditions controlled except for minor temperature fluctutions. Its main objective is quantitatively to describe the parameters of locomotion so as to provide realistic values for the construction of mathematical models of locomotion in an 'open field'. Such models will be used eventually in the assessment of the significance of environmental and physiological factors affecting the direction of locomotion, including orientation.

Methods Recording Techniques Monitoring of movements was done by the method described earlier (Kleerekoper 1967a; Kleerekoper et al. 1969). In the floor of a tank, 5.0 × 5.0 × 0.5 m deep, 1936 photoconductive cells are embedded, at 10-cm centres, in a square matrix. The photocells, their light sensitive faces turned upwards, are activated by light from a collimator which is suspended over the tank and covers the entire horizontal area of the tank uniformly. The colour temperature of the light source is about 2400°K (Fig. 1). The position in the matrix of a photocell whose resistance is increased as a result of the interception of the incident light by the presence of the fish is determined by means of a logic interface with a computer on line. This information, together with that on the time elapsed between successive photocell intercepts, forms the basis for the subsequent computations of all the parameters required for the quantitative description of locomotor behaviour. Velocities are calculated by dividing the distance between photocells intercepted by the time difference; turns are defined as changes in direction of progression indicated by three consecutive photocell intercepts. The resolution of the system is not less than 4 ° for fish of the length (30 cm) used in the experiments reported here. The data processing system is shown schematically in Fig. 2. The basic computations are carried out using the computer on line, the more time-consuming operations are done on an IBM 360 computer. The tank was supplied with tap water filtered 317

318

ANIMAL

BEHAVIOUR ~J

18,

2

--TT--CT--

Square matrix of lamps~

(J 1

/

Fresnel ]enses'~, "~- honeycomb collimator/

i

perforated baffle..~,

iI!

L [

i-

Eu

to

U a

--

500 cm I

B fl

2

L_~_,

. . . . . . .

L__

--

" N

computer

--

ij

uore matrix of photooeNsoo ~

IO ¢m centres

2

IV -"

Fig. 1. Cross-section of monitor tank, (1) Water inlet; (2) water outlet;

(3) standing pipe for water level regulation. From Kleerekoper et al. (1969). H temperature control] Motrix of 19.36 photocells I " ~ ' " ~ _ on I0 cm cenfres in botfom~d'--dTrectlonal controq of tank t i cof water flow ._.] " T ~ ....

~ie

interf, ce I

[on-line computer ~----['real time clockJ

interfoce ]~

] eventJ

aphic 1 ing ]

Fig. 2. Block diagram of data-processing system. through activated carbon. Water temperature was about 25°C with maximum fluctuations of about 1 °C. Flow of water across the tank was laminar at a velocity of 1.8 cm per min. To eliminate the possible effect on locomotor behaviour of 'conditioning' of the medium by the fish itself, the water was not recirculated. The monitor room as well as all aspects of the tank were painted flat black throughout and visual cues in the room which might have affected locomotor behaviour were largely eliminated. The height of the walls of the tank, combined with the proximity of the collimator suspended

above the water level, restricted the visual field of the fish mainly to the tank iself and its collimator ceiling. Subjects Nine goldfish, 30 cm total length, were used in these experiments. Three of the fish (nos. 3, 4 and 5) originated from a commercial pond in New Jersey, the remainder from Texas. All fish had been kept for several weeks in the laboratory in black, opaque holding tanks which measured 71 × 239 × 53 cm deep, each containing six to twelve fish in a group. Feeding was done daily with a dry, balanced diet; all

KLEEREKOPER ET AL.: LOCOMOTOR BEHAVIOUR OF GOLDFISH animals were sated at the start of the recordings. The water in these tanks was recirculated through activated carbon filters; its temperature fluctuated between 19 ° and 24°C. Each fish was used only once for the purpose of these recordings and had not been exposed to the monitor tank prior to recording.

..... ......

18 ¸

A. Turning Behaviour. I. The sizes of the angles of change in direction.

The general frequency distribution of the angles and the effects of sex and geographic origin are represented in Fig. 3(A) which is based on the combined data of seven of the fish with a total recording time of 150 hr comprising in excess of 89 000 events. Regardless of variations between individuals, and of those due to sex, origin, position in the tank, and other factors, the angles of highest frequency are always in the 0 ° to 10 ° class. To verify whether differences exist between animals of different origin, three Texas fish were compared with four New Jersey fish. The difference in angle distribution was highly significant with a greater variance in the distribution from the Texas fish. Within each of the populations, the sexes show differences in the distribution of the size of the angles. The variance is less for females. Both among females of different origin and among males of different origin the distributions are unlike but the male difference is greater. The effects of the walls on the distribution of angles were obtained by computing the angle values of turns made in reduced areas of the tank. It was thus possible to assess the effects of the walls on this distribution. In Fig. 3, angle distributions are graphed for: the whole area bounded by the walls (A), the same area less a peripheral band of 30 cm width (B), and the same less peripheral band of 70 cm width ((2), for the pooled data obtained from seven of the fish. The differences among the individual recordings are slight and not meaningful. All observa-

N =48,464 N=23,943 N =12,921

f--o.nI i 1

'

Results

The net, qualitative result of the observed 'open field' locomotor behaviour is reflected in locomotor patterns drawn by a computercontrolled plotter (Fig. 12). The characteristics of the patterns are determined by the turning behaviour of the animal: size, direction, frequency, sequence of angles of turns and the length of the steps which separate the turns. These parameters were analysed; the results are as follows:

A B C

319

I

i

15'

t i

CBA

I0" lu la ,/"

D. .E

f-.-1

/

r-Z3 t..j

i t.."

~'~.

i

o r--"g' I10 o

~.'~:~.1 left

Angles

~)o

righ!

i10 ~,

in I0 ° c l a s s e s

Fig. 3. Frequency distribution of angles in areas A, B and C; pooled data of seven fish (see text). tions demonstrate that the presence of the walls has a strong effect on the angle distribution (Fig. 3). However, the effect is already present at a distance of 30 cm away from any wall (B in Fig. 3) with the greatest effect at 40 cm distance. 2. Frequency of turning. The combined data of three fish average 2.2 turns per m distance travelled with little individual and temporal variation for the longest period recorded (11 hr). The effects of the walls on the frequency of turning are pronounced. In Fig. 4 the average number of turns per m distance travelled is entered. Between 30 and 70 cm away from the wails (band II) the fish increased their turning frequency. When a fish reached the extreme peripheral band of 30 cm (I) it sharply decreased turning in relation to distance travelled and thus moved predominantly in a straight pathway parallel to the walls. There was little variation in this behaviour among the individual fish in spite of the differences among them in the spatial

ANIMAL

320 0.9-1.9

BEHAVIOUR,

Mean angle in degrees

SD

N

3

+0'083

38"174

1737

4

--2'661

37.421

1864

5

+1,395

33'776

3859

2"562

15

+3.417

33'655

22894

15'341

17

+1.494

37.898

3793

2.427

18

+0.855

38"545

11605

2'392

Fish no.

30

40

crn

crn

2

Table II. Z Test for Handedness in Angle Distribution

I

(3)

18,

|

Z 0.091 --3'074

H0: g=0.0; //1: gO0.0. Critical value=l.96; a=0.05.

Positive angles represent turns to the left. Fig. 4. Range of ratios of average number of turns made

per m travelled in bands I and II, and in the remaining

central area of the tank (III). Number of fish in parentheses. Dimensions refer to the actual monitor area between baffles (see Fig. 1). distribution of the movements in the various areas of the tank (Table I). 3. 'Handedness'. Since the distribution of the angles of the turns was normal (Fig. 3) and the very large number of data are considered accurately to represent the population, the tendency to turn preferentially to the left or to the right ('handedness') can be assessed through the mean of the distribution. The results of the test for six goldfish are represented in Table II. At the 95 per cent confidence level four of the six fish are significantly left-handed and one is significantly right-handed. Hourly variation in handedness was analysed during a period of 11 hr in fish no. 18. With exception of the 8 hr, the hypothesis that the means are the same for consecutive hours cannot be rejected. Thus, with the exception mentioned, handedness did not change in the course of the 11-hr period in question. Table I. Spatial Distribution of Movements in the Tank

Fish no.

Total distance travelled(m)

Per cent of distance travelled in band I

II

III

15

7513"6

45

31

24

17

1192"5

37

35

28

18

3734"0

23

26

51

4. I n t e r d e p e n d e n c e o f c o n s e c u t i v e turns. The relationship of consecutive turns with respect to the alternation of direction was studied in three Texas fish. Table III shows the frequency with which consecutive turns maintain a same direction from one to five times in sequence, This relationship between turns was similar in the three animals and did not change in time. Table HI. Number of Turns in Same Direction as Per Cent of the Total Number of Turns

Size of group of turns in same direction

N=7970 fish no. 15

N=2968 fish no. 17

N=4972 fish no. 18

1

37.7

53'3

44.2

2

24.7

22.2

26"3

3

13.6

11.2

13"9

4

8.9

5"6

7"3

5

5.3

3.1

4'0

The dependence of the direction of any o n e turn on the immediately preceding one is tabulated in the contingency matrix of Table IV. The turns are separated by straight pathways or steps, the length of which is represented in the frequency distribution of Fig. 5, covering 1024 events. However, this distribution varies in time as is evident from the average values of the steps in consecutive 1-hr periods (Table V). The shortest steps tend to occur during the 1st hour of the recordings. The inverse relationship between the length of the steps and the frequency of turning is demonstrated in Fig. 6.

KLEEREKOPER ET AL.: LOCOMOTOR BEHAVIOUR OF GOLDFISH

321

Table IV. Dependence of the Direction of any Turn on the Direction of the Preceding Turn

Fish no.

No. of events

Per cent tr preceded by tr

15

18612

23.47

33.25

2•.64

295.825

17

3337

24.33

26.91

24.28

1.862

18

10379

25.85

27.98

23.08

60.535

28

1037

23.91

31.43

22.33

10.374

38

9097

24"18

28.36

23.73

21.856

Per cent t 1 preceded by tl

Per cent tr preceded by t~

Z2

tr = right turn, tl : left turn. trtl per cent = htr per cent; a = 0"01; Z 2 = 6.635. Table V. Average Lengths of Steps as a Function of Time

65-

Fish no. 15

50"

N=I,024

¢> u

¢~30'

.E ¢

la.

IO

o2o

50 Ioo Step (cm)

Fig. 5. Frequency distribution of length of straight pathways (steps); fish no. 18. 5. Angle compensation. A l l b u t one o f the g r o u p o f eight fish studied displayed the pheno m e n o n o f angle c o m p e n s a t i o n described b y K l e e r c k o p e r et al. (1969). Representative d a t a for one fish are entered in Fig. 7 in which all consecutive turns in one direction are g r o u p e d a n d the angles o f the individual turns in such a g r o u p cumulated. The heavy tracing represents direction to the left a n d the light tracing represents direction to the right. Variance analysis has shown that the p h e n o m e n o n is n o t due to a r a n d o m distribution o f the size, direction, a n d / o r sequence o f turns o r groups. F values for variance o f groups o f turns o f sizes f r o m 2 to 20 for four fish are plotted in Fig. 8. T h a t the

Consecutive No. of hours turns

Fish no. 18

Average No. of Average length of turns length of step between step between turns (cm) turns (cm)

1

1068

40.0

945

30.1

2

1305

55.8

873

36.8

3

1111

64-2

794

54.5

4

1023

60.5

735

58.2

5

1296

50.7

1065

42.0

6

1265

52'8

1107

37.9

7

1116

56'0

1165

39.4

8

1301

50'8

1204

31.4

9

1064

54'3

881

34.5

10

923

57"7

860

30"9

11

1123

55"0

738

33'3

12

969

76'7

13

1078

61"4

14

1011

57"4

15

1042

54"9

16

913

65"7

17

•004

53"6

distribution does n o t result f r o m interference by the walls o f the t a n k is shown in Fig. 9 in which the F values are entered for d a t a collected

322

ANIMAL

BEHAVIOUR,

18, -2

u~

~900q

-8oo~

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7°°1

,

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polhw~y

30-

?

4'0

,; Consecutive

5'0

events in thousands

Fig. 6. Relationshipbetweennumber of turns and averagelengthof straight pathway;fishno. 13. from areas A, B and C of the tank as defined in Fig. 3. B. Velocity In Fig. 10 the frequency distributions of the velocities recorded from four fish are plotted. Commonly observed maximum speeds in these distributions are consistently between 50 and 65 cm per s for all fish, or between 2-0 and 2-6 body lengths per sec. The average velocity of locomotion in the tank as a whole, computed for four fish, is presented in Table VI. However, these values are greatly different from bands I and II, and central zone III. By far the highest velocities are encountered in the central part of the tank with a considerable decrease in band II, and further reduction in the area adjoining the walls (Table VII). C. Locomotor Patterns During the First Hour In Fig. 12, the movements of fish no. 18 are plotted for consecutive 5-rain periods during the 1st hour in the novel environment of the tank. After an initial period of activity encompassing the whole area of the tank, the animal seems to restrict its movements to small areas at a time of different location. Similar results were obtained with a second fish tested for this behaviour. Discussion A. Turning Behaviour 1. Direction of turn. The locomotor behaviour of fish is represented in a temporal distribution of turns of certain magnitude and direction, separated by straight pathways of varying length. Thus, the resulting locomotor pathway is largely determined by turning behaviour which,

in rats, has been considered to be an aspect of exploratory behaviour. Extensive observations on the turning behaviour of rats in T and Y mazes, and to a limited extent in 'open fields', have demonstrated the now well known, but as yet not well understood, phenomenon of spontaneous alternation of turns (Tolman 1925; Dennis 1935) which occurs in a wide variety of other vertebrates (opossum: Tilley, Doolittle & Mason 1966; humans: Wingfield 1943; Sugimura & Iwahara 1958) but not in chicks (Hayes & Warren 1963). The explanation for the phenomenon has been sought primarily in the alternation of the response (Heathers 1940; Hull 1943) or that of the stimuli which evoked the response (Montgomery 1952a, b). Spontaneous alternation may be an expression of the tendency to vary the input to the central nervous system of novelty and complexity or to maintain a certain minimum total level of information input (Hebb 1955; Dember & Earl 1957; Glickman 1958; Zucker & Bindra 1961; Wimer & Sterns 1964). The behaviour would lead to the continuous acquisition of novel stimulation. Both response and stimulus alternation might be operative, alone or in combination, to maintain the required level of stimulus input (Rothkopf & Zeaman 1952; Walker et al. 1955a, b; B~ittig, Zahner & Grandjean 1964). The occurrence of spontaneous alternation has not been studied in fish by means of mazes, and was believed to be absent in these lower vertebrates (Amiguet & Bgttig 1965) although experimental data were lacking. The evidence in Table IV, which analyses the dependence of direction of a turn on the direction of the turn

KLEEREKOPER ET AL. : LOCOMOTOR BEHAVIOUR OF GOLDFISH 4O0

500

iI

200[-

too

-

/ .5 inhours ~..O Elapsedlime Fig. 7. Cm-nulated values of turns. Heavy tracing, left turns; light tracing, right turns (see text).

immediately preceding it, independently of any bias (handedness) the animal may have, speaks strongly against the hypothesis of spontaneous alternation by goldfish in 'open field' locomotion. The chance of the direction of a turn being the same as that of the turn preceding it is consistently greater than that of it being in the opposite direction. Thus in the open field, at least, there is no alternation of response. If

323

alternation of stimuli determines the directness of a turn in relation to the preceding turn, it must follow that, in consecutive turning in a same direction (i.e. no alternation), each turn had led to a novel stimulus situation by which stimulus satiation was avoided. On the other hand, a turn leading to a repetition of a same stimulus situation would be followed by a turn in the opposite direction, i.e. alternation. If this assumption were correct, it would have to be expected that the gradual decrease in novelty content accompanying exploratory behaviour be reflected in a change in the dependence of direction of consecutive turns, and that as novelty content decreases, the highly significant right-right and left-left dependencies decrease and give place to an increased right-left, leftright dependence. There is no evidence in the data that this indeed happens and the conchision is drawn that there is no obvious relationship between novelty content of the environment and direction of turns, at least during periods of up to 69 hr following the first exposure to that environment. A non-environmental cue, such as a sense of direction, affecting the direction of turning behaviour, will be discussed below (see angle compensation). Finally, it is to be noted that there seems to be a tendency by fish to revisit a same location in succession, rather than to avoid it as was observed in rats by B[ittig et al. (1964). 2. Frequency of turning. The finding that the average frequency of turns, regardless of sign or magnitude, in the tank as a whole, per unit distance travelled by fish, did not change as a function of time (.maximum duration of observations: 69 hr) may lead to the conclusion that the frequency of turning is not related to the novelty content of the environment. Such a conclusion would weaken the argument that turning increases the range of movements of an animal. However, the role of turning behaviour in exploration may be considered from a different viewpoint. No attention has been paid so far to the significance of locomotion along a straight pathway in exploratory locomotor behaviour. If, indeed, turning is adaptively significant in that it increases the opportunity of exposure to novel stimuli, it may be assumed that the absence of turning is maintained for as long as the input of novel stimuli remains at a required level. 3. Size of angles of turn. Although the number of fish is relatively small, the available

324

ANIMAL

BEHAVIOUR,

18,

2

1.0

® .. e~..,

.8

®...- L':. ,~ :,."• '..~\

........ '. . . .

S"

~'". •

..'-.

.i

~. x{

,,,,,,

.

o., ", lit

•...

/t i ~

..

~b

• I~

. aj/~

.: : ". 'i /~'

...,...

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r-,6 / °k

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/'e~'~°~

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'..,~

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,,-~/ "

. ~e~. ...,¢

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,4

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2

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I

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I

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s

5 SIZE

I

I

I0 OF

I

|

I

I

.L ~

_

J

_ ! _~

15

20

GROUP

Fig. 8. The total population of turns was divided into consecutive groups, each comprising a number of consecutive turns varying from 2 to 20. F values of inter/intragroup variance of turns in four goldfish for group sizes from 2 to 20 are shown (see text). ®, significance level at 0.01.

1.0

o ,8 k-~O k-

u-.S

\./" .4 SiZE

OF

GROUP

Fig. 9. Effect of walls of tank on the F values for fish no. 18. Ak, area A; ©, area B; O, area C (see Fig. 3).

KLEEREKOPER ET AL. : LOCOMOTOR BEHAVIOUR OF GOLDFISH 15-

325

Table VII. Effect of Walls of Tank on Velocity

15fish

15

Velocity =.,

Fish no.

o Q._

o

D._

IIIL,,,

o

2~ s'o

25-

Duration Band Central zone of record II III (hr)

Band I

Average v d o d t y (cm/s)

25

50

15

18.88

25.39

32.55

17

17

12.47

17.23

29.05

14

18

12'81

18'32

21"75

12

0.73

0.87

12

25-

Velocity (lengths/s) fish

17

fish

N = 4,49 5

18

18

0.51

N = 12,817

The corresponding frequency distributions are entered in Fig. 11. m

:0 25

o

o

50

Velocity

in

25

50

cm/s

I-"

N =1i,961

]I ..... ]I[ .....

N =7,379 N =5,996

2°1 n [i -,sJ

H

.-~lo-

.-"

~,

j

I

==

',

!

Fig. 10. Frequency distribution of velocity for four fish of 30 cm length, cm/s = 0.03 body length/s. Table VI. Average Veloeity of Loeomotion Fish no. 13

Velocity (cm/s) 43"33

15

41"69

17

25"47

18

19"96 or 0.8

evidence indicates that fish of different origin may be characterized by different turning behaviour. The distribution of angle sizes may be a genetic characteristic. Overriding the differences accompanying the origin of the fish studied are those related to sex. Sex differences in exploration have also been recorded in rats (Lester 1967). The great change in angle distribution observed in all fish in band II of the tank space, that is, well before the walls could interfere with the free movements of the animals, raises the question of how the wall is perceived. Negative accommodation (Beer 1894; yon Hess

i

r" r

~.

r

5

!

j

~ ..J

r" !

f-.J 0

-1 [ I

! ! 3

' i

!L-1 L~ i

,

;

L.~ ;

t L..

i

i

-1 L,~

85 50 Velocity in c m / s

Fig. 11. Effect of walls of tank on the frequency distribution of velocity for one fish.

1912), perspective vision, and distance perception have been demonstrated in fish generally (Lee 1898; Scheuring 1920; Tamura 1957), and in goldfish specifically, at distances not less than 50 cm (Herter 1930, 1953), that is, within the average distance of band II from the walls. However, recordings using fish with impaired vision will have to verify the role of this s e n s e in the behaviour question. The perception of the walls might also occur through the acousticolateralis system since blind and blinded fish can avoid surfaces or objects in a totally strange

326

ANIMAL

BEHAVIOUR,

18, 2

6

v

~

8

t2

Fig. 12. Successiveplots of 5 rnin duration each for fish no. 18 during first hour. environment (Crozier 1918; Dijkgraaf 1933, 1947; John 1957). 4. 'Handedness'. Bias in the direction of turning ('handedness') was reported by Herter (1930, 1948) who reported that half a group of thirty-three fish of various species showed a weak preference for turning to the right. Right handedness in goldfish was observed by Spencer (1939) but Breder & Nigrelli (1938) found left handedness in the same species. No preference

of direction could be observed by Janzen (1933); neither the unilateral elimination of paired fins nor total extirpation of the forebrain affected the condition. According to Herter (1948), handedness can be such a strong attribute in various species of fish that it is very difficult or altogether impossible to eliminate it through training. The handedness observed at the 95 per cent confidence level in all but one fish studied in the

KLEEREKOPER ET AL.: LOCOMOTOR BEHAVIOUR OF GOLDFISH

present investigation was not subject to change m time, although similar studies on a marine teleost (Sargus diplodus) and two elasmobranchs (Mustelus and Scyliorhinus) demonstrated that in these species handedness may vary in time (Kleerekoper 1967a, b). It may be assumed that the preference of direction of turning in these fish as reported in the present paper is a stable characteristic which must play a role in overall turning behaviour and, thus, in the resulting locomotor patterns. 5. Angle compensation. Through the phenomenon of angle compensation (Kleerekoper et al. 1969) it becomes possible to recognize an important correlation between the direction, magnitude, and sequence of individual turns. In angle compensation, the cumulative turning effect of a group of consecutive turns in a same direction becomes significant rather than the magnitude of the individual turns composing the group. The cumulative effect of groups of turns to the left and that of groups of turns to the right is a balance between the two directions which is maintained constant (maximum period of observation: 69 hr). Variance analysis has rejected with a very high degree of significance the hypothesis of randomness of turning. Therefore, the observed balance between the two directions must be attributed to an active compensation mechanism (Kleerekoper et al. 1969). The angular compensation is most likely mediated through the vestibular system but other mechanisms may be involved. It is of particular interest that spontaneous alternation is greatly reduced or abolished in rats in which middle ear disease had disrupted the vestibular system (Douglas 1966a, b), that maze learning in rats is dependent on the normal function of the semicircular canals (Watson 1907), and that distance sense in fish is lost when either the otoliths are removed or the macular nerves severed (Lee 1898). Since there is good evidence that sense of direction may be a factor in spontaneous alternation in rats (Dashiell 1920, 1932; Douglas 1964, 1966a, b; Sherrick & Dember 1966; Dember, Harris & Sherrick 1966), the hypothesis is advanced here that angle compensation is the primary mechanism of turning behaviour and that spontaneous alternation is only one of several possible aspects. The direction and magnitude of individual turns are in and by themselves unimportant from a functional aspect; the total effect of a change of direction remains the same whether that change is produced by several turns in sequence of a

327

few degrees each or by one or more larger turns. The relationship between alternation and exploratory behaviour may be far less important than its association with orientation behaviour, of which angle compensation must be an integral part. B. Velocity of Locomotion Much of the literature on swimming speed of fish was reviewed by Bainbridge (1958) and Blaxter & Dickson (1959). A comparison between natural and 'forced' maximal speeds was reported by Ohlmer & Schwartzkopff (1959). Nevertheless, the means of the distributions of velocities are subject to temporal variation. A trend seems to be present towards gradually increasing averages of velocity over a period of several hours, followed by a gradual decrease. Four such cycles seemed to occur in fish no. 13 over a period of 62 hr but no periodic analysis was carried out to verify the phenomenon. Cycles of activity in the goldfish have been reported by Szymanski (1914) and Spencer (1939). The recurrent maximum velocities between 50 and 65 cm per s (2.0 to 2.6 lengths per s) are low compared to the maximum theoretical speeds of ten times body-length per s postulated by Bainbridge (1958), and are below the values for average maximum speed of goldfish in conditions of forced locomotion observed by Blaxter & Dickson (1959) (150 to 159 and 69 to to 150 cm per s); Gray (1957) (70 to 169 cmper s). Additional data were reported by Radcliffe (1950), Breder & Nigrelli (1938), Schuett (1934) and Escobar et al. (1936). The values reported in the present paper may be related to the condition of isolation of the fish used in these recordings. Observations by Breder & Nigrelli (1938), Escobar et al. (1936) and Schuett (1934) point to a lower speed in goldfish swimming in groups as compared to that of single individuals. Goldfish run a maze more rapidly in a group than when isolated (Welty 1934). As to temperature, the best swimming performance (45.7 to 50.8 cm per s), measured in a rotating chamber, was obtained in acclimated fish, at tempratures between 20 ° and 30°C but well-defined optimal temperature could not be established (Fry & Hart 1948). Blaxter & Dickson (1959), studying several marine and freshwater species, including goldfish, could find no obvious correlation between temperature and swimming speed. It seems 'safe, in the light of these reports in the literature on the significance of temperature at least in acclimated fish, to deny significance to temperature as a factor determining the

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differences between swimming speeds reported in this paper and those recorded in the literature. A correlation between velocity and explora t o r y behaviour could not be found. In rats, such correlation does exist according to some observers (Glanzer 1961; but see B~ittig et al. 1964).

C. Evidence for Systematic Locomotor Exploration of the Environment The analysis, in 5-min. steps, of the initial phase of locomotor exploration strongly suggests that areas of the tank are explored in succession after an initial 'grand tour' of the new environment as a whole. Such behaviour would require memory of topography (Edinger 1899; Gerking 1959) and a sense of direction, attributes present in Gobius and Gasterosteus (Goldsmith 1914), perch (Triplett 1901), Fundulus (Thorndike 1911) and goldfish (Franz 1911; Churchill 1916). That rats have some idea o f spatial relationships in maze learnings has been demonstrated by several workers (Tolman, Ritchie & Kalish 1946a, b). A quantitative analysis of this behaviour, using a comparison between simulated locomotor patterns by a model, based on the experimental data presented in this paper and the empirical locomotor patterns observed will be the subject of a separate communication.

Summary The movements of individually observed naive goldfish, 25 to 30 cm long, in a novel 'open field' consisting of a tank measuring 5.0 × 5'0 × 0.5 m in constant environmental conditions, were continuously monitored during periods from 11 to 69 hr. The size, direction, and sequence of turns, length of steps, and velocities were computed, and their relationships analysed by a computer and data-processing system on line. Locomotor patterns were plotted and the effects of time (decrease in novelty content) assessed in the light of available data on these parameters in other species. It was concluded that spontaneous alternation may be related to orientation but not to exploratory behaviour.

Acknowledgment This investigation is part of a research project partially supported by Grant No. GB-8108 from the National Science Foundation to the senior author.

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(Received I0 June 1969; revised 8 December 1969; MS. number: A854)