Agonistic versus amicable targets of attack and defense: Consequences for the origin,function, and descriptive classification of play-fighting

Play-fighting appears to involve the behavior patterns of attack and defense otherwise seen in serious fighting. The degree of similarity, however, depends on the body targets attacked and defended during these forms of fighting. For many taxa, including diverse mammalian families and some birds, the same targets are attacked and defended during both play-fighting and serious fighting. However, for several species of muroid rodents, the targets of play-fighting are not the same as those of serious fighting. In these cases, the tactics of attack and defense are also different. It is argued that for these muroid species the playful targets have arisen from amicable behavior (e.g., social investigation, greeting, allogrooming) rather than, as appears to be the case in so many other taxa, from agonistic behavior. These data strongly suggest that “play-fighting” has evolved from different precursors in different taxa and thus has multiple origins. Furthermore, these data have an important bearing on the universal applicability of many of the suggested functions of play-fighting and also on how such behavior is to be described and classified.     

Targets of attack and defense in play-fighting of the Djungarian hamster Phodopus campbelli: Links to fighting and sex

Analysis of the body targets attacked and defended during play-fighting by juvenile Djungarian hamsters Phodopus campbelli revealed that about 70% of all attacks were directed at the mouth. If successfully contacted, the mouth was briefly licked and nuzzled. The remaining playful attacks were gentle bites directed at the rump, and to a lesser extent, the top of the head. During serious fighting the top of the head and the rump are targets of attack, whereas the mouth is not. Licking and nuzzling the mouth was found to be a behavior performed by adult males at the beginning of sexual encounters. Therefore, play-fighting in juvenile hamsters cannot be thought of merely as a form of “mock fighting” since the principal target is seemingly sexual, not agonistic. The data also show that of the sexual body targets contacted, adult females are more likely to defend the mouth. In this way it is suggested that targets attacked and defended during juvenile play-fighting are derived from adult contexts in which such targets are defended. This hypothesis accounts for the prevalence of agonistic targets in the play-fighting of many species, and may provide a rationale for classifying those amicable targets that are competed for during play-fighting.     

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.     

Identification of the possible origin of the body target that differentiates play fighting from serious fighting in syrian golden hamsters (Mesocricetus auratus)

Play fighting in the Syrian Golden hamster Mesocricetus auratus can be distinguished from serious fighting by the targets attacked in each case. In play fighting, the animals attack and defend the cheeks and cheek pouches, whereas in serious fighting they attack and defend the rump and lower flanks. Since play typically involves the use of behaviors borrowed from other functional contexts, this paper investigates the origin of the cheek target during play fighting. Comparison of resident-intruder serious fighting with awake and anesthetized intruders does not reveal the cheek to be an inhibited target for serious attack. Similarly, analysis of social investigation and allog-rooming, while revealing the ears to be important targets, do not show the cheeks to be targets in these behaviors. Sniffing, licking, and nibbling of the cheek area appear to occur mainly during sexual encounters by males. This area, seemingly a sexual target, may be the one utilized during play fighting.     

Ultrasounds produced by rats accompany decreases in intraspecific fighting

Male intruder rats were placed individually into the cage of an established resident on 2 occasions separated by a 7–8 day interval. Residents readily attacked intruders and both animals lost weight during the first encounter. In contrast, no serious fighting occurred on the second encounter, and both intruders and residents maintained their body weight during the 24-hr test. Observation of the intruder's behavior during the first 30 min of each encounter indicated that defensive-submissive postures represent a response to an attack that only temporarily inhibits aggression whereas the emission of 22 kHz calls by the intruder is associated with a relatively permanent decrease in the resident animal's aggressive response.     

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: The analysis of moment-to-moment decision making in animal combat

Even though injury and death are more common consequences of fighting among animals than once believed, they are still relatively infrequent. Modern evolutionary models of animal combat have emphasized that given the threat of retaliation, animals only escalate to more injurious fighting if the benefits outweigh the costs, and then only if threat and bluff fail to achieve the goal. Such models stress the role of communication as to whether animals decide to escalate or not. An alternative view is that failure to produce injury or death arises from the neutralization of one animal's attack by another's defense. That is, attack and defense end in a stalemate that may be misinterpreted by outside observers as an absence of injury producing behavior. As attack typically involves the biting or striking of specific body targets, movements and postures occurring during combat need to be analyzed with respect to their role in gaining or averting such contact. For example, in the combat of muroid rodents the attacker targets the lower dorsum and flanks (low threshold) or face (high threshold), whereas a defender may defensively launch counterstrikes against the attacker's face. Two combat tactics (supine defense and lateral attack) typically present in the fighting of muroid rodents are analyzed in detail to illustrate how targets constrain the movements of combatants. Such a functional analysis of combat assumes that the movements and postures performed are related to their role in the attack and defense of targets. Deviations from such a strict functional interpretation reveal some of the other factors that may constrain the combatants' behavior. For example, body morphology and the aggressiveness of the opponent are shown to be important in deciding the type of combat tactic to use and how it is performed. Finally, movements and postures that are neutral or even counterproductive for attack and defense may be revealed as communicatory. This approach provides a means of analyzing behavior during the "heat of combat" that is typically not dealt with in traditional evolutionary models. Aggr. Behav. 23:107–129, 1997.© 1997 Wiley-Liss, Inc.     

Reflexive fighting in response to aversive stimulation

Reflexive fighting was elicited between paired rats as a reflex reaction to electric shock prior to any specific conditioning. Such fighting was fairly stereotyped and easily differentiated from the rats' usual behavior. The strength of this reflex was not attributable to any apparent operant reinforcement. Elicitation of fighting was a direct function of the enclosed floor area and a nonmonotonic function of the shock intensity.

Failure to scramble the polarity of the electrified grid produced inconsistent fighting. Under optimal conditions fighting was consistently elicited by shock regardless of the rat's sex, strain, previous familiarity with each other, or the number present during shock. Repeated shock presentations did not produce an appreciable decrease in fighting until signs of physical debility appeared. Although shock did not cause a rat to attack inanimate objects, it did produce attack movements toward other small animals. Failure of guinea pigs to defend themselves revealed that the elicitation of fighting from the rat does not require reciprocal attack. Paired hamsters showed fighting reactions similar to those of the rats, whereas guinea pigs failed to fight. Electrode shock and a heated floor elicited fighting between the rats, but intense noise and a cooled floor did not.

     

Analysis of the targets and tactics of conspecific attack and predatory attack in northern grasshopper mice onychomys leucogaster

Comparisons of tactics of fighting between species are often difficult to make since the body targets attacked may differ. Thus it becomes difficult to assess whether differences in fighting tactics are due to species-specific differences in the tactics themselves or due to the different targets attacked. A solution to this problem is to analyse the tactics of a species that attacks different targets under different circumstances. In this way, differences in tactics can be more readily attributed to differences in targets. In this study, resident male northern grasshopper mice (Onychomys leucogaster) were tested against intruding male conspecifics and against laboratory mice (Mus musculus domesticus). Conspecifics were mainly bitten on the lower dorsum, whereas prey were bitten and killed by bites to the nape of the neck. Therefore, it was possible to analyze the tactics of attack by grasshopper mice when attacking different body targets. For example, in order to defend the lower dorsum and the nape, both intruding conspecifics and prey adopted an upright defensive posture. Resident grasshopper mice used the lateral attack tactic to gain access to the lower flanks but not the nape. This illustrates that the lateral attack tactic is not merely a tactic suitable for overcoming the upright defense tactic, but is used in this context only when the target attacked is on the opponent's posterior dorsum. Such withinpecies comparison enables the identification of the contextual rules which govern the use of fighting tactics. © 1992 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.     

Targets,tactics, and the open mouth face during play fighting in three species of primates

The play fighting of many mammals involves the nonserious use of behavior patterns derived from serious fighting. A major question of theoretical importance has been that of how, given this overlap in patterns of behavior, the animals can distinguish between playful and nonplayful intent. One proposed solution is that animals use play signals to inform each other about the playful intent of their actions. The most widely reported play signal amongst primates is the open mouth play face. The manner in which this so-called signal functions is based on correlational evidence, with most reports simply noting its presence or absence in a given species. This study involved a detailed video-based analysis of the occurrence of open mouths during the play fighting of three species of primates. One captive troop each of ring-tailed lemurs, black-handed spider monkeys, and patas monkeys was used. By examining all open mouths in the context of the species-typical style of play fighting, several conclusions were empirically verified. 1) Most open mouths occur as a functionally necessary precursor for biting. 2) Some open mouths occur as a defensive threat which deters further contact. 3) The residual open mouths which may function as contact promoting play signals, constituted about 20–25% of all open mouths by the lemurs and patas monkeys, but less than 5% for spider monkeys. These species differences appeared to arise from two causes. Firstly, the spider monkeys used another signal, the head shake, in situations where lemurs and patas monkeys used open mouths. Secondly, the style of play fighting greatly influenced the frequency and duration of open mouths. This was most marked in the face-to-face combat style of patas monkeys. These findings show that comparative studies of the occurrence and function of play signals need to take into account species-typical styles of playful combat. Aggr. Behav. 23:41–57, 1997. © 1997 Wiley-Liss, Inc.     

Estimation of the probability of fighting in fallow deer (Dama dama) during the rut

Fighting between males is a frequent component of the rutting behavior of Cervidae. Frequent conflicts are exhausting; fighting may be risky and can lead to serious injuries or even death. We focused on the process of assessment of the opponent's fighting ability and escalation of the combat, estimating the probability of fighting based on the encounter components such as groaning and parallel walk. In this study, we observed the agonistic behavior of fallow deer bucks (Dama dama) during the rut over four seasons. During this time, we recorded 205 encounters between bucks. Non-contact display, which allows contestants to assess their opponents fighting ability, occurred in 83% of the encounters. The highest predicted probability of a fight was found when both of the males vocalized and turned into the parallel walk. The chance of a clear outcome decreased when the males were fighting in comparison to when they did not fight. The initiator of the competitive encounter won 41% of the cases, while the attacked buck won 23% of the encounters. If the contestants avoided fighting, however, the initiator won 78% of encounters. Therefore, the initiator was more successful when no fight occurred compared to when the encounters escalated into fighting. In most cases where ritualized behavior occurred, one of the opponents left after vocalization or parallel walk occurred. Thus, vocalization and parallel walk increased the probability for a clear outcome. The probability of a fight was lowest in situations where the males displayed asymmetric behavior. Increased symmetry of the contestants' behavior was strongly correlated with a higher probability of a fight. Thus, these results indicate that fallow deer bucks use efficient tactic during the rut, which, in turn, minimizes the chance of injury while fighting during the breeding season.     

Role reversal changes during the ontogeny of play fighting in male rats: Attack vs. defense

From weaning until sexual maturity, the rates at which young male rats hold each other supine during play fighting appear to become progressively asymmetrical. These changes have been previously thought to reflect an initial lack of dominance and a later development of dominance-subordinance relationships. In this paper it is shown that pairs of male rats exhibit asymmetries in playful attack and playful defense throughout development. The changes, resulting in greater asymmetry of pinning rates, are shown to result from age-dependent changes in defensive tactics; the relationship, therefore, remains constant while the form of the behavior changes. Furthermore, it is not the animals showing the highest rates of playful attack who become dominant in older ages.     

Influence of timing of post-weaning isolation on play fighting and serious aggression in the male golden hamster (Mesocricetus auratus)

Effects of timing of social isolation on play fighting and serious fighting were studied at different ages in male golden hamsters. Litters were isolated at 21, 35, and 65 days of age, and tested in a resident-intruder paradigm. Behaviors were compared within grous and with a fourth group of socially reared conspecifics. The earlier the pups were isolated, the more they engaged in play activities. Later, in adulthood, the aggression level of the same animals was retested using the same paradigm. The three isolated groups showed a high level of aggression, with significant differences among them. When compared with socially reared subjects, a reliable difference in the level of aggression was also found. These results support the view that early social experience is important, suggesting that isolation during early critical periods of socialization has a significant impact on play fighting, whereas short periods of isolation may be enough to trigger adult agonistic behavior. © 1994 Wiley-Liss, Inc.     

The use of the bared-teeth display during play fighting in Tonkean macaques (Macaca tonkeana): sometimes it is all about oneself

Play signals are viewed as important means by which animals inform each other that bites, strikes, and throws that occur during play fighting are indeed playful rather than serious. One such signal is the open mouth play face that is common in primates and many other mammals. Unfortunately, as most play fighting involves biting, it can be ambiguous as to whether any instance of opening the mouth is performed to communicate playful intent or is simply a preparation for biting. In this study, open mouths co-occurring with the bared-teeth display (teeth-baring) in Tonkean macaques were used to assess the context in which facial gestures only relevant for signaling (i.e., teeth-baring is not necessary for biting) are used during play. Two predictions arising from the hypothesis that play signals are used to facilitate playful contact were tested: that the open mouth with teeth-baring should (1) be most frequent preceding contact, and (2) that it should be performed most often when bites are directed at orientations that is visible to the recipient. The data only partially support these predictions. The open mouth with teeth-baring is also frequently used when a monkey withdraws from playful contact. Moreover, it is associated with bites to body targets, such as the rump, that offer little prospect for detection by the recipient; this supports the possibility that play signals may sometimes be emitted not to communicate with the partner but with the performer itself. Thus, play signals serve multiple functions during play fighting.     

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.     

Effects of prenatal ethanol exposure on juvenile play-fighting and postpubertal aggression in rats

The effects of prenatal ethanol exposure on juvenile play-fighting and postpubertal aggressive behavior in rats were longitudinally assessed in the context of more conventionally applied physical and behavioral measures. Pregnant animals were treated with either 2 gm/kg/day ethanol or isocaloric sucrose over gestation Days 6-19. Reproduction and somatic variables included maternal weight over gestation, offspring weight over Days 1-90, and age at eye opening and incisor eruption. Behavioral variables consisted of negative geotaxis, olfactory discrimination, activity, juvenile play-fighting, and postpubertal aggression. Ethanol offspring had lower birth weights, but there was no significant prenatal treatment effect on subsequent offspring weights or on any other reproductive or somatic variable. Both male and female ethanol-exposed offspring exhibited more play-fighting responses when paired with same-sex controls. Postpubertal aggression levels were assessed in males only. Ethanol-exposed offspring were more aggressive than controls and there was a significant positive correlation between play-fighting and postpubertal aggression ranks. No other behavioral measures discriminated between prenatal treatment groups and none were significantly correlated with either play-fighting or postpubertal aggression rank. The results are consistent with the position that juvenile play-fighting and postpubertal aggression are subserved by common substrates. They also are consistent with predictions derived from the hypothesis concerning a response-inhibition deficit as an effect of prenatal ethanol exposure on behavior.     

Playful defensive responses in adult male rats depend on the status of the unfamiliar opponent

Adult male rats reared as pairmates from weaning were tested in a neutral arena with both members of another pair (one at a time). The unfamiliar pairs were found to engage in play fighting, although they were more likely to escalate the encounter into serious fighting than were pairs of familiar rats. Based on their within‐home pair behavior, each pairmate was designated as a dominant or a subordinate. When the test encounters between unfamiliar males were analyzed with regard to whether the pairings consisted of two dominants, two subordinates, or a mixed pair, the pattern of play fighting was found to be attenuated. Both dominants and subordinates were more likely to initiate playful encounters, to respond defensively during these encounters, and to do so using adult‐typical tactics of defense when paired with an unfamiliar rat that was dominant in its home cage. The mechanisms by which the home status of unfamiliar male rats can be identified by another male are discussed, particularly with regard to the role that play fighting may serve for this function. It is concluded that the data support the hypothesis that play fighting can be used by adult rats for social testing, which in this case seems to involve ascertaining the opponent's fighting capability. Aggr. Behav. 25:141–152, 1999. © 1999 Wiley‐Liss, Inc.