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 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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Social dominance, reproduction, and release of the maturation-delaying chemosignal in the urine of female house mice (Mus musculus)

Five experiments were performed to investigate the effects of social status in groups of female mice on reproduction and on the release or urinary chemosignals that accelerate or delay the onset of sexual maturation in young females. Treatment of young female mice with urine from bottom-ranking mice in groups of 5 adult females resulted in delays in puberty comparable to those produced by treatment with urine pooled from females housed at moderate to high densities. Treatment of young females with urine from top-ranking females from the same groups resulted in ages for puberty not different from those of control females treated with water. There was an interaction between the social rank of a female and the stages of the estrous cycle with respect to the presence in the urine of chemosignals from grouping that delay puberty and estrus that accelerate puberty. Within groups of 5 adult mice, top-ranking females were in estrus more frequently than bottom-ranking females. Individually caged adult females treated with urine from top-ranking females were in estrus more frequently than females treated with urine from bottom-ranking females. When grouped females were separated into individual cages and mated, there was differential reproductive success: More top-ranking females conceived and bore litters than bottom-ranking females. Bottom-ranking females produced more female pups, relative to top- and middle-ranking females.     

Peripheral oxytocin administration buffers autonomic but not behavioral responses to environmental stressors in isolated prairie voles

Negative social experiences such as social stressors and isolation influence mental and physical illnesses, including affective disorders and heart disease. Studies focused on socially monogamous prairie voles can provide insight into neurobiological systems that underlie the consequences of negative social interactions. Female prairie voles were exposed to 28 days of social isolation or pairing with a female sibling (control). Voles were administered daily oxytocin [20 μg/50 μl, subcutaneous (sc)] or saline vehicle (50 μl, sc) for 14 days and exposed to two behavioral stressors [elevated plus maze (EPM) and resident-intruder test]. Brain tissue was collected for analysis of central peptide levels in the hypothalamic paraventricular nucleus (PVN). Isolation produced autonomic changes [increased heart rate (HR) and decreased HR variability) during both acute stressors and increased anxiety behaviors in the EPM. Oxytocin injection prevented the autonomic consequences of the acute stressors in isolated prairie voles, but did not affect the behaviors tested under the present conditions. Oxytocin had no effect on the behavioral or autonomic responsiveness in paired prairie voles. Oxytocin injection may exert a beneficial effect on autonomic responses to stressors in isolated animals through increasing the number of oxytocin-containing neurons and decreasing the number of corticotropin-releasing hormone-containing neurons in the PVN. Oxytocinergic mechanisms may serve to compensate for autonomic responses associated with chronic isolation and exposure to both social and non-social acute stressors.     

Selective attention to signs of success: social dominance and early stage interpersonal perception

Results from two experiments suggest that observers selectively attend to male, but not female, targets displaying signs of social dominance. Participants overestimated the frequency of dominant men in rapidly presented stimulus arrays (Study 1) and visually fixated on dominant men in an eyetracking experiment (Study 2). When viewing female targets, participants attended to signs of physical attractiveness rather than social dominance. Findings fit with evolutionary models of mating, which imply that dominance and physical attractiveness sometimes tend to be prioritized preferentially in judgments of men versus women, respectively. Findings suggest that sex differences in human mating are observed not only at the level of overt mating preferences and choices but also at early stages of interpersonal perception. This research demonstrates the utility of examining early-in-the-stream social cognition through the functionalist lens of adaptive thinking.     

Behavioral and developmental consequences of early rearing experience for captive giant pandas (Ailuropoda melanoleuca)

Mother-reared (MR) and peer-reared (PR) captive giant panda (Ailuropoda melanoleuca) cubs were compared to evaluate the effects of early removal from mother on behavioral development. Males and females and twins and singletons were compared to assess the effects of social setting on behavioral development. Subjects included 2 PR females, 3 MR females, 3 MR males, and 3 mothers. MR cubs spent more time manipulating bamboo and fell more often than PR cubs. PR cubs spent more time inactive. Male cubs directed more playful behavior at their mothers. Twins spent more time play fighting with their mothers than with their siblings. The results suggest that peer-rearing does not provide young pandas with the same level of social stimulation as mother-rearing.     

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.     

Effects of food and mates on time budget in Aplysia fasciata: integration of feeding, reproduction, and locomotion

This study examines the time budgeted to different behaviors in Aplysia fasciata under three conditions: (1) animals have constant access to food and mates: (2) there is access to food, but not to mates; (3) neither food nor mates are present. The data suggest a number of rules underlying behavioral integration: (1) Feeding, reproductive behaviors, and activity seem to be natural categories for behavioral choice. Feeding and reproductive behaviors are controlled in tandem by a common arousal mechanism, while time left over after animals feed and reproduce is distributed in a fixed ratio between locomotion (crawling and swimming) and inactivity (immobility and movement in place). (2) Relative distribution between different forms of locomotion and inactivity is modified by changes in motivational state. More time is spent swimming than crawling when feeding and/or mating is prevented, while more time is spent moving in place than immobile when the arousal level is increased. (3) Feedback control of feeding and reproduction is asymmetric. Satiation of feeding inhibits the common arousal. In the absence of food, time spent on reproductive behaviors increases due to disinhibition of the common arousal. By contrast, positive feedback arising from sexual behavior excites the common arousal. When mating is prevented by removing potential mates, time spent feeding decreases. (4) Generally, animals choose between performing the three main categories of behavior. Although Aplysia simultaneously can feed and mate, or locomote and mate, they do so infrequently. By contrast, different types of reproductive behaviors (male mating, female mating, egg-laying) are commonly performed simultaneously.     

Social dynamics of group courtship behavior in male red-sided garter snakes (Thamnophis sirtalis parietalis)

Mating in red-sided garter snakes is characterized by the formation of mating balls. Up to 100 males simultaneously court single females. The social dynamics of the formation of these mating balls was examined to determine whether the mating balls are formed simply because of a common attraction to the female or whether males are stimulated by the mating balls themselves. A sexually attractive female garter snake appears to be even more attractive to a male when she is being courted by other males than when she is alone. Male garter snakes courted females more actively when other males were also courting the female than when they were alone with her. There is a positive correlation between the number of additional males present and the amount of courtship activity shown by the test male toward the stimulus female. The extent to which the courtship activity of the test males was stimulated by the presence of additional courting males was not influenced by how actively the additional males courted.     

Female Japanese quail (Coturnix japonica) mated with males that harassed them are unlikely to lay fertilized eggs

Results of previous studies of courtship and mating in Japanese quail (Coturnix japonica) suggest that females avoid conspecific males because, while courting and mating, males engage in behaviors that are potentially injurious to females. However, prior experiments provided no direct evidence that females avoided harassing males. Here the authors show that a female quail choosing between a previous sex partner and an unfamiliar male avoids the former if he engaged in relatively many potentially injurious acts while courting and mating, (Experiments 1 and 2) and that males behaving aggressively toward mates are less likely than are gentler males to fertilize the females' eggs (Experiment 3). Male sexual harassment appears to be a tactic both aversive to female quail and relatively ineffective in fertilizing them.