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.     

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.     

Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus

Play-fighting is often difficult to differentiate from inhibited or immature serious fighting because both may utilize many of the same behavior patterns. In the rat the two behaviors involve different targets of attack. During play-fighting, snout or oral contact is directed at the opponent's nape of the neck, whereas during serious fighting, male residents mostly direct their bites at the intruder's rump. Although similar to those used in serious fighting, the behavior patterns used during play-fighting are modified to achieve the different targets of attack. Even though the tactics of attack and defense appear more adult-like with increasing age, the playful targets persist well into adulthood.     

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.     

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.     

Lateral display as a combat tactic in richardson's ground squirrel Spermophilus richardsonii

During fighting, adult ground squirrels frequently face each other laterally, arch the back, and piloerect the tail. In a diurnal species, such distinctive visual cues seem consistent with the suggestion that the lateral display serves a communicatory function. However, a detailed analysis of videotaped sequences of free-living Richardson's ground squirrels from two consecutive mating seasons suggested that the lateral maneuver has a functional role in combat. Because most agonistic encounters involve chasing, the rump is the principal body area bitten. When stationary, however, the opponent's rump is bypassed, and bites are targeted at the shoulders. Defensively, a hip thrust is used to block such attacks to the shoulder by pushing the opponent's head away. Offensively, the lateral maneuver is used to push against the opponent, providing a vantage point from which to lunge at the opponent's shoulders. In addition, the defender can launch counterattacks at the side of the head. The lateral orientation provides the attacker with a means of evading such attacks, by swerving laterally away. In some encounters, both the offensive and defensive variations of the lateral maneuver were used by both opponents, often simultaneously. Therefore, irrespective of the signalling function of the lateral display, much of its occurrence during combat can be explained in terms of its role as a combat tactic. © 1996 Wiley-Liss, Inc.     

Rare male aggression directed toward females in a female‐dominated society: Baiting behavior in the spotted hyena

Spotted hyenas (Crocuta crocuta) are gregarious carnivores. The females are socially dominant to males, and adult males rarely direct aggression toward adult females. This study analyzed all cases in which adult immigrant males behaved aggressively toward adult females in a large population of free‐living hyenas in Kenya, observed for 11 years. Our goals were to describe the conditions under which male attacks on females occur, and address possible adaptive functions. Most aggression directed by adult immigrant males against females occurred when coalitions of two or more males attacked a single adult female, who typically responded by defending herself and fighting back. Male aggression against females frequently occurred at sites of ungulate kills, but males never behaved aggressively toward females over food, and all male attacks on females were unprovoked. Although no mounting or other copulatory behaviors ever occurred during or immediately after an attack, the number of male attacks on females peaked around the time of conception. Daily rates at which males attacked females did not vary with female social rank. However, daily attack rates did vary significantly with female reproductive state, and the highest rates of male attack on females were observed during the two stages of the reproductive cycle during which females were most likely to conceive litters. The adaptive significance of male aggression against females in this species remains unknown, but a tight association between male attacks on females and a female's time of conception provides strong evidence of some role for male aggression in hyena sexual behavior. In particular, our data are consistent with hypotheses suggesting that male aggression toward females in this species either serves to inform females about male fitness or represents sexual harassment. Aggr. Behav. 29:457–474, 2003. © 2003 Wiley‐Liss, Inc.     

Agonistic behaviour and bite wound patterns in wild water voles (Arvicola terrestris L.)

Intra‐specific aggression was investigated in a wild colony of Water voles between 1999 and 2004 in South Wales, UK. The occurrence and location (i.e. on the head, neck, body or tail) of bite wounds were recorded for adult and juvenile male and female voles. The greatest (33%) incidence of bite wounds were recorded on juvenile females and the lowest (18%) in adult females. Seasonal analysis of wound data in adults revealed that females were more likely to be bitten during the breeding season whereas bite patterns in males did not vary seasonally. Analysis of bite pattern topography revealed that most Water voles seemingly attempt to bite vulnerable target areas of the body (namely the head and tail). This is in contrast with studies on rats and mice where competitive forms of attack (particularly involving males) largely avoid these areas of the attacked animal's body. Targeting vulnerable areas is normally a characteristic of defensive modes of attack. Patterns of bite topography and agonistic behaviour in this species seem to reflect competitive interactions between individuals, particularly between territorial females and their female offspring, over access to essential resources. Aggr. Behav. 32:599–603. 2006. © 2006 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.     

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.     

Response of colony mice to intruders with different fighting experience

Six male mice placed in a large, moderately complex enclosure formed a stable dominance hierarchy in which two mice defended adjacent floor areas and the remaining four mice were subordinate and did not form territories. Intruder mice with winning or losing experience in prior paired encounters, or those with no fighting experience, were introduced individually into the colony for 30 minute periods. These intruders were attacked by the dominant members of the colony, and the fighting outcomes were strongly dependent upon the fighting experience of the intruder. Intruders with losing or no fighting experience engaged in little mutual fighting with residents, were easily defeated, and terminated attacks by engaging in subordinate behaviors. Intruders with winning experience fought vigorously with residents, attacked and, in many cases, defeated residents. These results suggest that relatively little winning experience gained in earlier paired encounters may be sufficient to overcome the various fighting advantages enjoyed by a dominant territorial holding member of a colony.     

Mousekilling,intermale fighting,and conditioned emotional response in rats

Several possible relationships between two forms of aggression in rats were studied. First, mouse killing and spontaneous intermale fighting were found to be correlated. Rats which attacked other rats were those most likely to kill mice. To determine whether aggressive and nonaggressive rats were also differentially responsive to other situations involving emotional arousal, but not aggression, mouse-killers and nonkillers were compared in a conditioned emotional response (CER) situation. Mouse-killers showed greater suppression to the conditioned stimulus (CS) and to the situational cues of the apparatus. Therefore, a common arousal mechanism may underlie a number of diverse agonistic responses. Nevertheless, extensive mouse-killing experience did not increase the tendency of rats to fight with either adult males or juvenile males.     

Intrasexual interactions among female golden hamsters (Mesocricetus auratus) over the estrous cycle

Social interactions of cycling female golden hamsters paired with ovariectomized animals in large enclosures were primarily agonistic over the 4-day estrous cycle. These aggressive interactions were intense as indicated by frequent occurrences of chase and flight behavior. Dominant and subordinate social ranks were established in the majority of pairs (96%) tested, and even females in sexual heat were capable of attacking and dominating their rivals. Furthermore, cycling females exhibited significantly more aggressive acts than ovariectomized opponents 1 day prior to sexual receptivity. No differences in fighting patterns were found between animals on the other 3 days of the estrous cycle. Additional analyses revealed clear differences in agonistic elements, including flank marking, between dominant and subordinate females regardless of whether they were gonadectomized or intact. These analyses also showed that dominant individuals frequently chased and bit opponents during encounters within their nesting area. The data are examined for implications on the adaptive organization of female hamster agonistic behavior and the neuroendocrine regulation of species-typical behavior over the estrous cycle.     

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.     

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.     

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.     

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.     

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.     

Offensive and defensive bite-target topographies in attacks by lactating rats

The attacks by resident lactating Wistar rats on sexually naive conspecifics of both sexes were examined. Male and female intruders were equally attacked in terms of frequency and number of bites, but the topographies of biting seen in these encounters were different. Similarly to male-male agonistic interactions, females were attacked in a fashion which avoided bites to the head and snout (“offensive” attack), whereas males were frequently bitten on such vulnerable regions (“defensive” attack). This dichotomy in bite pattern suggests that different motivations and functions underlay maternal aggression in these situations. The defensive attack on males may be a deterrent to infanticide since only male intruders counterattack lactating females and kill their pups. The attack on females may be concerned with resource competition.