Agonistic behaviour in males of five species of voles Microtus

Anirn. Behav., 1973,21, 471--480 AGONISTIC

BEHAVIOUR

IN MALES

OF FIVE SPECIES

OF VOLES

MICROTUS BY DALLAS V. COLVIN* Department of Biology, University of Colorado, Boulder, Colorado 80302 Abstract. Agonistic behaviour of Microtus pennsylvanicus, M. montanus, M. californicus, M. longicaudus, and M. ochrogaster was observed in 160 staged encounters; a natural observation of sympatric species is included. No difference in the character and movements of agonistic behaviour was apparent when arena size was reduced; only a difference in the frequency of postures and movements was observed. In the smaller arena, M. montanus and M. ochrogaster exhibited a significant increase in frequency of agonistic components. The other three species did not show a significant increase. In interspecific pairings, M. montanus won over M. pennsylvanicus, M. californicus and M. longicaudus; M. ochrogaster won over M. montanus and M. pennsylvanicus. Three species used mutual avoidance in maintaining individual distance. Despite the widespread and often overlapping distribution~of the various species of the mammalian genus Microtus and the possible role of agonistic behaviour influencing ecological distribution if not geographic distribution, this study is the first attempt .to execute a controlled, careful comparison of the agonistic behaviour of five species of Microtus. In all, the distribution of these five species, M. pennsylvanieus, M. montanus, M. californicus, M. longieaudus, and M. oehrogaster, includes nearly all of North America north of Mexico, with the exception of the extreme south and south-eastern portions of the United States (Hall & Kelson 1959; Burt & Grossenheider 1964). Previous investigations of behaviour of these five species of Mierotus have lacked consistency. Investigators have employed a wide variety of methods and typically have compared only two species under similar conditions (Getz 1962; Murie 1963, 1969; Miller 1969; Novak & Getz 1969; Krebs 1970; Robert Stoecker, personal communication). However, Cruzan (1968) compared the aggressive behaviour of three species, while Louch (1956), Martin (1956) and Tamura (1966) observed only one of the five species. In addition to a variety of methods and species combinations, the effects of olfactory cues, weight of individuals, pregnancies, and oestrous cycles on agonistic behaviour have often been woefully neglected in experimental designs. In addition to presenting the first comparison of agonistic behaviour of these five species, this study reports an observation of a natural *Present address: Department of Biological Sciences, California State College, Dorninguez Hills, California, 90747, U.S.A.

encounter by two males of two sympatric species and attempts to answer several important questions confronting investigators of agonistic behaviour in the laboratory (Banks & Fox 1968). Does agonistic behaviour as observed in the laboratory under controlled conditions actually occur in natural populations? Can one project the results of laboratory studies to natural environments, or are the laboratory results artifacts of captivity? How does the intensity of behaviour in nature compare with the intensity of behaviour in the laboratory? What effect does confinement as represented by the size of the enclosure have on agonistie behaviour? Finally, are there differences in agonistic behaviour among dosed related species of Microtus?

Methods Subjects The original stock of animals used in this study was live-trapped in the summer and autumn of 1968. The meadow vole, Microtus pennsylvanicus was taken from a swampy area at an elevation of 1570 m on the east side of Boulder Reservoir near Boulder, Colorado. The montane vole, M. montanus was caught near Magnolia, west of Boulder, in a large mountain meadow at an elevation of 2455 m. The California vole, M. californicus was trapped in a tidal salt marsh at the northern city limits of San Diego, California. The long-tailed vole, M. longicaudus, was trapped on the rocky bank of Boulder Creek, 19 km west of Boulder, at an elevation of more than 2135 m. The prairie vole, M. ochrogaster, which occupies a relatively dry 471

472

ANIMAL

BEHAVIOUR,

habitat, was trapped at the mouth of Left Hand Canyon, north of Boulder, Colorado, at an elevation of 1714 m. Only adult males were used in this study in order to eliminate the possible complicating behavioural factors associated with pregnancy or the oestrous cycles in females (Sadlier 1965). These males were either part of the original stock or their first generation offspring reared in our breeding colony (Colvin & Colvin 1970). Only wild stock or their first generation descendants were used in order to minimize possible detrimental effects of inbreeding. Adult males from the field and laboratory stocks were randomly selected and housed in separate cages, 18 x 24 • 18 cm. The subjects were fed lettuce, rolled barley, mouse chow, and water ad libitum. These males were kept under similar conditions of food, light, and temperature as males in the breeding colony and therefore, they were in breeding condition at the time of the tests.

Enclosures Two different sizes of circular metal enclosures were used for observing the agonistic behaviour of the voles. The circular shape was selected to eliminate corners and to reduce positional cues. The smaller enclosure was 0.46 m in diameter; the enclosure was large enough to allow one animal to avoid coming in contact with another. The larger enclosure was 1.27 m in diameter. This size was selected in an attempt to use a relatively large enclosure but to keep the animals in sight of one another. These small and large enclosures provided areas that were two-and-one-half and nineteen times larger, respectively, than the area of a 20-1itre container, such as the one used by King (1957) and Getz (1962) in their work. The interior surfaces of the walls were painted a dull white to allow the postures and movements of the voles to be more easily seen. The floor coverings of both enclosures consisted of layers of heavy plastic covered by several layers of newspapers. The plastic and newspapers were held firmly in place by the weight of the metal walls. Several precautions were used to minimize olfactory cues in the enclosures and to make the areas as neutral in odour as possible. Before every observation of both single and paired voles, the walls of the enclosures were cleaneff with both detergent and alcohol. The newspapers on the floor of the enclosures were replaced before every observation, and the plastic

21,

3

layer below the newspaper was cleaned when necessary. Since I considered the possibility that familiarity with a particular area might influence the outcome of the contests, encounters were staged in enclosures equally familiar to both animals (AUin & Banks 1968). Prior to the simultaneous introduction of both animals into an enclosure, each animal was introduced into the enclosure alone for an equal length of time. During this time the behaviour of each solitary animal was recorded for use as a baseline for comparison later when the animals were paired.

Sampling Method Two types of agonistic encounters, intraand interspecific, were staged in the small enclosure. The purpose for observing the intraspecific encounters was to determine the nature of agonistic encounters between conspecific males and to compare the agonistic behaviour of males of different species. Interspecific encounters were staged to determine the winner of agonistic encounters between different species. Only those species were paired which could possibly be in contact in nature. Thus M. montanus and M. longicaudus were paired since they occur sympatrically over a large part of their range (Cruzan 1968). The second combination, M. pennsylvanicus and M. ochrogaster, were paired since they are often sympatric, even though M. pennsylvanicus typically inhabits a wet area and M. ochrogaster a drier area (Getz 1962; Cruzan 1968). Although M. pennsylvanicus and M. montanus are not sympatric in Boulder County (Cruzan 1968), the distributions of the two species overlap farther north in the Rocky Mountains (Hall & Kelson 1959). The species involved in the fourth combination, M. montanus and M. ochrogaster, have not been reported as sympatric, but from their distributions (Hall & Kelson 1959) it is possible the two species in question meet where the prairie meets the mountains in Colorado and Wyoming. The species of the fifth combination, M. montanus and M. californicus, appear to be sympatric i n California and southern Oregon (Bailey 1900; Anderson 1959; Hall & Kelson 1959; Murray 1965). A total of 120 bouts, both intra- and interspecific, were held in the small enclosure. Twelve bouts were staged between members of the same species; hence, since there were five species, a total of sixty intra-specific encounters was observed. For the interspecific bouts, there were

COLVIN: AGONISTIC BEHAVIOUR OF VOLES

five interspecific pairings with twelve bouts staged for each pairing, giving a total of sixty interspecific encounters. The contestants were weighted prior to the encounters and three weight classes, light, medium, and heavy were established for each species (Table I). For the interspecific bouts, the following procedure was used. For half of the bouts, the animals were paired light with light, medium with medium, and heavy with heavy. In the rest of the encounters, the difference in weight of the paired animals was less than 2 g. This procedure was an attempt to minimize the effect of weight differences on the outcome of encounters. For the intraspecific bouts, similarly, half of the animals were paired light with light, medium with medium, and heavy with heavy. In the rest of the intraspecific encounters, animals of various weight differences were paired. Table L Weight in Grams of the Three Weight Classes

Used in Pairing Species of Microtus in Agonistie Encounters Species

Liglat

Medium

Heavy

M. pennsylvanicus

45-60

60-65

65-97

M. montanus

34--45

45-60

60-74

M. californicus

54-60

60-75

75-88

M. longicaudus

30-35

35--40

40--47

M. ochrogaster

39-45

45-55

55-63

For the second portion of my study, the results of encounters staged in both large and small enclosures were compared. This comparison was done to determine the effects, if any, of the area of the enclosure on agonistic behaviour. Most previous investigators used a wide variety of sizes of enclosure. For this part of the study, forty out of a total of 120 different pairings were selected prior to their actual observation in either enclosure. From each of the five interspecific combinations, four bouts were selected at random to be staged in both the large and small enclosures. Thus, a total of twenty interspecific pairings were staged in the two sizes of enclosures. Similarly, four pairings were selected at random from each of the five sets of contests among members of a species. Hence, twenty intraspecific bouts were also staged in both enclosures. Two precautions minimized the effects of sampling bias or prior experience of the subjects on the outcome of an

473

encounter. First, the pairings that were observed in both the large and small enclosures were selected before any observations were made: Second, of those encounters staged in both large and small enclosures, half were staged in the large enclosure first, while the other half were staged first in the small enclosure. Procedure All encounters were staged between 18.00 and 23.00 hours. During this time of day disturbances from other activities in the area of the research facilities were minimal. Room temperature during the observation was 20 ~ to 25~ The room was dark and the enclosures were dimly illuminated by a 100-W red bulb, centred 2.4 m above the floor of the enclosure. The introductions of the subjects were made with a minimum of disturbance to the animals. The subjects were allowed to walk into 1-1itre glass containers placed in their cages, and then they were introduced into the enclosure by slowly tilting their container just above the floor of the enclosure. For each encounter, both introductions were made in a similar manner, near the edge of the enclosure but 180~ apart. The encounters were timed with a stop-watch from the moment of the introduction of the voles into the test situation. Records of behaviour were made simultaneously for both animals on the one recorder. The frequency and duration of each component of the animals' behaviour and the amount of locomotor activity were recorded. The chart speed of the recorder was set at 15 cm per rain; at this speed the duration of each entry could be read easily to the nearest second. Encounters lasted 5 rain and during each encounter, two observers recorded the frequency and duration of the movements and postures. Each observer watched and recorded the behaviour of one vole. Many previous studies indicated that one observer watched both animals simultaneously. However, under those conditions accuracy is difficult to attain because during agonistic encounters the postures and movements of rodents are often fast. While observing a series of interspecifie contests, the investigators watched different species on successive observations to minimize the effect of any difference in recording techniques. The voles were identified during the encounters by individual characteristics (e.g. a crooked tail) and by size. No pelage markings, ear tags, or clipping of toes were required to identify in-

474

ANIMAL BEHAVIOUR,

dividua!s. Individual identification was easily double checked by weighing the vole in his glass container both before and after an encounter.

Components of Agonistie Behaviour The classification of agonistic behaviour components developed in a study of the collared lemming (Allin & Banks 1968) was used: (i) Approach: movement of the entire body or stretching in the direction of an opponent with attention focussed on the opponent; had to be initiated within approximately 15 cm of the opponent. (ii) Offence: body with its axis parallel to the floor, braced with its head toward the opponent's head; initiated within approximately 15 cm of the opponent and involved a lack of physical contact from a stationary position. (iii) Attack: a sudden lunge toward an opponent initiated within approximately 15 cm of the opponent; often involved biting; however, actual contact was not necessary. (iv) Chase: following rapidly behind a retreating animal. (v) Defence: animal balanced on his tail and hindlegs holding his forefeet off the floor; might lean toward or away from its opponent. (vi) Retreat: rapid escape usually after an attack or threatened attack by the opponent; mutual or one animal alone might be involved; had to be initiated within approximately 30 cm of its opponent. (vii) Vocalization: an audible cry. (viii) Box: both animals were in an upright position and facing each other, while balanced on their hind feet and tail; both used their forefeet to strike at their opponent's head and shoulder region. (ix) Wrestle: both animals engaged; might be at right angles to each other or head to tail; typically the action is rapid, with animals rolling about and neither standing on his feet; rump was often the site of injury, if any. Determining the Winner The winner of each contest was determined immediately following the contest. Two criteria were used. First, and most important for the winning animal, the record must show more locomotor activity than for the losing animal. Locomotor activity was defined as locomotion about the enclosure not associated with any behavioural component listed above. Second, and in addition, the winning animal must have exhibited a higher total number of approach,

21,

3

offence, chase, and attack movements or postures than its opponent. If either observer was in doubt regarding which animal was the winner, the contest was considered undecided.

Results Comparison of M. montanus and M. longlcaudus Under Controlled and Natural Conditions Field observations. On 17 September 1968 I observed an agonistic encounter between two males of sympatric species of Microtus under natural conditions. This observation occurred early in the afternoon along Boulder Creek, 19 km west of Boulder, Colorado, while I was ~valking in the stream bed looking for trapping areas along the bank. The stream bank was covered with large boulders and sparse clumps of shrubby vegetation. Little grass or undergrowth occurred at this location; hence little obstructed my view of the bank. The top of the bank was about eye-level. From where I was walking I could see the bank clearly. In this position, I observed five components of agonistic behaviour in two free-ranging individuals, namely, vocalization, chase, retreat, attack, and wrestle. Loud cries and rapid movements of the animals first attracted my attention. When they were 3 m away, I clearly observed two voles running along the bank toward me. The animals appeared completely oblivious to my presence. I saw that the vole nearest me was retreating rapidly from a second vole following close behind and obviously chasing him. In front of me, the chasing vole attacked the first vole from behind, and the two microtines began to wrestle. Locked together, they tumbled down the slope to within centimetres of my feet. I collected them while they were still wrestling. The two microtines were identified by morphological criteria as an adult male M. montanus and an adult male M. longicaudus. The M. longicaudus was bleeding from several wounds in the rump; the M. montanus was chasing the M. longicaudus and, although it was impossible to determine the winner because I observed the encounter only briefly, it seems likely from the injuries sustained by M. longicaudus that M. montanus was the winner. The animals were not weighed immediately after capture, but the M. rnontanus appeared larger than the M. longicaudus. Based on weight comparison of other specimens of the two species in the laboratory, the weight difference between the two contestants was estimated to be between 10

COLVIN: AGONISTIC BEHAVIOUR OF VOLES a n d 20 g. This weight difference was n o t u n reasonable for the two species (Table I). Laboratory observations. I n this p o r t i o n o f m y study, a total of twelve interspecific encounters were staged i n the small enclosure between eight M . rnontanus a n d eight M . longicaudus. I n those encounters i n which there were winners, M. montanus w o n nine out of eleven times. This was significant at a probability level o f less t h a n 0.05 (chi-square test for homogeneity, Z 2 = 4 . 4 5 ) . T h e frequencies o f occurrence o f the different c o m p o n e n t s of agonistic b e h a v i o u r a n d the a m o u n t of locomotor activity for interspecific contests between M . montanus a n d M . longicaudus are recorded in Table II. The w i n n e r of each encounter is indicated by the letter 'w'. Since wrestle a n d box involved b o t h

475

animals, the totals of these c o m p o n e n t s are repeated in the table. It is interesting to note that the five c o m p o n e n t s observed in the field encounter, namely, vocalization, attack, chase, retreat, a n d wrestle, are associated with decided contests i n the laboratory.

Comparison of Agonistlc Behaviour in Large and Small Enclosures Interspedfic encounters. Two interspecific encounters, namely, M . montanus versus M. longicaudus a n d M . rnontanus versus M . ochrogaster, showed significantly higher c o m p o n e n t frequencies i n the small enclosure t h a n in the large enclosure (Table III). The probabilities were P < 0 . 0 0 5 (Wilcoxon test) a n d P < 0 . 0 5 (Walsh test), respectively.

Table H. Outcome, Frequency of Behavioural Components,and Duration of Locomotion in Twelve Contests Staged in the Smaller Enclosure Between M. montanus and M. Iongicaudus Species M. montanus 34. longicaudus

Weihtg Component frequency Outcome (in g) Approach Offence Attack Chase Defence Retreat Vocal Wrestle Box w

M. montanus M. longicaudus

DuratiOnof loeomotion (S)

38"3 32.3

5 6

0 7

0 5

0 1

1 0

8 1

0 4

0 0

0 0

25 39

43"6 33-6

1 0

0 0

0 0

0 0

0 0

1 0

0 0

0 0

0 0

4 4

M. montanu~' M. Iongicaudus

w

67.4 42"8

20 0

12 2

6 0

14 0

1 34

2 27

0 11

16 16

0 0

67 2

Mr. montanus M. longicaudus

w

58-6 38-6

t0 0

0 0

0 0

0 0

0 0

0 2

7 5

0 0

0 0

75 6

M. montanus M. longicaudus

w

57-9 36.7

1 0

0 0

0 0

0 0

0 0

2 0

2 0

0 0

0 0

94 14

M. montanus

w

45"0 43"9

10 10

21 0

13 0

8 0

0 13

3 18

0 7

5 5

0 0

57 29

w

39"2 40.9

43 0

5 0

2 2

6 0

0 34

4 29

0 27

1 1

0 0

148 10

38"3 39"9

1 6

0 2

0 5

0 5

10 1

10 1

0 9

3 3

0 0

38 40

M. longicaudus M. montanus M. longicaudus M. montanus M. longicaudus

w

M. montanus M. longicaudus

w

39:2 39.4

28 0

8 0

0 9

0 0

1 23

14 27

0 33

0 0

1 1

123 8

M. montanus M, longicaudus

w

65"8 43"9

29 0

8 0

0 1

0 0

2 40

13 14

5 5

0 0

0 0

160 8

M. montanus M. longicaudus

w

43"6 43"9

4 0

1 0

1 0

0 0

0 2

0 2

1 2

0 0

0 0

35 19

M. montanus M. longicaudus

w

39"2 39.9

16 6

0 1

0 4

1 0

4 0

18 3

4 2

0 0

1 1

49 27

ANIMAL

476

BEHAVIOUR,

Table HI. Frequencies of Behavioural Components Observed During Contests Between Species of Microtus in Both Large and Small Enclosures

21r montanus vs M. longicaudus

M. montanus vs M. ochrogaster

Large

Small

Large

Small

28

77

40

72

Offence

9

14

25

52

Attack

0

6

19

39

Chase

0

6

14

0

Defence

7

78

9

12

Retreat

28

64

45

71

Component

Approach

Vocalization

1

40

3

0

Box

0

2

0

2

Wrestle

0

0

0

0

P<0.005

P<0.05

In contrast, the two interspecific combinations involving M . pennsylvanicus and the one interspecifie combination involving M. californicus produced no significant difference in component frequencies between large and small

2t,

3

enclosures (Table IV). Here using the Wilcoxon test, none of the three combinations were significant at the 0.05 level. lntraspecifie encounters. In the intraspecific bouts for M . montanus, M . californicus, and M . ochrogaster (Table V), all three species showed significant increases in the frequencies of components in the small enclosure, P < 0 . 0 1 (Wilcoxon test), P=0.031 (sign test), and P < 0 . 0 1 (Wilcoxon test), respectively. In contrast, the intraspecific encounters of M. pennsylvanicus and M . longicaudus showed no significant increase in component frequencies in the small enclosure (Table VI). Using the Wilcoxon test, the P-values were not significant at the 0.05 level. Comparison of postures and movements. Perhaps the most significant finding in the com-

parison o f observations in large and small enclosures was in the comparison of the postures and movements in these two sizes o f enclosures. There was no apparent difference in the character of the postures and movements in the large and small enclosures. Intra- and Interspeeific Agonistic Behaviour Under Controlled Conditions

The results of the five interspecific combinations (Table VII) show that M . montanus won significantly more contests than M . pennsyh'an-

Table IV. Frequencies of Behavioural Components Observed During Contests Between Species of Mierotus in Both Large and Small Enclosures ,

L

i

,

i

iF,,

,

M. pennsylvanicus

M. pennsylvanicus

VS

M. montanus

VS

M. montanus

Component

VS

AI. ochrogaster

M. californieus

Large

Small

Large

SmaU

Large

Small

Approach

20

15

13

12

23

56

Offence

15

6

2

2

4

5

Attack

1

0

I0

1

3

9

Chase

2

0

0

I

I

0

Defence

13

10

17

7

0

9

Retreat

21

24

17

8

20

56

Vocalization

8

11

0

1

0

5

Box

0

0

0

0

0

0

Wrestle

0

0

0

0

8

0

P>O.O5

P>O.05

P>O.05

COLVIN:

AGONISTIC BEHAVIOUR OF VOLES

477

Table V, Frequencies of Behavioural Components Observed During Intraspecifie Contests Among Species of Microtus in Both Large and Small Enclosures

Component

M. montanus

M. californicus

M. ochrogaster

Large

Small

Large

Small

Approach

28

71

0

2

10

40

Offence

16

55

0

1

3

9

Attack

0

15

0

8

7

34

Chase

6

1

0

0

6

2

Defence

6

64

0

0

7

36

Retreat

31

68

0

I0

10

41

Vocalization

7

117

0

2

0

24

Box

0

0

0

0

0

4

Wrestle

0

4

0

0

0

0

P<0"01

P=0"031

Table VL Frequencies ot Behavioural Components Observed During Intraspeciiic Contests Among Species of Microtns in Both Large and Small Enclosures

Component

M. pennsylvanicus

M. longicaudus

Large

Small

Approach

5

7

12

24

Offence

1

3

2

0

Attack

0

0

0

0

Chase

0

0

6

8

Defence

3

6

2

15

Retreat

1

2

15

46

Vocalizatioa

0

0

0

18

Box

0

0

0

0

Wrestle

0

0

0

0

P>O.05

Large

Large

Small

P>0.05

icus, M . californicus, a n d M . longicaudus; the chi-square tests o f h o m o g e n e i t y for these results were significant ( Z 2 = 5 . 4 4 , P < 0 . 0 2 ; Z2=8.00, P<0.01; Z2=4,45, P<0.05, respectively). I n two o t h e r interspecific c o m b i n ations, M . ochrogaster w o n significantly m o r e contests t h a n M . pennsylvanicus a n d M . montanus. T h e chi-square values for the c o m b i n a t i o n s

Small

P<0'01

were, respectively: Z 2 = 4 . 5 , P < 0 . 0 5 ; Z 2 = 7 " 3 6 , P < 0 . 0 1 . I n s u m m a r y , in all five interspecifie c o m b i n a t i o n s , the results were statistically significant at the 0.05 level o f p r o b a b i l i t y , with one result significant a t the 0-02 level a n d two results highly significant a t the 0.0I level o f p r o b a b i l i t y (Siegel 1956). Table VII. Frequencies of Decided Contest Winners in Sixty lnterspocitle Contests Among Five Species of Mierotus (Twelve Contests/Pairing) Staged in the Smaller Enclosure :ill

LI

~ll'l

9

Species paired

llJ~l

L

I

No. of winners

M. montaaus vs M. pennsylvanicus

$

M, montanus vs M. californieus

8

M. montanus vs M. longicaudus

9

M. ochrogaster Vs M. pennsylvanicus M. oehrogaster

Z2 = 5.44, P < 0 . 0 2

1 Z2 = 8.00, P<0.01

0 Z 2 ~ 4-45, P<0-05

2 7

Z2 = 4"5, P<0"05

1 10

vs

M. montanus

Chi-square and probability values

1

X2 = 7"36, P<0'01

ANIMAL

478

BEHAVIOUR,

The number of intraspecific encounters demonstrating mutual avoidance for each of the five species is shown in Table VIII. Mutual avoidance is here defined as the condition or situation in which both opponents positioned themselves as far as possible from each other in Table VIII. Frequencies of Contests in the Smaller Enclosure Exhibiting Mutual Avoidance During Intraspecific Encounters for the Five Species of Mierotus

No. of contests Species

No Avoidance avoidance

Chi-square and probability values

M. montanus

0

12

Z2 -- 12-0, P<0.001

M. ochrogaster

0

12

Z2 = 12-0,P<0.001

M.pennsylvanicus 5

7

Z2 = 0"33,P>0.05

M. californicus

5

7

X2 = 0"33,P>0"05

M. longicaudus

8

4

X2 = 1.33, P>0"05

the enclosure and remained relatively immobile during the 5-min encounter. The animals constantly watched each other and pressed against the walls o f the enclosures. I f one animal changed his position, the other animal also moved, keeping as much distance as possible between himself and his opponent. When, prior to the paired observations, the animals exhibiting mutual avoidance were observed alone, they moved freely about the enclosure and no differences in behaviour between species were observed. By inspection there appeared to be two separate groups of species (Table VIII). The first group includes two species, M. montanus and M. ochrogaster. In all twelve contests, each species failed to exhibit mutual avoidance (Z 2 = I2.0, P<0.001). The second group includes three species, M. pennsylvanicus, M. californicus, and M. longicaudus. In five, five, and eight contests, respectively, the animals exhibited mutual avoidance. Here using chi-square, P > 0.05 in all three cases. Discussion

Banks & Fox (1968) maintained that the study of agonistic behaviour by sympatric microtines under natural conditions would be extremely difficult. The present study presents the first observation of agonistic behaviour by sympatric microtines under natural conditions in which the species and sex o f the opponents were deter-

21,

3

mined and confirms that ag0nistic encounters do actually occur between sympatric microtine species in nature. The question of whether or not the types of behaviour I observed in the laboratory are artifacts o f captivity can be answered by two statements. First, I observed an encounter in nature which demonstrated that agonistic encounters do occur. Second, the postures and movements observed in the field appeared identical to those observed in the laboratory. Since M. longicaudus observed in the field was bitten by his opponent, it is interesting to note that only on one occasion of the 160 contests staged in the laboratory, the third encounter of Table II, was an animal bitten severely enough to bleed. Hence, I suggest that encounters in nature can be as intense as any I observed in the laboratory. Studies by previous investigators of agonistic behaviour have been carried out in a wide variety o f sizes and shapes of enclosures, with two investigators rarely using a similar enclosure. Because of this lack of consistency and the wide disparity in experimental methods, it has been difficult to correlate their findings. In addition, the results o f many studies have been considered artifacts o f too-small enclosures. The results of the second portion of my study indicate that among males of these five species o f Microtus, no difference in the character of the postures and movements of agonistic behaviour is apparent when the area in which encounters occur is reduced, although a difference in the frequency of occurrence of these postures and movements is observed. However, not all five species o f Microtus reacted alike when they were placed in a smaller enclosure under controlled conditions. Like Novak & Getz (1969) I found that M. penn~ aylvanicus did not show a significant increase in intensity of agonistic behaviour when observed in a smaller enclosure. In addition, I found that neither M. californicus nor M. longicaudus showed a significant increase in intensity o f behaviour in the small enclosure. However, M. montanus and M. ochrogaster did show a significant increase in the frequency of occurrence of agonistic components in the small enclosure. These results may reflect basic differences in the social behaviour among the five species tested. At this point one may question whether there was something in the micro-environment of the encounter arena that inhibitied some species and not others. In my method I attempted to

COLVIN: AGONISTIC BEHAVIOUR OF VOLES

rule out this possibility by allowing subjects individually to explore the arena prior to the encounters. During this time, I observed no difference in behaviour among species. Also, it is unlikely that individuals in my study had definite territories and were defending actual topographic locations in the enclosure since the voles were introduced simultaneously into a neutral situation for only 5 min. This time limit should have also prevented the establishment of a social hierarchy (Ginsburg & Allee 1942). The effects of isolation on the development of behaviour patterns of mice and rats have been reviewed by several authors (e.g. Scott & Fredericson 1951; Scott 1966). In the present study the males were experienced adults, and none were isolated prior to 3 months of age. Hence the effect of the isolation period on behaviour development was probably minimal. When I paired species in staged encounters, weight of the species was apparently not a deciding factor. Comparing Table I with Table VII, one can note M. montanus won over M. longicaudus, a lighter .species, and both M. pennsylvanicus and M. californicus, two heavier species; M. ochrogaster won over M. pennsylvanicus, a heavier species and M. montanus, a species nearly equal in weight. No matter what the level of significance in a controlled study one must be cautious when generalizing from a laboratory population to nature or from the behaviour of a relatively few subjects to a species. The genetic variation within a species related to population density (Krebs 1970) or the artificial selection pressure imposed by confinement may also complicate any comparisons. Most of the previous work on agonistic behaviour has been restricted to studies of attack or threat, and little has been reported on mutual avoidance and its significance in the behaviour of microtines. In fact avoidance has previously been observed in only one species of Microtus, M. pennsylvanicus, by Getz (1962) and Krebs (1970). From the analysis of my data, it seems likely that M. pennsylvanicus, M. californicus, and M. longicaudus all use mutual avoidance in maintaining individual distance between males and that the other two species tested, M. montanus and M. ochrogaster, maintain individual distance between males by attacking or threat. Getz (1962) suggested that where M. penn~ sylvanicus and M. ochrogaster overlap, M. pennsylvanicus may be excluded from the drier

479

areas by the behaviour of M. ochrogaster, Based on my observations of the two species, I contend that M. pennsylvanicus was attempting to avoid the other species. Likewise, where the distributions of M. pennsylvanicus and M. montanus overlap, M. pennsylvanicus may again be avoiding the other species, in this case M. l~lolltaHus.

In areas where M. montanus and M. californicus overlap, M. californicus may avoid M. montanus since M. californicus uses mutual avoidance in contests within the species, as does M. pennsylvanicus. Hence avoidance again may help to maintain habitat segregation in nature. Where the ranges of M. montanus and M. ochrogaster overlap, avoidance is probably not involved in maintaining habitat segregation since neither M. montanus nor M. ochrogaster showed mutual avoidance in my study. Microtus ochrogaster might use threat and attack to exclude M. montanus from the drier lowland areas. In contrast to work of Cruzan (1968), I found M. montanus won significantly more encounters than M. longicaudus; interestingly he noted that M. rnontanus seemed to be bold and aggressive while M. longicaudus was timid and cautious. I found M. longicaudus most abundant along the rocky stream banks of Boulder Creek. In addition to its use in tail-rattling (Colvin 1970), the long muscular tail of this species is well suited as a balancing organ for an animal climbing over the rough terrain. The use of the tail by Peromyscus in a semi-arboreal habitat has been shown to be adaptive (Homer 1954). I suggest that M. longicaudus locally utilizes an area of rocky stream banks and attempts to avoid M. montanus. Since the morphology and behaviour of M. longicaudus appears adaptive in the stream bank habitat, this may allow the two species to coexist in nature.

Acknowledgments This study was supported by a Research Grantin-Aid from the Society of the Sigma Xi. It constitutes a portion of a thesis submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Biology of the University of Colorado. I thank Dr Olwen Williams, Dr Margaret Altmann, Dr William H. Burt and Dr Paul Winston for their encouragement and criticism of the manuscript. My wife, Dr Margaret Ann Colvin, worked with me throughout the study

480

ANIMAL

BEHAVIOUR,

and deserves credit for her assistance and encouragement. REFERENCES Allin, J. T. & Banks, E. M. (1968). Behavioural biology of the collared lemming Dicrostonyx groenlandicus (Traill). I. Agonistic behaviour. Anbn. Behav., 16, 245-262. Anderson, S. (1959). Distribution, variation, and relationships of the montane vole. Mierotus montanus. Univ. Karts. Pubis., Mus. nat. Hist., 9, 415--511. Bailey, V. (1900). Revision of American ~,oles of the genus Microtus. U.S. Dept. Agric., Bur. Biol. Surv. N. Amer. Fauna, 17, 1-88. Banks, E. M. & Fox, S. F. (1968). Relative aggression of two sympatric rodents: a preliminary report. Commun. behav. Biol., 2, 51-58. Burt, W. H. & Grossenbeider, R. P. (1964). A Field Guide to the Mammals. Boston: Houghton Mifflin. Colvin, D. V. (1970). Agonistie behavior in five species of Microtus. Ph.D. thesis, University Colorado. Colvin, M. A. & Colvin, D. V. (1970). Breeding and fecundity of six species of voles (Microtus). J. Mammal., 51, 417-419. Cruzan, J. (1968). Ecological distributions and interactions of four species of Microtus in Colorado. Ph.D. thesis, University Colorado. Getz, L. L. (1962). Aggressive behavior of the meadow and prairie voles. J. Mammal., 43, 351-358. 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. Hall, E. R. & Kelson, K. R. (1959). The Mammals of North America. New York: Ronald. Homer, B. E. (1954). Arboreal adaptations of Peromyscus, with special reference to use of the tail. Contr. Lab. Vertebr. Biol. Univ. Mich., 61, 1-84. King, J. A. (1957). Intra- and interspecific conflict of Mus and Peromyscus. Ecology, 38, 355-357.

21,

3

K.rebs, C.J. (1970). Microtus population biology: Behavioral changes associated with the population cycle in M. ochrogaster and M. pennsylvanicus. Ecology, 51, 34-52. Louch, C. D. (1956). Adrenocortical activity in relation to the density and dynamics of three confined populations of Microtus pennsylvanicus. Ecology, 37, 701-713. Martin, E. P. (1956). A population study of the prairie vole (Microtus ochrogaster) in northeastern Kansas. Univ. Karts. Pubis., Mus. nat. Hist., 8, 361--416. M~ler, W. C. (1969). Ecological and ethological isolating mechanisms between Microtus pennsylvanicus and Microtus ochrogaster at Terre Haute, Indiana. Am. Midl. Nat., 82, 140-148. Murie, J. O. (1963). Investigations of habitat segregation in Microtus in Western Montana. M.A. Thesis, UniV. Mont. Missoula. Murie, J. O. (1969). An experimental study of substrate selection by two species of voles (Microtus). Am. Mtdl. Nat., 82, 622--625. Murray, K. F. (1965). Population changes during the 1957-1958 vole (Microtus) outbreak in California. Ecology, 46, 163-171. Novak, M. A. & Getz, L. L. (1969). Aggressive behavior of meadow and pine voles. J. Mammal, 50, 637-639. Sadlier, R. F. M. S. (1965). The relationship between agonistie behavior and population changes in the deermouse, Peromyscus maniculatus (Wagner). J. Antm. EcoL, 34, 331-352. Scott, J. P. (1966). Agonistic behavior of mice and rats: a review. Am. ZooL, 6, 683-701. Scott, J. P. & Fredericson, E. (1951). The causes of fighting in mice and rats. PhysioL ZooL, 24, 273-309. Siegel, S. (1956). Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill. Tamura, M. (1966). Aggressive behavior in the California meadow mouse (Microtus californicus). M.A. thesis, Univ. Calif., Berkeley. (Received 24 August 1971; revised 13 May 1972; MS. number: A1221)