Play fighting and the development of agonistic behavior in male and female rats

Two longitudinal studies were conducted to quantify the social behaviors exhibited by both male and female Long-Evans rats from the immediate postweaning period until young adulthood. In Experiment 1, male sibling pairs engaged in a high level of play fighting during the early juvenile period but such activity declined to a level significantly lower than that of female and mixed-sex pairs after 54 days of age. In Experiment 2, social exchanges during maturation were examined during the presence and absence of the piloerection response in an effort to distinguish play fighting from agonistic interactions. In male pairs, piloerection was rarely seen before 55–75 days of age but thereafter occurred with increasing frequency especially among dominant males. Furthermore, subordinate males retreated from their dominant partners and remained in an escape chamber for a significant amount of time only during encounters involving the exhibition of piloerection. This finding suggests that piloerection can be useful in identifying play and aggressive interactions. In female and heterosexual pairs, piloerection was observed infrequently during social encounters occurring throughout maturation. In addition, when given the opportunity to escape, females were less likely to retreat from play activity if their partner was another female than a male.     

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.     

Attack and defense in conspecific fighting in tree shrews (Tupaia belangeri)

Principles of conspecific defense have been analyzed for rodents, in which specific target sites for biting by attackers on defenders serve as an important determinant of the actions involved in both attacker and defender behavior. In an effort to determine the generality of these principles, attack and defensive behaviors and target sites for biting attack were evaluated in a nonrodent species, the tree shrew (Tupaia belangeri). Brief daily and repeated conspecific dyadic encounters between adult, socially experienced males (dominants, attackers), and adult, socially naive males (subordinates, defenders) that had been transferred into the territory of the dominants, produced a polarization of attack and defense. The dominant males showed chase, chase attack, jump attack, and biting behaviors, while the subordinates displayed flight and freezing. The vast majority of bites, as well as wounds and bruises, were on the subordinates’ backs. These patterns are very similar to those previously found in rats and mice and suggest that the organization of fighting, with targets of biting (or other painful) attack serving as an important determinant of both attacker (dominant) and defender (subordinate) behavior, may show considerable generality across nonrodent as well as rodent species. Although relatively few wounds were found after 28 days of repeated and daily encounters, the subordinate tree shrews show a variety of behavioral, neuroendocrine, and central nervous changes, indicating that they are stressed by these encounters per se. Aggr. Behav. 27:139–148, 2001. © 2001 Wiley‐Liss, Inc.     

Juvenilized play fighting in subordinate male rats

As pairs of male juvenile sibling rats that are housed together become sexually mature, they develop a dominance-subordinance relationship. These dominance relationships appear to be reflected in the play fighting of the pairmates both as juveniles and as young adults, in that the seemingly subordinate partner initiates more playful attacks at both ages. However, as adults, even though it is the subordinate that initiates more playful attacks, it is the subordinate that is pinned on his back by the partner most often. Dominant pairmates were found to switch to defensive patterns typically found in adult males. In contrast, the subordinates, when contacted on the nape, were more likely to retain the juvenile pattern of turning over to supine. Therefore, the subordinate pairmate of an adult pair of male siblings both initiates more playful attacks and defends itself in a more juvenile manner than its dominant partner, and this leads to it being pinned more frequently. This pattern of behavior by subordinate rats is suggested to function as a friendship maintenance mechanism permitting co-existence in multimale colonies.     

Social dominance and individual aggressiveness

Male rats exhibiting high, moderate, or low levels of offensive aggressive behavior in interactions with intruders in their home cage were grouped in mixed-sex colonies with 1 male of each aggression-level group in each colony. Agonistic interactions measured 1, 2, 3, 7, 14, 21, and 22 days after colony formation indicated that highly aggressive males on pretests continued to be more aggressive, becoming the dominant colony male in five of seven colonies and attacking intruders more often than less aggressive males. In the two remaining colonies the moderately aggressive male became dominant. This relationship, which was consistent over a number of indices, including offensive and defensive behaviors, and wound counts and wound sites, was seen even when a substantial weight differential favored the less aggressive animal. Dominance relationships were rapidly established and within-group fighting declined significantly over the 21-day test period. Pretest offensive levels also influenced the behavior of subordinates, with high or moderately aggressive subordinates showing more defense in interactions with dominants and receiving more wounds than did low-aggression subordinates. Dominant males also showed more defense in interacting with those subordinates which had been more aggressive during pretests. This pattern of results suggests that aggression level of the subordinate as well as the dominant may be an important factor determining the intensity of agonistic interactions in male rats.     

Some subordinates are more equal than others: Play fihgting amongst adult subordinate male rats

Adult male rats living together form dominance relationships, with one dominant and the remainder adopting subordinate roles. In previous studies, it was shown that in adult male pairs, the subordinate rat initiates more playful contacts and retains a more juvenile response to the playful contacts by the dominant. In this experiment, triads were used to examine the play between subordinate males. The subordinates directed fewer playful contacts to each other than to the dominant rat, and there was a symmetrical play relationship between the subordinates. After the dominant was removed from the colony, one subordinate became the dominant. Playful interactions amongst these pairs increased, with the subordiante intiating more playful contacts than the dominant. Furthermore, from a similarly low frequency of juvenile-type response to playful contact to each other when in triads, the subordinate in the dyads increased its frequency of juvenile responses to the dominant partner. This supports the hypothesis that the playful behavior of subordinate male rats towards the dominant is an adaptive response, playful behavior of subordinate male rats towards the dominant is an adaptive response, serving a “friendship maintenance” function. Finally, when in triads, one subordinate was more playful with the dominant than the other subordinate. It was the least playful subordinate that was the most likely to become the dominant. This sugests that within a colony, not all subordinates are the same. © 1993 Wiley-Liss, Inc.     

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.     

Effects of prior agonistic experience on risk assessment and approach behavior evoked by familiar or unfamiliar conspecific odors

Risk assessment and appetitive behaviors in response to familiar and unfamiliar conspecific odors were measured in mice rendered dominant or subordinate by a series of resident-intruder encounters. Subordinate mice showed elevated levels of risk assessment in response to the odors of both familiar dominant and unfamiliar males. These behaviors were almost totally absent among dominant males exposed to familiar subordinate or unfamiliar male odors. Subordinate mice showed a marginally significant elevation in latencies to approach familiar, but not unfamiliar, dominant odors. Dominant and subordinate mice spent comparable amounts of time in the cage area containing familiar antagonist odors, however, and the durations of subordinates were mildly elevated, rather than decreased, when unfamiliar conspecific odors were present. There were no group differences in any of the appetitive behaviors. These findings suggest that apparent preferences for conspecific odors may arise from quantitatively and/or qualitatively differing emotional states. The inclusion of risk assessment measures is suggested to be a useful adjunct for studies of olfactory preference/rejection. © 1994 Wiley-Liss, Inc.     

Play fighting between kindling-prone (FAST) and kindling-resistant (SLOW) rats

Differences in the play behavior of 2 strains of rats suggest that different components of play fighting can be modified independently. The development of play fighting in cross-strain pairs of familiar and unfamiliar rats was examined to determine whether interacting with a non-congruent pair-mate would alter the pattern of play typical for each strain. In both strains, changes in play fighting were observed throughout development, but partner identity appeared to influence play fighting in different ways depending on age. These data suggest that some components of play may be more impervious to changes in social environment than other components.     

Aggressiveness and memory: subordinate crabs present higher memory ability than dominants after an agonistic experience

A relationship between aggressiveness and memory has been proposed in several studies with different animal species. Here, we study this possibility in the crab Chasmagnathus granulatus, using the context-signal memory model (CSM) that involves an association between the learning context and a visual danger stimulus. Each experiment consisted of an agonistic phase and a memory one. During the former, matched pairs of male crabs were staged in two 10-min encounters and the dominant or subordinate condition of each member of the dyad was determined. During the memory phase, crabs were trained to acquire CSM and tested 24 h later. Results showed that the agonistic encounter, staged 48 h before the acquisition of CSM, can modulate memory according to the dominance condition of the fighter; in such a way that memory retention of subordinates results higher than that of dominants. By contrast, when the memory phase preceded the agonist one, forthcoming dominants and subordinates did not differ in their memory ability. The memory modulation would not be linked to a dominance status but to a persistent dominance relationship fully reconstructed in each encounter between the same opponents. Therefore, the crab's CSM would not depend directly on predetermined intrinsic properties, but on the outcome of the fight, which would be determined in turn by the relative aggressiveness of the fighters. The finding that the agonistic episode modulates memory opens the possibility of using this episodic interference to probe the function of diverse phases of CSM.     

Short-term effects of residence on the testosterone responses to fighting in alpha male guinea pigs

The short-term effects on testosterone (T) levels of (a) taking blood samples, (h) fighting in one's own home cage, and (c) fighting in another male's home cage were examined in eight alpha male guinea pigs, each living together with two females and two subordinate males in their home cages for 4 months. Every male was given two 5-minute agonistic encounters, one in his home cage and one in another male's home cage. After the encounter, intruder males were returned to their home cages. Three blood samples were taken 10 minutes before and 5 and 45 minutes after the agonistic encounters (sampling times were designated as 0, 20, and 60 minutes, respectively). One week before the agonistic encounters were conducted, blood samples were taken from each male on the same time schedule (0, 20, and 60 minutes). The main findings were as follows: (1) the animals showed an increase in T-levels after an agonistic encounter in their home cages and a decline in T-levels after an agonistic encounter in the home cages of other alpha males' irrespective of being the winner or the loser and the degree of escalation during the encounter; (2) the smaller the differences in T-titers between both opponents 10 minutes before the encounter, the more escalated the agonistic encounter.     

Sexual and aggressive play fighting of sibling Richardson’s ground squirrels

Play fighting in many species of squirrels can involve sexual play and aggressive play, both of which can lead to wrestling which appears superficially similar. Such convergence can make scoring of the relative frequencies of these two types of play difficult and can lead to the mistaken conclusion that they grade into one another. In this study, both staged laboratory encounters between sibling pairs and spontaneous encounters between siblings in free‐living litters of Richardson’s ground squirrels (Spermophilus richardsonii) were videotaped. Frame‐by‐frame analyses using the Eshkol‐Wachman Movement Notation were employed to record the correlated movements of attack and defense by the partners and to reveal the body areas targeted during each play bout. Whereas sexual play was organized around access to the rump, aggressive play was organized around the shoulders. Although in most cases the defender’s tactics blocked access to the respective target, when contact did occur, it involved mounting in sexual play and nosing or biting in aggressive play. Eighty‐six percent of play fights could be unambiguously categorized as either sexual or aggressive play. Of these, the majority (?80%) involved sexual play. The sex of the participants did not affect the frequency of aggressive play, but in sexual play, males initiated more attacks than females. Once initiated, each form of play fighting remained distinct—if a bout began as sexual play, it would end as sexual play. Furthermore, a counterattack following sexual play was significantly more likely to be sexual than aggressive, and vice versa for counterattacks following aggressive play. Therefore, all the evidence suggested that the two forms of play fighting were not intermixed in Richardson’s ground squirrels. Aggr. Behav. 27:323–337, 2001. © 2001 Wiley‐Liss, Inc.     

Biochemical costs of a three day long cohabitation in dominant and submissive male Betta splendens

A 3 day long cohabitation in pairs of previously isolated adult male Betta splendens was studied. The first two mornings started with intense fighting, the frequency of which decreased during the day. The bursts of aggression noticed in the mornings were associated with a significant carbohydrate metabolism activation, while daytime activity resulted in a reduction of muscle proteins in the evenings. These changes were more pronounced in submissives than in dominants. The third day marked a shift in the behavior of the pairs: bursts of attack activity were not noticed, while the threatening display frequency increased. During this day a similar reduction in lipids was observed in dominants and submissives. While during the first 2 days the dominant position offered some metabolic advantage, this advantage disappeared during the third day when both members of the dyad seemed to do equally less well than their isolated counterparts. Combined with previous findings obtained in this series of experiments, the present results support the assumption that in this species the presence of one opponent is less well tolerated than the presence of four conspecifics. © 1994 Wiley-Liss, Inc.     

Responses of dominant and subordinate male rats to the odors of male and female conspecifics

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. Resident males were significantly more aggressive than intruders and spent more time investigating 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 subordinates but not unfamiliar subordinates. The importance of olfactory learning during aggressive interactions is discussed.     

Dominance and age-related changes in the play fighting of intact and post-weaning castrated male rats (Rattus norvegicus)

The play fighting behaviour of male rats (Rattus norvegicus) castrated at weaning was compared to that of intact controls during the juvenile and post-pubertal phases of development. Following puberty, both the castrated and intact animals exhibited an age-related change in their play fighting; the frequency of initiating play fighting decreased and juvenile patterns of playful defense were replaced by more adult-like patterns. As these changes occurred even in the absence of the pubertal surge of gonadal hormones, they were more likely to result from the organizational effects of gonadal hormones in the perinatal period than the activational effects of these hormones at puberty. Although the castrated animals exhibited the age-related changes in behaviour, they did not exhibit the asymmetries in play associated with dominance relationships. As demonstrated in previous studies, in pairs of intact rats, the animal that attacks the most and uses more juvenile defenses during play fighting and weighs the least is typically the subordinate. In the castrates, asymmetries in weight and playful defense are not related to play frequency, indicating the absence of a dominance relationship. Although the characteristic changes in male play fighting at puberty are independent of the activational effects of gonadal hormones, dominance relationships and their associated changes in play fighting are dependent on these hormones. Therefore, in the perinatal period gonadal hormones most likely organize the age-related changes in play behaviour, whereas post-pubertally gonadal hormones activate dominance relationships and thus, indirectly modify play fighting by affecting dominance-associated assymetries in behaviour. © 1996 Wiley-Liss, Inc.     

Neonatal testosterone augmentation increases juvenile play fighting but does not influence the adult dominance relationships of male rats

Neonatal male rats were either injected subcutaneously with testosterone propionate (TP) or oil vehicle. When weaned, each treated pup was paired with an untreated male sibling. The play fighting of TP-and oil-treated rats were compared at the juvenile phase (30–36 days), and in adulthood (84–90 days). In the juvenile phase, the rate of initiating playful attacks was significantly greater for TP-treated rats. Playful defense in response to such attacks did not differ between TP- and oil-treated rats. At the completion of the study, cortical thickness was measured for all the groups of rats. Oil treatment decreased overall cortical thickness relative to untreated pairmates, whereas TP treatment did not. Both oil and TP treatment abolished the asymmetry in hemispheric thickness, which was present in the untreated pairmates. The reversal of at least one of these injectioninduced changes in the cortex by TP provided independent evidence for the effectiveness of the TP treatment. As adults, neither the TP treatment nor the oil treatment influenced which pairmate became dominant. Dominance was judged by which pairmate initiated less playful attacks. Therefore, it is concluded that the early neonatal testosterone surge is not likely to be a factor in influencing the behaviors that lead to adult dominance. In contrast, play fighting is influenced by hormonal events in this early neonatal phase. It thus appears that play fighting and the aggressive systems subserving dominance relationships are differentially controlled. © 1992 Wiley-Liss, Inc.     

Social structure features in three inbred strains of mice, C57Bl/6J, Balb/cj, and NIH: a comparative study

Some features of social living were investigated in three inbred strains of mice: C57Bl/6j, Balb/cj, and NIH. Five social behaviors--Aggression, Submission, Allogrooming, Social Rest and Rest Alone, as well as Wheel Running Activity--were recorded 2 h daily for a week, in 26 groups of seven male mice living in an enriched environment. Dominants and subordinates among strains shared some behavioral characteristics, but strain contributions upon social structure were also detected. Similarities among strains included the appearance of a single dominant mouse per group rated as the most aggressive, besides from being the animal presented with most Submissions. Allogrooming was more frequent among subordinates than among dominants and subordinates. Differences among strains were that agonistic behavior among subordinates was higher in the Balb/cj and NIH groups than in the C57Bl/6j mice. NIH mice were recorded in Rest Alone more often than mice from the other strains. C57Bl/6j dominants showed higher rates of Wheel Running Activity than subordinates.     

Competitive fighting in the rat.

Competitive fighting was obtained in pairs of like-sexed laboratory rats by placing a single piece of food into the food hopper following 48 hr. of food deprivation. The fighting was characterized by offensive sideways posture, full aggressive posture, and bite and kick attack. Tests were conducted at 110-120 days of age on pairs of animals that had been housed together since weaning. Fighting was more frequent in pairs consisting of nonlittermates than in pairs of littermates, and it was equally frequent in male and female pairings. Probability of fighting was enhanced by prior experience with food deprivation, and attack was most often initiated by the heavier animal of the pair.     

The organization of play fighting in the grasshopper mouse (Onychomys leucogaster): Mixing predatory and sociosexual targets and tactics

The body targets contacted, the type of contact made, and the patterns of defense and counterattack elicited by those attacks are examined in the play fighting of captive male and female pairs of grasshopper mice. The nape was the most frequently contacted body target, irrespective of the type of contact made, be it nosing, allogrooming, biting, or striking with a forepaw. The types of defense varied with both body area contacted and type of attack performed. Based on the topography and pattern of contact, it was concluded that grasshopper mice, as is the case for many other muroid rodents, primarily attack and defend targets otherwise contacted during precopulatory encounters. However, grasshopper mice, which are obligate carnivores, also attack and defend predatory targets, although less frequently than sociosexual targets. Surprisingly, predatory attacks were more likely to be counterattacked with predatory attacks, whereas sociosexual attacks were more likely to be counterattacked with sociosexual attacks. Conspecific aggression involves bites directed at the face, lower flanks, and dorsum. Neither the biting of these areas nor the tactics of attack and defense usually associated with such bites were observed during the juvenile interactions. There were no sex differences in either frequency or patterns of attack and defense in play fighting. The data presented for grasshopper mice shed light on the issue of mixing behavior patterns from multiple functional systems during play. Aggr. Behav. 26:319–334, 2000. © 2000 Wiley‐Liss, Inc.     

Targets and tactics of agonistic and precopulatory behavior in montane and prairie voles: Their relationship to juvenile play-fighting

Play-fighting by juvenile montane and prairie voles involves attack and defense of the head, neck and shoulders. Since during play animals typically borrow behavior patterns from other functional contexts, two adult behavioral contexts were compared to juvenile play-fighting. These were serious fighting and sexual encounters. During serious fighting in a resident-intruder paradigm, most bites are directed at the rump and lower flanks. During sexual encounters, especially in precopulatory behavior, the head, neck and shoulders are gently contacted. Therefore, play-fighting by juveniles would appear to involve attack and defense of areas of the body contacted in adult precopulatory behavior, not adult fighting. Furthermore, the species-specific differences in juvenile play-fighting were also found to be matched by species-specific differences in precopulatory behavior. In both playful and precopulatory encounters, montane voles contacted the head and used upright defensive behaviors more often than prairie voles. In contrast, prairie voles made mutual contact more often and were more likely to rotate to supine in defense of contact to the nape and head. These findings support our hypothesis that juvenile play-fighting in muroid rodents involves the precocial expression of precopulatory, not agonistic behavior.