Changes in male odours and urinary marking patterns due to inhibition of aggression in male mice

The effects of active inhibition of aggression on male odours and urinary marking patterns were studied in mice belonging to a highly aggressive strain the TA (Turku Aggressive), which has been developed by selective breeding through 37 generations. These males were defeated by trained fighters until they showed no aggression. Individually housed TA males served as controls. Mice from the parental or Normal Strain, which is intermediate in aggression, were exposed to the odours. The males from the Normal Strain were tested for aggression against male castrates to which urine from the two types of TA males or water had been applied. The urine from the highly aggressive control TA males evoked most aggression. The Normal males were later tested against castrates on soiled sawdust. Fewer attacks occured on sawdust soiled by the urine from the control TA males. The preferences for areas covered with soiled sawdust were also assessed. The males from the Normal Strain preferred areas soiled by the TA males trained to nonaggressiveness while the females preferred areas soiled by the highly aggressive control TA males. Subsequently the size and number of urinary marks deposited were examined. The TA males trained to nonaggressiveness voided urine in fewer but larger pools. The differences showed the same direction as those previously found between the TA and TNA strains, selectively bred for aggression and non-aggression, respectively. In mice the odour signals and urinary marking patterns seem to be correlated with the level of aggressiveness, either hereditarily determined or acquired through learning.     

Postweaning environmental and social factors influencing the onset and expression of agonistic behavior in Norway rats

Two studies were conducted to determine the importance of the postweaning environment and social milieu in regulating the expression of intraspecific aggression in Norway rats. In Experiment 1, male rats were housed either individually or in pairs at 21 days of age. In addition, one-half of the singly housed and paired animals were given experiences with intruders during maturation. At 85 days of age, all animals were given a brief intruder test and then removed from their postweaning environment and provided individually with homecages for a two week period until tested for aggression toward intruders. Results of intruder tests given during maturation indicated agonistic exchanges appeared earlier and more frequently in cages housing a single resident than cages with cohabiting males. However, agonistic exchanges between singly reared residents and intruders had detrimental consequences in adulthood especially under long-term combat situations. That is, although individually reared animals, with early fighting experiences, were capable of initiating intraspecific aggression, such individuals were unable to defend their homecage over a long period of time as evidenced by the high number of wounds and tendency to lose body weight during adult fighting.In Experiment 2, male Norway rats were reared in pairs from 21 days of age and identified as dominant or subordinate on the basis of intracolony social interactions shown during maturation. At 80 days of age, animals were paired with individually reared males in an unfamiliar cage for a 20 day period and examined for agonistic behavior toward intruders at 100 days of age. Group-reared subordinate males exhibited defensive behavior during confrontations with individually reared animals and incurred more wounds and lost more body weight than their cohabiting partner. In addition, subordinate males showed significantly fewer offensive postures toward intruders than individually reared cohabitants. In contrast, group-reared dominant animals did not differ from individually reared males in display of agonistic patterns, in number of wounds, and body weight changes during the period of cohabitation. These findings demonstrate that early rearing factors have pronounced effects on agonistic behavior. Animals experiencing defeat during development are more likely to lose agonistic confrontations in unfamiliar territory than either animals dominant in their early social interactions or animals without the experience of winning or losing agonistic encounters. These results have implications for the understanding of agonistic behavior and predicting outcomes of animal contests, and reveal important differences in agonistic experiences among animals reared in groups.     

Sex differences in scent marking in Propithecus edwardsi of Ranomafana National Park, Madagascar

In this study we compared the scent-marking rates of females with those of males. Specifically, we examined the ability of season, dominance status, and natal status to explain the frequency of scent marking in female sifakas living wild in Ranomafana National Park, Madagascar, and compared the results with those published for males [Pochron et al., American Journal of Primatology, in press]. We also sought to determine whether vulnerability to infanticide affects marking frequency in adults of either sex, and whether female reproductive status affects female marking behavior. We found that males marked at twice the rate of females, and like males, females in single-female groups marked at the highest rates. Dominant females and non-natal females marked at higher rates than did subordinate females and natal females, a pattern also seen in males. This suggests that scent marks may convey important information about status. Neither females nor males varied their marking frequency with the presence of vulnerable infants. Females did not alter marking frequency with reproductive state, and like males, they marked at higher rates in the period prior to the mating season than they did in the mating season itself. This implies that females may use scent marks more for intrasexual aggression or territoriality than for mate attraction.     

Long-term effects of husbandry procedures on stress-related parameters in male mice of two strains

In socially unstable groups of male laboratory mice, individuals may experience a chronic stress situation. Previous experiments have shown that the transfer of specific olfactory cues during cage cleaning, and the provision of nesting material decrease aggression and stress in group-housed male mice. In this study, the combined effect of these husbandry procedures were tested for their long-term effect on stress in groups of moderately aggressive (BALB/c) and severely aggressive (CD-1) male mice. The physiological and behavioural stress-related parameters used were body weight, food and water intake, spleen and thymus weight, adrenal tyrosine hydroxylase activity, urine corticosterone levels and behaviour in a cage emergence test. Long-term provision of nesting material and its transfer during cage cleaning was found to influence several stress-related physiological parameters. Mice housed in cages enriched with nesting material had lower urine corticosterone levels and heavier thymuses, and they consumed less food and water than standard-housed mice. Furthermore, marked differences were found between strains. CD-1 mice were less anxious in the cage emergence test, weighed more, ate and drank more, and had heavier thymuses but lighter spleens and lower corticosterone levels than BALB/c mice. We conclude that the long-term provision of nesting material, including the transfer of nesting material during cage cleaning, reduces stress and thereby enhances the welfare of laboratory mice.     

The influence of females on male territorial dominance and female preference in dwelling place in laboratory mice

The influence of female mice (Mus musculus) on intermale aggression and the female choice between dominant and subordinate males were tested. Normal male mice were paired with a castrated male or a female. Two pairs of the same kind were housed together after acclimation for 3 days in half (home cage) of the apparatus, which was composed of eight cages connected by tunnels. One of the two normal males became dominant. The dominant males became more aggressive in the presence of females than in the presence of castrated males. The two normal males dwelt in their own home cages. The two females dwelt together and preferred to dwell in the home cages of the dominant male. The two castrated males dwelt together and seemed to decide their dwelling cage more freely than the subordinate normal male. Received: August 20, 1999 / Accepted: December 6, 1999     

Etude des interactions sociales entre male et femelle chez la Genette (Genetta genetta L.): Relations entre marquage olfactif et agression

Study on Social Interactions between Male and Female Genets (Genetta genetta L.): Relations between Scent Marking and Aggression The aim of this work was to study the relations between marking behaviour and aggression in genets (Genetta genetta L.). Observations on social interactions were made on a socially stable pair and during encounters between unfamiliar pairs. In the first case, there appeared to be a relationship between marking activity in the male and aggression. During aggression periods, marking with the ano-urogenital region increased in the male and decreased in the female. Another striking variation concerned flank rubbing and hindleg rubbing. In both male and female these marking frequencies increased significantly during aggression periods and flank rubbing was modified by visual cues. Data recorded during encounters between unfamiliar pairs (one male being introduced in a female's cage) showed that agonistic behaviours were released through visual cues in females and olfactory cues in males. The same changes in marking frequencies were observed. These results also showed that ano-urogenital marking was inhibited in females during aggression periods. The adaptative significance of these phenomena is discussed.     

Assessment of dominance hierarchy through urine scent marking and its chemical constituents in male blackbuck Antelope cervicapra, a critically endangered species

In ungulates the process of chemical communication by urinary scent marking has been directly related to reproductive dominance, territorial defense and proximity to resources. The differences in the frequency of urine marking and chemical composition of urine of males Antelope cervicapra before, during and after the dominance hierarchy period were assessed. The variations in the urine marking and its chemical profiles of dominant males (n = 9), bachelors (n = 5) and sub-adult males (n = 5) were compared to find out how the dominance hierarchy influences the confined blackbuck herd under semi-natural captive conditions. The frequency of urine marking is significantly higher (p < 0.001) in dominant males. Twenty-eight major constituents were identified in the urine of dominant males (before, during and after the dominance hierarchy period), bachelor and sub-adult males. Among these, three specific compounds namely, 3-hexanone (I), 6-methyl-5-hepten-2-one (II) and 4-methyl-3-heptanone (III) were seen only in dominant males urine during the dominance hierarchy period. Based on the behavioural observation and the unique chemical constituents in the urine, it is concluded that the dominant male scent odor suppresses aggression, scent marking, scent production and territorial patrolling activities of subordinate males, through which the dominant male establish their hierarchy and attains success in reproduction.     

Transient hypertension and sustained tachycardia in mice housed individually in metabolism cages

The novel environment of a metabolic cage can be stressful for rodents, but few studies have attempted to quantify this stress-response. Therefore, we determined the effects on mean arterial pressure (MAP) and heart rate (HR), of placing mice of both sexes in metabolism cages for 2 days. After surgical implantation of a carotid artery catheter mice recovered individually in standard cages for 5 days. Mice then spent 2 days in metabolism cages. MAP and HR were monitored in the standard cage on Day 5 and in metabolism cages on Days 6-7. MAP increased by 18+/-3 and 22+/-4 %, while HR increased by 27+/-4 and 27+/-6 %, in males and females, respectively, during the first hours after cage switch. MAP decreased to baseline in the fourth and eighth h following metabolism cage switch in males and females, respectively. However, HR remained significantly elevated in both sexes during the entire two-day period in metabolism cages. Females had lower MAP than males both pre- and post-metabolism cage switch, but there were no sex differences in HR. These results demonstrate sustained changes in cardiovascular function when mice are housed in metabolism cages, which could potentially affect renal function.     

Changes in social behavior of the male golden hamster accompanying photoperiodic changes in reproduction

Testicular regression and decreased serum testosterone levels result when male hamsters are placed in a short-day photoperiod, and these changes are reversed after reexposure to long-days. The present study was undertaken to determine whether these physiological changes lead to modifications in social behavior in the male hamster. Animals in a nonstimulatory short-day (LD 6:18) or a stimulatory long-day (LD 14:10) photoperiod were observed every 3 weeks for 21 weeks. After 9 weeks, half of the LD 6:18 males were returned to LD 14:10 and showed rapid testicular recrudescence. The other half remained in LD 6:18 and showed a slower rate of testicular recrudescence. Assessment of aggression was accomplished by placing an intruder in the home cage of a test animal and recording latency to attack, decisive encounters, number of attacks, and number of aggressive postures. Dominance was evaluated in a neutral arena with opponents of different weights, using the same parameters. Scent-marking was recorded in response to both bedding from an intact male and bedding from an ovariectomized female in a clean cage. Short-day animals undergoing testicular regression showed heightened levels of aggression and an upward shift in their dominance status. Alteration of the photoperiod did not affect the pattern or number of scent marks. As animals underwent testicular recrudescence, there was a return to lower levels of aggression and to a lower dominance status. Males undergoing rapid testicular recrudescence also showed the most rapid decline in aggressive behaviors. These results suggest that levels of agonistic behavior in the male hamster are inversely related to serum testosterone levels. Scent-marking appears to be unreleated to androgen levels in the male hamster and its role in hamster social behavior remains unclear.     

Intermittent stimulation and acceleration of puberty by urinary chemosignals in female mice (Mus musculus domesticus)

A sequence of 17 experiments was used to test the effects of intermittent stimulation with urinary chemosignals on the age of puberty in young female mice. The three chemosignals tested all accelerate the age of sexual maturation: urine from adult males, urine from females in estrus, and urine from females that are pregnant or lactating. The basic technique involved presenting the prepubertal females with 'Nestlets' on which the urine was placed. The 'Nestlets' were placed in the cages of the test females for a 15-min period, removed for a variable period, and then replaced in the cage for 15 min. In this manner it was possible to vary the number of exposures, the total length of exposure, and the total time period over which the exposures occurred. Control procedures, involving exposures of young females to cotton squares with water rather than urine placed upon them, resulted in no alterations in puberty relative to untreated females. For mice exposed to the urine-treated cotton squares, acceleration of puberty occurred with less total stimulus-exposure time when the stimulus was presented in short exposures over a number of hours than in previous investigations when the exposure to the urinary chemosignal occurred in a single block of time of one or two hours. For each of the three acceleratory chemosignals, there was a diminution of acceleratory effect when the ratio of total stimulus-exposure time to total exposure time grew smaller. This diminution was more pronounced for urine from pregnant or lactating females than for urine from males or from females in estrus.(ABSTRACT TRUNCATED AT 250 WORDS)     

Marking behaviour in two lemur species (L. fulvus and L. macaco): relation to social status, reproduction, aggression and environmental change.

The influence of social status, reproductive and agonistic contexts and environmental change on scent-marking and allomarking rates were studied in captive groups of Lemur fulvus and Lemur macaco. No evidence of female social dominance over males appeared in either species. In L. fulvus, intrasexual relationships were characterized by the dominance of one adult male over another and by the existence of female affiliative association ('central' vs. 'peripheral' females). In L. macaco, no intrasexual dominance relationships were apparent except for a brief ostracism of one female. In both species, (1) intrasexual differences in social status were related to differences in marking rates, (2) no direct relation appeared between marking rates and aggression or reproduction, (3) allomarking was not differentially directed towards specific individuals and (4) physical environmental factors clearly influenced scent-marking and allomarking rates. These results are discussed in relation to the possible functions of marking behaviour in intragroup relations.     

Aggression in male rats receiving anabolic androgenic steroids: effects of social and environmental provocation.

This study examined the effects of anabolic androgenic steroids (AAS) on aggression under different social and environmental conditions. Three AAS were tested in gonadally intact male rats: testosterone propionate (TP), nandrolone (ND), and stanozolol (ST). Doses of 5 mg/kg were given 5 times/week, with gonadally intact controls receiving vehicle only (propylene glycol). Animals received six weekly tests under each condition in a counterbalanced order. Results show that the three AAS differed in their ability to elicit aggression. Males receiving TP were more aggressive than controls, ND males were similar to controls, and ST males were less aggressive than controls. In the social and environmental provocation tests TP-treated males were more aggressive than other groups, but were able to discriminate between intact and castrated opponents and between their home cage and a neutral cage. In the environmental provocation test, TP males were also more aggressive against opponents when tested in the opponent's home cage. It is suggested that chronic exposure to high levels of TP does not eliminate the ability to discriminate between social or environmental cues, as might be expected if it induces a " 'roid rage." However, TP does increase the likelihood that the animal will respond with aggression/dominance in a provoking situation. All three AAS variably affected serum testosterone and LH levels, as well as testes, seminal vesicle, and prostate weights. No effect on body weight was observed.     

Competition for limited environmental resources on the social dominance model in laboratory mice

Asymmetry of social rank in the competition for food and female was studied using the social dominance model with only two male mice. Marking activity was recorded as a useful indicator of the social status. Social rank was determined by asymmetry in aggressive behavior. A food test was presented for 10 min daily within 5 days of the experiment, whereas a sexual test was performed only on the 5th day for 30 min. Marking behavior was estimated twice: before the first interaction and on the 4th day of the experiment. The competition for food was accompanied by active attacks, escapes, vertical defense postures, and sniffing. The level of aggression, sniffing, and food activity was higher in dominant than submissive males. Time course of aggressive, defensive, and sniffing behaviors was characterized by maximum scores in the period of formation of social hierarchy; however, the rate of food activity in this period was low and increased only to the 4th day. Introduction of a receptive female into the male group with the stable social hierarchy stimulated the intermale aggression, defensive and sniffing behaviors. Dominant males were characterized by a greater number of victories over and sniffing contacts with both male and female. Marking activity was also more intense in dominants. Thus, significant unidirectional rank differences in agonistic, sniffing, food, sexual, and marking behaviors were shown on the social dominance model with the minimum number of partners.     

Atp1a3‐deficient heterozygous mice show lower rank in the hierarchy and altered social behavior

Atp1a3 is the Na‐pump alpha3 subunit gene expressed mainly in neurons of the brain. Atp1a3‐deficient heterozygous mice (Atp1a3^+/?) show altered neurotransmission and deficits of motor function after stress loading. To understand the function of Atp1a3 in a social hierarchy, we evaluated social behaviors (social interaction, aggression, social approach and social dominance) of Atp1a3^+/? and compared the rank and hierarchy structure between Atp1a3^+/? and wild‐type mice within a housing cage using the round‐robin tube test and barbering observations. Formation of a hierarchy decreases social conflict and promote social stability within the group. The hierarchical rank is a reflection of social dominance within a cage, which is heritable and can be regulated by specific genes in mice. Here we report: (1) The degree of social interaction but not aggression was lower in Atp1a3^+/? than wild‐type mice, and Atp1a3^+/? approached Atp1a3^+/? mice more frequently than wild type. (2) The frequency of barbering was lower in the Atp1a3^+/? group than in the wild‐type group, while no difference was observed in the mixed‐genotype housing condition. (3) Hierarchy formation was not different between Atp1a3^+/? and wild type. (4) Atp1a3^+/? showed a lower rank in the mixed‐genotype housing condition than that in the wild type, indicating that Atp1a3 regulates social dominance. In sum, Atp1a3^+/? showed unique social behavior characteristics of lower social interaction and preference to approach the same genotype mice and a lower ranking in the hierarchy.     

A comparison of scent marking between a monogamous and promiscuous species of peromyscus: pair bonded males do not advertise to novel females

Scent marking can provide behavioral and physiological information including territory ownership and mate advertisement. It is unknown how mating status and pair cohabitation influence marking by males from different social systems. We compared the highly territorial and monogamous California mouse (Peromyscus californicus) to the less territorial and promiscuous white-footed mouse (P. leucopus). Single and mated males of both species were assigned to one of the following arenas lined with filter paper: control (unscented arena), male scented (previously scent-marked by a male conspecific), or females present (containing females in small cages). As expected, the territorial P. californicus scent marked and overmarked an unfamiliar male conspecific's scent marks more frequently than P. leucopus. Species differences in responses to novel females were also found based on mating status. The presence of unfamiliar females failed to induce changes in scent marking in pair bonded P. californicus even though virgin males increased marking behavior. Pair bonding appears to reduce male advertisement for novel females. This is in contrast to P. leucopus males that continue to advertise regardless of mating status. Our data suggest that communication through scent-marking can diverge significantly between species based on mating system and that there are physiological mechanisms that can inhibit responsiveness of males to female cues.     

Preference for social contact versus environmental enrichment in male laboratory mice

Due to their aggressive nature, male mice are less frequently used than female mice in biomedical research. When aggressive males are being used, individual housing is common practice. The question arises whether this is an acceptable housing for a social species. The present study was designed to gain more insight into the nature of inter-male social contact and into the potential of a form of environmental enrichment (nesting material) to compensate for the lack of social contact. In a series of tests, we analysed whether male mice of different ages preferred to spend time (1) near a familiar cage mate versus an empty cage, or (2) near to a familiar cage mate versus direct contact with nesting material (tissues). Dwelling time in each of the test cages and sleeping sites was recorded, as was the behaviour of the test mice. Results indicated that when other conditions were similar, male mice preferred to sleep in close proximity to their familiar cage mate. Furthermore, the need to engage in active social behaviour increased with age. Tissues were used to a large extent for sleeping and sleep-related behaviour. It is concluded that single housing in order to avoid aggression between male mice is a solution with evident negative consequences for the animals. When individual housing is inevitable due to excessive aggressive behaviour, the presence of nesting material could partly compensate for the deprivation of social contact.     

Scent marking strategies of New World primates

This paper reviews recent findings on scent-marking behavior in wild New World primates. These findings are used to examine three functional hypotheses: territoriality, regulation of social and reproductive dominance, and mating competition/mate attraction. Available data provide little evidence for a territorial function of scent-marking behavior in New World primates. Evidence for a function in the regulation of social and reproductive dominance is ambiguous. The patterns of scent marking found so far (i.e., rates of scent marking according to sex and social or reproductive status, and the spatial distribution of scent marks), and the sparse information on responses to scent marks are consistent with a hypothesized function in intrasexual competition and intersexual mate choice. Suggestions for future research are made.     

Dispersal mechanisms in a captive wild house mouse population (Mus domesticus Rutty)

The ecological implications of dispersal have been discussed in many studies of wild animals in the field but little is known about the social mechanisms leading to the emigration of certain members of a group. To study the social background of dispersal in wild house mice ( Mus domesticus Rutty) a population cage system was evaluated that allowed permanent observation of individually marked animals. It consisted of ten cages connected to a central cage by transparent plastic tubes. Two of these cages were defined as 'dispersal cages' and could be reached only by swimming through a water basin. Dispersal was defined as a permanent stay in one of these cages for at least 4 days. At the beginning of the experiment one pair of house mice with their litter was placed into the cage system. Each of six experiments lasted for 6 months during which data on spacing, social interactions, body condition, reproduction, mortality and dispersal were collected by daily observations. Results regarding this study could be summarized as follows: (1) dispersal in house mice is male-biased; (2) there are interfamiliar differences in dispersal age, dispersal rate, and in the development of the population structure; (3) after reaching sexual maturity subdominant males are evicted by the dominant one; (4) reproductive rate among females drops with increasing birth order, thus only the oldest females within a group reproduce; (5) females born under high population density conditions can only reproduce after dispersal.     

Communication impairments in mice lacking Shank1: reduced levels of ultrasonic vocalizations and scent marking behavior

Autism is a neurodevelopmental disorder with a strong genetic component. Core symptoms are abnormal reciprocal social interactions, qualitative impairments in communication, and repetitive and stereotyped patterns of behavior with restricted interests. Candidate genes for autism include the SHANK gene family, as mutations in SHANK2 and SHANK3 have been detected in several autistic individuals. SHANK genes code for a family of scaffolding proteins located in the postsynaptic density of excitatory synapses. To test the hypothesis that a mutation in SHANK1 contributes to the symptoms of autism, we evaluated Shank1(-/-) null mutant mice for behavioral phenotypes with relevance to autism, focusing on social communication. Ultrasonic vocalizations and the deposition of scent marks appear to be two major modes of mouse communication. Our findings revealed evidence for low levels of ultrasonic vocalizations and scent marks in Shank1(-/-) mice as compared to wildtype Shank1(+/+) littermate controls. Shank1(-/-) pups emitted fewer vocalizations than Shank1(+/+) pups when isolated from mother and littermates. In adulthood, genotype affected scent marking behavior in the presence of female urinary pheromones. Adult Shank1(-/-) males deposited fewer scent marks in proximity to female urine than Shank1(+/+) males. Call emission in response to female urinary pheromones also differed between genotypes. Shank1(+/+) mice changed their calling pattern dependent on previous female interactions, while Shank1(-/-) mice were unaffected, indicating a failure of Shank1(-/-) males to learn from a social experience. The reduced levels of ultrasonic vocalizations and scent marking behavior in Shank1(-/-) mice are consistent with a phenotype relevant to social communication deficits in autism.     

Urine marking in male common voles: Does behavioural activity matter?

Rodent urine provides animals with a large amount of information, from the identity of the animal through its physical condition to social status. Many studies therefore focus on rodent urine-marking behaviour and use marking frequency as an indicator of social status or competitive ability. However, marking, like many other aspects of rodent behaviour, may be affected by individual behavioural activity, a factor that has not been examined so far. We therefore studied a relationship between male urine-marking in reaction to another male's marks (standard opponent) and individual personality profile, characterised by behavioural activity in an open field test (OFT). The marking appeared to be consistent and specific for particular individuals as there was a significant positive relationship between individual markings in two different phases of the experiment. The linkage between behavioural activity in the OFT and urine-marking frequency was non-linear (quadratic), which suggested that males with intermediate activity marked more intensively than males from the extremes of the behavioural spectra. The relationship between the opponent's and the tested males' markings was positive, however, we found no statistically significant evidence that the voles would attempt to overmark the opponent. Marking thus seems to have more of a self-advertising than a competitive function in the common vole. Further, as high marking activity is under strong intra- or intersexual selection, the result might suggest a stabilising selection of the personality trait described as behavioural activity in our study.