Ovarian hormones influence odor cues emitted by female meadow voles, Microtus pennsylvanicus.

During the spring-summer breeding season female meadow voles emit odors that are preferred by males, whereas in the autumn-winter season of reproductive quiescence females emit odors that are not preferred by males, but are attractive to females. The effects of daylength and ovarian hormones on salience of female odors were determined by assaying male responses to odors. Females housed in long and short photoperiods transmitted odors that elicited responses similar to those of spring and autumn female voles, respectively. The odor cues emitted by ovariectomized (OVX) females, irrespective of photoperiodic history, were similar to those generated by females during the nonbreeding season. In the absence of ovarian hormones, long daylengths were not sufficient to induce females to broadcast the spring odors preferred by males. Spring-type odor cues were, however, emitted by OVX voles housed in either photoperiod and treated with estradiol. Ovarian hormones appear necessary and sufficient to generate breeding season odor cues and sufficient to induce production of such cues during the nonbreeding season. We conclude that daylength affects odor cues emitted by females by altering ovarian hormone activity.     

Seasonal differences in self-grooming in meadow voles, Microtus pennsylvanicus

We determined whether seasonal differences exist in the amount of time meadow voles, Microtus pennsylvanicus, self-groom when they encounter the scents of conspecifics. To do so, we used voles that were born and reared under long photoperiod (LP) and short photoperiod (SP). LP voles represent those found in free-living populations during the spring and summer breeding season, whereas SP voles characterize those found in free-living populations during the fall and winter nonbreeding season. Experiment 1 showed that LP male and female voles self-groomed more in response to odors of LP opposite-sex conspecifics as compared to those of other LP and SP conspecifics, suggesting that they may be self-grooming to signal sexual interest or excitement to potential mates. Experiment 2 demonstrated that SP males self-groomed more in response to scents of LP female voles and those of SP males as compared to scents of LP males and SP females, whereas SP females spent similar amounts of time self-grooming in response to scents of LP males, LP females, SP females, and SP males. These seasonal differences in self-grooming may reflect differences in the messages produced by groomers when they broadcast their odors as well as differences in the meaning of such odors to opposite-sex conspecifics. Alternatively, these data may be associated with seasonal differences in sexual motivation of the groomers when exposed to scents of particular conspecifics.     

Sex differences in olfactory social recognition memory in meadow voles,Microtus pennsylvanicus

Terrestrial mammals, like rodents, use odors, and scent marks to indicate their presence in an area to conspecifics. These odors convey information about the scent donor's genotype, sex, condition, and age. The ability to discriminate among the scent marks of conspecifics and later recollect the identity of the donor is essential for choosing between familiar and unfamiliar mates. We tested the hypothesis that the promiscuous meadow vole (Microtus pennsylvanicus) can recollect the odor of a familiar, opposite-sex conspecific and distinguish it from that of an unfamiliar, opposite-sex conspecific. We also hypothesized that because reproductive success is highly skewed among male meadow voles and competition for mates is intense, males will be more likely than females to recollect the odor of a familiar, opposite-sex conspecific and distinguish it from that of an unfamiliar, opposite-sex conspecific, for a longer period of time. Using a habituation task, we first exposed the voles, 4 times successively, to the anogenital area scent of an opposite-sex conspecific. Then, 1 hr, 24 hrs, 72 hrs, or 96 hrs after the fourth exposure, voles were presented with the odor of the donor from the exposure phase (familiar donor) and that of an unfamiliar, opposite-sex conspecific. Female meadow voles spent similar amounts of time investigating the scent of the familiar male donor and that of an unfamiliar male donor after the 1-hr and 24-hr intervals. Male meadow voles, however, spent more time with the scent of an unfamiliar female donor than that of the familiar female donor after the 1-hr, 24-hr, and 72-hr intervals, suggesting that male voles could recollect the scent mark of a familiar female for at least three days. The implications of these sex differences in social memory may reflect the different strategies male and female meadow voles use in the recognition of previous and potential mates. Recognition of an individual's scents may enhance fitness by allowing animals to direct appropriate behaviors toward those individuals.     

Seasonal control of odour preferences of meadow voles (Microtus pennsylvanicus) by photoperiod and ovarian hormones

During the spring-summer breeding season, female meadow voles prefer odours of males over those of females, but in the autumn-winter season of reproductive quiescence this preference is reversed. Females housed in long (14 h light/day) and short (10 h light/day) photoperiods, respectively, had odour preferences comparable to those of spring and autumn voles, respectively. The preference of long-photoperiod voles for male over female odours was reversed by ovariectomy and restored by treatment with oestradiol. By contrast, neither ovariectomy nor oestradiol affected odour preferences of short-photoperiod voles. Long days appear to influence olfactory preferences by altering ovarian hormone secretion. The failure of oestradiol to affect odour preferences in short photoperiods suggests that the neural substrates mediating this behavioural response are refractory to oestrogens during the nonbreeding season.     

Self-grooming and sibling recognition in meadow voles,Microtus pennsylvanicus,and prairie voles,M. ochrogaster

Self-grooming in response to the odours of an opposite-sex conspecific may reflect sexual motivation on the part of the actor. We tested the hypothesis that meadow voles, Microtus pennsylvanicus, and prairie voles,M. ochrogaster , both self-groom at different rates when exposed to the odours of their siblings as compared to those of nonsiblings. This prediction was studied under the context of social memory for siblings and the effects of isolation on memory for siblings. The hypothesis explains the self-grooming responses of meadow voles isolated from their siblings for 10 days and of prairie voles isolated from their siblings for 20 days. However, 20 days of isolation for male and female meadow voles, and 30 days of isolation for male prairie voles were sufficient to induce these animals to self-groom at a similar rate to both sibling and nonsibling odours, suggesting that after isolation these animals no longer recognized their opposite-sex siblings. Female prairie voles isolated for 30 days self-groomed more in response to the odours of male nonsiblings than to those of male siblings, suggesting that female prairie voles still recognize their male siblings after isolation. This study is the first to provide empirical evidence that, in the context of sibling recognition, self-grooming behaviour is directed at unfamiliar opposite-sex conspecifics, and that the communicative function of self-grooming (sexual motivation) is associated with social memory for siblings. Differences in the self-grooming behaviour of meadow voles and prairie voles may be associated with several aspects of their life history characteristics.     

Influence of odours of male organ homogenates on maturation of young female meadow voles,Microtus pennsylvanicus

Female meadow vole weanlings exposed to odours from homogenates of bladder and testis taken from sexually mature males showed more rapid maturation (earlier vaginal perforation, heavier uteri, adrenal glands, and ovaries with more and larger Graafian follicles, and cornified smears lacking mucus) than controls exposed to distilled water. Females exposed to kidney homogenates showed similar responses except that their time of vaginal perforation and adrenal weight did not differ from controls, and some had mucous smears. Seminal vesicle, preputial, and prostate homogenates produced only occasional effects on these indicators of reproductive maturation. The pheromone responsible for these effects, known to be present in urine, is deduced to enter the urine stream at the kidney rather than at the level of the sexual accessories.     

Influence of gonadal hormones on odours emitted by male meadow voles (Microtus pennsylvanicus).

Free-living male meadow voles (Microtus pennsylvanicus) emit odours that are attractive to females at the beginning, but not at the end, of the breeding season. The effect of gonadal hormones on female-attractant cues was examined in males born and reared in long (14 h light day-1) and short (10 h light day-1) photoperiods that simulate daylengths in the breeding and nonbreeding seasons, respectively. Gonadectomy affected the attractant properties of odours emitted by long photoperiod, but not short photoperiod, males. Long photoperiod females preferred odours of intact rather than those of gonadectomized long photoperiod males, and odours of gonadectomized long photoperiod males rather than those of intact short photoperiod males. Females did not show a preference between the odours of intact and castrated short photoperiod males. Gonadal hormone replacement in males affected female responses to the odours emitted by long photoperiod, but not short photoperiod, gonadectomized males. Long photoperiod females did not display a preference between odours of intact long photoperiod males and gonadectomized long photoperiod males treated with testosterone or oestradiol. We conclude that in spring and summer gonadal hormones increase attractiveness of male odours; this effect may require aromatization of testosterone to oestradiol. Substrates that control attractiveness of odour cues in male voles appear to be unresponsive to androgens during the nonbreeding season.     

Seasonal and interindividual variation in field water metabolism of female meadow voles Microtus pennsylvanicus.

We analyzed variations in water flux rates on a large sample of meadow voles (Microtus pennsylvanicus) to quantify the effect of season on water metabolism of individuals and to examine patterns of intra- and interindividual variability. Voles were nonreproductive females maintained in outdoor enclosures where they fed on natural vegetation. They were injected one to three times with doubly labeled water, which resulted in one to six measures of daily water flux rate per individual. Summer water flux rates of voles were 258% of the predicted values for herbivorous eutherian mammals of similar size. To date, very few studies have focused on mammals with such high water flux rates. Body water volume of individuals was higher in summer than in winter (75.6% vs. 72.5%), and water flux rate of animals was 12.5% higher in the winter season (0.99 vs. 0.88 mL H2O g-1 d-1). Between-season differences in water fluxes were proportional to differences in energy expenditures, hence the water economy index remained constant across seasons (0.30 mL H2O kJ-1). Intraindividual variability of water flux rate was high compared to interindividual variability (repeatability, r<0.30), which will make it difficult to study natural selection of water metabolism in a microevolutionary framework, at least in meadow voles.     

The influence of multiple photoperiods and pinealectomy on gonads, pelage and body weight in male meadow voles, Microtus pennsylvanicus

1. Chronic exposure of male Microtus pennsylvanicus to photoperiods with 8, 10 and 12 hr of light per day results in gonadal regression, molt to winter pelage and significant reductions in body weight and food consumption relative to voles kept on photoperiods with 13 and 14 hr of light per day. 2. A precise critical daylength is observed in this species as exposure to photoperiods with 12 or fewer hours of light per day results in complete gonadal involution, seasonal molt and loss of body weight. 3. Pinealectomy abolishes all short-photoperiod induced responses in this species.     

Aggressive behavior of adult meadow voles (Microtus pennsylvanicus) towards young

Summary Field evidence indicates that adult microtines, especially females, may be a major cause of poor juvenile survival and this may be instrumental in their population regulation. This suggests that males and females behave differently towards young animals. To examine how adult males, nonlactating females, and lactating females behave towards strange young, I introduced young animals into the home cage of the adults. Lactating females were most aggressive towards young; most males investigated them; most nonlactating females ignored them. However, discriminant function analysis indicated a great deal of overlap in the behavior of the classes. None of the classes behaved differently towards young of either sex. Females did not vary their behavior during lactation. Behavior varied among lactating females, with 55% showing little aggression and 20% showing a great deal. Most lactating females showed similar behavior in each of their bouts: docile females remained docile, aggressive females remained aggressive. I conclude that lactating females are most aggressive towards strange young. These results are consistent with the field evidence, which suggests that adult females depress juvenile survival and recruitment and that the main culprits are breeding females.     

Reliability of transferrin and leucine aminopeptidase phenotyping in wild meadow voles (Microtus pennsylvanicus)

Replicate plasma samples from wild Microtus pennsylvanicus were typed by gradient polyacrylamide gel electrophoresis for the transferrin and leucine aminopeptidase polymorphisms. Phenotypes remained the same through major seasonal changes in reproductive activity and environmental conditions. Possible explanations for the anomalous phenotypic variation seen in Microtus ochrogaster [McGovern M., and Tracy, C. R. (1981). Oecologia 51:276] are discussed.     

Gonadal hormones modulate sex differences in judgments of relative numerousness in meadow voles, Microtus pennsylvanicus

Animals in a variety of taxa discriminate between a greater quantity and a lesser quantity of the same object, an ability that is referred to as relative numerousness judgment. For example, meadow voles can distinguish between areas containing more over-marks by one opposite-sex scent donor and fewer over-marks by another opposite-sex scent donor. Females appear to be able to make better discriminations between more or less over-marks than do males. In that gonadal hormones have been implicated in modulating cognitive function associated with spatial tasks, we tested the hypothesis that high titers of testosterone and estradiol are necessary for male and female voles, respectively, to distinguish between the top- and bottom-scent donors in an area containing mixed over-marks. We gonadectomized voles, giving them either gonadal hormone replacement (testosterone for males and estradiol for females) or no hormone replacement, and tested their spontaneous judgments of distinguishing between the top- and bottom-scent donors in an area containing mixed over-marks; a task involving judgments of relative numerousness. Female voles given replacement estradiol performed better than did female voles not given replacement estradiol in determining the top-scent and bottom-scent males in areas containing mixed over-marks. In contrast, males not treated with replacement testosterone performed better than did males treated with testosterone in determining the top-scent and bottom-scent males in areas containing mixed over-marks. Thus, high titers of estradiol and low titers of testosterone are associated with better performance on tasks involving relative numerousness in female and male voles, respectively. The results of this task on relative numerousness judgments are discussed in relation to the effects of gonadal steroid hormone on spatial ability, a closely related cognitive domain, and the social biology of meadow voles.     

The effects of mate removal on pregnancy success in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus).

The effects of removing the stud male have not been controlled in many studies relating pregnancy block to the presence of an unfamiliar male. We examined the effects of removing the male on pregnancy success in prairie voles and meadow voles, two species that differ in degree of paternal investment. Whereas prairie vole males provide extensive care to offspring and accelerate pup development, meadow vole males display little or no care and delay development of pups. We predicted that removal of the stud male would decrease pregnancy success in prairie voles and either have no effect or increase success in meadow voles. In experiment 1, females were in male-induced estrus, and their mates were either left with them or were removed 4 h, 1 day, 2 days, or 8 days after mating. In experiment 2, females were in postpartum estrus, and their mates were either left with them or were removed 1 day, 2 days, or 8 days after birth of their first litter. Removal of the male soon after mating in postpartum estrus decreased pregnancy success in prairie voles and increased success in meadow voles. Thus, although removal of the stud male influenced litter production, the direction of the effect varied with species.     

Mating system of the meadow vole, Microtus pennsylvanicus

Previous studies on parental and spacing behavior of Microtuspennsylvanicus suggest a promiscuous mating system, but attemptsto find multiple paternity in single litters have been unsuccessful.In this paper we present evidence of multiple paternity in singlelitters conceived in the wild early in the breeding season.The proportion of litters sired by multiple males was estimated,by a conservative method, to be 33.1%.We argue that the presenceof promiscuity, rather than polygyny, in M. pennsylvanicus isthe result of two factors. First, overwintered breeding malesare similar in age and size, resulting in small variation incompetitive ability among males. This reduced variation in competitiveability reduces the possibility that some males defend severalfemales and others defend none. Second, the habitat structureof the meadow vole makes it difficult for a male to detect othermales nearby, and this reduces the possibility that one maleexcludes others from mating when a female comes into estrus.     

The effect of familiarity on social interactions in meadow voles,Microtus pennsylvanicus: a laboratory and field study

The role of familiarity in affecting the outcome of social interactions among meadow voles was investigated in both a laboratory and a field experiment. In the laboratory, captive meadow voles, Microtus pennsylvanicus, were exposed to a conspecific's odour. The voles were then placed into two groups: familiar and unfamiliar. Familiar voles were individuals who underwent staged dyadic encounters with the conspecific to whose odours they had been exposed. Unfamiliar voles were individuals who underwent paired encounters with conspecifics to whose odours they had not been exposed. In the field experiment, familiar voles were neighbours that were trapped within each other's home ranges over two consecutive bi-weekly trapping sessions. Unfamiliar voles were individuals that were trapped on different trapping grids. The results of the laboratory and field studies were similar. Encounters between familiar females resulted in less agonistic behaviour and more amicable acts than encounters between unfamiliar females. In contrast, encounters between familiar males resulted in more agonistic behaviour than encounters between unfamiliar males. Familiarity did not affect the outcome of male-female interactions. These results are discussed in the framework of the social system of the meadow vole.