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.     

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.     

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.     

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.     

Social transmission and memory of food preferences in pine voles (Microtus pinetorum)

The social transmission of food preferences is affected by factors including the length of time a preference is maintained. The authors investigated the social transmission of food preferences in pine voles (Microtus pinetorum) and whether food items had to be present for memory to persist. A demonstrator vole was fed cocoa-flavored food, a nonpreferred food. After interacting with a demonstrator vole, observer voles preferred cocoa-flavored food as compared with either naive voles that had not interacted with demonstrators or voles that had been exposed to odors. Observers retained this preference for 72 hr after interacting with an observer whether or not flavored foods were present. The ability to learn which food items are palatable and safe may benefit a generalist herbivore that has faced selection to avoid toxic baits.     

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.     

Meadow voles, Microtus pennsylvanicus, can distinguish more over-marks from fewer over-marks

Is it possible that voles have a sense of number? To address this question, we determined whether voles discriminate between two different scent-marking individuals and identify the individual whose scent marks was on top more often than the other individual. We tested whether voles show a preference for the individual whose scent marks was on top most often. If so, the simplest explanation was that voles can make a relative size judgement—such as distinguishing an area containing more of one individual’s over-marks as compared to less of another individual’s over-marks. We found that voles respond preferentially to the donor that provided a greater number of over-marks as compared to the donor that provided a lesser number of over-marks. Thus, we concluded that voles might display the capacity for relative numerousness. Interestingly, female voles were better able than male voles to distinguish between small differences in the relative number of over-marks by the two scent donors.     

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.     

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.     

Gonadal hormones and intrasexual aggressive behavior in female bank voles (Clethrionomys glareolus)

The effects of gonadal hormones on aggressive behavior in the female bank vole was investigated in 10 min home cage tests. Ovariectomized (ovx) or intact females injected with oil, with progesterone (P), with a mixture of progesterone and estrogen (P+E), or with testosterone (T) alone were confronted in a resident-intruder test with unfamiliar, nonoperated females as intruders. Intact females showed aggressive behavior more frequently than ovx females. Ovx females injected with P, with P+E, or with T made significantly more attacks, and these attacks lasted longer than those observed for oil-treated voles. The results indicate that P, the typical female hormone, is responsible for aggressive behavior in female bank voles; however, only T increased the duration of interfemale aggression. Aggr. Behav. 24:63–70, 1998. © 1998 Wiley-Liss, Inc.     

The development of olfactory preferences for artificial odors briefly experienced by the precocial spiny mouse young

Groups of pups, aged 2, 4, 6, 12, 16, and 18 days of the precocial murid rodent spiny mouse (Acomys cahirinus), were each exposed for 1.5 h to one of the experimental odors, cinnamon or cumin, present in the surrounding environment. The odors were not contingent upon home-cage odors or any other reinforcers. This simple exposure produced a strong preference for the exposed odor in multichoice preference tests carried out 48 h after the exposure in pups from groups aged 2 through 16 days. Older pups exposed to cinnamon or cumin at Day 18 did not show a significant preference for the familiar odor. Both experimental odors used were found to be neutral for control experimentally naive pups within a tested age span. These results point at a stimulus familiarity, rather than associative learning in the development of olfactory preferences in young spiny mouse pups.     

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.     

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.     

Agonistic behavior and social reactivity of LG/J mice in both an arena and a seminatural setting

In order to determine the relatively long-term effects of having been primed for agonistic behaviors in an arena setting, 28 male LG/J mice were observed for these behaviors in a seminatural environment for a period of 5 days following a 20 min arena test. The mice were first placed in an arena in which they were allowed either immediate physical contact with another strain (control condition) or were briefly separated from another strain by a transparent partition before being allowed physical access to them (priming condition). Subjects, recorded as either having fought or not fought in the arena, were then placed in a 101 cm square seminatural setting. Seven trials, using 8 LGs each (4 arenaexperienced males and 4 naive females), were made, and agonistic behaviors were recorded for the priming and control condition subjects. The results showed that the control condition fighters (CF) like the priming condition fighters (PF) fought in the arena situation, but different agonistic patterns in the seminatural setting were noted. While in the seminatural environment, both CF and PF mice were attacked frequently and submitted frequently, but PF mice attacked opponents more frequently than did CF subjects (p < 0.025) and elicited significantly more submissions from opponent mice than did CF mice (p < 0.025). It is concluded that: (1) there are more and different agonistic behavior patterns available in the more natural environment than in the arena setting, and more specifically (2) there is a greater effect on agonistic behaviors in a seminatural environment for mice that fought when exposed to the arena priming procedure as compared with mice having fought in the arena control condition.     

Does spatial learning ability of common voles (<Emphasis Type="Italic">Microtus arvalis</Emphasis>) and bank voles (<Emphasis Type="Italic">Myodes glareolus</Emphasis>) constrain foraging efficiency?

Place learning abilities represent adaptations that contribute also to foraging efficiency under given spatio-temporal conditions. We investigated if this ability in turn constrains decision making in two sympatric vole species: while the herbivorous common vole (Microtus arvalis) feeds on spatio-temporally predictable food resources (e.g. roots, tubers and shoots of plant tubers), the omnivorous bank vole (Myodes glareolus) additionally subsists on temporally unpredictable food resources (e.g. insects and seeds). Here, we compare the spatial reference memory and working memory of the two species. In an automated operant home cage with eight water places, female voles either had to learn the fixed position of non-depletable places (reference memory task) or learn and avoid previously visited water places depleted in a single visit (win-shift task). In the reference memory task, Microtus females required significantly more choices to find all water places, initially performed slightly worse than Myodes females, and displayed slightly lower asymptotic performance. Both species were highly similar in new learning of the same task. In the more complex win-shift task, asymptotic performance was significantly lower in Microtus (72% correct) than in Myodes (79%). Our results suggest that both vole species resemble each other in their efficiency to exploit habitats with low spatio-temporal complexity but may differ in their efficiency at exploiting habitats with temporally changing spatial food distributions. The results imply that spatial ability adjusted to specific food distributions may impair flexible use of habitats that differ in their food distribution and therefore, decrease a species’ chances of survival in highly dynamic environments.     

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.     

Pharmacological Shock Therapy as a Psycho-Biological Problem

Five mothers of 50 newborn rat pups were maintained on either standard lab chow or a diet composed of the same chow with onion powder added. Taste preference tests administered during weaning indicated that the pups whose mother was fed the onion chow showed a preference for onion diet, but that such preference dissipated across the five day testing period. A control group of pups who were exposed to any onion diet cues available through channels other than the mother's milk did not show a preference for onion diet. It was concluded that exposure to onion taste in mother's milk was responsible for an initial preference for onion diet.     

Paternal behavior in the spiny mouse (Acomys cahirinus)

The responsiveness of adult male spiny mice (Acomys cahirinus) to both their own and alien precocial young was investigated. Paternal behavior was manifested primarily by the males huddling with their offspring and the coordination of pup attendance between adult males and females. With less than 2 days exposure to their own neonates, males were found to discriminate between their own and alien young. Experience plays an important role in the development of paternal behavior in spiny mice. Males who have never had pups of their own sniff and attack unfamiliar neonates more than males who have fathered pups. The adaptive significance of paternal investment in this uniquely precocial murid rodent was discussed.