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.     

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.     

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.     

Estrus induction in four species of voles (Microtus).

Male-induced estrus was examined in montane (Microtus montanus), meadow (M. pennsylvanicus), prairie (M. ochrogaster), and pine (M. pinetorum) voles. Duration of male contact needed for receptivity, effects of parity, and vaginal cytology were assessed. Among nulliparous females, montane voles attained receptivity with less male contact than prairie voles. Meadow and pine voles showed very low receptivity rates. Among parous females, montane and meadow voles did not differ in duration of male contact needed for receptivity and required less than prairie voles. Overall, parous females had higher receptivity rates than nulliparous females. When isolated from males, prairie and pine voles had more leukocytes and fewer cornified cells in vaginal smears than montane or meadow voles. Species differences in estrus induction are discussed in relation to species differences in social organization.     

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.     

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.     

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.     

Aggression as a function of the intensity and pattern of attack

Forty Ss competed with an opponent in a reaction time task to avoid receiving shock. The opponent provided either consistently high intensity attack, increasing, decreasing, or consistently low attack. The S's shock settings for the opponent on each trial and ratings of the opponent after the task served as dependent measures. High intensity attack resulted in high intensity counterattack and negative ratings of the opponent. Low intensity attack resulted in low intensity counterattack and relatively positive ratings for the opponent. Decreasing attack resulted in decreasing counterattack and positive ratings of the opponent. Increasing attack resulted in increasing counterattack and comparatively high aggression ratings of the opponent.     

A comparative study of rodent ultrasonic vocalizations during copulation

The temporal patterning of ultrasonic vocalizations (USVs) during copulation was recorded for male-female pairs of Djungarian hamsters (Phodopus campbelli), prairie voles (Microtus ochrogaster), and montane voles (Microtus montanus). Each species appears to utilize a single major frequency band for USVs, centered around 31 kHz for the vole species and 71 kHz for hamsters. Djungarian hamsters exhibited low rates of USVs prior to introduction of the female and following ejaculation, but a high USV rate during periods of copulatory activity. Both vole species called at high rates during all stages of the copulatory sequence, although calling rates decreased following ejaculation. Anesthetization trials, where one pair member was awake and the other anesthesized, suggest that it is the male of each species that produces most USVs. The results were compared with six other muroid species for which data on the temporal patterning of USVs during copulation are available. These data extend our knowledge of the patterning of USVs during copulatory behavior and suggest the need for additional comparative investigations.     

Aggressive behavior of adult bank voles (Clethrionomys glareolus) towards conspecifics

Male and female bank voles reared in different conditions were investigated for their aggressiveness in order to show how social factors modify intermale and interfemale behavior. Singly reared males or females were paired with a tested animal for 10 min. The number of attacks and the accumulative attack times of singly reared males were higher than for females reared in similar conditions. The differences were not, however, statistically significant due to the variation among tested animals. There were significant differences in aggressiveness of females reared in various conditions before the test. Most attacks were observed in females reared with intact males. In this group, the accumulative attack time was significantly higher than that of singly reared, grouped females, or females kept with castrated or castrated-testosterone-treated males. Also, the aggression of males was affected by breeding. Both the number of attacks and the accumulative attack times were elevated in intact males kept with females. Housing of males in groups and castration significantly decreased the number of attacks of these animals. Injection of testosterone increased aggression in castrated males. It is suggested that olfactory signals in bank voles released by males increase aggression in females and the female's signals stimulate male behavior.     

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.     

High maternal aggression in dwarf hamsters (Phodopus campbelli and P. sungorus)

The defense of offspring, termed maternal aggression, is a highly conserved behavior in mammals, including rodents. This study examined relative levels of maternal aggression in two closely related dwarf hamster species, Phodopus campbelli and P. sungorus, that normally inhabit high latitude, boreal environments. When tested with first litters and with the breeder male remaining with the female (for P. campbelli the male is necessary for successful rearing of offspring), both species exhibited high levels of maternal aggression with average duration of aggressive behavior>80 sec for a 10 min test. For P. sungorus, males are not required to rear offspring. P. sungorus females with either one or multiple litters (singly housed after impregnation) exhibited significantly higher levels of aggression (>300 sec) relative to females co‐housed with the sires. In terms of species differences in attack style, P. campbelli exhibited a boxing or clawing strategy for ～50% of total attack time, but for P. sungorus, this form of attack occurred<5% of the time. For P. sungorus, attacks to the vulnerable belly and flank constituted>90% of all attacks, but these regions were attacked ～50% of the time for P. campbelli. A survey of levels of maternal aggression of rodents in other genera suggests that maternal aggression in Phodopus is at the high end of the spectrum. Results of this study suggest that the presence of the breeder male may actually suppress aggression in P. sungorus. This fact, as well as its high level of aggression and its distant relationship to mice and rats, suggest P. sungorus as a possible model for future studies on the neurobiological basis of maternal aggression. The relationship between the high rates of maternal aggression and life history strategy in Phodopus is discussed. Aggr. Behav. 00:000–000, 2005. © 2005 Wiley‐Liss, Inc.     

The Physiological Control of Judgments of Duration: Evidence for a Chemical Clock

Six prairie dogs (Cynomys ludovicianus) were given reversal training on a spatial discrimination reversal task in a Wisconsin General Test Apparatus (WGTA). As with many other species, more errors occurred on the first reversal problem than during acquisition of the original discrimination. However, performance improved over training until each S eventually reversed after a single nonreinforced error. Initial findings indicate that prairie dogs perform at high levels in discrimination learning experiments and could be valuable subjects for psychological research.     

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.     

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.     

A possible function of the preference for hind nipples in prairie voles (Microtus ochrogaster)

Prairie vole pups (Microtus ochrogaster) in laboratory cages prefer hind nipples. In this research, the author observed 8 litters of prairie voles in a seminatural environment to confirm the preference for hind nipples and to determine if young on hind nipples were groomed more frequently or dislodged less frequently than were young on other nipples. Prairie vole pups in seminatural environments preferred hind nipples; this preference was illustrated by the progressive use of more anterior nipples only as litter size increased and by the reluctance of pups to voluntarily release their hold on hind nipples. Maternal grooming of young did not vary with suckling location. Prairie vole young on hind nipples, however, were dislodged less frequently than were young on other nipples. Less frequent dislodgment from hind nipples during maternal movements may play a role in the preference for hind nipples in prairie voles.     

The relation between social engagement and pretend play in autism

The focus of this study is the nature and concomitants of pretend play among young children with autism. Age‐ and language‐matched children with autism (n= 27), autism spectrum disorder (n= 14), and developmental disorders without autism (n= 16) were administered the Test of Pretend Play (ToPP; Lewis & Boucher, 1997 ), with an additional rating of ‘playful pretence’. As predicted, children with autism showed less playful pretend than participants with developmental disorders who did not have autism. Across the groups, playful pretence was correlated with individual differences in communication and social interaction, even when scores on the ToPP were taken into account. Limitations in creative, playful pretend among children with autism relate to their restricted interpersonal communication and engagement.     

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.