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Social dominance in wild and domestic Norway rats (Rattus norvegicus)
Anim. Behav.,1972,20, 534--542
SOCIAL DOMINANCE IN WILD AND DOMESTIC NORWAY RATS
(RA TTUS NOR VEGICUS ) BY JOHN BOREMAN* & EDWARD PRICE
Department of Forest Zoology, State University College of Forestry, Syracuse, New York 13210 Abstract. Differences in the relative social dominance of wild, hybrid and domestic strains of Norway rats are observed in mixed groups (twelve animals each) housed in a large room for 13 consecutive days. Domestic subjects are dominant to wild rats in both spontaneous and competitive interactions. Hybrids are intermediate. Explanations offered for the superior dominance of the domestic strain included: (a) the lack of social inhibitions displayed by domestic rats as reflected in frequent play-motivated interactions ('bully effect'), and (b) the larger body size of the domestic subjects. Domestic subjects are most active and interacted most frequently. Dominance behaviour does not influence nest box utilization. Dominance in spontaneous and competitive interactions is not correlated suggesting that in the rat social dominance is not a unidimensional trait. Social organization is an effective means of establishing priorities in competition for potentially limited resources (Brown 1964). Aggressive potential evolves for its role in the establishment and maintenance of social organization (EiblEibesfeldt 1970). In captivity competition for food, water, mates, and so on has been largely eliminated and space is often not economically defendable due to high densities. Thus, in captivity much of the adaptive value of social organization is lost. Consequently, one would expect selection for aggressive potential to be relaxed. Relaxed selection would also occur for those 'aggressive' behaviours associated with interspecific encounters (e.g. predator-prey interactions). In addition, artificial selection for reduced aggression would facilitate animal care and handling and permit the maintenance of captive populations of animals at relatively high densities. Hence, it seems reasonable to hypothesize that the process of domestication (implying genetic change through natural and artificial selection) is accompanied by a reduction in aggressive potential. The following study was designed to test one aspect of this problem, differences in social dominance between wild, hybrid and domestic Norway rats.
Differences in the social behaviour of wild and domestic Norway rats (Rattus norvegicus) have been discussed by Barnett (1960, 1963) and Boice (1969). Barnett noted that laboratory rats lack certain stereotyped social responses common to their wild counterparts (e.g. threat posture, 'crawling under', and so on). In addition, aggression was only mildly expressed and resembled the playful wrestling of immature or female wild rats. Strange domestic rats introduced into established domestic colonies are soon accepted into the social group (Barnett 1960) whereas wild rats are extremely aggressive towards intruders, often inflicting serious injury (Barnett 1960; Calhoun 1963; Galef 1970). Barnett & Stoddart (1969), in a study comparing field-trapped R. norvegicus with laboratoryreared subjects some six to nine generations removed from the wild, found a significant reduction of aggression in the laboratory-bred group. Resident laboratory-bred rats exhibited fewer threats and more abbreviated attacks toward interlopers than did wild-trapped individuals. Boice (1969) studied the social dominance of wild (field-trapped) and domestic rats in both segregated and mixed groups. Wild subjects engaged in infrequent but intense bouts of aggression. Domestic and hybrid rats interacted frequently but wounds and deaths were uncommon. In mixed groups domestic and wild rats engaged in segregated interactions almost exclusively. Therefore, strain differences in dominance were not reported.
Methods Subjects Forty-eight rats were employed representing the three genetically distinct strains in equal numbers (sixteen rats per strain, sexes divided equally). (a) Domestic subjects were obtained from a population of genetically heterogeneous rats derived from cross-mating individuals of the
*Present address: Department of Natural Resources, State University College of Agriculture, Cornell University, Ithaca, New York 14850, U.S.A. 534
BOREMAN & PRICE: SOCIAL DOMINANCE IN WILD AND DOMESTIC NORWAY RATS Sprague-Dawley, Long-Evans, Wistar and Holtzman inbred strains (fourteen litters represented). (b) Wild subjects were the laboratory-reared first generation offspring of wild-caught parents (five litters represented). (c) Hybrid rats were the offspring of domestic females and wild-caught male rats (seven litters represented). Each group was divided into eight unisexual pairs at weaning (27• days) and housed in 35.6 x 35.6 x 17.8cm wire cages. The subjects from each strain were 4 to 7 months of age at testing. Individuals were identified by shaving patches of hair from the dorsal mid-line. Hybrids were distinguished from wild subjects by shaving the head between the ears. This procedure had no apparent effect on the behaviour of the subjects.
boxes. Two 56-8-1itre cans with wire bases provided food ad libitum throughout the experiment. A 1.1-litre bottle with a sipper tube recessed 2.5 cm from a 2.8-cm hole in a sheet metal cover was used for water consumption, enabling only one rat to drink at a time. Procedure The forty-eight subjects were tested in four replications of twelve animals each (unisexual groups of four animals per strain). Observations for each replication were made over a 13-day period, 6 days of which the animals were placed on a restricted drinking schedule to increase the frequency of competitive interactions. Table I presents the schedule for observation and drinking.
Apparatus The experimental room measured 7.6 x 3.6 x 2.7 m. Observations were made externally through a one-way mirror. The two near corners were observed through mirrors suspended from the ceiling along the far wall (Fig. 1). A 12 9 12 light-dark regime was utilized with the light cycle (3-25-1x at floor level) commencing at 07.00 hours and ending at 19.00 hours. Red flood lights were activated between 18.30 hours and 07.00 hours and provided sufficient light for observation during the dark period. Twelve wooden nest boxes measuring 30.5 x 30.5 x 7.6 cm were placed in 'V' formation on the tiled floor (Fig. 1). Hinged lids enabled the observer to determine the tenancy of the nest
Social interactions were recorded as: (a) spontaneous, if the interaction did not involve apparent competition for a tangible commodity (e.g. water, food, nest box, and so on); or (b) competitive, if the interaction involved competition for the opportunity to drink, (No competitive interactions related to food or nestbox utilization were observed). The observer recorded only those spontaneous interactions in which a definite submissive posture (lying on side or back under dominant animal) was displayed by one individual (Grant 1963). Competitive interactions occurred when one rat displaced another at the drinking tube (pushing or shoving) or when one rat was actively m
WATER BOTTLE MIRROR
MIRROR
rnD 0 !
'
I
I
D
~""FOODHOPPERS -'~ 0
D DD f NESTING BOXES
I
535
I
OBSERVATION WINDOW
Fig. 1. Composition of the experimental room.
I
ZI D
V1
536
ANIMAL
BEHAVIOUR,
Table L Schedules for Observation and Water Availability During the 13-Day Test Period
Day
Time observed
Drinking schedule
1
1900 to 19.30 hours
ad libitum
2
19.00 to. 19.30, 21.30 to 22. 30 hours
ad libitum
3
19.00 to 19.30, 19.30 to 20.30 hours
ad libitum
4
19.00 to 19.30, 21.00 to. 22.00 hours
ad libitum
5
19.00 to 20.00 hours
ad libitum
6
19.00 to 19.30, 21.30 to 22.30 hours
ad libitum
7
19.00 to 19.30, 21.45 to 22.45 hours
19.00 to 23.00
8
19.00 to 20.30 hours
19.00 to 23.00
9
19.00 to 20.30 hours
19.00 to 23.00
10
19.00 to 20.30 hours
19.00 to 23.00
11
19.00 to 20.00 hours
Total Dep.
12
19.00 to 20.30 hours
19.00 to ad libitum
13
19.00 to 19.30 hours
ad libitum
prohibited from drinking by another (Schumsky & Jones 1966; Boice 1969; Baenninger 1970). Forty-eight hours prior to testing the four subjects representing each strain were marked for individual identification. On test day 1 the subjects were weighed and simultaneously released into the experimental room at 13.00 hours. At 18.30 hours daily, 30 rain before the dark cycle began, the tenancies of the subjects in the twelve nest boxes were recorded. F r o m 19.00 to 19.30 hours daily the following data were recorded: (a) spontaneous and competitive interactions, including the individuals involved and their dominant-subordinate relationships; and (b) activity as measured by the number of rats outside the nest boxes at 5-rain intervals. Additional observation periods were utilized on days 2 to 12 (see Table I). Only social interaction data were recorded during these periods. In order to assess strain differences in relative dominance a dominance score was computed for each subject based on the ratio of dominant and subordinate interactions with each individual o f the two opposing strains, f f dominant inter-
20,
3
actions with a given individual outnumbered subordinate interactions, the subject was awarded + 1. I f the number of subordinate interactions were greater, the subject was awarded - - 1 . I f the numbers of dominant and subordinant interactions were equal each animal was given a value of 0. The dominance score for each individual was then determined by summing the eight values. An individual dominant over all eight cross-strain subjects would thus receive a dominance score of + 8 , and an individual subordinate in all cases would have a dominance score o f - - 8 . By this system strain and individual differences in interaction rate did not influence the determination of strain differences in relative dominance. I f two individuals did not interact, a value from - - I to + 1 was awarded each individual based on its relative dominance in other cross-strain pairings. Dominance (D) scores could, thus, be computed by the formula:
D=(d--s) b/a where d = number of cross-strain subjects with which wins exceeded losses; s = number of cross-strain subjects with which losses exceeded wins; a = number of cross-strain subjects with which interactions occurred; b = number of cross-strain subjects in the group. Since the data for social dominance are not independent, non-parametric statistics were used to analyse all dominance related data. Results
Cross-strain dominance scores were computed for each subject for both spontaneous and competitive interactions. Dominance scores correlated significantly (Spearman R a n k Correlation Coefficient; Siegel 1956) with per cent cross-strain interactions won (Table II). D o m inance scores for spontaneous and competitive interactions were not correlated in three of the four replications (rs = 0.23, 0 . 2 I , - - 0 . I 5 and 0.88 for replications 1 to 4, respectively). Hence, strain differences in relative dominance were computed separately for the two interaction categories. The cross-strain dominance scores of the twelve individuals in each replication were ranked for each interaction category and applied to a Kruskal-Wallis One-Way Analysis of Variance by Ranks Test (Siegel 1956). M e a n strain dominance ranks and Kruskal-Wallis ' H ' values are presented in Table III. Wild rats
BOREMAN & PRICE: SOCIAL DOMINANCE IN WILD AND DOMESTIC NORWAY RATS
537
Table lI. Means and Standard Deviatians for Cross-Strain Dominance Scores (A) and Per Cent Cross-Strain Interactions Won (13). Spearman Rank Correlation Coefficients between Variables A and B are Presented in (C) Spontaneous interactions
Competitive interactions
Replications Wild 1
A B
--4.74•
A B
A B
--4.754-3.22 0-25•
+2-584-4.71 0-58•
+3.73• 0.794-0.13
Wild
---2"144-0"76 +2-304-5"83 0.274-0.05
0.64•
q- 1.96•
0.32•
--5"334-4"62
--4-004-6.93
B
0.174-0.29
0-274-0.47
C
--0.144-4.24 0.484-0.15
= 0"85 (P<0.001)
rs
-t-3"194-1"27 --4.38• 0-67•
Domestic
0.56d:0.06
--3"34•
0.29:~0-06
-t-6.194-2.23
0.364-0.19
0.70•
rs = 0"89 (P<0"001) q-0"604-7"82 ---4"144-2"62 --4"074-2"80 0.51 4-0.47
0.394-0-05
rs = 0.87 (P<0.001)
A
Hybrid
--3.08•
= 0.92 (P<0'001)
rs
C 4
0-59+0.31
Domestic
= 0.92 (P<0.001)
rs
C
3
q-2.904- 5.58
0.294-0.20
C
2
Hybrid
+7"334-1"34
0.384-0.11
0-68 •
rs = 0.81 (P<0.01) +7.004-2.00 0"854-0"31
--2.384-3.45
--2.844-2.80
+4"754-1.16
0.354-0.19
0.424-0-05
0.62-t-0.03
rs = 0"98 (P<0'001)
rs = 0"85 (P<0.001)
Table IH. Mean Strain Dominance Ranks (Scale = 1-12) for Cross-Strain Spontaneous and Competitive Interactions and Kruskal-Wallis Analyses ( ' H ' values) for Strain Differences in Dominance Spontaneous interactions
Replications Wild
Hybrid
Competitive interactions
Domestic
Wild
Hybrid
Domestic
1
2.75
7.88 H=6.04 (P<0.04)
7.83
4.25
8.25 H=2.58 (NS)
7.00
2
3"00
8.25 H=5.65 (/'<0'05)
8"25
4.00
4.00 H=7.00 (P<0.02)
9.50
3
4.50
6.12 H=0.39 CNS)
5.38
3"50
3 "50 H=6-55 (P<0"02)
8.50
4
3-33
3.83 //=6.05 (P<0-03)
8"38
4-62
4-38 H=7-39 (P<0"02)
10-50
Total
3.40
7.46
4.09
6.52
were least d o m i n a n t in b o t h s p o n t a n e o u s a n d competitive interactions. The m e a n d o m i n a n c e ranks o f hybrid a n d domestic subjects were nearly equal for s p o n t a n e o u s interactions. However, i n competitive interactions the d o m i n a n c e ranks of the hybrid a n d wild strains were most similar. Since strain differences in b o d y weight existed for each replication (Table IV) correlation analyses ( S p e a r m a n R a n k Correlation Co-
5.03
8.88
efficient) were conducted o n b o d y weight a n d cross-strain d o m i n a n c e scores. Significant correlations were f o u n d for half of the replications in each interaction category (Table IV). However, if d o m i n a n c e scores based o n c o m b i n e d s p o n t a n e o u s a n d competitive interactions were employed, significant correlations were f o u n d with b o d y weight in all four replications. Correlation analyses were conducted between b o d y weight a n d within-strain d o m i n a n c e scores
538
ANIMAL
BEHAVIOUR,
20,
3
Table IV. Means and Ranges of Body Weight (gm) for Each Strain in Each Replication, Analysis of Variance ('F') Values for Strain Differences in Body Weight and Spearman Rank Correlation Coefficients (rs) for Body Weights and Cross-Strain Dominance Scores
Strain
Replication 1
Wild
Hybrid
Domestic
Correlation body weight and dominance scores
Analysis of variance
Spontaneous
109-7
0.75
Competitive
179-4
216.9
300.0
Females
172-188
202-233
288-317
P<0.001
P<0.01
2 Males
283-5 268-300
373.0 348-394
378.0 282-426
6.8 P<0.025
0.49 NS
0.42 NS
3 Females
173.8 156-202
231.6 206-254
281.0 227-332
13.0 P<0.001
0-35 NS
0.65 P<0.05
4 Males
250.9 217-286
343.9 330-350
490.5 474-504
170.1 P<0.001
0-76 P<0.01
0-77 P<0.01
(spontaneous and competitive interactions combined) for each replication (twelve analyses). Non-significant correlations were obtained (range: rs-------0.25 to 0.40) in all but one analysis. No correlation was observed between within-strain dominance score and age o f the subject. Strains did not differ in total (13 days)crossstrain spontaneous interactions (Kruskal-Wallis H=0.03). Within-strain spontaneous interactions were more than twice as numerous for the domestic subjects than for their wild counterparts (Table V). The domestic and hybrid strains exhibited significantly more cross-strain competitive interactions than the wild subjects
0-31 NS
(H=8-75, P<0.02). Within-strain competitive interactions were nearly ten times more numerous for the domestic rats than for the wild subjects (Table V). The more dominant rats tended to interact more frequently than the subordinate subjects (Table V), but the alpha individual was not necessarily the most responsive nor was the fourth ranked subject least responsive. Interaction frequencies for sexes and interaction categories were compared in a two-factor analysis of variance (strains combined). Crossstrain competitive interactions were significantly more numerous than cross-strain spontaneous interactions ( F = 62-7; df~ 1/92; P < 0.001 ). The
Table V. Mean Total No. of Interactions Per Subject in Cross-Strain and Within-Strain Encounters (Replications Combined). Cross-Strain Values are Presented According to Dominance Rank
Spontaneous
Competitive
Wild
Hybrid
Domestic
Wild
Hybrid
Domestic
1
12-8
11.0
9 "4
38 "0
59.8
50.4
2
20.4
11"6
13"9
39.5
27-2
56'0
3
9.2
10"1
8"8
20.7
47.8
35"8
4
17"0
12'7
11"7
28.5
39"2
36"0
Total
17'6
18"2
17"1
26"8
43"4
44"5
Within-strain total
2.4
3"1
5-9
2-2
7-2
21-3
20.0
21.3
23.0
29.0
50"6
65"8
Cross-strain dominance rank
Total all interactions
BOREMAN & PRICE: SOCIAL DOMINANCE IN WILD AND DOMESTIC NORWAY RATS
main effect for sex was non-significant (F=0.56, 1/92) as was the interaction between these two variables (F=0.23, df----1/92). The ratio of activity for wild, hybrid and domestic strains was 1 to 1.84 to 2.37, respectively. Whereas this difference between wild and domestic rats was significant (F----5.75, df-----2/546, P<0.005), hybrids did not differ from either parent strain ('New Multiple Range' analysis: Li 1964). The main effect for days was, likewise significant (F=2.26, df= 12/546, P<0.01). Activity was greatest during the days of restricted drinking, reaching a peak on day 12 when water was provided after 44 hr of total deprivation (Fig. 2). Sex and all interaction effects were nonsignificant. Few competitive interactions were observed until the subjects were placed on a restricted drinking schedule (Fig. 2). Both competitive interactions and activity (strains combined) increased under the restricted drinking schedule
df=
I
I
--w"d 1
/
!
---Hybrid I-Activity
I
/
i:if 160]-"
j.. ,,ok
,ool-
i~=** aop/
--
//,/4,
539
and were significantly correlated (rs = 0.53; P<0-05). Total spontaneous interactions did not change appreciably over test days and did not correlate with activity (rs = 0-22). Nest-box tenancy was examined daily to determine the effect of social behaviour on nestbox utilization. Although a nest box was provided for each rat, less than half of the boxes were generally utilized by the population on any given day. Means and standard deviations for daily number of nest boxes utilized were 4.1591.07, 6.08• 5.77• and 4.77• for replications one to four, respectively. A mean number of 1.96 rats were found in each nest box utilized on a given day (replications combined) suggesting a certain degree of mutual tolerance. Rats did not segregate by strains in nest box utilization. Some nest boxes were utilized more than others (F----5.95, df----ll/36, P<0.001). Nest-box utilization ranged between 0.23 and 2.33 rats per day depending on its location. Nest boxes nearest and farthest from the observation window (Fig. 1) were utilized most frequently suggesting a preference for shelter at the ends of a row of potential sites. Some subjects were not always found in nest boxes at 18.30 hours daily. The total number o f days in which individuals were not residing in nest boxes averaged 1.62, 2.94 and 1.81 for wild, hybrid and domestic rats, respectively. The mean for the hybrid subjects was elevated by two rats which were found in nest boxes a combined total of only three times. These strain differences were not significant (F=1.35, df= 2/45). The mean number of consecutive days in which rats were found in the same nest box were surprisingly low (Table VI). Correlations between this variable and cross-strain dominance scores were not significant for competitive interactions (Table VI) and two of the four spontaneous interaction analyses. Strains did not differ in the number of consecutive days of nest box residency (F=0.86, df=2/45). The number of different next boxes utilized by individuals during the 13-day test period (adjusted for total number of days tenancy in nest boxes) did not differ for strains (~----6.4, 7-4, and 6.9 for wild, hybrid and domestic rats, respectively; F-- 1.28, df=2/45).
.of... &.._I',9,: I 2 ~ 4- 5 6 7 8 9 IO II 12 13 14 15 DAYS Fig. 2. Tota| no. of spontaneous and
competitive inter-
actions and strain differences in activity over the 13-day test period (replications combined).
Discussion Domestic rats were most dominant in both spontaneous and competitive cross-strain ifiteractions. Assuming that a positive correlation
540
ANIMAL
BEHAVIOUR,
20,
3
Table VI. Mean No. of ConsecutiveDays in the Same Nest Box and Correlation CoefficientsBetweenIndividual Values and Spontaneous and Competitive Cross-Strain Dominance Scores
Replication
Spearman rank correlation coefficient
Strain Wild
Hybrid
Domestic
1
1.61
1.23
2.~0
--0.03 NS
--4).31 NS
2
1-21
1.16
1.19
0.35 NS
0.29 NS
3
1.29
1.53
1.26
0.69 P<0-05
--0-20 NS
4
1-16
1-15
1.26
0.64 P<0.05
0.55 NS
Total
1.32
1.27
1.43
exists between aggressive potential and dominance (which may not be a valid assumption) this result does not support the hypothesis (Barnett 1963; Robinson 1965)that the laboratory rat is more 'docile' and less aggressive than its wild ancestors. It also argues against the notion that the laboratory rat is biologically 'degenerate' (Lockard 1968) due to a century or more of breeding in captivity (Robinson 1965). However, it does not refute the finding (Barnett 1960, 1963; Calhoun 1963; Galef 1970) that the wild Norway rat is more aggressive than the domestic rat when approached by a strange individual in a familiar environment, since, in the present study, all individuals were placed in the experimental room at the same time. The superior dominance of the domestic rats in the present study can be explained in several ways. Hall & Klein (1942) reported marked differences in aggressiveness between two strains of rats bred for open-field elimination (emotional reactivity). The non-emotional subjects initiated 326 aggressive encounters in contrast to sixty-eight interactions for the emotional strain. The emotionally reactive subjects retaliated only 18 per cent of the times they were attacked. Billingslea (1941), likewise, reported reduced aggression among rats of an emotional strain relative to rats of a non-emotional strain in competition for food. Barnett (1963) and Robinson (1965) have summarized the wealth of literature documenting the high emotional reactivity of the wild Norway rat relative to its domesticated counterpart. If emotional reactivity and aggressive tendencies are negatively correlated, one would predict
Spontaneous
Competitive
wild rats to be socially subordinate to domestic rats. The highly developed inhibitions of the wild rat in response to novelty may be based on factors promoting social inhibitions as well. Lorenz (1965) has asserted that one of the effects of breeding animals in captivity is a gradual loss of social inhibitions (p. 94). Spontaneous interactions initiated by laboratory rats often appear to be highly play-motivated (Grant & Chance 1958; Baenninger 1970). Domestic rats may engage in such spontaneous interactions with few social inhibitions. Seward (1945) characterizes much o f the dominant behaviour of laboratory rats as 'bullying'. The more socially inhibited wild rat may interpret the play-oriented activities of the laboratory rat as dominance displays and sustain psychological defeat without engaging in a dominance determining contest ('bully effect'). Dominantsubordinate relationships so established could be maintained during subsequent competitive encounters until a dominance-determining struggle confirmed or reversed the relationship. A second explanation for the superior dominance of the domestic subjects concerns the postulated increased gonadal activity of the domestic strain (Richter 1954; Richter & Uhlenhuth 1954). A positive relationship between gonadal funtion (specifically, androgens) and aggressive behaviour has been documented (Rothballer 1967; Sigg 1969). Hence, on this basis one could predict higher levels of aggressiveness in the domestic subjects than in their wild counterparts. Although increased gonadal function is believed to accompany the domestication process (Hale 1962) it would seem mal-
BOREMAN & PRICE: SOCIALDOMINANCE IN WILD AND DOMESTIC NORWAY RATS adaptive for a population of captive animals to exhibit a corresponding increase in aggressive behaviour (Price & King 1968). Perhaps the dominant status of the domestic rats is not earned as much as it is 'forced' upon them in response to a general submissive attitude of the wild rats in cross-strain interactions. A third explanation relates to strain differences in body size. Correlations were found between body weight and cross-strain dominance scores in half of the replications of both spontaneous and competitive interactions. Correlations were significant in all four replications when dominance scores were based on the combined outcomes of spontaneous and competitive interactions. In addition it was noted that correlations were greatest in those replications in which strain differences in body weight were greatest (Table IV). On the other hand, within-strain dominance did not correlate with body weight, confirming the report of Baenninger (1970) but conflicting with Hall & Klein (1942) and Schumsky & Jones (1966). In addition, hybrid dominance varied considerably between spontaneous and competitive interactions suggesting that, if important, body size does not confer the same advantages in spontaneous and competitive interactions. Body size may influence strain differences in relative dominance only when marked strain differences in body size exist. The superior dominance of the domestic strain in competitive interactions cannot be explained by strain differences in water requirements (thirst), in that daily water intake per unit body weight is similar for both wild and domestic strains (Sloan, personal communication). The lack of correlation between dominance scores in spontaneous and competitive interactions was also reported by Baenninger (1970) for the laboratory rat. This result seems as valid for wild rats as for their domestic counterparts. As Baenninger (1970) and Grant & Chance (1958) suggest, spontaneous interactions may lack much of the aggressive motivation of competitive struggles and may, in fact, represent responses akin to play. In any case, the data obtained in this study supports the thesis that dominance is not a unidimensional trait; that the expression of dominance may, at least in part, be dependent on the motivational state of the interacting animals. Domestic rats interacted more frequently than wild rats, with the exception of cross-strain spontaneous encounters (Table V). The ratio of
541
total spontaneous and competitive interactions was much more divergent for domestic subjects than their wild counterparts. The interaction rate of the domestic subjects changed (increased) most abruptly in response to competition for the opportunity to drink. This may have been due, in part, to the greater activity (availability) of the domestic rats, particularly during the period of restricted drinking or it may be related to strain differences in relative dominance. Baenninger (1966) found that rats higher in the hierarchy engage in more interactions than those lower in rank. Boice (1969) reported frequent physical contact in groups of all hooded rats, wheres in groups of wild-caught rats physical contact was relatively limited. The lack of nest-box defence, the frequent shifts in nest-box utilization by both dominant and subordinate subjects, and the simultaneous occupancy of nest-boxes by both wild and domestic rats, suggest that territoriality had little or no influence on the outcome of social interactions observed. The fact that all subjects were placed in the experimental room at the same time could have inhibited any expression of territorial behaviour. This same stock of wild rats was found to be extremely aggressive toward domestic rats when the latter were introduced into an area familiar to the former (Price, personal observation) whereas 'established' domestic rats showed little or no aggression toward intruders. This finding supports Barnett's (1963) hypothesis that the true aggressive potential of the wild rat is best expressed in the context of territorial defence, whereas domestic rats may be more adapted for the social hierarchy, a natural consequence of high density interactions in confined populations (Davis 1958; Anderson 1961). An analogous phenomenon has been reported for the wild house mouse, Mus musculus, in which its social organization shifts from territoriality to the dominance hierarchy when it is taken from the field and placed in captivity (Crowcroft 1955). Thus, wild and domestic rats may have evolved different social behaviours to maximize fitness in their respective 'natural' environments.
Acknowledgments This investigation was supported by State University of New York Research Foundation Grant 10-7104-A and a National Science Foundation Undergraduate Research Participation Grant to the State University of New York College of Forestry. Mr Boreman collected the
542
A N I M A L BEHAVIOUR
d a t a a n d D r Price is responsible for the m a n u script. REFERENCES Anderson, P. K. (1961). Density, social structure and non-social environment in house-mouse populations and the implications for regulation of numbers. Trans. IV. Y. Aead. ScL, 23, 447--451. Baenninger, L. P. (1966). The reliability of dominance orders in rats. Anim. Behav., 14, 367-371. Baenninger, L. P. (1970). Social dominance orders in the rat: "spontaneous", food, and water competition. J. comp. physioL PsyehoL, 71, 202-209. Barnett, S. A. (1960). Social behaviour among tame rats and among wild-white hybrids. Proe. zooL Soe. Lond., 134, 611-621. Barnett, S. A. (1963). The Rat: A Study in Behaviour. Chicago: Aldine. Barnett, S. A. & Stoddart, R. C. (1969). Effects of breeding in captivity on conflict among wild rats. J. MammaL, 50, 321-325. Billingslea, F. Y. (1941). The relationship between emotionality and various other salients of behavior in the rat. J. comp. PsyehoL, 31, 69-77. Boice, R. (1969). Dominance and survival in stressed wild and domesticated Norway rats. Proc. Am. PsyehoL Ass., 77th Ann. Cony., pp. 187-188. Brown, J. (1964). The evolution of diversity in avian territorial systems. Wilson Bull., 76, 160--169. Calhoun, J. B. (1963). The Ecology and Sociology of the Norway Rat. Bethesda, Maryland: United States Department of Health, Education and Welfare, Crowcroft, P. (1955). Territoriality in wild house mice, Mus museulus L. J. MammaL, 36, 299-301. Davis, D. E. (1958). The role of density in aggressive behaviour of house mice. Anim. Behav., 6, 207210. Eibl-Eibesfeldt, I. (1970). Ethology: The Biology of Behavior. New York: Holt, Rinehart & Winston. Galef, B. G. (1970). Aggression and timidity: responses to novelty in feral Norway rats. J. eomp. physiol. PsychoL, 70, 370--381. Grant, E. C. (1963). An analysis of the social behaviour of the male laboratory rat. Behaviour, 21, 260281. Grant, E. C. & Chance, M. R. A. (1958). Rank order in caged rats. Anita. Behav., 6, 183-194.
20,
3
Hale, E. B. (1962). Domestication and the evolution of behaviour. In: The Behaviour of Domestic Animals (Ed. by E. S. E. Hafez). Baltimore: Williams & Wilkins. Hall, C. S. & Klein, S. J. (1942). Individual differences in aggressiveness in rats. J. comp. Psychol., 33. 371-383. Li, J. C. R. (1964). Statistical Inference. Ann Arbor: Edwards Bros. Lockard, R. B. (1968). The albino rat: a defensible choice or a bad habit 9. Am. PsychoL, 23, 734-742. Lorenz, K. (1965). Evolution and Modification of Behavior. Chicago: University of Chicago Press. Price, E. O, & King, J. A. (1968). Domestication and adaptation. In: Adaptation of Domestic Animals (Ed. by E. S. E. Hafez), pp. 34-45. Philadelphia: Lea & Febiger. Richter, C. P. (1954). The effects of domestication and selection on the behavior of the Norway rat. J. nat. Cancer Inst., 15, 725-738. Richter, C. P. & Uhlenhuth, E. H. (1954). Comparison of the effects of gonadectomy on spontaneous activity of wild and domesticated Norway rats. Endocrinology, 54, 311-322. Robinson, R. (1965). Genetics of the Norway Rat. Oxford: Pergamon Press. Rothballer, A. B. (1967). Aggression, defense and neurohumors. In: Aggression and Defense: Neural Mechanisms and Social Patterns (Ed. by C. D. Clemente & D. B. Lindsley), pp. 135-170. Los Angeles: University of California Press. Schumsky, D. A. & Jones, P. D. (1966). Reliable paired comparison dominance orders in rats. Psychol. Ree., 16, 473--478. Seward, J. P. (1945). Aggressive behavior in the rat. I. General characteristics: age and sex ~lifferences. J. comp. PsychoL, 38, 175-197. Siegel, S. (1956). Nonparametric Statistics. New York: McGraw-Hill. Sigg. E. B. (1969). Relationship of aggressive behaviour to adrenal and gonadal function in male mice. In: Aggressive Behaviour (Ed. by S. Garattini & E. B. Sigg), pp. 143-149. New York: Wiley. (Received 15 May 1971; revised 29 July 1971; second revision 3 November 1971; MS. number All70)
SOCIAL DOMINANCE IN WILD AND DOMESTIC NORWAY RATS
(RA TTUS NOR VEGICUS ) BY JOHN BOREMAN* & EDWARD PRICE
Department of Forest Zoology, State University College of Forestry, Syracuse, New York 13210 Abstract. Differences in the relative social dominance of wild, hybrid and domestic strains of Norway rats are observed in mixed groups (twelve animals each) housed in a large room for 13 consecutive days. Domestic subjects are dominant to wild rats in both spontaneous and competitive interactions. Hybrids are intermediate. Explanations offered for the superior dominance of the domestic strain included: (a) the lack of social inhibitions displayed by domestic rats as reflected in frequent play-motivated interactions ('bully effect'), and (b) the larger body size of the domestic subjects. Domestic subjects are most active and interacted most frequently. Dominance behaviour does not influence nest box utilization. Dominance in spontaneous and competitive interactions is not correlated suggesting that in the rat social dominance is not a unidimensional trait. Social organization is an effective means of establishing priorities in competition for potentially limited resources (Brown 1964). Aggressive potential evolves for its role in the establishment and maintenance of social organization (EiblEibesfeldt 1970). In captivity competition for food, water, mates, and so on has been largely eliminated and space is often not economically defendable due to high densities. Thus, in captivity much of the adaptive value of social organization is lost. Consequently, one would expect selection for aggressive potential to be relaxed. Relaxed selection would also occur for those 'aggressive' behaviours associated with interspecific encounters (e.g. predator-prey interactions). In addition, artificial selection for reduced aggression would facilitate animal care and handling and permit the maintenance of captive populations of animals at relatively high densities. Hence, it seems reasonable to hypothesize that the process of domestication (implying genetic change through natural and artificial selection) is accompanied by a reduction in aggressive potential. The following study was designed to test one aspect of this problem, differences in social dominance between wild, hybrid and domestic Norway rats.
Differences in the social behaviour of wild and domestic Norway rats (Rattus norvegicus) have been discussed by Barnett (1960, 1963) and Boice (1969). Barnett noted that laboratory rats lack certain stereotyped social responses common to their wild counterparts (e.g. threat posture, 'crawling under', and so on). In addition, aggression was only mildly expressed and resembled the playful wrestling of immature or female wild rats. Strange domestic rats introduced into established domestic colonies are soon accepted into the social group (Barnett 1960) whereas wild rats are extremely aggressive towards intruders, often inflicting serious injury (Barnett 1960; Calhoun 1963; Galef 1970). Barnett & Stoddart (1969), in a study comparing field-trapped R. norvegicus with laboratoryreared subjects some six to nine generations removed from the wild, found a significant reduction of aggression in the laboratory-bred group. Resident laboratory-bred rats exhibited fewer threats and more abbreviated attacks toward interlopers than did wild-trapped individuals. Boice (1969) studied the social dominance of wild (field-trapped) and domestic rats in both segregated and mixed groups. Wild subjects engaged in infrequent but intense bouts of aggression. Domestic and hybrid rats interacted frequently but wounds and deaths were uncommon. In mixed groups domestic and wild rats engaged in segregated interactions almost exclusively. Therefore, strain differences in dominance were not reported.
Methods Subjects Forty-eight rats were employed representing the three genetically distinct strains in equal numbers (sixteen rats per strain, sexes divided equally). (a) Domestic subjects were obtained from a population of genetically heterogeneous rats derived from cross-mating individuals of the
*Present address: Department of Natural Resources, State University College of Agriculture, Cornell University, Ithaca, New York 14850, U.S.A. 534
BOREMAN & PRICE: SOCIAL DOMINANCE IN WILD AND DOMESTIC NORWAY RATS Sprague-Dawley, Long-Evans, Wistar and Holtzman inbred strains (fourteen litters represented). (b) Wild subjects were the laboratory-reared first generation offspring of wild-caught parents (five litters represented). (c) Hybrid rats were the offspring of domestic females and wild-caught male rats (seven litters represented). Each group was divided into eight unisexual pairs at weaning (27• days) and housed in 35.6 x 35.6 x 17.8cm wire cages. The subjects from each strain were 4 to 7 months of age at testing. Individuals were identified by shaving patches of hair from the dorsal mid-line. Hybrids were distinguished from wild subjects by shaving the head between the ears. This procedure had no apparent effect on the behaviour of the subjects.
boxes. Two 56-8-1itre cans with wire bases provided food ad libitum throughout the experiment. A 1.1-litre bottle with a sipper tube recessed 2.5 cm from a 2.8-cm hole in a sheet metal cover was used for water consumption, enabling only one rat to drink at a time. Procedure The forty-eight subjects were tested in four replications of twelve animals each (unisexual groups of four animals per strain). Observations for each replication were made over a 13-day period, 6 days of which the animals were placed on a restricted drinking schedule to increase the frequency of competitive interactions. Table I presents the schedule for observation and drinking.
Apparatus The experimental room measured 7.6 x 3.6 x 2.7 m. Observations were made externally through a one-way mirror. The two near corners were observed through mirrors suspended from the ceiling along the far wall (Fig. 1). A 12 9 12 light-dark regime was utilized with the light cycle (3-25-1x at floor level) commencing at 07.00 hours and ending at 19.00 hours. Red flood lights were activated between 18.30 hours and 07.00 hours and provided sufficient light for observation during the dark period. Twelve wooden nest boxes measuring 30.5 x 30.5 x 7.6 cm were placed in 'V' formation on the tiled floor (Fig. 1). Hinged lids enabled the observer to determine the tenancy of the nest
Social interactions were recorded as: (a) spontaneous, if the interaction did not involve apparent competition for a tangible commodity (e.g. water, food, nest box, and so on); or (b) competitive, if the interaction involved competition for the opportunity to drink, (No competitive interactions related to food or nestbox utilization were observed). The observer recorded only those spontaneous interactions in which a definite submissive posture (lying on side or back under dominant animal) was displayed by one individual (Grant 1963). Competitive interactions occurred when one rat displaced another at the drinking tube (pushing or shoving) or when one rat was actively m
WATER BOTTLE MIRROR
MIRROR
rnD 0 !
'
I
I
D
~""FOODHOPPERS -'~ 0
D DD f NESTING BOXES
I
535
I
OBSERVATION WINDOW
Fig. 1. Composition of the experimental room.
I
ZI D
V1
536
ANIMAL
BEHAVIOUR,
Table L Schedules for Observation and Water Availability During the 13-Day Test Period
Day
Time observed
Drinking schedule
1
1900 to 19.30 hours
ad libitum
2
19.00 to. 19.30, 21.30 to 22. 30 hours
ad libitum
3
19.00 to 19.30, 19.30 to 20.30 hours
ad libitum
4
19.00 to 19.30, 21.00 to. 22.00 hours
ad libitum
5
19.00 to 20.00 hours
ad libitum
6
19.00 to 19.30, 21.30 to 22.30 hours
ad libitum
7
19.00 to 19.30, 21.45 to 22.45 hours
19.00 to 23.00
8
19.00 to 20.30 hours
19.00 to 23.00
9
19.00 to 20.30 hours
19.00 to 23.00
10
19.00 to 20.30 hours
19.00 to 23.00
11
19.00 to 20.00 hours
Total Dep.
12
19.00 to 20.30 hours
19.00 to ad libitum
13
19.00 to 19.30 hours
ad libitum
prohibited from drinking by another (Schumsky & Jones 1966; Boice 1969; Baenninger 1970). Forty-eight hours prior to testing the four subjects representing each strain were marked for individual identification. On test day 1 the subjects were weighed and simultaneously released into the experimental room at 13.00 hours. At 18.30 hours daily, 30 rain before the dark cycle began, the tenancies of the subjects in the twelve nest boxes were recorded. F r o m 19.00 to 19.30 hours daily the following data were recorded: (a) spontaneous and competitive interactions, including the individuals involved and their dominant-subordinate relationships; and (b) activity as measured by the number of rats outside the nest boxes at 5-rain intervals. Additional observation periods were utilized on days 2 to 12 (see Table I). Only social interaction data were recorded during these periods. In order to assess strain differences in relative dominance a dominance score was computed for each subject based on the ratio of dominant and subordinate interactions with each individual o f the two opposing strains, f f dominant inter-
20,
3
actions with a given individual outnumbered subordinate interactions, the subject was awarded + 1. I f the number of subordinate interactions were greater, the subject was awarded - - 1 . I f the numbers of dominant and subordinant interactions were equal each animal was given a value of 0. The dominance score for each individual was then determined by summing the eight values. An individual dominant over all eight cross-strain subjects would thus receive a dominance score of + 8 , and an individual subordinate in all cases would have a dominance score o f - - 8 . By this system strain and individual differences in interaction rate did not influence the determination of strain differences in relative dominance. I f two individuals did not interact, a value from - - I to + 1 was awarded each individual based on its relative dominance in other cross-strain pairings. Dominance (D) scores could, thus, be computed by the formula:
D=(d--s) b/a where d = number of cross-strain subjects with which wins exceeded losses; s = number of cross-strain subjects with which losses exceeded wins; a = number of cross-strain subjects with which interactions occurred; b = number of cross-strain subjects in the group. Since the data for social dominance are not independent, non-parametric statistics were used to analyse all dominance related data. Results
Cross-strain dominance scores were computed for each subject for both spontaneous and competitive interactions. Dominance scores correlated significantly (Spearman R a n k Correlation Coefficient; Siegel 1956) with per cent cross-strain interactions won (Table II). D o m inance scores for spontaneous and competitive interactions were not correlated in three of the four replications (rs = 0.23, 0 . 2 I , - - 0 . I 5 and 0.88 for replications 1 to 4, respectively). Hence, strain differences in relative dominance were computed separately for the two interaction categories. The cross-strain dominance scores of the twelve individuals in each replication were ranked for each interaction category and applied to a Kruskal-Wallis One-Way Analysis of Variance by Ranks Test (Siegel 1956). M e a n strain dominance ranks and Kruskal-Wallis ' H ' values are presented in Table III. Wild rats
BOREMAN & PRICE: SOCIAL DOMINANCE IN WILD AND DOMESTIC NORWAY RATS
537
Table lI. Means and Standard Deviatians for Cross-Strain Dominance Scores (A) and Per Cent Cross-Strain Interactions Won (13). Spearman Rank Correlation Coefficients between Variables A and B are Presented in (C) Spontaneous interactions
Competitive interactions
Replications Wild 1
A B
--4.74•
A B
A B
--4.754-3.22 0-25•
+2-584-4.71 0-58•
+3.73• 0.794-0.13
Wild
---2"144-0"76 +2-304-5"83 0.274-0.05
0.64•
q- 1.96•
0.32•
--5"334-4"62
--4-004-6.93
B
0.174-0.29
0-274-0.47
C
--0.144-4.24 0.484-0.15
= 0"85 (P<0.001)
rs
-t-3"194-1"27 --4.38• 0-67•
Domestic
0.56d:0.06
--3"34•
0.29:~0-06
-t-6.194-2.23
0.364-0.19
0.70•
rs = 0"89 (P<0"001) q-0"604-7"82 ---4"144-2"62 --4"074-2"80 0.51 4-0.47
0.394-0-05
rs = 0.87 (P<0.001)
A
Hybrid
--3.08•
= 0.92 (P<0'001)
rs
C 4
0-59+0.31
Domestic
= 0.92 (P<0.001)
rs
C
3
q-2.904- 5.58
0.294-0.20
C
2
Hybrid
+7"334-1"34
0.384-0.11
0-68 •
rs = 0.81 (P<0.01) +7.004-2.00 0"854-0"31
--2.384-3.45
--2.844-2.80
+4"754-1.16
0.354-0.19
0.424-0-05
0.62-t-0.03
rs = 0"98 (P<0'001)
rs = 0"85 (P<0.001)
Table IH. Mean Strain Dominance Ranks (Scale = 1-12) for Cross-Strain Spontaneous and Competitive Interactions and Kruskal-Wallis Analyses ( ' H ' values) for Strain Differences in Dominance Spontaneous interactions
Replications Wild
Hybrid
Competitive interactions
Domestic
Wild
Hybrid
Domestic
1
2.75
7.88 H=6.04 (P<0.04)
7.83
4.25
8.25 H=2.58 (NS)
7.00
2
3"00
8.25 H=5.65 (/'<0'05)
8"25
4.00
4.00 H=7.00 (P<0.02)
9.50
3
4.50
6.12 H=0.39 CNS)
5.38
3"50
3 "50 H=6-55 (P<0"02)
8.50
4
3-33
3.83 //=6.05 (P<0-03)
8"38
4-62
4-38 H=7-39 (P<0"02)
10-50
Total
3.40
7.46
4.09
6.52
were least d o m i n a n t in b o t h s p o n t a n e o u s a n d competitive interactions. The m e a n d o m i n a n c e ranks o f hybrid a n d domestic subjects were nearly equal for s p o n t a n e o u s interactions. However, i n competitive interactions the d o m i n a n c e ranks of the hybrid a n d wild strains were most similar. Since strain differences in b o d y weight existed for each replication (Table IV) correlation analyses ( S p e a r m a n R a n k Correlation Co-
5.03
8.88
efficient) were conducted o n b o d y weight a n d cross-strain d o m i n a n c e scores. Significant correlations were f o u n d for half of the replications in each interaction category (Table IV). However, if d o m i n a n c e scores based o n c o m b i n e d s p o n t a n e o u s a n d competitive interactions were employed, significant correlations were f o u n d with b o d y weight in all four replications. Correlation analyses were conducted between b o d y weight a n d within-strain d o m i n a n c e scores
538
ANIMAL
BEHAVIOUR,
20,
3
Table IV. Means and Ranges of Body Weight (gm) for Each Strain in Each Replication, Analysis of Variance ('F') Values for Strain Differences in Body Weight and Spearman Rank Correlation Coefficients (rs) for Body Weights and Cross-Strain Dominance Scores
Strain
Replication 1
Wild
Hybrid
Domestic
Correlation body weight and dominance scores
Analysis of variance
Spontaneous
109-7
0.75
Competitive
179-4
216.9
300.0
Females
172-188
202-233
288-317
P<0.001
P<0.01
2 Males
283-5 268-300
373.0 348-394
378.0 282-426
6.8 P<0.025
0.49 NS
0.42 NS
3 Females
173.8 156-202
231.6 206-254
281.0 227-332
13.0 P<0.001
0-35 NS
0.65 P<0.05
4 Males
250.9 217-286
343.9 330-350
490.5 474-504
170.1 P<0.001
0-76 P<0.01
0-77 P<0.01
(spontaneous and competitive interactions combined) for each replication (twelve analyses). Non-significant correlations were obtained (range: rs-------0.25 to 0.40) in all but one analysis. No correlation was observed between within-strain dominance score and age o f the subject. Strains did not differ in total (13 days)crossstrain spontaneous interactions (Kruskal-Wallis H=0.03). Within-strain spontaneous interactions were more than twice as numerous for the domestic subjects than for their wild counterparts (Table V). The domestic and hybrid strains exhibited significantly more cross-strain competitive interactions than the wild subjects
0-31 NS
(H=8-75, P<0.02). Within-strain competitive interactions were nearly ten times more numerous for the domestic rats than for the wild subjects (Table V). The more dominant rats tended to interact more frequently than the subordinate subjects (Table V), but the alpha individual was not necessarily the most responsive nor was the fourth ranked subject least responsive. Interaction frequencies for sexes and interaction categories were compared in a two-factor analysis of variance (strains combined). Crossstrain competitive interactions were significantly more numerous than cross-strain spontaneous interactions ( F = 62-7; df~ 1/92; P < 0.001 ). The
Table V. Mean Total No. of Interactions Per Subject in Cross-Strain and Within-Strain Encounters (Replications Combined). Cross-Strain Values are Presented According to Dominance Rank
Spontaneous
Competitive
Wild
Hybrid
Domestic
Wild
Hybrid
Domestic
1
12-8
11.0
9 "4
38 "0
59.8
50.4
2
20.4
11"6
13"9
39.5
27-2
56'0
3
9.2
10"1
8"8
20.7
47.8
35"8
4
17"0
12'7
11"7
28.5
39"2
36"0
Total
17'6
18"2
17"1
26"8
43"4
44"5
Within-strain total
2.4
3"1
5-9
2-2
7-2
21-3
20.0
21.3
23.0
29.0
50"6
65"8
Cross-strain dominance rank
Total all interactions
BOREMAN & PRICE: SOCIAL DOMINANCE IN WILD AND DOMESTIC NORWAY RATS
main effect for sex was non-significant (F=0.56, 1/92) as was the interaction between these two variables (F=0.23, df----1/92). The ratio of activity for wild, hybrid and domestic strains was 1 to 1.84 to 2.37, respectively. Whereas this difference between wild and domestic rats was significant (F----5.75, df-----2/546, P<0.005), hybrids did not differ from either parent strain ('New Multiple Range' analysis: Li 1964). The main effect for days was, likewise significant (F=2.26, df= 12/546, P<0.01). Activity was greatest during the days of restricted drinking, reaching a peak on day 12 when water was provided after 44 hr of total deprivation (Fig. 2). Sex and all interaction effects were nonsignificant. Few competitive interactions were observed until the subjects were placed on a restricted drinking schedule (Fig. 2). Both competitive interactions and activity (strains combined) increased under the restricted drinking schedule
df=
I
I
--w"d 1
/
!
---Hybrid I-Activity
I
/
i:if 160]-"
j.. ,,ok
,ool-
i~=** aop/
--
//,/4,
539
and were significantly correlated (rs = 0.53; P<0-05). Total spontaneous interactions did not change appreciably over test days and did not correlate with activity (rs = 0-22). Nest-box tenancy was examined daily to determine the effect of social behaviour on nestbox utilization. Although a nest box was provided for each rat, less than half of the boxes were generally utilized by the population on any given day. Means and standard deviations for daily number of nest boxes utilized were 4.1591.07, 6.08• 5.77• and 4.77• for replications one to four, respectively. A mean number of 1.96 rats were found in each nest box utilized on a given day (replications combined) suggesting a certain degree of mutual tolerance. Rats did not segregate by strains in nest box utilization. Some nest boxes were utilized more than others (F----5.95, df----ll/36, P<0.001). Nest-box utilization ranged between 0.23 and 2.33 rats per day depending on its location. Nest boxes nearest and farthest from the observation window (Fig. 1) were utilized most frequently suggesting a preference for shelter at the ends of a row of potential sites. Some subjects were not always found in nest boxes at 18.30 hours daily. The total number o f days in which individuals were not residing in nest boxes averaged 1.62, 2.94 and 1.81 for wild, hybrid and domestic rats, respectively. The mean for the hybrid subjects was elevated by two rats which were found in nest boxes a combined total of only three times. These strain differences were not significant (F=1.35, df= 2/45). The mean number of consecutive days in which rats were found in the same nest box were surprisingly low (Table VI). Correlations between this variable and cross-strain dominance scores were not significant for competitive interactions (Table VI) and two of the four spontaneous interaction analyses. Strains did not differ in the number of consecutive days of nest box residency (F=0.86, df=2/45). The number of different next boxes utilized by individuals during the 13-day test period (adjusted for total number of days tenancy in nest boxes) did not differ for strains (~----6.4, 7-4, and 6.9 for wild, hybrid and domestic rats, respectively; F-- 1.28, df=2/45).
.of... &.._I',9,: I 2 ~ 4- 5 6 7 8 9 IO II 12 13 14 15 DAYS Fig. 2. Tota| no. of spontaneous and
competitive inter-
actions and strain differences in activity over the 13-day test period (replications combined).
Discussion Domestic rats were most dominant in both spontaneous and competitive cross-strain ifiteractions. Assuming that a positive correlation
540
ANIMAL
BEHAVIOUR,
20,
3
Table VI. Mean No. of ConsecutiveDays in the Same Nest Box and Correlation CoefficientsBetweenIndividual Values and Spontaneous and Competitive Cross-Strain Dominance Scores
Replication
Spearman rank correlation coefficient
Strain Wild
Hybrid
Domestic
1
1.61
1.23
2.~0
--0.03 NS
--4).31 NS
2
1-21
1.16
1.19
0.35 NS
0.29 NS
3
1.29
1.53
1.26
0.69 P<0-05
--0-20 NS
4
1-16
1-15
1.26
0.64 P<0.05
0.55 NS
Total
1.32
1.27
1.43
exists between aggressive potential and dominance (which may not be a valid assumption) this result does not support the hypothesis (Barnett 1963; Robinson 1965)that the laboratory rat is more 'docile' and less aggressive than its wild ancestors. It also argues against the notion that the laboratory rat is biologically 'degenerate' (Lockard 1968) due to a century or more of breeding in captivity (Robinson 1965). However, it does not refute the finding (Barnett 1960, 1963; Calhoun 1963; Galef 1970) that the wild Norway rat is more aggressive than the domestic rat when approached by a strange individual in a familiar environment, since, in the present study, all individuals were placed in the experimental room at the same time. The superior dominance of the domestic rats in the present study can be explained in several ways. Hall & Klein (1942) reported marked differences in aggressiveness between two strains of rats bred for open-field elimination (emotional reactivity). The non-emotional subjects initiated 326 aggressive encounters in contrast to sixty-eight interactions for the emotional strain. The emotionally reactive subjects retaliated only 18 per cent of the times they were attacked. Billingslea (1941), likewise, reported reduced aggression among rats of an emotional strain relative to rats of a non-emotional strain in competition for food. Barnett (1963) and Robinson (1965) have summarized the wealth of literature documenting the high emotional reactivity of the wild Norway rat relative to its domesticated counterpart. If emotional reactivity and aggressive tendencies are negatively correlated, one would predict
Spontaneous
Competitive
wild rats to be socially subordinate to domestic rats. The highly developed inhibitions of the wild rat in response to novelty may be based on factors promoting social inhibitions as well. Lorenz (1965) has asserted that one of the effects of breeding animals in captivity is a gradual loss of social inhibitions (p. 94). Spontaneous interactions initiated by laboratory rats often appear to be highly play-motivated (Grant & Chance 1958; Baenninger 1970). Domestic rats may engage in such spontaneous interactions with few social inhibitions. Seward (1945) characterizes much o f the dominant behaviour of laboratory rats as 'bullying'. The more socially inhibited wild rat may interpret the play-oriented activities of the laboratory rat as dominance displays and sustain psychological defeat without engaging in a dominance determining contest ('bully effect'). Dominantsubordinate relationships so established could be maintained during subsequent competitive encounters until a dominance-determining struggle confirmed or reversed the relationship. A second explanation for the superior dominance of the domestic subjects concerns the postulated increased gonadal activity of the domestic strain (Richter 1954; Richter & Uhlenhuth 1954). A positive relationship between gonadal funtion (specifically, androgens) and aggressive behaviour has been documented (Rothballer 1967; Sigg 1969). Hence, on this basis one could predict higher levels of aggressiveness in the domestic subjects than in their wild counterparts. Although increased gonadal function is believed to accompany the domestication process (Hale 1962) it would seem mal-
BOREMAN & PRICE: SOCIALDOMINANCE IN WILD AND DOMESTIC NORWAY RATS adaptive for a population of captive animals to exhibit a corresponding increase in aggressive behaviour (Price & King 1968). Perhaps the dominant status of the domestic rats is not earned as much as it is 'forced' upon them in response to a general submissive attitude of the wild rats in cross-strain interactions. A third explanation relates to strain differences in body size. Correlations were found between body weight and cross-strain dominance scores in half of the replications of both spontaneous and competitive interactions. Correlations were significant in all four replications when dominance scores were based on the combined outcomes of spontaneous and competitive interactions. In addition it was noted that correlations were greatest in those replications in which strain differences in body weight were greatest (Table IV). On the other hand, within-strain dominance did not correlate with body weight, confirming the report of Baenninger (1970) but conflicting with Hall & Klein (1942) and Schumsky & Jones (1966). In addition, hybrid dominance varied considerably between spontaneous and competitive interactions suggesting that, if important, body size does not confer the same advantages in spontaneous and competitive interactions. Body size may influence strain differences in relative dominance only when marked strain differences in body size exist. The superior dominance of the domestic strain in competitive interactions cannot be explained by strain differences in water requirements (thirst), in that daily water intake per unit body weight is similar for both wild and domestic strains (Sloan, personal communication). The lack of correlation between dominance scores in spontaneous and competitive interactions was also reported by Baenninger (1970) for the laboratory rat. This result seems as valid for wild rats as for their domestic counterparts. As Baenninger (1970) and Grant & Chance (1958) suggest, spontaneous interactions may lack much of the aggressive motivation of competitive struggles and may, in fact, represent responses akin to play. In any case, the data obtained in this study supports the thesis that dominance is not a unidimensional trait; that the expression of dominance may, at least in part, be dependent on the motivational state of the interacting animals. Domestic rats interacted more frequently than wild rats, with the exception of cross-strain spontaneous encounters (Table V). The ratio of
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total spontaneous and competitive interactions was much more divergent for domestic subjects than their wild counterparts. The interaction rate of the domestic subjects changed (increased) most abruptly in response to competition for the opportunity to drink. This may have been due, in part, to the greater activity (availability) of the domestic rats, particularly during the period of restricted drinking or it may be related to strain differences in relative dominance. Baenninger (1966) found that rats higher in the hierarchy engage in more interactions than those lower in rank. Boice (1969) reported frequent physical contact in groups of all hooded rats, wheres in groups of wild-caught rats physical contact was relatively limited. The lack of nest-box defence, the frequent shifts in nest-box utilization by both dominant and subordinate subjects, and the simultaneous occupancy of nest-boxes by both wild and domestic rats, suggest that territoriality had little or no influence on the outcome of social interactions observed. The fact that all subjects were placed in the experimental room at the same time could have inhibited any expression of territorial behaviour. This same stock of wild rats was found to be extremely aggressive toward domestic rats when the latter were introduced into an area familiar to the former (Price, personal observation) whereas 'established' domestic rats showed little or no aggression toward intruders. This finding supports Barnett's (1963) hypothesis that the true aggressive potential of the wild rat is best expressed in the context of territorial defence, whereas domestic rats may be more adapted for the social hierarchy, a natural consequence of high density interactions in confined populations (Davis 1958; Anderson 1961). An analogous phenomenon has been reported for the wild house mouse, Mus musculus, in which its social organization shifts from territoriality to the dominance hierarchy when it is taken from the field and placed in captivity (Crowcroft 1955). Thus, wild and domestic rats may have evolved different social behaviours to maximize fitness in their respective 'natural' environments.
Acknowledgments This investigation was supported by State University of New York Research Foundation Grant 10-7104-A and a National Science Foundation Undergraduate Research Participation Grant to the State University of New York College of Forestry. Mr Boreman collected the
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d a t a a n d D r Price is responsible for the m a n u script. REFERENCES Anderson, P. K. (1961). Density, social structure and non-social environment in house-mouse populations and the implications for regulation of numbers. Trans. IV. Y. Aead. ScL, 23, 447--451. Baenninger, L. P. (1966). The reliability of dominance orders in rats. Anim. Behav., 14, 367-371. Baenninger, L. P. (1970). Social dominance orders in the rat: "spontaneous", food, and water competition. J. comp. physioL PsyehoL, 71, 202-209. Barnett, S. A. (1960). Social behaviour among tame rats and among wild-white hybrids. Proe. zooL Soe. Lond., 134, 611-621. Barnett, S. A. (1963). The Rat: A Study in Behaviour. Chicago: Aldine. Barnett, S. A. & Stoddart, R. C. (1969). Effects of breeding in captivity on conflict among wild rats. J. MammaL, 50, 321-325. Billingslea, F. Y. (1941). The relationship between emotionality and various other salients of behavior in the rat. J. comp. PsyehoL, 31, 69-77. Boice, R. (1969). Dominance and survival in stressed wild and domesticated Norway rats. Proc. Am. PsyehoL Ass., 77th Ann. Cony., pp. 187-188. Brown, J. (1964). The evolution of diversity in avian territorial systems. Wilson Bull., 76, 160--169. Calhoun, J. B. (1963). The Ecology and Sociology of the Norway Rat. Bethesda, Maryland: United States Department of Health, Education and Welfare, Crowcroft, P. (1955). Territoriality in wild house mice, Mus museulus L. J. MammaL, 36, 299-301. Davis, D. E. (1958). The role of density in aggressive behaviour of house mice. Anim. Behav., 6, 207210. Eibl-Eibesfeldt, I. (1970). Ethology: The Biology of Behavior. New York: Holt, Rinehart & Winston. Galef, B. G. (1970). Aggression and timidity: responses to novelty in feral Norway rats. J. eomp. physiol. PsychoL, 70, 370--381. Grant, E. C. (1963). An analysis of the social behaviour of the male laboratory rat. Behaviour, 21, 260281. Grant, E. C. & Chance, M. R. A. (1958). Rank order in caged rats. Anita. Behav., 6, 183-194.
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