Behavioural biology of the collared lemming Dicrostonyx groenlandicus (Traill): I. Agonistic behaviour

Anim. Behav ., 1968, 16, 24 5-262

BEHAVIOURAL BIOLOGY OF THE COLLARED LEMMING

DICROSTONYX GROENLANDICUS (TRAILL) : I . AGONISTIC BEHAVIOUR* BY

JOHN T . ALLIN & EDWIN M . BANKS

Department of Zoology, University of Illinois, Urbana, Illinois 61801

The collared lemming of North America, genus Dicrostonyx Gloger, inhabits the tundra regions of Canada, Alaska and Greenland . It is represented by three allopatric species, D . groenlandicus (Traill), D . hudsonius (Pallas), and D . exsul Allen (Hall & Kelson, 1959) . D . exsul is restricted to St Lawrence Island, while D . hudsonius inhabits unforested regions of the Ungava Peninsula . D . groenlandicus has the widest distribution, its ten subspecies ranging from Churchill, Manitoba, north to Greenland, and from Alaska on the west to Hudson Bay on the east . Very little is known about the behaviour and habits of collared lemmings, although certain features have been discovered through field observations. Lemmings remain active the year round, burrowing under the snow in winter and in some years breeding in the winter and spring (Krebs, 1964) . Summer food consists of green plants, whereas dormant buds and roots are taken in winter . Like many other microtines, collared lemmings undergo fairly large, regular fluctuations in numbers . A peak population followed by a decline occurs about every 4 years . Krebs (1964) studied the population cycle in two species of lemmings, Dicrostonyx groenlandicus and Lemmus trimucronatus, near Baker Lake, N .W .T . He found no extensive migrations to occur in these species such as are described for Norwegian lemmings (Lemmus lemmus) (Collett, 1895 ; Aho & Kalela, 1966) . However, local movements do take place in the spring during years of particularly high numbers . Animals moving about on the lake ice are never observed to travel together or form groups of any kind . This is the only information available on the degree of sociality in feral collared lemmings . Territoriality in this species has not been investigated . It is clear that practically no information is available regarding the social behaviour of collared lemmings . The present study is an

attempt to analyse intraspecific agonistic behaviour in male Dicrostonyx groenlandicus, specifically to describe the major components of the behaviour and to investigate the sequential relationships between these components . Methods The original wild stock of lemmings, from which the colony at the University of Toronto was established, was trapped during the summer of 1963 in the region of Baker Lake, N .W .T. In this study only sexually mature males were used . These males were either part of the original wild stock or their descendants born in the laboratory . The lemmings were housed in cold rooms maintained at 12°+3°C the year round . At first the colony room was subject to the normal diel light fluctuations at Toronto ; later the colony was subjected to continuous artificial illumination in an effort to enhance the reproductive rate . Animals were confined in individual cages except when pairs were formed for breeding purposes . A pair was usually maintained until the female was patently pregnant, at which time the male was removed from the cage . All cages were galvanised, 3-in . mesh wire cages of dimensions 15 in . x 9 in . x 73 in . Each animal was provided daily with an excess of carrots, cabbage, and rolled oats . In addition, a considerable quantity of hay was placed in each cage to serve both as food and nesting material . The hay was replaced once a week when the cages were cleaned . The animals received no water other than that which they obtained from fresh food . Young lemmings were weaned at the age of 6 weeks, and at about 3 months of age were separated from their littermates . At the time of weaning each pup was provided with a numbered plastic tag for purposes of identification . These tags, commonly used to mark fish, were sewn to the animal's skin between the shoulders . In order to minimize the influence of familiarity as a factor in determining fighting success, encounters were staged in an arena equally

*This study was conducted at the University of Toronto, Toronto, Canada D

245



246

ANIMAL

BEHAVIOUR,

familiar to all animals. This arena was approximately semicircular in shape with sides of galvanised tin, a plywood floor, and a front wall of glass through which the animals could be observed. The sides and floor were painted white to provide a suitable background for photographing the animals . The glass wall measured 20 in. in length, and like the sides of the arena, was 10 in . high . Floor space totalled 257 in 2. These dimensions reflected an attempt to design a rather small enclosure which would keep the animals in sight of one another and yet allow an animal to avoid another to some extent . The semicircular shape was chosen in order to reduce the number of comers in the arena. The recording system used in this study consisted of a 20-pen Esterline-Angus event recorder activated by a push-button keyboard . The chart on which the behaviour was recorded advanced at a speed of 6 in . a min and duration was read from the chart to 0 . 1 sec . Since the behaviour of more than one animal could be recorded simultaneously, sequences of acts and postures involving one or more animals could be investigated. A limited number of permanent records of agonistic encounters were filmed with a 16 mm movie camera. A time and motion projector (Bell and Howell 173), equipped with a frame counter permitted extremely accurate determinations to be made . of the durations of agonistic components . Photographs of acts and postures were taken with a 35 mm single lens reflex camera using electronic flash for light . All experiments were carried out in a room maintained at approximately 15°C . Animals were transported to and from the colony room in individual plastic cages measuring 11 in . x 7 in. x 5 in . Subjects were introduced into and retrieved from the arena directly from these transfer cages . The arena was lighted by a desk lamp containing a 40-W bulb situated about 30 in above its floor . Diffuse lighting was produced by placing a piece of frosted glass immediately beneath the bulb . No other light source was used during the experiments . The floor of the arena was cleaned and covered with fresh sawdust at the beginning of each experiment. A black curtain was suspended from the ceiling on both sides and in front of the arena . Observations were made at a distance of about 3 ft from the front of the arena through a hole cut in the curtain . Several different types of experiments were performed during the course of the study .

16,

2-3

Habituation Experiments Before each lemming was used in a staged encounter it was first subjected to a series of ten habituation trials. Each trial consisted of placing the animal alone in the arena and observing its subsequent behaviour . This procedure allowed the animal to explore and to become familiar with the arena, and at the same time permitted observation of the behaviour of a single animal . Thus a base-line measure associated with exploration of the arena was obtained, permitting this behaviour to be distinguished from agonistic behaviour in subsequent paired encounters . Habituation periods were 15 min long and were usually separated by intervals of about 24 hr for any particular animal . Recorded Experiments Siblings and animals which appeared to be in poor health were never used in paired encounters . No attempt was made to match the animals of a pair for age, weight or experience . In general, an animal was used for the first time in a contest within a week of its last experience in the arena during habituation trials . Clipping the fur in various patterns permitted observer identification of individuals. A partition was employed to allow each animal 2 min at the beginning of the experiment to explore its half of the arena . The partition was then removed and agonistic behaviour recorded for a standard period of 15 min . At the end of the experimental period the animals were separated with the partition and removed from the arena . Twenty-one such paired encounters were conducted . Results In this study eleven acts and postures were distinguished as components of the agonistic repertoire which occur most frequently . These components have been given descriptive names for ease of discussion. A motivational connotation is not implied by this nomenclature. It must be emphasized that the recorded components are the products of an arbitrary division ; they are in fact elements of a continuum in which one act or posture grades into another . 1 . Components of Agonistic Behaviour APPROACH (A) . This is defined as a movement toward an opponent which is either stationary or is itself moving towards the first animal . Such movements incorporate walking or running ; they do not include head movements in the absence of whole body motion .



ALLIN & BANKS : BEHAVIOURAL BIOLOGY OF THE LEMMING RETREAT (R) . This is a movement away from the opponent involving motion of the entire body . A retreat is considered to occur only if the movement is initiated within 6 in . of the opponent. This arbitrary limit was imposed to eliminate movements bearing no obvious relationship to the position of the opponent . CHASE (C). This is a movement towards a retreating opponent. The motion is typically more rapid than in approach . ATTACK (Ak) . This is defined as a jump towards the opponent. It is usually initiated from an upright posture, the head being drawn back momentarily before the hindlegs are extended in launching the animal forward (Fig . 1, Plate V) . The forelegs may strike the opponent, usually in the face or throat ; the opponent is typically knocked over by the attacker . Often little or no contact is made, and the attacker's leap carries it past the opponent . During an attack the animal's mouth is frequently open, but no bites were ever observed in this situation . The attacker may land on top of the opponent or to one side . It usually maintains its balance and lands on all fours . An attack is usually given when the opponent is within one body length. Although attack most frequently occurs from an upright posture, it may be given by an animal chasing its opponent . A bite may be delivered from this type of attack, usually directed at the rump or flank of the retreating opponent . TUMBLE (T) . This is the most intense component of fighting behaviour in that almost all biting occurs while the two animals are so engaged . The animals come together, usually after one has attacked or chased the other, and become locked at right angles to each other forming a `ball' . Each animal clasps the other behind the shoulder and along the side with its forelegs, thus maintaining the ball . Each delivers bites to the head and shoulder regions of the opponent, and as the animals roll back and forth the ball moves across the floor of the arena . If one animal is considerably larger and stronger than the other it may remain on top for as long as the animals remain locked together, so that the ball is more or less stationary . During tumble bits of fur are frequently pulled out as the animals bite each other, and occasionally biting is audible as a `crunching' sound . Although no fatal wounds were ever observed in these experiments, superficial cuts were often received in bouts of tumble . These were almost all restricted to the head and shoulder regions, the

247

cheeks and lower lip being the most common sites of injury. Tumble is usually terminated when one of the animals breaks away from its opponent and retreats . BOXING (B) . Like Tumble, this is an act in which both animals participate, pushing at each other with their forelegs while in upright postures (Fig . 2, Plate V) . Frequently both lean against one another while maintaining their balance by movement of the hindfeet . The forelegs are typically pushed against the opponent's neck and shoulders, and the act is terminated when one loses its balance and falls . Bites were never observed to occur during boxing . OFFENSIVE (0) . This is a term which includes all postures in which the animal leans towards or positions itself over the opponent (Fig. 3, Plate VI) . The head is oriented towards the opponent, and one or both forelegs are raised off the floor. The hindlegs alone support the body since the rump is elevated as the animal leans forward . Offensive postures include a range of body stances, the long axis of the body varying from about 30 to 90 degrees from the floor . The animal may be oriented at any angle to the opponent, but if it is positioned over the opponent directly from the rear, no more than its head may be over the opponent's rump for the posture to be labelled offensive . This serves to distinguish postures of this type from those in which the animal attempts to climb onto the opponent's back using its forelegs . The latter postures are described later under `mount' . Attacks and boxing may be initiated from offensive postures, usually from the more upright stances . Animals in offensive postures frequently display teeth-gnashing, but were never observed to utter any squeals . DEFENSIVE (D) . This includes all postures in which the animal leans away from its opponent . This is reflected by the position of the head which is typically held up and away from the opponent (Fig . 4, Plate VI) . When the teeth are bared, this head position makes the teeth very conspicuous, at least to a human observer . One or both forelegs are raised off the floor, and the animal supports itself with its hindlegs and rump as it leans back . At times the wall or corner of the arena may be used for support as well . The animal's back tends to be arched, except in the more upright positions . Also included under the term `defensive' is a variety of postures in which the animal lies completely or partly on its back . All four feet



248

ANIMAL BEHAVIOUR, 16, 2-3

may be used to ward off the opponent, which is typically in an offensive posture and positioned over the opponent . Occasionally a posture is seen which is characterized by the animal lying on its back making little or no effort to ward off the opponent or to flee (Fig . 3, Plate VI) . It often utters loud, sustained squeals. This posture may be maintained long after the opponent has withdrawn . It is included as a defensive posture because of its close resemblance to other defensive postures, notably those in which the animal is positioned on its back in a corner and is partly supported by the wall of the arena . In these situations it is difficult to observe whether the animal is attempting to ward off its opponent or not . Throughout the range of defensive postures there is a tendency for the eyelids to be partly closed . DIG (Dg) . This is a motor pattern which differs both in form and intensity from solitary digging . The head is typically held up nearly level with the back, and the animal usually orients itself so that its side or rump faces the opponent . Vigorous strokes of the forelegs propel sawdust backward past the side of the animal, or sawdust may be piled under the body, and the hindfeet are then used to expel it . This display tends to occur near the centre of the arena. The animal, when digging, often moves away from the opponent, and the latter may be hit with sawdust causing it to jump and retreat . These digging movements are generally more vigorous than those displayed in solitary digging observed during habituation trials . MOUNT (M) . Here the animal positions itself over the opponent's back with its body parallel to that of the opponent . Using its hindlegs for support, it grasps the sides of the opponent with its forelegs and pulls itself onto the opponent's rump and back . The term `mount' includes postures where the animal simply positions itself over the opponent as well as active motor patterns with pelvic oscillations . These patterns are characterized by the position of the animal, which is well forward so that the head is over the opponent's neck and shoulders (Fig . 5, Plate VII) . One hindleg remains on the floor for support and the other is raised to a varying degree and vigorously oscillated up and down . GROOM (Gr) . This act usually takes place when the opponent is in a defensive posture or curled up with its eyes partly closed . The grooming animal places its forelegs on the opponent's back or side and proceeds to moisten the latter's

fur. The head, back, and rump regions are those typically groomed . The grooming may be continued for an extended period of time if the opponent does not retreat . Groom is also frequently displayed by an animal while in a mounted position (Fig. 6, Plate VII) . Occasionally a bite is delivered during groom . 2. Duration of Individual Displays of Agonistic Components To investigate the quantitative characteristics of each act and posture, particularly with regard to the variation in the time required for individual displays of components, data from ten contests involving fourteen individuals were pooled and forty displays of each component were chosen at random for analysis . In the case of boxing, which was displayed somewhat less frequently than the other components, data from all twenty-one contests were pooled . Table I indicates the mean duration and standard deviation for the forty displays of each component . Also included for comparison are the results of the time-motion film analysis of seven contests involving ten individuals . The large standard deviations for both sets of data indicate much variation in the duration of individual displays. This variation is particularly great for the display of offensive and defensive postures and is least for attack. Mean durations of agonistic components from the recorded experiments in most cases do not differ greatly from the more accurate values of the film contests. The notable exception is that of defensive postures whose mean duration in the recorded experiments is much greater than in the filmed contests. It is doubtful whether such a large discrepancy is due simply to inaccurate recordings . Considerable variation in the results might be expected due to the different sample sizes involved coupled with the great variation in the display durations . It should be noted that the mean durations of agonistic components from the recorded experiments are consistently somewhat greater than corresponding values from the filmed contests. This may reflect the greater ability of the observer to detect brief pauses in the action on film than in the recorded experiments, where two displays of an act or posture separated by a very brief interval may be recorded as one continuous display . 3. Total Durations and Frequencies of Agonistic Components The total duration and frequency of each



249

ALLIN & BANKS : BEHAVIOURAL BIOLOGY OF THE LEMMING Table I . Duration of Individual Displays of Agonistic Components Films

Recorded experiments Agonistic component

N*

M**

* ** SD

N

M

SD

Approach

40

0 .5

0.4

198

0 . 33

0 . 30

Retreat

40

0 .7

0.6

226

0 .46

0 .28

Chase

40

0. 7

0.4

59

0 . 41

0 . 26

Attack

40

0.2

0. 1

69

0 . 17

0 . 10

Offensive

40

2.2

3 .4

278

0 . 87

1 .40

Defensive

40

10 . 7

28 . 5

176

1 . 02

1 . 77

Dig

40

1 .4

1 .8

38

0 . 73

0 . 49

Groom

40

2 .4

5.4

24

0.84

0 .84

Mount

40

2.3

2. 1

15

0.43

0.41

Tumble

40

2.9

9 .2

14

0 . 53

0 . 51

Boxing

40

0.8

0.9

26

0 . 59

0 . 62

N• is the number of displays analysed M** is the mean duration of the displays in seconds sD s * * is the standard deviation of the display durations in seconds

display component were calculated for each animal . These results were plotted in the form of two histograms for each contest ; samples of frequency histograms are presented in Figs 7 to 9 . a. Contest types. In general the ethological literature dealing with agonistic behaviour in vertebrates has employed certain similar measures of fighting behaviour to characterize the social status of each animal in the society . These measures usually concern the more prominent agonistic displays such as attacking or chasing behaviour . In the present study the display of a submissive posture could not be employed to distinguish a subordinate animal since no such posture could be said to be characteristic of a defeated lemming . Consequently, the frequencies with which an animal displayed both chase and attack were used to determine its status relative to that of the opponent. Chi-square tests were carried out for each contest to compare the chase and attack frequencies of each animal of the pair. In this study a lemming is designated as the `dominant' animal (Dom .) if it displays a significantly higher frequency (0-p5 level, 1 df, Yates' correction applied for expected frequencies of between 3 .0 and 5 .0) of either DD

No . 23

No. 5766 SUBORDINATE

DOMINANT

45

40

N

r7

35

f

30

z n 25 Ir

a

U z

20 1S

0 10

A

R

C Ak O D Dg Gr M T 8 A R C Ak O D Dg Gr M COMPONENT

Fig. 7. Frequency of recorded acts and postures in a typical contest of type I (see text for definition of code) . Solid bar represents act engaged in simultaneously by both animals.

chase or attack than does its opponent . The latter is termed the `subordinate' (Sub.). Such a dominance-subordination relationship can be demonstrated in twelve of the twenty-one





250

ANIMAL

BEHAVIOUR, 16, 2-3

No.68

No. 5729

INACTIVE

ACTIVE 50 45

35 30

A R C Ak O D 09 Gr M T B A R C Ak 0 D Dg Gr M COMPONENT

Fig. 8. Frequency of recorded acts and postures in a typical contest of type II (see text for a definition of code) . Solid bar represents act engaged in simultaneously by both animals. No.68

No . 513

CHASER

ATTACKER

90 8o N

70 z f 60

so 40 z W

° 20 10

M A R C Ak 0 D Dg Gr M T B A R C Ak 0 D Dg Gr M COMPONENT

Fig . 9 . Frequency of recorded acts and postures in a typical contest of type III (see text for a definition of code) . Solid bars represent acts engaged in simultaneously by both animals.

recorded experiments. These contests will subsequently be referred to as contests of type I . In the remaining nine contests neither animal was shown to be dominant to its opponent, using the criteria outlined above . In seven of these nine contests neither animal displayed attack or chase with a significantly higher frequency than did its

opponent . These encounters are designated as contests of type II. In the two remaining contests one animal displayed chase with a frequency significantly greater than did the other, while the latter displayed attack significantly more often . These two encounters are referred to as contests of type III . Chi-square tests were also carried out to test the significance of differences between the animals in display frequencies of the other acts and postures . For contests of type II these results showed that one animal consistently displayed a higher frequency of approach than did its opponent. This provided a convenient means of differentiating between the animals of a pair so that their behaviour could be compared in other respects . The lemming displaying the higher frequency of approach will subsequently be referred to as the `active animal (Act .), whereas its opponent will be designated as the `inactive' animal (Inact .) . The two animals in contests of type III are differentiated by the frequency with which they display attack and chase . The animal displaying chase more often is referred to as the `chaser' (Ch.) and its opponent, which displays a significantly higher frequency of attack, is called the `attacker' (At.). In Table II are presented details of the twentyone recorded contests . Individuals in each encounter are indicated by their identification numbers, followed by an abbreviation showing their status in that encounter as determined from the frequency analysis just described . The type of contest resulting is also indicated . No attempt has been made to analyse the variability in behaviour exhibited by those individuals participating in more than one encounter . b . Temporal change in activity . Changes in the amount of vigorous fighting activity occurred throughout the course of a contest, as revealed by dividing the 15-min contest into three intervals of 5 min duration . Table III presents the total frequency analysis of chase, attack and tumble for each 5-min segment . In contests of type I approximately one-half of the chase displays took place in the first 5 min, with equal frequencies occurring in the second and third intervals . The frequencies of attack and tumble dropped considerably and progressively from the first to the third intervals . Changes in chase frequencies in type II contests resembled those of type I, with a large proportion of displays occurring in the first portion of the encounters, and similar, lower frequencies occurring in the



ALLIN & BANKS : BEHAVIOURAL BIOLOGY OF THE LEMMING

first 5-min interval . The data for contests of type III illustrate a somewhat different temporal pattern of fighting activity . Although the majority of attacks occurred in the first portion of the contests, the frequencies of chase are rather similar in each of the three 5-min intervals . No conclusion can be drawn regarding tumble because of the extremely small number of times this act occurred. The results thus indicate that in contests of both type I and type II vigorous fighting occurred for the most part during the first portion of the encounters and decreased to very low levels toward the end of the 15-min period. Such was not the case for type III contests, where one animal persistently chased the other throughout the encounters .

second and third intervals . The number of attacks decreased progressively throughout the contests . Almost all displays of tumble occurred in the Table II. Status of Individuals in Recorded Experiments Date of encounter

Type of contest resulting

Animals

18/9/64

5729 (Act.) x 9 (Inact .)

II

23/9/64

23 (Dom .) x 71 (Sub .)

I

14/10/64

5729 (Act.) x 68 (Inact .)

II

16/10/64

23 (Dom .) x 511 (Sub .)

I

22/10/64

13 (Inact .) x 5766 (Act.)

II

26/10/64

68 (Dom .) x 511 (Sub .)

I

9/11/64

23 (Inact .) x 59 (Act.)

II

12/11/64

78 (Inact.) x 5766 (Act .)

H

18/11/64

79 (Dom .) x 513 (Sub .)

I

19/12/64

5729 (Ch .) x 13 (At.)

III

19/12/64

23 (Dom.) x 5766 (Sub .)

I

19/12/64

68 (Dom.) x 511 (Sub .)

I

19/12/64

6 (Sub.) x 71 (Dom .)

I

13/1/65

68 (Dom.) x 513 (Sub .)

I

13/1/65

80 (Dom .) x 511 (Sub.)

I

28/1/65

23 (Dom.) x 5766 (Sub .)

I

4/2/65

78 (Act.) x 59 (Inact.)

II

4/2/65

68 (Ch .) x 513 (At .)

III

18/6/65

258 (Dom .) x 276 (Sub .)

I

21/6/65

269 (Act .) x 266 (Inact .)

II

21/6/65

268 (Dom.) x 292 (Sub.)

I

4. Analysis of Behavioural Sequences . a. Sequences displayed by an individual . Of fundamental importance in any description of behaviour is the patterning of behavioural elements in time . An animal's actions at any particular moment may depend to a considerable degree on preceding events, including the animal's own behaviour. The dependence of one act on the occurrence of another may be investigated by determining the frequency with which a particular element of behaviour is followed by another. It is reasonable to assume that the dependence of an act on the preceding one decreases as the interval between the acts increases . Thus events which are separated from one another by intervals of long duration can be considered to be relatively independent . Preliminary observation indicated that during interactions in this species, agonistic components are typically separated by very brief intervals . As a first approximation, a maximum time of 5 sec was arbitrarily chosen as a suitable interval separating events of a sequence . Consequently, the term `sequence' will be used here to denote a series of consecutive acts performed by the same animal with a maximum time lapse of 5 sec

Table III . Frequencies of Certain Agonistic Components in S-minute Intervals for Each Contest Type Type I interval Agonistic component

251

Type II interval

Type III interval

1

2

3

1

2

3

1

2

3

Chase

130

63

60

16

3

3

20

28

17

Attack

121

43

12

32

10

5

17

8

6

Tumble

57

11

7

9

2

0

2

0

2



252

ANIMAL BEHAVIOUR, 16, 2-3

between the end of one act and the beginning of the next . The frequencies with which all pairs of agonistic components occur in sequence have been tabulated in the form of contingency tables . Pooled data for individuals in the twelve type I contests are treated in the following . The code for the agonistic components used in these tables is identical to that described previously . Initial acts are listed in the horizontal rows and the acts following -are listed in the vertical columns . Thus the frequency of any sequence is found by reading down to the row corresponding to the initial act of the pair and then across to the column for the second act . This method of tabulating results was employed by Grant (1963) in his analysis of behavioural sequences in the rat . Series of more than two acts are not tabulated as such, but are broken down into two-act sequences . The row total for each act indicates the number of times it follows other acts. These totals allow the observed frequency for each cell to be compared with that expected on the assumption that each act is displayed independently . Expected values thus represent the frequencies which would occur if acts were displayed completely at random . A comparison of observed and expected frequencies for each sequence permits the relationship between acts to be investigated . Discrepancies between these frequencies are subject to

analysis of chi-square only if the sequences displayed by each individual in each contest are considered separately. This was done employing 2 x 2 tables for all sequences in each contest in which the expected value exceeded 3 .0 (Yates' correction applied for expected values between 3 . 0 and 5 . 0) . The null hypothesis of independence between each pair of acts was rejected if the difference between observed and expected frequencies was significant at the 0 . 05 level of confidence for one degree of freedom . It should be noted that chi-square values obtained in this way are not additive . The sum of such chi-squares for all cells in a contingency table does not equal the total chi-square value for the table, a value that was not computed in this study . The number of contests in which differences between observed and expected frequencies are significant has been tabulated for individuals in each type of contest . Table IV shows the frequencies with which dominant animals displayed each of the possible sequences in type I contests . The three most frequently occurring sequences are approachoffensive, offensive-attack, and offensive-offensive . These results suggest that the dominant individual commonly approached the subordinate, adopted an offensive posture,' and then attacked. Attacks were almost always delivered from an offensive posture, but occasionally

Table IV. Contingency Table for All Sequences of Agonistic Components Displayed by Dominant Lemmings in Twelve Contests of Type I A

R

C

Ak

0

D

Dg

Gr

M

T

B

A

72

49

24

6

139

6

5

1

5

3

0

310

R

89

12

2

1

15

16

21

1

0

1

0

158

C

20

9

40

24

78

9

2

4

12

18

0

216

Ak

18

11

17

4

58

4

3

0

0

30

0

145

0

25

73

85

111

104

78

5

82

22

10

67

662

D

9

23

19

2

65

17

2

0

10

4

2

153

Dg

22

10

0

0

1

0

32

0

0

3

0

68

Gr

0

4

4

0

81

2

1

3

0

0

0

95

M

1

1

1

0

22

17

0

5

6

0

0

53

T

4

3

28

6

17

2

2

0

0

6

0

68

B

1

1

0

0

66

1

0

0

0

0

0

69

261

196

220

154

646

152

73

96

55

75

69

1997=N

Column totals

Row totals



253

ALLIN & BANKS : BEHAVIOURAL BIOLOGY OF THE LEMMING

occurred following chase . It is interesting to note that the sequence offensive-chase occurred eighty-five times compared to only seventeen for attack-chase, suggesting that the subordinate usually retreated before the dominant could attack, and was then pursued by the dominant . The dominant animal frequently approached after retreating, an indication that it persistently initiated contact with its opponent and did not show avoidance . Bouts of dig usually occurred together in sequence, the dominant typically retreating before displaying this act . Groom, mount, and boxing usually followed the adoption of an offensive posture, whereas tumble followed chase or attack . A comparison of row and column totals for approach reveals that this act preceded more acts (310) than it followed (261), and therefore constitutes a beginning of sequences of agonistic behaviour . Conversely, retreat is an end point of social interactions . Totals for the other acts and postures are very similar, indicating that no other agonistic component tends to initiate or terminate social interactions. Table V shows the number of contests in which observed frequencies of sequences displayed by the dominant individual are significantly greater or less than expected values . Only a small number of sequences occurred with frequencies deviating considerably from the expected values, and the

proportion of contests in which these differences occurred was quite small in most cases . Thus no sequence consistently occurred throughout these contests with frequencies higher than those expected on the basis of random occurrence of events. However, many sequences in individual experiments could not be tested since expected values were less than 3 . 0 . The fact that the frequencies of those sequences which did deviate from the expected values did so uniformly, that is, were either higher or lower than expected frequencies, is an indication that the behaviour of dominant individuals was not, in fact, contradictory. Sequences tending to occur with higher than expected frequencies were approachoffensive, offensive-attack, and retreat-approach . Boxing and offensive, as well as groom and offensive, also occurred together in several contests . These acts are therefore positively associated, the succedent act in each sequence being dependent to some degree on the display of the initial act . Thus the occurrence of approach increases the probability that the animal will subsequently adopt an offensive posture . Similarly, the display of offensive increases the likelihood of an attack being delivered . Conversely, certain pairs of acts are negatively associated . Offensive tends to follow approach, groom, and boxing, but not retreat, an indication that the dominant animal displays an offensive

Table V. Number of Type I Contests in which Observed Sequence Frequencies for Dominant Animals Differ Significantly from Expected Values A

R

C

Ak

0

D

Dg

Gr

M

T

B

A

2

3

0

(2)

4

0

(1)

0

0

0

0

R

4

(1)

(1)

0

(4)

0

0

0

0

0

0

C

0

0

1

1

2

0

0

0

0

0

0

Ak

0

0

(1)

(1)

1

0

0

(1)

0

1

0

0

(7)

1

2

6

(9)

2

0

3

0

0

4

D

0

1

1

0

1

(1)

0

0

0

0

0

Dg

0

0

0

0

(2)

0

1

0

0

0

0

Gr

0

0

0

(1)

3

0

0

(1)

0

0

0

M

0

0

0

0

0

1

0

0

0

0

0

T

0

0

1

(1)

0

0

0

0

0

(1)

0

B

0

0

0

0

4

0

0

0

0

0

0

Contests in which sequence frequencies are less than expected are in parentheses D ifferences significant at 0 . 05 level of confidence



254

ANIMAL BEHAVIOUR, 16, 2-3

posture only when in close contact with the opponent . Furthermore, although the sequence offensive-offensive occurred with a very high frequency in these contests, in nine of the twelve contests its frequency was actually less than the expected value . This fact reveals that the frequency of this sequence was quite low in relation to the occurrence of offensive postures, and that the adoption of an offensive posture decreases the probability that the next display will also be offensive. Table VI shows the frequencies with which subordinate animals displayed each sequence of acts . Those displayed most frequently were retreat-retreat, retreat-defensive, and defensiveretreat. Thus the subordinate individual regularly retreated from the dominant animal, often displaying a defensive posture before retreating again. Offensive postures preceded and followed retreat somewhat less often than did defensive postures. Tumble usually occurred following a retreat of the subordinate . Subordinates retreated forty-six times after tumble while dominants did so only on three occasions (Table IV) . Subordinates also differed from dominants in displaying defensive postures more frequently both before and after boxing . As for dominant individuals, dig was usually displayed following retreat.

A comparison of row and column totals supports the previous evidence from the results for dominant animals that approach tends to initiate sequences of agonistic behaviour whereas retreat tends to terminate them . Row and column totals for the other acts and postures are very similar. Table VII indicates that observed frequencies for subordinate animals deviated from expected values in fewer contests than did those for dominant animals. This observation, in part, reflects the smaller frequencies with which subordinate animals displayed most postures, thereby reducing the number of sequence frequencies which could be tested statistically . Nevertheless, the results do reveal a positive association between retreat and defensive postures, since both the sequences retreat-defensive and defensive-retreat occurred more frequently than expected in three contests . Conversely, negative associations are apparent between offensive, as well as defensive postures . The sequences retreat-retreat and offensive-retreat suggest some degree of inconsistency among the animals since they both occur with higher than expected frequencies in one contest but lower than expected frequencies in two contests . b . Responses of an individual to actions of its opponent . The nature of behavioural interactions between two animals can be investigated by

Table VI. Contingency Table for All Sequences of Agonistic Components Displayed by Subordinate Lemmings in Twelve Contests of Type I

A

R

C

Ak

0

D

Dg

Gr

M

T

B

Row totals

A

12

27

0

0

21

5

6

0

1

2

0

74

R

21

157

1

6

75

94

20

1

1

43

0

419

C

2

2

1

0

10

0

1

0

2

0

0

18

Ak

2

8

0

0

7

1

0

0

0

3

0

21

0

8

89

14

11

34

53

4

15

6

6

45

285

D

2

127

2

2

52

42

0

0

0

12

24

263

0

0

43

Dg

14

12

0

0

4

1

12

0

0

Gr

0

0

2

0

12

0

0

0

0

0

0

14

M

0

0

0

0

8

1

0

0

0

0

0

9

T

0

46

1

1

2

15

0

0

0

8

0

73

B

0

4

0

0

40

24

0

0

0

0

0

68

62

472

21

20

265

236

43

16

10

74

69

Column totals

1287=N



255

ALLIN & BANKS : BEHAVIOURAL BIOLOGY OF THE LEMMING

Table VU. Number of Type I Contests in which Observed Sequence Frequencies for Subordinate Animals Differ Signlfcantly* from Expected Values A

R

C

Ak

0

D

Dg

Gr

M

T

B

A

0

0

0

0

0

0

0

0

0

0

0

R

(1)

0

(1)

1

3

1

0

0

2

(1)

C

0

0

0

0

0

0

0

0

0

0

0

Ak

0

0

0

0

0

0

0

0

0

0

0

0

(1)

1,(2)

0

0

(3)

1

(1)

1

0

0

1

D

0

3

0

0

1

(4)

0

0

0

0

1

Dg

0

0

0

0

(1)

0

0

0

0

0

0

Gr

0

0

0

0

1

0

0

0

0

0

0

M

0

0

0

0

0

0

0

0

0

0

0

T

0

1

0

0

0

0

0

0

0

(1)

0

B

0

(2)

0

0

1

1

0

0

0

0

0

1,(2)

Contests in which sequence frequencies are less than expected are in parentheses 'Differences significant at 0 .05 level of confidence determining the effect of the acts of one animal on the behaviour of the other . This was accomplished in the present study by comparing the frequency with which each agonistic component, when displayed by one lemming, was followed by the display of a particular act or posture by the opponent . As for sequences displayed by an individual, 5 sec was selected as the maximum interval separating events of a sequence . Each pair of acts, performed by alternate animals and separated by a maximum time lapse of 5 sec, will be referred to as a `response-sequence' . Any act which follows within 5 sec of the display of an act by the opponent will be designated as a `response' . The frequencies with which all pairs of acts occur in response-sequences have been tabulated in contingency tables . Only data for individuals in type I contests were pooled and considered. Acts in columns of the tables are responses to the acts in rows. The row total for each act indicates the number of times the act was followed by a response, and the column total gives the number of times it occurred as a response . Expected frequencies for each responsesequence were calculated in the same manner as for sequences displayed by individuals . These values represent the frequencies which would occur if the animals acted independently of one another. A large deviation of the observed frequency from the expected value for any

response-sequence indicates a dependence of one animal's behaviour on the actions of its opponent. The significance of deviations between observed and expected frequencies was tested in each contest by means of a chi-square analysis similar to that employed for sequence displayed by individuals . Table VIII shows the frequencies of responsesequences in which the dominant animal displays the response following an act of the subordinate . Although the responses to most acts are variable, certain response-sequences occur with extremely high frequencies . Thus retreat by the subordinate animal frequently led to chase or approach by the dominant, while the adoption of a defensive posture was usually followed by a display of offensive . Defensive, however, very rarely led to defensive postures by the opponent, indicating that both animals were seldom in defensive postures simultaneously . Attack usually occurred following a display of defensive by the subordinate . Chase by definition follows retreat exclusively. Some evidence for the dependence of the dominant's behaviour on that of the subordinate is apparent from the results of the chi-square analysis in Table IX. In several contests retreat of the subordinate was followed by approach and chase more frequently than expected . Thus the probability of the dominant approaching or chasing the



256

ANIMAL BEHAVIOUR, 16, 2-3

Table VIII . Contingency Table for Responses of Dominant Animals to Actions of Subordinates in Twelve Contests of Type I

A

R

C

Ak

0

D

Dg

Gr

M

T

B

Row totals

A

12

13

0

0

16

5

8

3

2

2

0

61

R

140

29

201

48

89

8

22

18

20

43

0

618

C

1

3

0

1

4

2

0

0

0

0

0

11

Ak

0

1

0

3

3

1

0

0

0

3

0

11

81

71

4

3

16

6

45

278

0

10

37

0

5

D

65

81

0

82

280

25

18

47

8

12

24

642

Dg

13

4

0

0

1

0

0

0

0

0

0

18

Gr

0

1

0

0

0

1

0

0

0

0

0

2

M

1

4

0

0

1

5

0

0

0

0

0

11

T

2

2

0

4

4

0

0

0

0

8

0

20

B

0

0

0

0

66

2

0

0

0

0

0

68

244

175

201

143

545

120

52

71

46

74

69

Column totals

1740=N

Table IX. Number of Type I Contests in which Observed Response Frequencies for Dominant Animals Differ Significantly' from Expected Values A

R

C

Ak

0

D

Dg

Gr

M

T

B

A

0

0

0

0

0

0

0

0

0

0

0

R

3

(3)

7

(2)

(8)

(3)

0

0

1

1

(4)

C

0

0

0

0

0

0

0

0

0

0

0

Ak

0

0

0

0

0

0

0

0

0

0

0

0

(1)

1

(3)

0

(2)

3

0

(1)

0

0

1

D

(1)

2

(4)

1

5

0

0

2

0

(1)

(2)

Dg

0

0

0

0

(1)

0

0

0

0

0

0

Gr

0

0

0

0

0

0

0

0

0

0

0

M

0

0

0

0

0

0

0

0

0

0

0

T

0

0

0

0

0

0

0

0

0

0

0

B

0

0

0

0

3

0

0

0

0

0

0

Contests in which response-sequence frequencies are less than expected are in parentheses 'Differences significant at 0 . 05 level of confidence



ALLIN & BANKS : BEHAVIOURAL BIOLOGY OF THE LEMMING

subordinate increases following retreat by the latter. Conversely retreat decreases the probaability that the dominant will display retreat, offensive, defensive, or boxing . Offensive postures led to defensive rather than offensive postures, while defensive led to offensive postures . Offensive also occurred as a response to boxing more frequently than expected . The most frequent response-sequences for subordinate animals were approach-retreat, offensive-retreat, and offensive-defensive (Table X) . Thus as the dominant approached and adopted an offensive posture, the subordinate either quickly retreated or adopted a defensive posture before retreating . The subordinate also tended to retreat after being attacked . Table XI yields little information regarding the effect of the dominant's behaviour on that of the subordinate due to the small number of observations of most acts . There is, however, a suggestion of a positive association between approach and retreat and between offensive and defensive, although both sequences occurred less frequently than expected in one contest . It is also apparent that retreat occurred as a response to mount more frequently than expected . Discussion In this study lemmings were placed in a situation designed to permit the observer to

257

view agonistic interactions between two males in a neutral area . Although the effect of certain external factors, namely the actions of the opponent, on the agonistic behaviour has been examined, no attempt has been made to study the internal factors or the motivational variables involved . A comparison of the acts and postures displayed during aggressive encounters by male collared lemmings with those of a number of other rodents has been made by Allin (1966) . Amount of Fighting The presence of a strange male is sufficient to elicit chasing and attacking behaviour in at least one member of the pair . Despite this propensity for aggression, the actual time spent in fighting is but a small fraction of the period of exposure to another male . Furthermore, the animals seldom injure one another seriously . Similar results are reported for other species, although Clough (1965) observed deaths among captive Norwegian lemmings as a result of fighting . The relatively small amount of vigorous fighting is particularly striking when the size of the arena used in this study is considered . Flight in these contests was restricted and an aggressive animal had the opportunity to attack its opponent persistently . None the less, the animals typically spent a considerable amount of time engaged in solitary behaviour, namely

Table X. Contingency Table for Responses of Subordinate Animals to Actions of Dominants in Twelve Contests of Type I

A

R

C

Ak

0

D

Dg

Gr

M

T

B

Row totals

A

5

128

0

7

18

36

2

0

0

3

0

199

R

21

6

16

0

7

1

5

0

2

1

0

59

C

1

50

0

0

8

34

1

0

0

18

0

112

Ak

0

40

0

2

2

18

0

0

0

30

0

92

0

2

120

0

2

80

116

5

0

1

10

67

403

D

6

34

0

5

72

12

4

15

5

4

2

159

Dg

9

7

0

0

0

0

3

0

0

3

0

22

Gr

0

7

0

0

1

2

0

0

0

0

0

10

M

0

48

0

0

15

5

0

0

1

0

0

69

T

0

38

0

2

2

12

0

1

0

6

0

61

B

0

1

0

0

39

22

0

0

0

0

0

62

44

479

16

18

244

258

20

16

9

75

69

Column totals

1248=N



258

ANIMAL BEHAVIOUR, 16, 2-3

Table XI. Number of Type I Contests in which Observed Response Frequencies for Subordinate Animals Differ Significantly* from Expected Values A

R

C

Ak

O

D

Dg

Gr

M

T

B

0

0

0

0

(1)

0

0

0

0

0

0

A

0

3,(1)

0

0

0

R

0

(1)

0

0

(2)

C

0

1,(1)

0

0

0

1

0

0

0

0

0

Ak

0

(1)

0

0

0

0

0

0

0

1

0

0

(1)

(1)

(1)

0

(1)

3,(1)

0

0

0

0

5

D

0

0

0

0

0

(1)

0

1

0

0

0

Dg

0

0

0

0

0

0

0

0

0

0

0

Gr

0

0

0

0

0

0

0

0

0

0

0

M

0

2

0

0

(1)

0

0

0

0

0

0

T

0

0

0

0

0

0

0

0

0

(1)

0

B

0

(2)

0

0

2

1

0

0

0

0

0

Contests in which response-sequence frequencies are less than expected are in parentheses *Differences significant at 0 .05 level of confidence

exploratory and maintenance activities . This suggests partial `acceptance' of, or toleration for, the opponent, particularly on the part of the more aggressive individual . Further evidence of toleration is provided by the observed changes in amount of fighting with time . Most vigorous fighting occurred during the first 5 min of a contest, and the frequencies of chase, attack and tumble consistently showed declines from the first to the third 5-min interval . Some adjustment to the situation is made by the animals and aggression is in some way inhibited . Such toleration, coupled with individual recognition, is basic to the effectiveness of dominance hierarchies in regulating aggressiveness and allowing animals to remain together . It would, however, be incorrect to conclude that male collared lemmings are capable of living together peaceably in a confined area . In the present study contests were not extended beyond 15 min in length, and the amount of fighting over a long period of time is unknown . It is also possible that deaths might occur after some time due to a physiological change that may accompany social stress (Barnett, 1964) . The adrenal glands of aggressive as well as submissive rats tend to be enlarged as a result of hostile social interactions . Such homeostatic adjustments are characteristic of rats in strife-ridden colonies in which mortality is typically high (Barnett,

1958). The occurrence of physiological changes in male lemmings confined to a small area should be thoroughly investigated in view of their possible role in population cycles of these animals . Despite the generally small proportion of time spent in fighting throughout the contests, there was great variation among the animals in the total time spent in the performance of each agonistic component . A similar observation was made by Barnett (1958) in his study of wild rats . The amount of fighting displayed by each pair of lemmings is thus subject to a great deal of variation, yet certain similarities are apparent from the consistent patterns of behaviour observed in the three types of contests . Relatively little agonistic behaviour occurred in contests of type II when compared with those of type I and type III . This was particularly true of the more vigorous forms of fighting, namely chase, attack and tumble . Contests of type I were characterized by a large disparity in the aggressiveness of the two combatants . In type II contests neither animal displayed much aggressive behaviour, and although the active individual did tend to initiate most of the contacts between the pair, the opponent was rarely attacked . Conversely, in contests of type III both animals exhibited aggressive tendencies, one individual performing high frequencies of chase and the



ALLIN & BANKS : BEHAVIOURAL BIOLOGY OF THE LEMMING

other attack. The reasons for such great variation in the aggressiveness of individuals are not clear. Animals may be thought of as possessing different thresholds for aggressive response . The factors known to influence aggressiveness in mice have been reviewed by Lagerspetz (1964) . Genetic variation has been shown to be of importance, the existence of strain differences being well documented . The hormonal support of aggressive behaviour has also been demonstrated . Variation in endocrine output may thus be responsible for differences in thresholds for aggression . Another important variable is the past experience of the individual . Ginsburg & Allee (1942) found that dominance relationships in mice are largely maintained by conditioning . Dominant animals experimentally subjected to severe attacks by more aggressive individuals eventually became submissive, while subordinate animals could be trained to be aggressive . Since in the present study certain individuals were exposed to the fighting situation on several occasions, it seems likely that the aggressiveness of such animals was to some degree affected by previous experience in the arena . Experiences in early periods of development may also affect adult behaviour . In the absence of experimental evidence concerning the influence of these factors on aggressiveness in collared lemmings, the extent to which such factors were operative in the present study is unknown . It was found that both dominant and active animals initiated many contacts with the opponent in contests of types I and II, respectively . The behaviour of these animals subsequent to approaching differed greatly . The sequential analysis indicated that dominant animals tended to adopt offensive postures and then commonly attacked the subordinate. Active males tended only to retreat after approaching the opponent . It seems likely that this difference in behaviour was partly due to the difference in responses of subordinate and inactive animals . Response frequencies for subordinte animals indicated that these individuals frequently retreated following an approach by the dominant. They also commonly adopted defensive postures before retreating. Contrary to this, inactive animals less often retreated and at times adopted offensive postures . There was a great difference in the general deportment of these animals throughout the contests . Inactive individuals displayed much less avoidance behaviour and indeed exhibited very little agonistic behaviour of any kind . They often tended to remain in one place for long

259

periods of time and were generally inert . Lagerspetz (1964) found that mice which behaved very passively evoked relatively little aggressive behaviour in their opponents . She also demonstrated that movement of the opponent acted as a releasing stimulus for attack . It is thus, possible that the impassivity of the inactive animal was largely responsible for the lack of aggressive behaviour exhibited by active individuals . In contests of type III the attacker usually retreated or adopted a defensive posture after being chased . It sometimes attacked the approaching animal as well . This tendency towards active response may in turn have stimulated the chaser to behave more aggressively . Only two of twenty-one encounters were classified as type III contests . It was thus uncommon to find that both individuals of a pair displayed much aggressive behaviour . It would seem likely that had the duration of these contests been extended past 15 min . a dominancesubordination relationship would have emerged . This is suggested by the fact that the frequency of chase remained fairly high throughout these contests, while the number of attacks progressively declined . Thus the chaser continued to behave aggressively whereas the attacker did not, an indication that the chaser was, in fact, emerging as the dominant animal . Relationships between Components of Agonistic Behaviour The behaviour of an individual at any time is to some extent dependent on antecedent social events . Such dependencies in lemming behaviour are clear from the results of the statistical analyses of both sequences (two-act sequences by one individual) and response-sequences (twoact sequences between two individuals) . A lemming's actions at any particular moment are thus partly dependent on its own antecedent behaviour, partly on that of its opponent . These events are of course interrelated since the opponent's actions are also influenced by the animal's previous behaviour . It has been shown that certain agonistic components tend to occur together in sequences more frequently than would be expected if acts were being displayed in a random order . Such relationships provide evidence of affinities between the acts . Conversely, certain acts and postures occur together less frequently than expected, and possess a negative association. It is conceivable that still other acts might have no influence on the subsequent behaviour of the



260

ANIMAL BEHAVIOUR, 16, 2-3

individual . These acts would then be followed by a random distribution of events . It was not possible to identify acts of this type in the present study, however, due to the small number of observations of some acts, which in many cases precluded any demonstration of either positive or negative associations . Nevertheless, relationships between components where testable were very consistent. Affinities between certain acts are evident throughout the contests . Offensive and attack are strongly correlated, as are defensive and retreat . Offensive postures are also associated with approach, groom, boxing and chase. Conversely, displays of offensive, defensive and retreat are negatively correlated among themselves . In addition, offensive and retreat are negatively associated . Offensive and defensive thus tend to occur in somewhat different contexts, the latter usually being associated with avoidance behaviour . These results are similar in many respects to those of Grant (1963) for the rat . He proceeded to devise a motivational model based upon opposing drives, in which each posture reflected certain levels of these drives . In general, approach and retreat showed a strong positive relationship in these contests . The dominant, the active animal, and the chaser all tended to approach after retreating . As mentioned previously, subsequent behaviour differed greatly. Active animals and the chaser frequently retreated once more, while dominant animals tended to adopt offensive postures. Despite such large variation in the `choice' of response, no serious contradictions in the associations between acts and postures were found . The relationships between components of agonistic behaviour thus possess a considerable degree of stability, as would be expected if they reflect certain internal states of the animal . The frequency of tumble was in general too low to allow its relationship to the other acts to be demonstrated, although it usually occurred following an attack or simultaneous chase and retreat of the two agonists . Similarly, no conclusion can be drawn regarding the relationships of dig or mount to other agonistic components . Communication during Paired Encounters That the behaviour of one animal can influence the behaviour of another is fundamental to the study of social behaviour . Communication of information between animals enhances their ability to behave in a manner appropriate to the requirements of a given situation . Fight-

ing in a non-competitive context is effective in regulating living space only if the actions of each individual serve to repulse others from the immediate area. At the same time, certain behaviours must act to inhibit aggression in others if a group of animals is to remain together . Some suggestion of communication between lemmings was provided by the lack of stereotypy in the durations of individual displays . With the exception of attack, no acts or postures were found to be rigidly timed . The variation was particularly great for offensive and defensive postures . It seems likely that this variation in part reflects the information which the animal receives from its opponent . An obvious illustration of this effect is the dependence of chase on the duration of the opponent's retreat . In order to investigate the actual effect of each act and posture on the behaviour of the opponent, the interactions between animals must be examined quantitatively . A communicatory function can be ascribed to an act or posture only if it can be shown to be followed by a change in the opponent's behaviour . This study has attempted to detect communication of information to the opponent by determining what statistically significant changes occur following the display of each agonistic component. No assumptions have been made as to the mechanism by which these components affect the opponent's behaviour. Consequently, they have not been referred to as `releasers' . Certain response sequences were found to occur consistently with frequencies greater than expected . Retreat by an animal was followed by approach or chase of the opponent . Conversely, retreat did not lead to retreat, offensive, defensive or boxing . The opponent thus tended to initiate further contact between the pair following a retreat by the animal . This result is in accord with those reported by Scott & Fredericson (1951) for mice and rats . In their survey of behaviour which evokes aggression, these authors state ' . . . The sight of an animal running away also appears to be effective' . Several other acts were also frequently followed by statistically significant changes in the opponent's behaviour . Approach often led to retreat, while boxing was followed by offensive . Although occurring in but a few contests, mount tended to be followed by a retreat of the opponent. One of the most consistent relationships found was that between offensive and defensive postures. Each of these components led to the other



ALLIN & BANKS : BEHAVIOURAL BIOLOGY OF THE LEMMING

but not to itself. Thus the animals tended not to be in offensive or defensive postures simultaneously, the adoption of one being followed by a display of the other by the opponent . Several acts, including chase, attack and tumble, could not be shown to influence consistently the behaviour of the opponent . Since these are the most vigorous components of agonistic behaviour, it might be expected that they would have a substantial effect in determining the nature of subsequent events . The generally low frequencies with which these acts occurred in each experiment, however, precluded the demonstration of their communicatory function . It is, of course, possible that an act might not effect any change in the opponent, or that the effect might not be expressed immediately . Thus a behaviour pattern might transmit information to the opponent but affect only the results of later interactions . Such influences would not be revealed by analysis at the two-act level. Despite the paucity of information concerning the effect of certain acts, the present study has provided quantitative evidence of the communicatory function of the majority of components . Such knowledge is valuable in that it enables social behaviour to be predicted . The accuracy of these predictions depends upon the completeness of descriptions of behavioural interactions, as well as the consistency of behaviour in the species . Sequences of the type demonstrated in this study, where the probability of an event is determined by the nature of the preceding act, are known as first-order Markov chains (cf . Nelson, 1964) . This is the simplest type of dependency and may incompletely describe the nature of interactions between lemmings. It is possible that dependencies of a higher order exist, that is, that an animal's behaviour is determined not only by the immediately preceding event, but also by still earlier events . In his study of the stochastics of communication in rhesus monkeys, Altmann (1965) carried the analysis of temporal patterning through sequences of four acts . Each successive analysis of a higher order further decreased the uncertainty in predictions of behaviour . Nelson (1964) investigated the effect of the penultimate antecedent event on behaviour displayed by a glandulocaudine fish, Corynopoma riisei. He concluded that in this species the probability of occurrence of an act is dependent only upon the nature of the immediately preceding event . The present study has dealt only with two-act E

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sequences . The number of longer sequences in each 15-min contest was typically small, precluding statistical analysis of sequences greater than two-acts in length . It would seem likely that dependencies of a higher order exist for lemmings . Some suggestion of the influence of the penultimate antecedent event is provided by the results of the sequential analysis for individuals . It was found that an animal's behaviour is partially dependent upon its immediately preceding behaviour . This indicates that the context in which the opponent acts is also of importance in determining present behaviour. Thus it would appear that acts preceding the ultimate antecedent event also influence a lemming's behaviour . Finally, it must be emphasized that the agonistic behaviour studied here is effective essentially through the modalities of vision and touch . It is conceivable that the communicatory function of certain acts or postures may be partly dependent on means of perception other than sight and touch . Thus, olfactory and auditory communication might also be of importance . Some of the variation seen in response to various acts could be due to variations in the information received through these senses . Variation could also result from subtle differences in visual signals which are not detected by the human observer . It will be clear that the methodology employed in the present study permits of only an incomplete analysis of communication, and further investigations are essential to an understanding of the complexities involved . Summary 1 . Agonistic behaviour displayed by male collared lemmings, Dicrostonyx groenlandicus (Traill), was studied by means of observations of paired encounters in a neutral arena . Cinematography was employed in order to facilitate a structural analysis of the behaviour . 2 . Eleven major components of agonistic behaviour were described and recorded quantitatively . The recording system allowed both the duration and frequency of components to be recorded and the sequential nature of these events to be investigated . 3 . Fighting invariably occurred following brief investigatory activity . Aggressive responses were evoked rapidly, but the cues eliciting attack are unknown . Actual time spent in aggression was small, and injuries of a serious nature were rare . The incidence of vigorous fighting typically



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ANIMAL BEHAVIOUR, 16, 2-3

decreased with time, indicating some degree of tolerance for the opponent. 4 . Little evidence of any rigid timing in the display of acts and postures was obtained . It was suggested that the observed variability in display durations reflected the dependence upon the opponent's behaviour . 5 . Significant differences between combatants in the frequencies of chase and attack displays were employed as criteria for the existence of dominance-subordination relationships . Such relationships were demonstrable in 12 of 21 recorded contests . Large interindividual variation in aggressiveness was observed, although rarely were both animals extremely aggressive . It was postulated that the extreme passivity of certain animals had an inhibitory effect on aggression in their opponents . Other factors with possible influence on individual aggressiveness are discussed . 6 . Relationships between agonistic components were investigated by means of an analysis of their distribution in time . Certain two-act sequences occurred with frequencies significantly greater than expected, indicating affinity between approach and retreat, defensive and retreat, and between offensive and the acts approach, groom, boxing and chase . Contrary to this, a negative association existed between offensive and retreat, and between displays of offensive, defensive and retreat. 7 . Communication between animals was evident from the significant changes in the opponent's behaviour which followed the display of various agonistic components . Certain acts and postures had consistent effects on the opponent's actions . Retreat was followed by approach or chase but not by retreat, offensive, defensive or boxing . Approach and mount led to retreat by the opponent, and boxing was followed by offensive . Offensive and defensive postures led to each other, but not to themselves . 8 . It was found that an animal's behaviour at any time is partly determined by the opponent's antecedent display, although dependencies of a higher order may exist . Present behaviour is also influenced by the individual's preceding action, indicating that the context in which the opponent's display occurs is of importance in determining the individual's response .

Acknowledgments This study was supported, in part, by the National Research Council, Canada, the National Science Foundation and the Society of the Sigma Xi . It represents a portion of a thesis submitted by John T. Allin in partial fulfilment of the requirements for the M .A . degree at the University of Toronto . We acknowledge the helpful criticisms provided by Dr John A . King and his colleagues, Michigan State University . Dr A . W . Ghent, School of Life Science, University of Illinois, was consulted on statistical procedures used in this study . REFERENCES Aho, J . & Kalela, O . (1966). The spring migration of 1961 in the Norwegian lemming, Lemmus lemmus (L .), at Kilpisjarvi, Finnish Lapland . Ann. Zoo!. Fenn ., 3, 53-65 . Allin, John T. (1966) . Agonistic behaviour in the varying lemming, Dicrostonyx groenlandicus (Tr.), Master's thesis on file, Library of the University of Toronto . Altmann, S. A . (1965) . Sociobiology of rhesus monkeys . II : Stochastics of social communication . J. theoret. Biol., 8, 490-522. Barnett, S . A . (1958) . An analysis of social behaviour in wild rats. Proc. zoo!. Soc. Lond., 130, 107-152 . Barnett, S. A . (1964). Social stress. Viewpoints Biol., 3, 170-218 . Clough, G. C . (1965). Lemmings and population problems . Am. Scientist, 53, 199-212. Collett, R. (1895) . Myodes lemmas, its habits and migrations in Norway. In Christiana VidenskabsSelekabs Forhandlinger 1895, No . 3. Ginsburg, B . & Allee, W. C. (1942). Some effects of conditioning on social dominance and subordination in inbred strains of mice. Physiol. Zool., 15, 485-506. Grant, E. C. (1963). An analysis of the social behaviour of the male laboratory rat. Behaviour, 21, 260-281 . Hall, E . R. & Kelson, K. R. (1959). The Mammals of North America. 2 vols . New York : Ronald Press . Krebs, C. J. (1964) . The lemming cycle at Baker Lake, Northwest Territories during 1959-62 . Arctic Inst. N. Am . tech . Paper No. 15. Lagerspetz, Kirsti (1964) . Studies on the aggressive behaviour of mice . Ann . Acad. Sci. Fennicae, Ser. B ., 131, 1-131 . Nelson, K . (1964). The temporal patterning of courtship behaviour in the glandulocaudine fishes (Ostariophysi, Characidae) . Behaviour, 24,90-146. Scott, J. P . & Fredericson, E . (1951) . The causes of fighting in mice and rats. Physiol. Zool., 24, 273-309. (Received 10 February 1967 ; revised 2 August 1967 ; Ms . number: A556)