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.     

Different levels of complexity in the play-fighting by muroid rodents appear to result from different levels of intensity of attack and defense

Play-fighting in deer mice, Peromyscus maniculatus bairdii, prairie voles, Microtus ochrogaster, and montane voles, M. Montanus, was compared to that of laboratory rats, Rattus norvegicus. Play in rats appears more complex for two reasons: 1) more of the playful contacts elicit defensive behaviors, and 2) more of these defenses lead to counterattacks, and hence, role reversals between attackers and defenders. Neither high levels of defense, as shown by montane voles, nor high levels of counterattack, as shown by prairie voles, produce rat-like play-fighting. This only occurs when high rates of defense involving turning to face the attacker and counterattack are combined, as in rats. These two components are rarely combined together by deer mice, and so this species rarely exhibits rat-like play-fighting. Furthermore, playful counterattack appears to arise from playful attack, and not from an escalation of defense. These data suggest that the more complex forms of social play, such as play-fighting, have evolved, in part, via the escalation of defense in response to playful attack.     

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.     

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.     

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.     

Differences in affiliative behavior, pair bonding, and vaginal cytology in two species of vole (Microtus ochrogaster and M. montanus)

Prairie voles (Microtus ochrogaster) and montane voles (M. montanus) display marked differences in social organization in the field. Trios of 1 male and 2 females were studied in a large enclosure for a 10-day period. Prairie voles spent 59% of the observation time in side-by-side contact, whereas montane voles spent only 7% of the time in contact. Vaginal smears indicated female-female suppression of estrus in prairie voles; female montane voles appeared to cycle in the presence of males. Male prairie voles preferentially paired and nested with 1 of the females, and vaginal estrus generally followed pair formation by 2 days. Male montane voles did not spend time preferentially with either female, even after mating. These results suggest that the contrasting mating systems of these species result from differences in the propensity for affiliative behavior and social bonding rather than from mate availability or female receptivity.     

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.     

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.     

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.     

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.     

Contextual conditioning and the control of copulatory behavior by species-specific sign stimuli in male Japanese quail

Three experiments were conducted to identify species-specific sign stimuli sufficient to elicit copulatory behavior in male Japanese quail and to determine how learning is involved in the control of behavior by these sign stimuli. In Experiment 1, sexually experienced subjects were tested for copulatory behavior with a live female quail and with a model consisting of a female quail's head and neck mounted in front of a foam pad. Comparable levels of copulatory behavior were observed in the two tests, indicating that static visual cues provided by a female quail's head and neck are sufficient to elicit copulatory behavior in this species. Experiment 2 showed that male birds that previously received numerous opportunities to copulate with a live female quail in the test situation were significantly more likely to copulate with the head + neck model than were sexually inexperienced subjects. Experiment 3 showed that prior sexual experience with live quail facilitated responding to the head + neck model only if the sexual experience was provided in the same place where subjects were later tested with the model. This last finding suggests that sexual experience facilitates control of copulatory behavior by species-specific sign stimuli through contextual conditioning. Contextual conditioning may lower the threshold for sexual behavior with the result that a stimulus as impoverished as an immobile model containing only the head and neck of a female quail becomes sufficient to elicit normal levels of copulatory behavior. The results are also discussed as an example of conditioned stimulus facilitation of responding to an unconditioned stimulus.     

Ejaculate disruption in two species of voles (Microtus): on the PEI matching law.

We permitted male prairie and montane voles (Microtus ochrogaster and M. montanus) five thrusts, without ejaculation, with a female at variable times after a 1st male ejaculated. In both prairie and montane voles, there were fewer sperm, in relation to control conditions, in the female's tract 1 hr after ejaculation if the female received thrusts immediately or 15 min after the ejaculate. There was no such effect after a 50-min delay. There was no significant decrease in litter production in prairie voles caused by thrusts delivered either immediately or after a 15-min delay. Sperm transport in these species is susceptible to disruption for a longer period than in deer mice or rats. The proposal that the postejaculatory interval protects a male from disrupting its own sperm transport (the PEI matching law) appears not to hold for these species.     

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.     

Incompatability between the pigeons' unconditioned response to shock and the conditioned key-peck response

High-speed photography was used to compare the pigeon's response to unsignalled shock with the pigeon's key-peck response. During shock, pigeons flex their neck (i.e., the distance between their eyes and shoulders decreases). Following shock, the neck is extended. During key pecking, the neck remains extended and the head moves toward the key in a slight arc as though attached to a fixed fulcrum. Response topography during pecking and shock appear to be incompatible, and it is concluded that the difficulty in key-peck training pigeons to escape electric shock is due to interference from the unconditioned flexion response. This conclusion supports the species-specific defense theory of escape and avoidance 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.     

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.     

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.     

Social influences on parental and nonparental responses toward pups in virgin female prairie voles (Microtus ochrogaster)

Pair-bonded prairie voles (Microtus ochrogaster) are biparental after the birth of pups. However, whereas most adult virgin males are parental, most virgin females are not. In 6 experiments, influences on the parental behavior of virgin female prairie voles were examined. It was found that (a) young virgin females were more maternal than older females, (b) the postweaning sex ratio of cage-mates did not affect females' responses to pups, (c) females raised to adulthood with their parents and younger siblings present were highly parental, (d) 48-hr exposure to pups beginning at weaning increased some aspects of later maternal responding, (e) rearing to adulthood with the parents even in the absence of younger siblings also increased females' maternal responding, and (f) the increase was seen only if both parents were present. Continued parental presence promotes alloparental behavior, possibly important if daughters do not disperse from the natal nest.     

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.