Anim. Behav., 1974, 22, 634-637

SEXUAL AROUSAL, THE COOLIDGE EFFECT AND DOMINANCE IN THE RAT (RA TTUS NOR VEGICUS)

BY RICHARD E. BROWN Department of Psychology, Dalhousie University

Abstract. Male rats were ranked in dominance orders, were allowed to copulate to exhaustion and then were tested for sexual rearousal in five different treatment conditions. Novel females rearoused 60 per cent of the males to ejaculation. Five-minute encounters with dominant or subordinate males stimulated 33 per cent to ejaculation with a familiar female. Fifteen per cent ejaculated with the familiar female after a 5 rain rest and 15 per cent after an encounter with an unknown male. The degree of re- arousal was not related to fighting or to mounting during male-male encounters, nor did the dominant males show a higher degree of sexual potency.

Male rats that copulate to exhaustion with a single female show a greater renewal of sexual behaviour when the familiar female is replaced by a novel female than when the same female is removed and replaced. This rearousal phenom- enon, termed the Coolidge effect, occurs whether the novel female is fresh (unmated) or has mated recently with another male (Wilson, Kuehn & Beach 1963). Attempts to rearouse sexual behaviour by replacing the familiar female after moving the exhausted male to a new test environment (Beach & Ransom 1967) or after allowing the exhausted male one intro- mission with a novel female.(Cherney & Bermant 1970) have not been successful. Cherney & Bermant suggested that the male's capacity for sexual rearousal may depend on particular patterns of social behaviour of the species, such as dominance in a male hierarchy.

Dominance orders have been reported for both wild (Barnett 1967) and laboratory rats (Baenninger 1966, 1970). The high incidence of courtship behaviour (sexual rolls and rubs) shown by dominant males following a chase or fight led Calhoun (1962, p. 182) to suggest that aggression increased sexual arousal. A high potential for sexual rearousal in species having dominance orders therefore may be due to the association of sexual arousal with non-sexual emotional arousal such as that caused by aggression.

The aim of the present experiment is to test the hypothesis that sexually exhausted dominant males will be more highly rearoused to resume copulation with a familiar female following an aggressive encounter than will subordinate males.

Methods Subjects

The subjects were twenty, male, Long-Evans

rats. The stimulus females used were thirty rats of the same strain. Males were purchased when 30 days of age and housed in groups of four in 24 x 46 x 15-cm clear plastic cages which had wire tops and sawdust-covered floors. Females were purchased when 70 days of age and kept in groups of three in the same type of cages. At the start of the dominance tests the mean age of the males was 42 days and at the start of the sexual rearousal tests, 100 days. Females were ovariectomized when about 80 days old, and their mean age at the start of the sexual rearousal tests was 110 days.

Both males and females were housed in the same room under a 16-hr light cycle with the dark period beginning at 13.00 hours standard time. Testing was carried out between 13.30 and 18.00 hours. Two 25-W red lights were on continually in the housing room. Except during dominance tests, food and water were available ad libitum.

Apparatus Dominance tests were conducted in a 23 x 41

x 38-cm high plywood box which had a black floor and walls. A food cup with a 3-cm opening was recessed into the centre of the floor. Sexual rearousal tests were conducted in two semi- circular arenas which were 30.5 cm in radius and 25.4 cm high. These arenas had plywood floors and stainless steel sides with Plexiglas fronts and tops. Sawdust covered the floor and was replaced after each test period. Mounted on the top of each arena was a 7.6 x 15.2 x 7.6-cm high stainless steel holding box with a sliding floor from which females and stimulus males were introduced.

Procedure Subjects took part in nine dominance com-

634

BROWN: SEXUAL AROUSAL, COOLIDGE EFFECT AND DOMINANCE IN RATS 635

petitions with each of the three cage mates and then in a set of five sexual rearousal tests, each with a different rearousal treatment.

Dominance. Subjects were familiarized with the dominance arena by being fed wet mash in it for 15-rain periods on four consecutive days. On the latter two periods the subjects had been 22-hr food deprived and were kept on this deprivation schedule during the dominance tests. These tests were conducted in nine 'round robins' (Becker & Flaherty 1968) with each male competing for wet mash with each of the other three members of his cage. Each subject participated in one 5-min test per day. The time spent dominating the food cup by each subject during the competition was indicated on a constant speed pen recorder. Following the first, third, fifth and seventh round robins, 3-day rest periods were given with food available ad libitum so that normal growth would be main- tained.

Sexual rearousal. After completion of the dominance tests each male was given sexual experience by being placed with an oestrous female for 1 hr per day until at least one intro- mission was recorded. For most males this required one to three sessions.

Females were brought into oestrus by intra- muscular injection of 0.1 mg estradiol benzoate in 1 ml corn oil 60 to 72 hr and 1.0 mg proges- sterone in corn oil 4 to 6 hr before the start of each test. About 30 min before the test period females were checked for behavioural oestrus by placing them with an indicator male, and only those showing lordosis and accepting intro- mission subsequently were employed.

Subjects took part in five sexual rearousal tests spaced 13 to 20 days apart. Each test consisted of three phases: exhaustion, rearousal stimulus, and rearousal test. In the exhaustion phase, males were placed in the arena for 5 min before a female was introduced. Copulation

then continued undisturbed until one of two criteria for sexual exhaustion was satisfied: 30 min without intromission or 2 hr without ejaculation. The female then was removed and the second phase began. This phase lasted 5 min and consisted of a rest period in two treatment conditions and the introduction of a male rearousal stimulus in the other three. The stimulus male then was removed and the familiar female or a novel female replaced to start the third phase which continued until the criterion for sexual exhaustion was satisfied a second time. The five rearousal treatments are shown in Table I.

The treatments were given in random order with the restriction that each cage of subjects receive a different treatment on the first rearousal test. The dominant subject in each cage did not take part in treatment (Dom.), nor did the sub- ordinate subject take part in treatment (Sub.). These subjects received only phase one of these treatment conditions but did receive all other treatments. In all test periods (dominance, exhaustion and rearousal) the test room was dark except for a 25-W red light positioned 60 cm above the apparatus.

The following measures of sexual behaviour were recorded: (a) intromission latency (IL): latency from the introduction of the female to the first intromission; (b) mount frequency (MF): number of mounts without intromission before each ejaculation; (c) intromission frequency (IF): number of mounts with intromission before each ejaculation; (d) ejaculation frequency (EF): number of ejaculations before exhaustion; (e) exhaust time (ET): the time between the first intromission and the final ejaculation.

Results Dominance. A dominance order was calculated for each cage by ranking the subjects on the number of competitions of each round robin

Table I. Five Treatment Conditions Following Sexual Exhaustion (Phase One)

Group Phase two rearousal stimulus Phase three rearousal test

Familiar female (Fam.)

Novel female (Nov.)

Dominant male (Dom.)

Subordinate male (Sub.)

Unknown male (Un.)

5 min rest Familiar female

5 min rest Novel female

Dominant male Familiar female

Subordinate male Familiar female

Unknown male Familiar female

636 A N I M A L B E H A V I O U R , 22, 3

Table II. Coefficient of Concordance (W) for the Stability of Dominance Orders in the Five Cages of Males

Cage W X2*

1 0"837 20"09

2 0"287 6"89

3 0-427 10-25

4 0"754 15"83

5 0.801 19-22

*Z2(0.05; 3) = 7-82

in which they dominated the food cup for at least 6 s longer than their competitor. Few responses to the food were shown during the first round robin; therefore, these results were omitted from the calculation of dominance orders. The results of a Kendall coefficient of concordance (Siegel 1956) shown in Table I I indicate that four cages had dominance orders which were stable at the 0-05 level of significance. The fifth was stable at the 0.10 level.

Pairwise comparisons computed using the Wilcoxon matched-pairs-signed ranks test (Siegel 1956) indicated that the dominant males reliably dominated all three of their sub- ordinates in cages 1 and 5, the lower two in cages 3 and 4, and only the most subordinate in cage 2.

S e x u a l rearonsal. Table I I I shows the mean percentage of males in each rearousal treatment achieving at least one mount, intromission or ejaculation in phase three and the error mean square (b2) from a randomized block analysis of variance. This analysis indicated that the only behaviour influenced significantly by the treat- ments was the percentage of males ejaculating.

With Rodger's (1967) method for unrestricted tests which uses the special value F = 1.85

for df= 4, 16 and sets the rate of null contrast rejection at 0.05, a set of four mutually ortho- gonal contrasts was found with one null rejection. This rejection indicated that the introduction of a novel female rearoused significantly more males to ejaculate than replacing the familiar female after a rest period or stimulation by an unknown male. Taken as a set, decisions for the four contrasts indicate that stimulation by a known male, whether subordinate or dominant, rearoused more males than a rest period or stimulation by an unknown male, but not as many as the introduction of a novel female.

The number of mounts and fights during the male-male interaction (phase two) was not correlated with the degree of sexual rearousal in phase three. Mounting occurred about twice as often as fighting whether or not the males subsequently ejaculated.

S e x u a l behaviour during phase one. A com- parison of sexual behaviour recorded during phase one failed to show increased sexual potency in dominant males. The results of randomized block analysis of variance on the mean scores for each behavioural pattern using Rodger 's special F = 2.36 for error-rate 0.05 and df = 3, 12 are shown in Table IV.

Discuss ion The results suggest that sexual rearousal can be increased following interaction with a known male, but not to the degree that it is increased by the introduction of a novel female. Actual aggression, however, was not a necessary stimulus for sexual rearousal; nor was the dominant male more sexually potent than the subordinates.

Non-sexual stimuli have been shown to increase sexual behaviour by causing moderate increases in arousal. Beach (1947) states that male dogs and chimpanzees may display erection

Table IlI. Mean Percentage of Males in Each Treatment Condition Aehievhig One Mount, One Intromission, or One Ejaculation in Phase Three. Abbreviations are Explained in Table I.

Treatment condition

Behaviour Fam. Nov. Dom. Sub. Un. 6 z F

Ejaculation 15 60 33 33 15 645.63 2"64

Intrornission 65 75 53 60 55 1253.38 0.31

Mount 90 95 87 80 85 582.44 0"33

No response 10 5 13 20 15 m - -

BROWN: SEXUAL AROUSAL, COOLIDGE EFFECT AND DOMINANCE IN RATS 637

Table IV. Mean Sexual Behaviour Measures During Phase One in Relation to Dominance Order. Abbreviations are Explained in the Text

Dominance Order

Behaviour 1 2 3 4 ~ 2 F

IL (s) 117-5 87-6 60-2 99-3 5061-68 0.57

EF 6.2 5-6 5-8 5'8 0'95 0.32

MF 59 "8 41 "4 50.6 53 "0 301-29 0-96

IF 55 "6 47-0 55"0 55 "8 171 '64 0.53

ET (rain) 97.7 90.0 90-6 101.0 97.87 1.48

and ejaculation in the presence of fear-producing stimuli. Painful electric shocks will arouse and cause pacing of sexual behaviour in male rats (Barfield & Sachs 1968), and also increase copulat ion in the number of virgin males on their first contact with a female (Caggiula & Eibergen 1969).

Acknowledgments I would like to express thanks to Dr R. S. Rodger and Dr P. H. R. James for their suggestions and criticisms.

The research was supported by a grant from the Nat ional Research Council of Canada to Dr P. H. R. James.

REFERENCES Baenninger, L. (1966). The reliability of dominance orders

in rats. Anita. Behav., 14, 367-371. Baenninger, L. (1970). Social dominance orders in the

rat: 'spontaneous', food and water competition. J. comp physiol PsychoL, 71, 202-209.

Barfield, R. J. & Sachs, B. D. (1968). Sexual behaviour: stimulation by painful electrical shock to skin in male rats. Science, N.Y., 161, 392-395.

Barnett, S. A. (1967). A Study in Behaviour. London: Methuen.

Beach, F. A. (1947). A review of physiological and psychological studies of sexual behaviour in mammals. Physiol. Rev., 27, 240-307.

Beach, F. A. & Ransom, T. W. (1967). Effect of environ- mental variation on ejaculatory frequency in male rats. J. comp. physioL PsychoL, 64, 384-387.

Becker, G. & Flaherty, T. B. (1968). Group size as a determinant of dominance--hierarchy stability in the rat. J. comp. physioL PsychoL, 66, 473-476.

Caggiula, A. R. & Eibergen, R. (1969). Copulation of virgin male rats evoked by painful peripheral stimulation. J. comp. physiol. PsychoL, 69, 414- 419.

Calhoun, J. B. (1962). The Ecology and Sociology of the Norway Rat. Public Health Service Publication No. 1008, U.S. Department of Health, Education and Welfare.

Cherney, E. F. & Bermant, G. (1970). The role of stimulus female novelty in the rearousal of copulation in male laboratory rats (Rattus Norvegicus). Anita. Behav., 18, 567-574.

Rodger, R. S. (1967). Type II errors and their decision basis. Br. J. Math. & Star. PsychoL, 20, 187-204.

Siegel, S. (1956). Nonpararnetric Statistics. New York: McGraw-Hill.

Wilson, J. R., Kuehn, R. E. & Beach, F. A. (1963). Modification in the sexual behaviour of male rats produced by changing the stimulus female. J. comp. physioL PsychoL, 56, 636-644.

(Received 3 August 1972; revised 8 January 1973; second revision 11 December 1973; MS. number: A1361)

SWANSON: SEX DIFFERENCES IN BEHAVIOUR OF THE MONGOLIAN GERBIL

P L A T E X X I

Illustration of some postures shown by gerbils in a mixed sex encounter. The female is marked on the back with black hair dye. (1) Female noses male; male turns away with ears back. (2) Mutual posing. (3) Male sniffs female's ventral scent gland. (4) Male sniffs female's ano-genital region; sniff and follow. (5) Female threatens male in upright offensive posture; male threatens in sideways offensive posture ambivalent). (6) Male marks sawdust with ventral scent gland.

Swanson, Anita. Behav., 22, 3

A N I M A L B E H A V I O U R , 2 2 , 3

P L A T E X X I I

Sequence of action shots during fight between two gerbils of opposite sex. The female is marked on the back with black hair dye. (1) Mutual investigation: note that the male has his ears back and eyes partly closed indicating a defensive attitude. (2) Male sniffs female's chin, but female's head is higher than male's suggesting an offensive position. (3) Female attacks male. (4) Fight breaks off and female chases male. (5) Fight resumes and becomes so violent that both animals jump into the air still locked together. (6) Male jumps to evade female. (7) Fight continues on ground. (8) Fight ends by female chasing male, who flees with tail in the air.

Swanson, Anim. Behav., 22, 3