AGGRESSIVE BEHAVIOR Volume 18, pages 129-138

Responses of Dominant and Subordinate Male Rats to the Odors of Male and Female Conspecifics Richard E. Brown

Department of Psychology, Dalhousie Universiu Halifax, Nova Scotia, Canada

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The resident-intruder paradigm was used to examine the effects of social dominance and individual recognition on odor preferences and urine-marking in male rats. Resi- dent males were significantly more aggressive than intruders and spent more time inves- tigating the odors of familiar intruders. Resident males urine-marked most over the odors of females and familiar intruders while intruders marked least over the odor of the familiar resident. Intruders did not avoid investigating nor marking over the odors of familiar resident males or other conspecifics. These results suggest that individual odors of male rats may be more salient than a general odor of dominance, and that the dominant males increase their investigation and marking over the odors of familiar sub- ordinates but not unfamiliar subordinates. The importance of olfactory learning dur- ing aggressive interactions is discussed.

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Key words: aggression, dominance, individual odors, odor preferences, urine-marking, rats, Ra#us

norvegicus

INTRODUCTION

The odors released from the urine, feces, and specialized scent glands of mammals can be used to identify the species, colony, age, sex, reproductive state, social status, and the individual identity of the animal that produces them [Brown, 1979, 1985al. An animal carries its “social odor” with it and scent-marks its environment with this odor, both actively and passively, so that its home area is pervaded with olfactory signposts. In many species of mammals, scent-marking is related to an animal’s

Received for publication September 26, 1990; accepted February 12, 1991.

Address reprint requests to Richard E. Brown, Department of Psychology, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4J1.

This research was supported by grant A7441 from the NSERC of Canada. I would like to thank Sonya Major and Robin Kind for their assistance with this study.

0 1992 Wiley-Liss, Inc.

130 Brown

dominance status and is motivated by prior sexual and aggressive encounters and by the presence of the odors of conspecifics [Gosling, 1982; Johnson, 1973; Ralls, 19711.

During social interactions, rats learn to associate the odors of conspecifics with their behavioral responses and form an odor-based “social memory,” which can be used in future social interactions [Thor, 1979; Thor and Holloway, 19821. Isolation rearing removes the opportunity to learn appropriate responses to the olfactory signals of con- specifics and short periods of sociosexual experience reinstate normal odor preferences [Brown, 1985b, 19911. Sexual experience increases the responsiveness of male rats to female odors [Brown, 1977, 19911 and establishes a preference for the odor of estrus over diestrus females [Lydell and Doty, 19721 and social interactions with other males influence responses to the odors of these males [Birke and Sadler, 1984; Brown, 19911.

Rats can discriminate between dominant and subordinate males by their odor alone [Krames et al., 19691; between the odors of individual males [Brown, 1988; Hopp et al., 19851 and between the odors of familiar and unfamiliar males [Krames and Shaw, 19731, so each male’s odor contains information on his individual identity as well as his dominance status [Brown, 19791. The odors of dominant males may be qualita- tively or quantitatively different than those of subordinate males, but the odors of indi- vidual dominant and subordinate males also show differences in chemical profiles, at least in mice [Apps et al., 19881; thus, it is possible that rats may be able to discrimi- nate between the odors of individual dominant and subordinate males.

Dominant male rats urine mark more than subordinates [Adams, 1976; Taylor et al., 19881 and, after being attacked and bitten by a resident male, male rats show reduced investigation and urine-marking in the home cage of that resident male [Adams, 19761. These results suggest that the rat’s experience with a particular dominant male alters its response to the individual odor of that male. It is, therefore, possible that the individ- ual odor of the dominant male is learned during an agonistic interaction and that fol- lowing this agonistic encounter, subordinate males avoid the odor of the individual male that defeated them, but not the odor of other, unfamiliar dominant males. Such a result might be predicted from the results of Adams [1976], but the response of the defeated male to unfamiliar dominant males was not examined in this study. If, on the other hand, male rats respond to a general odor of dominance, as suggested by Krames, Can; and Bergman [ 19691, subordinant males should avoid the odors of both familiar and unfamiliar dominant males. Likewise, dominant males may respond differently to the odors of individual subordinate males or respond to a general odor of subordinate males.

Rats show two responses to the odors of conspecifics: investigation and urine-marking; and social experience in adulthood modifies both of these responses [Birke and Sadler, 1984; Brown, 1977, 1985b, 1986, 1991; Hopp and Timberlake, 19831. The present study, therefore, examines the investigation and urine-marking responses of dominant and subordinate male rats to the odors of familiar and unfamiliar males as well as a neutral odor and the odors of female rats. The first question of interest is whether resi- dent and intruder males respond differently to the odors of familiar and Unfamiliar males. Previous experiments have shown that male rats investigate and urine-mark the odors of female rats more than the odors of males, irrespective of the stage of the female’s estrus cycle [Brown, 1977, 1985b, 19861. Thus the second question of interest is whether resident and intruder males respond differently to the odors of females.

The preference test method can be used to investigate both the attraction and aversion of rats to the odors of conspecifics by comparing the responses of rats to these odors and to a

Dominance Status and Odor Preferences 131

neutral odor, such as water. An odor is attractive if it is preferred to the neutral odor and is aversive if the neutral odor is preferred to it [Irwin, 19611.

MATERIALS AND METHODS Subjects

Twenty male Long-Evans hooded rats, born at Dalhousie University to parents pur- chased from Charles River Canada (St. Constant, Quebec), served as subjects. After weaning at 22 days of age, they were housed in groups of four in 46 X 64 X 16 cm Wahman hanging cages. At about 90 days of age they were housed individually in 23 X 46 x 16 cm plastic cages with wire tops and wood shavings for bedding. All animals were maintained on a 12:12 reversed 1ight:dark cycle with lights off at 10:00 A.M. and all experimental procedures were conducted during the dark phase. Throughout the study all rats had ad lib access to Purina Rodent Laboratory Chow and water.

Procedure The resident-intruder paradigm for eliciting aggressive behavior was used to estab-

lish pairs of dominant and subordinate male rats [Adams, 1976; Barfield et al., 19721. Since sexually experienced males show an increase in aggressive behavior [Flannelly and Lore, 19771 and investigate odors and urine-mark more than sexually naive males [Brown, 1977, 19911, all of the subjects were given sexual experience. The experi- ment thus had three phases: sexual experience; resident-intruder interactions; and odor investigation and urine marking tests.

Sexual experience. All males received sexual experience with an estrus-induced ovariectomized female when they were between 100 and 120 days of age. Females were brought into estrus with injections of 0.05 mg estradiol benzoate (Sigma) in corn oil 54 hr before testing and 0.5 mg progesterone (Sigma) in corn oil 4-6 hr before testing. Estrous females were placed into the male’s home cage for 12 hr on each of two occa- sions, separated by a one week interval.

Resident-intruder interactions. Immediately following their sexual experience, males were randomly assigned to pairs with one designated as the “Resident” and the other as the “Intruder.” The intruder was then placed into the home cage of the resident for a 5 min period every second day for 10 trials and the agonistic behaviors recorded. To allow greater room for the rats to maneuver and greater visibility for the experimenter, the metal cage top was removed during these encounters and an empty plastic cage, identical to the housing cage, was placed upside-down over the home cage and held in place by metal clips.

During the agonistic interactions the frequency of each of eight behaviors was recorded for each male. These behaviors were sniff; aggressive groom; offensive sideways pos- ture; full aggressive posture; bite and kick attack; crouch; defensive sideways posture; and the full submissive posture [Grant, 1963; Grant and MacKintosh, 1963; Lehman and Adams, 19771. The mean frequency of bouts of sniffing the other rat, an aggres- sion score (sum of aggressive groom, offensive sideways posture, full aggressive pos- ture, and bite and kick attack), and a submission score (sum of crouch, defensive sideways posture and full submissive posture) were calculated over the 10 trials, and correlated samples t-tests were used to compare the resident and intruder males on each of these three scores.

132 Brown

Odor investigation and urine-marking tests. Following the agonistic interactions, males were rehoused in Wahman hanging cages (so their urine could be collected) and given a series of odor investigation and urine marking tests. At the start of the odor investigation tests, the subjects were about 156 days of age and weighed an average of 451.8 ? 5.7 g. Resident males (449.7 * 8.7 g) weighed slightly less than intruders (454.0 2 7.9 g), but this difference was not significant (t(9) = 0.305).

Stimulus odors. The stimulus odors used for the odor investigation tests included urine from male rats (M) and intact cycling female rats (F) and a neutral odor (N = water). The subjects in the experiment served as the male urine donors and six intact females served as female urine donors. Urine was collected by attaching a stainless steel funnel beneath the animal’s home cage so that urine could be collected without disturbing the donor. The funnels had two layers of wire mesh (0.5 cm2 and 0.2 cm2) and drained into a urine collection bottle which was covered in gauze bandage to pre- vent feces and other debris from landing in the urine [Brown, 19881. Urine was col- lected for 4-6 hr and then kept refrigerated in covered glass beakers at 4°C and was used within 24 hr of being collected. The funnels were cleaned daily to prevent contamination.

Test procedure. Odor investigation and urine-marking tests were conducted in clear plastic cages which were identical to the rat’s home cages (23 X 43 X 16 cm). These cages were placed upside-down on a Lucite table top covered with unprinted newsprint and used as test arenas. Odors were presented by placing .05 ml urine from a syringe onto a 10 X 5 X 2.5 cm wire mesh block covered with a 20 X 20 cm piece of paper towelling which was held in place with masking tape. One block was placed at each end of the test arena. After each odor preference test the newsprint was removed, the table top was cleaned with warm water, and fresh newsprint laid down. Fresh test blocks were used for each subject, and these blocks were washed each day with warm water and detergent (Ivory liquid), dried, and not used again for 24 h.

Each rat was tested with all pairs of four different odors, resulting in six, 5-min preference tests. The order of presentation of these tests was randomized over 6 test days for each male. Testing took place in a dimly lit room (40 W bulb in a lamp on the floor) during the first 6 hr of the dark phase of the 1ight:dark cycle. The odors used were water, a neutral odor (N) and urine from intact females (F), familiar males (Mf) and unfamiliar males (Mu). Familiar males were those individuals with whom the test male had interacted for ten trials in the agonistic interactions. Unfamiliar males were males in the same group as the familiar male (resident or intruder) whom he had not met in a social interaction. Thus, resident males were tested with all possible combina- tions of the neutral (N), familiar male intruder (Mf), unfamiliar male intruder (Mu), and intact female (F) odors. Intruder males were tested with all combinations of the neutral (N), familiar resident male (Mf), unfamiliar resident male (Mu), and intact female (F) odors.

Two experimenters conducted the study, with one placing the urine on the blocks and the rat in the test arena and the second observing and recording investigation time and scoring urine-marking. The observer was thus blind to the odors used in each test and whether the subject being tested was a resident or intruder.

Data Recording and Analysis Investigation time. For each of the six pairwise odor tests the time spent sniffing

or manipulating each odorized block was recorded on a running time meter using a set

Dominance Status and Odor Preferences 133

of pushbuttons. To compare the absolute odor investigation scores, the mean time spent investigating each odor was averaged over the three tests in which that odor was paired with all other odors and these times were analyzed in a 2 X 4 (group by odor) split plot Anova [Kirk, 19681.

Urine-marking. After the completion of each 5-min odor preference test, the paper towelling covering each block was removed and the area covered by urine-marks out- lined in pencil. A graduated plastic cover plate was then used to calculate the area marked over each block in cm2 and the transformation X = loglo (cm2 + 1) was then used to establish homogeneity of variance within groups. To compare levels of urine- marking, the areas urine marked over each odor were averaged over the three tests in which that odor was paired with all other odors and split plot ANOVAs were conducted as described for investigation time.

RESULTS Agonistic Behaviors

Resident males sniffed intruders more than intruders sniffed residents and resident males showed more aggressive postures than intruders (Table I). Although the intrud- ers showed more submissive behavior than the residents, this difference was not signif- icant. Using the measure of aggressive behavior, the resident males were considered the dominant and the intruders the subordinate members of the pair.

Odor Preference Tests There was no significant difference in the overall time spent investigating odors by

the resident and intruder males (F (1, 18) = 2.45; Fig. l), but there was a significant difference in time that each odor was investigated (F (3,54) = 13.19, P < . O l ) , and a significant interaction between dominance status and odors (F (3,54) = 3.62, P < .02). Tests of simple main effects [Kirk, 19681 indicated that the only odor which resident males investigated significantly more than intruders was the familiar male odor (F (1, 54) = 11.36, P < .01). Although resident males spent more time investigating female odors than intruders, this difference was not significant. Post hoc contrasts using the method of Rodger [ 19751 indicated that resident males 1 ) did not investigate odors of unfamiliar males more than no odor, 2) did not investigate odors of females more than those of familiar males, and 3) investigated both the odors of females and those of familiar males more than the odors of unfamiliar males and the no odor stimulus (P < .01). Intruder males investigated the odors of females more than the no odor stimulus

TABLE I. Mean ( f SEM) SnitTng, Aggression, and Submission Scores Per 5 Min Interaction for Resident and Intruder Males

Behavior Group

Resident Intruder t"

Snifftng bouts 4.90 (0.27) 3.63 (0.25) 2.28* Aggression score 1.70 (0.22) 0.54 (0.10) 2.35* Submission score 0.24 (0.06) 0.77 (0.47) 1.85

Torrelated samples t-test, two-tailed. *P < .05.

134 Brown

~~ ~

s i d ent s

24 c 0 Intruders

20

16 m

; 12

( “ 8

4

N Mf M” F

Odor

Fig. 1 . Mean time (k SEM) spent by residents and intruders investigating each odor averaged over the three tests with that odor. Abbreviations for odors: N = neutral (water); Mf = familiar male; Mu = unfa- miliar male; F = female.

(P < .05), but did not investigate the odors of familiar or unfamiliar males more than no odor.

Urine-Marking

There were no overall differences between resident and intruder males in the amount of urine marking (F (1, 18) = 1.12) nor any main effects of stimulus odor (F (3, 54) = 1.93), but there was a significant group by odor interaction (F (3, 54) = 4.30, P < .01; Fig. 2) . Resident males marked more than intruders over non-odorized blocks and those with the odors of familiar males and the odors of females, but intruders marked more over blocks with the odor of an unfamiliar male. Intruders marked less over odors of familiar males than over any other odor. Post hoc contrasts indicated that resident males marked more over female odors than the odors of unfamiliar males (P < .Ol) . Intruders showed no significant differences in the amount of urine-marking over the four odors.

The urine marking scores were positively correlated with aggression scores (Pear- son’s r = .26, df = 18) and negatively correlated with submission scores (Pearson’s r = - .36, df = 18) but neither of these correlations was significant at the .05 level.

DISCUSSION

The only significant difference in the odor investigation and urine-marking scores of residents and intruders was in their response to the odors of other males. Residents investigated and urine-marked the odors of familiar intruders more than intruders inves- tigated and marked the odors of familiar residents. These results indicate that rats learn

Dominance Status and Odor Preferences 135

Residents

0 I n t rude rs I 1.2 I-

N Mf M" F

Odor

Fig. 2. Mean area ( 2 SEM) urine marked over each odor by residents and intruders averaged over the three tests with that odor. Abbreviations for odors: N = neutral (water); Mf = familiar male; Mu = unfa- miliar male; F = female.

the individual odor of their social partner during an agonistic encounter. Rats which win agonistic encounters with a particular male come to know the odor of that male and increase their investigation and marking of his odor when it is encountered in a neutral arena. Rats which lose agonistic encounters do not avoid investigating the odor of the male that defeated them, but urine-mark less over this odor than other conspe- cific odors. Thus, the odor of dominance [Krames et al., 19691 seems less salient than the odor of a particular individual male [Halpin, 19801.

These results support previous studies with gerbils and hamsters which indicate that subordinate males do not avoid the odors of males which have defeated them in agonis- tic encounters [Fullenkamp et al., 1987, 1985; Halpin, 19781. Significant inhibition of scent-marking by subordinate males may occur only after prolonged male-male encoun- ters in which the subordinate is severely attacked as has been found in male rats [Adams, 19761, gerbils [Thiessen et al., 19711, mice [Desjardins et al., 19731, and desert woodrats [Fleming and Tambosso, 19801. This decline in marking following defeat in agonistic encounters is situation specific. Male gerbils which lost agonistic encounters to a group of alien gerbils were inhibited from marking in areas which were impregnated with the odors of these gerbils, but were not inhibited from marking in clean areas [Nyby et al., 19701. Similarly, subordinate male desert woodrats decrease marking in the presence of male odors, but mark at high rates in the presence of female odors [Fleming and Tambosso, 19801. As reported by Adams [1976] intruder male rats do not stop urine- marking in a strange environment until after they have been attacked quite violently (bite and kick attack) by the resident male.

Although the resident males in this study were more aggressive than the intruders, the attacks were not violent. In no cases did fighting between residents and intruders result in cuts or bleeding. Thus, if the agonistic encounters had been more intense, the

136 Brown

intruders may have shown a higher level of avoidance of the odor of the familiar resi- dent male. One might hypothesize that learned avoidance of the odor of the dominant male is proportional to the amount of aggression shown by that male. If social condi- tioning is occumng, males should respond differently to the conditioned odors but not to the unconditioned odors, and this is what occurred in the present study. If one were to further examine this social learning, a proper conditioning paradigm should be used, i.e., the conditioned stimulus (odor) should be present before the unconditioned stimu- lus (aggression by the resident male). Conditioning may occur to visual and other cues as well as olfactory cues associated with defeat [Yahr, 19771.

Scent-marks of resident males may provide intruders with a means of assessing poten- tial competitors [Gosling, 19821. According to this hypothesis, the intruder first learns the odor of the resident from his scent-marks and then, when the intruder meets the resident, he compares the scent of the resident with the odor which has previously been encountered, and “when these scents match then the resident is identified and the intruder responds appropriately, usually by withdrawal” [Gosling, 1982, p. 941. Gos- ling and McKay [ 19901 have collected data from house mice which support this hypoth- esis; thus, it is apparent that the relationship between olfactory signals and behavior is reciprocal: behavioral interactions can modify later responses to conspecific odors and olfactory signals can modify later social behavior.

The pattern of olfactory learning and behavioral change may be different for the domi- nant and subordinant males. The dominant male may learn the odor of the subordinate during the social encounter and increase his scent-marking in response to the odor of the subordinate male. When the subordinate male encounters this odor, he may show reduced aggression in a subsequent encounter. Thus, if animals learn to avoid the odors of individuals that are dominant to them (as a result of defeats in agonistic encounters or otherwise), the use of such odor displays could reduce the probability of an actual fight occurring [Brown, 1979, p. 1381. Similar reciprocal interactions occur in the relationship between olfactory signals and sexual behavior. Sexual expe- rience increases the responses of male rats to female odors and priming a female with a male’s odor enhances mating with that individual male [Coopersmith and Banks, 19831.

The “olfactory signature” of the male rat may, therefore, function as an advertise- ment in both agonistic and sexual interactions. Dominant male rats are able to inhibit mating by subordinates [Thor and Carr, 19791 and female rats prefer to mate with dom- inant males [Carr et al., 19821. Male rats urinate prior to copulation and females find this urine attractive [McIntosh et al., 19791. Female rats are attracted more to the odors of males with high testosterone levels than those with low testosterone levels [Brown, 1977; Taylor et al., 19821 and estrous female mice, hamsters, and brown lemmings all prefer the odors of dominant males to those of subordinates [Huck et al., 1981; Jones and Nowell, 1974; White et al., 19841. Female rats are able to identify individual males by their odor [Krames, 19701 and the presence of a male’s urine may enhance the female’s copulatory behavior [Geyer et al., 19781.

Since rats have a “social memory” for the odors of individual conspecifics [Sawyer et al., 19841, there may be many situations in which rats learn to respond to individual animals or their odors in a particular manner. Such a social learning approach will aid our understanding of olfactory communication in rodents and may also provide infor- mation on the biological basis of learning.

Dominance Status and Odor Preferences 137

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