Aversive odors of male mice: Experiential and castration effects,and the predictability of the outcomes of agonistic encounters

The relationship between the aversive urine odors of adult male mice and their agonistic interactions was examined. The urine of 28 isolated intact donors was tested for its aversiveness before the donors had won or lost an agonistic encounter, by spotting a portion of an open field with their urine. Group-housed males (n = 28), each tested with the urine of an ultimate winner and loser, as well as a castrate, avoided both intact types. The urine of castrates was not aversive. Another group of subjects (n = 28), tested with urine collected following the encounter between donors, provided identical results. A second experiment examined the aversiveness of urine from 24 isolate mice, and their responsiveness to urine of other isolates, prior to their encounter. The urine was not highly aversive to the isolates However, winners and losers differed in their responsiveness, as ultimate winners exhibited greater aversion. The results are discussed with regard to territorial maintenance via odors, and how differential responsiveness to odors may influence the outcomes of agonistic encounters.     

Male mice: Social dominance influenced by strange male odors

Male mice (N = 34) were individually raised with a castrated male cagemate from 5 to 15 weeks of age. Half of them were subsequently isolated in clean cages for 2 weeks, while the other half were housed in isolation for 2 weeks in cages that had previously housed a strange male. After 14 days of isolation-housing, one subject from each condition was placed into pairs and observed for 30 min in a neutral arena. On the next day, weights of their preputial glands were measured. Males exposed to strange male odors were more likely to be dominant during the 30-min test and to have heavier preputial glands than were males that had been housed in clean cages.     

Ontogeny of aggressive-sexual behavior between males in lines of Japanese quail (Coturnix coturnix japonica) selected for male mating frequency

Japanese quail from lines bidirectionally selected for high and low male mating frequency and from the random-bred base population were observed in an ontogenetic study of aggressive-sexual behavior. Quail were reared in sex-intermingled flocks until 28 days of age at which time half of the males from each line were housed as all-male flocks and half were transferred to individual cages. At 41 days of age, individually caged males exhibited mounting behavior to win encounters with other males. By 45 days, males from the high and control lines exhibited significantly more aggressive-sexual behavior than those from the low lines. Line x Rearing Experience interactions for mounting behavior at 45 and 56 days of age were due to the individually caged high- and control-line males' winning encounters by mounts; those maintained in flocks rarely mounted. Although some low-line males won encounters by mounts, occurrence of this behavior was infrequent. Males maintained in flocks were placed in individual cages at 57 days of age. When these males were compared with those housed in individual cages from 28 days of age, at 84 days of age and older, the Line x Rearing Experience interaction observed previously disappeared, and only differences among genetic lines were evident. Genetic and rearing experience effects are discussed as influencing agonistic and sexual behaviors.     

Repeated tests of intermale aggression in mice (Mus musculus) are influenced by housing and test conditions

Young adult male Binghamton Heterogenous (HET) mice were housed either individually or in groups of four, in two-tiered cages for 11 days before their agonistic behavior was observed. Pairs of male mice were tested 3 min each day for 9 consecutive days. Agonistic behavior was observed in two-tiered cages in which there were either clean pine shavings or shavings soiled by young adult female HET mice. Housing and shaving conditions interactively influenced aggression observed over the course of testing. That is, when individually housed mice were tested with clean shavings and when group-housed mice were tested with female-soiled shavings, agonistic behavior decreased over days, but when isolated mice were tested in soiled shavings and when group-housed mice were tested in clean shavings, aggression increased over the course of the 9-day test period.     

Effects of losing and testosterone upon subsequent behavior in male and female S3 (Tryon Maze Dull) rats

Attempts were made to determine whether modification of agonistic behavior by experience differs in the sexes and if so, whether testosterone is involved in this response. Gonadectomized male and female CPB-S3 (Tryon Maze Dull) rats were treated with testosterone propionate (TP, 250 μg) or vehicle and subjected to tests in which they became either winners or losers. S3 males and females were tested against Long Evans rats to become losers or against Wistar rats to become winners. Subsequently, S3 winners were tested against losers. In addition, winners and losers were tested against naive S3 opponents of the same sex. After varied agonistic experiences, all animals were tested for social preference in a situation in which they could choose between their respective opponents without the possibility of social interaction. Thereafter, they were also exposed to a two-choice passive avoidance learning procedure to see if the behavioral effects of aggressive interactions generalized to nonsocial learning. Males and females reacted differently to winning or losing, the presence of testosterone being a critical factor in the manifestation of this sex difference. Relatively permanent effects on aggressive and other behaviors were only established in TP-treated males. Losing experiences in the social-preference test generally led to a slight preference for naive, less aggressive animals. Testosterone-treated male losers, the group expected to be most vulnerable to generalized inhibition and impairment of learning, did not differ from other categories in the two-choice passive avoidance procedure, although marked differences were observed between the sexes and between testosterone and oil-treated animals.     

Behavioral consequences of agonistic experiences in the male S3 (Tryon Maze Dull) rat

Aggression occurring during an initial confrontation between two rats may result in significant behavioral changes in one or both animals. The present experiment was designed to study behavioral changes occurring in the course of an agonistic interaction and the consequences of winning or losing. In order to ensure winning, male CPB-S3 Tryon Maze Dull) rats were confronted with males of a more aggressive strain (Long Evans); and to ensure losing they were confronted with those of a less aggressive strain Wistar). Winners were tested against losers, this test being repeated after an interval of 17 days. Winners and losers were also tested with naive S3 opponents. Possible effects of winning and losing in nonagonistic behavioral tests were then examined. These measured open field activity, passive avoidance learning, and masculine sexual behavior. The results replicate and extend earlier findings using a different strain, indicating that significant and relatively permanent behavioral changes are induced in male winners and losers. Behavioral change is most prominent in the losers. Despite the behavioral differences between winners and losers in tests for agonistic behavior, no consistent differences were noted in any of the other behavioral tests.     

Differential sexual activity of isolated and grouped male mice despite testosterone administration

In Experiment 1, adult male C57 mice were castrated, housed individually or in groups of four, and repeatedly injected with either of two doses of testosterone. Control mice were sham-castrated, individually or group housed, and injected with oil vehicle. In repeated tests of sexual behavior with receptive females, isolated males in all surgery-dose combinations showed significantly more mounts and intromissions than did their group-housed counterparts. Ejaculations were fully restored by testosterone in castrated grouped males but not in castrated isolated males. In Experiment 2, administration of either of two doses of testosterone failed to elevate the sexual behavior of intact group-housed males. These experiments show that housing with other males depresses all major measures of sexual behavior, and suggest that this is probably independent of testicular hormones.     

Male-related chemical cues promote sexual receptivity in the female musk shrew

The role of conspecific chemical cues in the activation of sexual behavior was investigated in the female musk shrew (Suncus murinus). In Experiment 1, virgin female musk shrews were exposed to either clean cages or cages recently vacated by an adult male. Regardless of whether the male used for the sexual behavior test was "familiar" to the female (having spent the 24 h exposure in his vacant cage) or "unfamiliar," females exposed to male-related cues received mounts from males significantly sooner than females exposed to clean cages. In Experiment 2, females housed for 24 h in a cage soiled by an adult male allowed males to mount significantly sooner than females housed in a cage soiled by a castrated male, another female, or a clean cage. These results demonstrate that chemical cues, produced exclusively by adult males, promote sexual receptivity in female musk shrews.     

Maternal aggression toward infanticidal males of different social status in wild house mice (Mus musculus domesticus)

Maternal aggression was examined in wild female mice (Mus musculus domesticus) derived from animals trapped in Alberta, Canada. Lactating females were tested for their behavior toward intruder males during the time of postpartum estrus while housed in a two-cage apparatus containing a defensible nest area. Prior to being used as intruders, sexually naive males were screened for their behavior toward a newborn pup (83% exhibited infanticide). Only infanticidal males were then housed in pairs and allowed to establish a dominance hierarchy. Dominance status was further verified by a urine marking test. The dominant and subordinate infanticidal males were then placed into a lactating female's cage and observed for 1 hr. The test was terminated immediately when a male began to attack the pups. Lactating females attacked the males in both groups, but subordinate males received more intense attacks than dominant males. Dominant males elicited significantly more fear/defense behavior than subordinate intruders. All of the dominant males and only one submissive male attacked the pups. Females were thus successful in blocking infanticide only by infanticidal subordinate males. Since females do not persist in attacking males with high fighting ability, one function of maternal aggression could be to assess the fighting, and resource holding, potential of a future mate. © 1994 Wiley-Liss, Inc.     

An ephemeral sex pheromone in the urine of female house mice (Mus domesticus).

From previous research, the ultrasonic vocalizations of male mice (Mus domesticus) to female mouse urine were hypothesized to be learned as a result of classical conditioning during adult heterosexual encounters. According to this interpretation, a previously neutral conditioned stimulus in female urine comes to elicit vocalizations as a result of its association with some other unknown unconditioned stimulus associated with adult females. However, the research from which this hypothesis was derived utilized urine collected from females housed in metabolic cages. Three experiments further examined the classical conditioning hypothesis using two types of female urine: (i) metabolic-cage-collected urine and (ii) freshly voided urine. Experiment 1 demonstrated that, in contrast to vocalizations to metabolic-cage-collected urine, adult heterosexual experience was not necessary for males to vocalize to freshly voided female urine. In addition, unlike metabolic-cage-collected urine (Experiment 3), freshly voided urine remained a potent stimulus for eliciting vocalizations during repeated testing (Experiments 2 and 3). Finally, freshly voided urine appeared to cause a previously neutral stimulus (cotton swab) to acquire ultrasound eliciting properties (Experiment 2). We suggest from these findings that two chemosignals that elicit vocalizations from males may exist in female mouse urine: (i) a potent, but volatile or easily degraded, unconditioned stimulus to which males vocalize without sexual experience and (ii) a nonvolatile, chemically stable conditioned stimulus.     

Variation in aggressive behavior and anatomo-physiological correlates generated by crowding without physical contact in the house mouse

Behavioral, physiological (i.e., endocrine), and anatomical consequences of crowding in mice were studied in a situation where animals were in auditory, visual, olfactory, and tactile contact but restrained from full physical interactions, to prevent overt aggression. Males that cohabited with females undisturbed by neighboring conspecifics showed greater propensity to attack same-sex intruders and had higher plasma testosterone levels than did their “crowded” counterparts, that is, males cohabiting with females and housed adjacent to other male/female pairs. In this respect, the latter animals resembled submissive males. However, a significant increase in weight of androgen-dependent target organs (i.e., seminal vesicles and preputial glands) was found in crowded males. These data indicate that despite the observed inhibition of social aggression these males are not physiologically comparable (homologous) to male mice that experienced defeat and the stress of submission during fighting. The intriguing possibility that different conversion pathway of testosterone are accelerated, as a result of social communication, in males living in these two environments and the behavioral implications of these possibilities are discussed. Finally, the parental behavior of crowded animals, although not freely interacting with each other, was disrupted, causing a marked decrease in reproductive success. In this situation a high incidence of infanticide of their offspring by both parents was observed, whereas this behavior was virtually absent in non-crowded male/female pairs.     

Influence of dominance on the development of play fighting in pairs of male Syrian golden hamsters (Mesocricetus auratus)

In the highly social rat, male juvenile and adult subordinates initiate more playful contacts with dominant pairmates than vice versa. This study examined the effect of dominance on playful contacts in the relatively asocial golden hamster. Pairs of male hamsters were reared together from weaning, and their play was filmed in the juvenile (28-36 days) and the young adult (60-70 days) stages of development. By the adult stage, it became clear that one pairmate was dominant over the other. The dominant pairmate launched all aggressive attacks (i. e., bites to the lower flanks and rump), and the subordinate pairmate performed all the submissive gesturing (e. g., tail up submissive posture). Playful contact, which in this species involves gentle nibbling of the posterior cheeks, was more frequently launched by the dominant than by the subordinate. This was not only true at the adult stage, but also at the juvenile stage, before dominance-subordination relationships were sharply polarized. Therefore, it would appear that in the relatively asocial hamster, the subordinates tend to avoid playful contact with dominants. This is markedly different to rats, where the subordinates actively seek out and engage dominants in play. This contrast further supports our hypothesis that subordinate male rats use play as a means of maintaining familiarity with dominants. © 1993 Wiley-Liss, Inc.     

Causal attributions and emotional reactions to outcome in a sporting contest

24 male and 22 female undergraduates competed in same-sex pairs in a bicycle ergometer ‘race’. Ratings of how important participants felt it was to win were gathered before the race. After the contest, ratings of satisfaction with performance and attributions for the causes of winning or losing together with ratings of the intensity of a variety of emotional feelings, were made by participants. Results showed that both male and female race winners attributed their win to internal factors (the effort they made, their motivation and personality). Losers attributed their loss to external factors (their opponent's effort and personality). For both winners and losers, however, emotional reactions were related only to internal attributions. Feelings of satisfaction among winners, and feelings of irritation experienced by losers, were related to internal attributions irrespective of how important participants thought it was to win the race. But the relationship between attributions and feelings of pride in winners and feelings of unhappiness in losers were influenced by the importance attached to winning the race. Some evidence emerged to suggest that losers who had considered it important to win, used defences against emotional feelings of disgust, dissatisfaction and discontent.     

Effects of pre- and postpubertal social experience on sexual and social behavior in male and female brown lemmings (Lemmus sibiricus)

The effects of prepubertal social contact and postpubertal mating experience on sexual behavior were examined in male and female brown lemmings (Lemmus sibiricus). Subjects of both sexes were either isolated at weaning (18 days) or then housed with siblings for another 10 days before being isolated. Before testing for sexual behavior at the age of 75 days, half of each group of males received a series of exposures to estrous females and half of each group of females was housed with a stud male. The results of mating tests indicated that whereas prior sexual experience facilitated subsequent copulatory behavior in both sexes, prepubertal interactions subsequently facilitated contact social and sexual behavior in males but did not increase the behavioral scores of females, which engaged in high levels of sexual behavior regardless of prepubertal experience. The effect of prior copulatory activity on male sexual performance could not be attributed to increasing age (i.e., maturational processes) because the behavior of males tested once but at different ages did not differ appreciably. Prepubertal social interaction appeared to predispose males to benefit from sexual experience later in life.     

Pregrouping aggression and defense scores influences alcohol consumption for dominant and subordinate rats in visible burrow systems

Five male/two female rat colonies were established in visible burrow systems, with males selected for pregrouping attack scores and also evaluated in open field and cat odor tests. Dominant-subordinate pregrouping attack differences suggested that the males becoming dominant are those showing more persistent and higher level attack. For six colonies showing dominant-subordinate behavioral differences, pregrouping defense tests failed to predict subordinate status. However, pregrouping defense scores were reliably correlated with subordinate pre-postgrouping change scores for voluntary ethanol consumption. Subordinates showed higher ranked ethanol consumption than dominants, but these groups were not different on pregrouping ethanol consumption. Subordinate postgrouping ethanol consumption was positively correlated with pregrouping attack toward an adult intruder, consonant with previous findings that highly aggressive subordinates are the targets of more intense attack by dominants. These results provide further support for a view that subordination stress increases voluntary ethanol consumption in male rats and suggest some additional individual differences factors that may be involved in increased ethanol consumption for male subordinates. © 1992 Wiley-Liss, Inc.     

The effects of urine on aggressive responses by male golden hamsters

Twenty adult male golden hamsters were isolated into individual cages for a period of six weeks, at the end of which time they had introduced into their home cages, on three occasions, a castrated male intruder. On each occasion the castrated intruder was daubed on the anogenital region with urine from one of three sources: (1) intact females, (2) other castrated males, and (3) intact males. Urine from a different source was applied to the castrated intruder on each of the three tests. Resident males consistently showed more aggression, sniffing, and following and less defensive behavior than the intruders. However, aggression by the resident males showed a significant variance over the three urine treatments given to the intruder. It is concluded that like male mouse urine, male hamster urine contains attack-provoking cues, but that unlike that of the mouse, female urine does not appear to be attack-inhibiting in this species.     

A sensory contact model for the study of aggressive and submissive behavior in male mice

The technique for simultaneous development of aggressive and submissive behaviors as a result of successive experiences of defeats or victories in daily intermale confrontations in male mice permanently living under sensory contact conditions is offered for behavioral, pharmacological, and neurophysiological studies of mechanisms of agonistic social relations. Distant sensory contact is achieved by placing a pair of males into a common cage separated by a transparent partition with holes permitting visual contact and the individuals perceiving each other's odors but preventing any physical at contact all times except for 10-min daily tests. These conditions essentially elicit aggression in winner males and quickly result in submission by losers of the same strain of mice. The meaning of consecutive stages of the technique, the problem of controls, and applications of this model are discussed.     

Effect of intrauterine position and social density on age of first reproduction in wild-type female house mice (Mus musculus)

In laboratory strains of mice, reproductive maturation is influenced by both the fetal and the peripubertal social environments experienced by females. Intrauterine position (IUP) for female fetuses is identified by the number of adjacent males; where 0M have zero, 1M have one, and 2M have two male neighbors. We sought to confirm, using wild-type female house mice (Mus musculus), the previous finding in the CF-1 strain of laboratory mouse that males prefer 0M over 2M females as mates. We recorded the age at first reproduction for females of known IUP housed either individually with a male or in a group of 6 females and a male. In neither housing condition were there significant differences in age of first reproduction among females of different IUPs, but 0M females that were group housed had perforate vaginas at an earlier age than other group-housed females. Mean (+/- SE) age at first reproduction was 58.1 (+/- 3.3) for paired and 126.6 (+/- 5.1) for group-housed females. The reproductive suppression observed in the grouped females was probably due to the interaction of inhibitory urinary chemosignals, low body weights, and female dominance hierarchies.     

Isolation-induced facilitation of male sexual behavior in mice

Sexual performance of male mice housed individually or in groups of 3 or 12 was compared. Experiment 1 examined naive males presented at weekly intervals with ovariectomized, estrogen-primed, progesterone-treated females. Performance in isolates was consistently superior and reached an asymptote that was twice that of grouped animals. Reversal of housing conditions reversed performance. Experiment 2 varied intervals of isolation among subjects, finding facilitation at several intervals. Experiment 3 compared animals under different population densities. Density did not alter the effects of isolation and grouping. In all experiments, additional tests with target males indicated that aggressive and sexual performance were moderately correlated and responded similarly to parametric manipulations. These results parallel and extend studies of isolation-induced aggression.     

Stress in cynomolgus monkeys (Macaca fascicularis) subjected to long-distance transport and simulated transport housing conditions

The stress associated with transportation of non-human primates used in scientific research is an important but almost unexplored part of laboratory animal husbandry. The procedures and routines concerning transport are not only important for the animals' physical health but also for their mental health as well. The transport stress in cynomolgus monkeys (Macaca fascicularis) was studied in two experiments. In Experiment 1, 25 adult female cynomolgus monkeys were divided into five groups of five animals each that received different diets during the transport phase of the experiment. All animals were transported in conventional single animal transport cages with no visual or tactile contact with conspecifics. The animals were transported by lorry for 24 h at ambient temperatures ranging between 20 degrees C and 35 degrees C. Urine produced before, during and after transport was collected and analysed for cortisol by enzyme-linked immunosorbent assay (ELISA). All monkeys exhibited a significant increase in cortisol excretion per time unit during the transport and on the first day following transport.Although anecdotal reports concerning diet during transport, including the provision of fruits and/or a tranquiliser, was thought likely to influence stress responses, these were not corrobated by the present study. In Experiment 2, behavioural data were collected from 18 cynomolgus macaques before and after transfer from group cages to either single or pair housing, and also before and after a simulated transport, in which the animals were housed in transport cages. The single housed monkeys were confined to single transport cages and the pair housed monkeys were kept in their pairs in double size cages. Both pair housed and singly housed monkeys showed clear behavioural signs of stress soon after their transfer out of their group cages.However, stress-associated behaviours were more prevalent in singly housed animals than in pair housed animals, and these behaviours persisted for a longer time after the simulated transport housing event than in the pair housed monkeys. Our data confirm that the transport of cynomolgus monkeys is stressful and suggest that it would be beneficial for the cynomolgus monkeys to be housed and transported in compatible pairs from the time they leave their group cages at the source country breeding facility until they arrive at their final laboratory destination in the country of use.