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.     

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.     

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.     

The effects of cross-fostering on the development of social preferences in meadow voles (Microtus pennsylvanicus)

To determine the role of the parental environment in the formation of species attachments in the meadow vole (Microtus pennsylvanicus), young of this species were fostered to either meadow vole parents (in-fostered young) or to prairie vole parents (M. ochrogaster; cross-fostered young). At 50 to 60 days of age, subjects were tested for social preference in an environment that simulated the conditions of a runway system. The testing design assessed the reaction of fostered animals to a novel species (M. pinetorum) as well as to the parental and biological species. The proportion of total test time spent near stimulus animals did not vary as a function of rearing condition. However, when compared to in-fostered controls, cross-fostered meadow voles displayed increased preference for prairie voles. Novelty did not appear to be a significant factor in test animal choice. These results suggest that in meadow voles, preference for the species of social partner is dependent on postnatal experience with parents.     

Sex differences in spatial ability and activity in two vole species (Microtus ochrogaster and M. pennsylvanicus)

The hypothesis that sex differences in maze learning result from sex differences in activity was tested with wild-caught prairie (Microtus ochrogaster) and meadow (M. pennsylvanicus) voles. For 38 voles error production and activity were simultaneously measured in a series of 7 symmetrical mazes. Repeated-measures analyses of variance (ANOVAS) examined species, sex, maze, and interaction effects for 3 dependent variables: errors, activity, and errors/activity. The pattern of significant effects was very different for the errors and activity ANOVAS, which suggests that differential activity cannot explain differential error rates. In contrast, the pattern of effects was very similar for errors and errors/activity ANOVAS, which suggests that controls for activity do not remove differences in error production. These results fail to support the activity hypothesis.     

Meadow voles, <Emphasis Type="Italic">Microtus pennsylvanicus</Emphasis>, have the capacity to recall the “what”, “where”, and “when” of a single past event

Some non-human animals may possess the ability to recall the “what”, “where”, and “when” of a single past event. We tested the hypothesis that male meadow voles posses the capacity to recall the “what”, “where”, and “when” of a single past event associated with mate selection in two experiments. Briefly, male voles were allowed to explore an apparatus that contained two chambers. One chamber contained a day-20 pregnant female (24 h prepartum). The other chamber contained a sexually mature female that was neither pregnant nor lactating (REF female). Twenty-four hour after the exposure, the males were placed in the same apparatus, which was empty and clean. At this time, the pregnant female would have entered postpartum estrus (PPE), a period of heightened sexual receptivity. Males initially chose and spent significantly more time investigating the chamber that originally housed the pregnant female (now a PPE female) than the chamber that originally housed the REF female. Male voles also explored an apparatus containing a chamber with a PPE female and one chamber containing a REF female. Twenty-four hour later, males were placed into an empty and clean apparatus. The males did not display an initial choice and they spent similar amounts of time investigating the chamber that originally housed the PPE female (now a lactating female) and the chamber that originally housed the REF female. The results of these and additional experiments suggest that male voles may have the capacity to recall the “what”, “where”, and “when” of a single past event, which may allow males to remember the location of females who would currently be in heightened states of sexual receptivity.     

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.     

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.     

Female-female interactions and social stress in prairie voles

Trios of prairie voles (Microtus ochrogaster) composed of either two estrous sibling or nonsibling females and one male were monitored via time-lapse videotaping over 72 hr. Social and sexual behaviors were analyzed as a function of trio type (sibling or nonsibling) and fate (survivor or nonsurvivor) across 12-h time blocks. Within nonsibling trios, females that were able to maintain prolonged physical contact with the male within the first 3 days of trio formation later survived and successfully produced litters; females that did not maintain male contact later died of undetermined causes, presumably related to social stress. Frequencies of sexual behavior were similar in both trio types and both surviving and nonsurviving females received equivalent amounts of copulatory stimulation from the male. Sibling groups exhibited higher levels of female-female side-by-side contact; nonsibling groups exhibited greater amounts of female-initiated anogenital sniffing, and female-initiated aggression. Female-female social interactions may be determined by prior familiarity and/or relatedness and may play a dominant role in determining the social organization and mating system of this species.     

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.     

Social and environmental factors influence the suppression of pup-directed aggression and development of paternal behavior in captive meadow voles (Microtus pennsylvanicus)

During summer, female meadow voles (Microtus pennsylvanicus) maintain territories and males do not engage in paternal care. As day length shortens, territories dissolve and males nest with females and young. Because paternal behavior has never been studied in free-living meadow voles during colder months or in the laboratory under short photoperiods, the authors examined whether males housed in short day (SD) lengths exhibited more frequent or better quality paternal behavior than males housed in long day (LD) lengths. Sexually and parentally inexperienced (naive) SD males exhibited proportionally more and qualitatively better paternal care than naive LD males. SD males were more responsive than LD males to classic social cues associated with prepartum aggression inhibition and paternal onset. SD sires also displayed qualitatively better paternal behavior than LD sires. These data suggest that meadow vole paternal state is regulated by specific social and environmental cues that may contain reliable information about ecological conditions that favor paternal care.     

Female meadow voles,Microtus pennsylvanicus,respond differently to the scent marks of multiple male conspecifics

Many nonhuman animals are capable of discriminating a group or entity containing more objects from one containing less of the same objects. The capacity for making judgments of numerousness may also allow individuals to discriminate between potential mates. Female meadow voles (Microtus pennsylvanicus) may use judgments of relative numerousness to distinguish between potential suitors by selecting males that signal their interest by depositing more scent marks relative to other males. We used a familiarization–discrimination paradigm in the absence of training to test the hypothesis that female voles will discriminate between the different numerosities of scent marks of two male conspecifics that are similar in features of their phenotype and quality. During the exposure phase, we presented female voles with different ratios of feces scent marks from two males. During the test phase, we presented females with a single, fresh fecal scent mark from each of the two male donors, whose marks they had previously encountered during the exposure phase. In both phases, females spent more time investigating the scent mark(s) of the male that deposited more scent marks than that of the male that deposited fewer scent marks provided the difference in the ratio of scent marks provided by the male donors in the exposure phase was ≥2. Our results are consistent with studies on a variety of taxa, suggesting that numerosity discriminations are evolutionarily ancient and spontaneously available to nonhuman animals and humans.     

Olfactory discrimination of estrous condition by the male golden hamster (Mesocricetus auratus)

After repeated exposure to receptive and nonreceptive females, male golden hamsters were tested for olfactory preferences in a four-choice olfactometer. Males discriminated between the odor of anesthetized females in different stages of their estrous cycle when the airstreams carrying the stimulus odors were diluted. Previous failures to demonstrate such an ability were probably due to ceiling effects resulting from laboratory testing. Males preferred the odor of females on the day before receptivity (a day coincident with maximal scent marking by the female) and least preferred the odor of females on diestrus-1 (the day on which females attacked and chased males during pretesting encounters). Detection and quick response to an impending estrus would be especially important for males of a solitary and promiscuous species in which there is a first male mating advantage.     

The relationship between dominance rank and spatial ability among male meadow voles (Microtus pennsylvanicus)

Males of many mammalian species exhibit contest competition and scramble competition for mates, but the relationship between these 2 forms of competition remains poorly understood. The authors measured dominance rank and spatial ability as traits likely to be selected by contest and scramble competition, respectively, among male meadow voles (Microtus pennsylvanicus). The spatial ability of males was assessed using water maze tests, and dominance rank was determined using paired trials in a neutral arena. Dominant males had better spatial-learning ability and tended to have quicker learning speed but did not have better spatial memory than less aggressive subordinates. Therefore, the authors found no evidence that contest and scramble competition have favored alternative reproductive phenotypes among male meadow voles.     

Acceleration and delay of sexual maturation in female house mice (Mus domesticus) by urinary chemosignals: mixing urine sources in unequal proportions

Urine from male mice, from estrous female mice, and from pregnant or lactating female mice accelerate first vaginal estrus in females, whereas urine from grouped female mice delays first estrus. Nine experiments were used to test the effects of treatment of young female mice with urinary chemosignals that influence the onset of first estrus using unequal proportions of urine from the different sources. At ratios of 10-20 parts acceleratory chemosignal to 1 part delay chemosignal the acceleratory effect overrides the delay chemosignal, and the mice attain first estrus at earlier ages than controls. Ratios of about 4 to 1 up to 7 to 1 result in mean ages for puberty that are not accelerated or delayed relative to controls. Over a modest range of actual dose amounts of urine, the ratio effects are the same regardless of the actual quantities of urine employed in treating test females.     

Female meadow voles (Microtus pennsylvanicus) demonstrate same-sex partner preferences

Female meadow voles (Microtus pennsylvanicus) are territorial during warm months but demonstrate social tolerance under low temperatures. In spring, females nest together and some pairs participate in communal nursing and rearing of young. Because communal nursing involves significant cooperation, selective pair-bonds may develop between 2 nestmates. Using a choice apparatus, the authors determined that (a) captive females demonstrated partner preferences for a nestmate; (b) partner preferences were enduring and persisted after dyadic separation; and (c) following the loss of a nestmate, females did not develop preferences for a new nestmate, even after extended cohabitation. Data support the hypothesis that captive meadow voles develop selective and enduring same-sex social bonds that may, under free-living conditions, facilitate communal nesting and cooperative rearing of young.     

Effects of experience and motivation on symmetrical-maze performance in the prairie vole (Microtus ochrogaster)

Sex differences in spatial skills are sometimes attributed to sex differences in spatial experience. This hypothesis rests on two assumptions: Spatial experience typically differs with sex and spatial experience has lasting effects on spatial cognition. We tested the latter assumption in a controlled experiment with wild-caught prairie voles (Microtus ochrogaster) and their spatially deprived, laboratory-reared, first-generation offspring; we found the assumption to be unjustified. Although major differences in spatial experience had no effect on maze performance, relatively small differences in motivation produced a significant difference in error rates.     

Sexual behaviour in injecting drug users

A survey of the self-reported sexual behaviors of 1239 intravenous drug users recruited off the streets in Sydney, Australia, highlighted the impact of both sexual orientation and gender on the risk of human immunodeficiency virus (HIV) infection in this population. The sample included 908 men (mean age, 27.9 years) and 331 women (mean age, 26.3 years), the majority of whom were unemployed or receiving social security benefits. Among male respondents, 50 were homosexual, 117 were bisexual, and 719 were heterosexual; for females these numbers were 10, 95, and 220, respectively. Oral and vaginal sex were the most commonly reported practices among heterosexuals, while homosexuals primarily reported manual stimulation and oro-genital contact. The regular sexual partners of male intravenous drug users tended not to be addicts, while female drug users were primarily involved with male partners who also abused drugs. Among male respondents, condom use was highest among homosexuals, followed by bisexuals, and lowest among heterosexuals; there were no significant differences by sexual orientation in female respondents' condom use. Overall, condoms were most likely to be utilized in anal sex and least likely in the case of oral sex. Condom use was about 5% lower when a regular as opposed to casual sexual partner was involved. Most of the 64 HIV-positive respondents were homosexuals, suggesting that sexual orientation rather than drug abuse was the primary risk factor. Given the finding that there is substantial variation in condom use among subgroups of intravenous drug abusers, it is recommended that HIV prevention programs adopt a diversified rather than uniform approach.     

Role of female aggression in prevention of infanticidal behavior in male common voles,Microtus arvalis (Pallas, 1779)

Infanticidal behavior of male common voles (Microtus arvalis) was investigated in relation to the age of unfamiliar pups. Sires from 18 pairs were removed after parturition of their offspring and replaced by unfamiliar males at different ages of the neonates. In group 1, containing six females with their offspring, the new male was introduced into the females' cages on day 1 after the parturition. In group 2 the new male was introduced on day 5 after parturition and in group 3 on day 9 after parturition. The male was removed after 3 days and the neonates recounted. Male common voles killed up to 100% of the neonates in litters containing neonates younger than 9 days by rapid bites to the head of the neonates (groups 1 and 2, mortality rates of 0.86 and 0.38). However, with older pups, a mortality rate of 0.06 was observed while 33% of the intruder males showed signs of injuries (group 3). These findings show that infanticidal behavior of male common voles represents one factor of pup mortality. The results are discussed in relation to changes in the degree of maternal aggression and in the context of the social system of the common vole for solving the conflict between postpartum estrous mating and infanticidal behavior of male common voles. Aggr. Behav. 23:293–298, 1997. © 1997 Wiley-Liss, Inc.