Meadow Voles (Microtus pennsylvanicus, Arvicolidae) Over-mark and Adjacent-mark the Scent Marks of Same-sex Conspecifics

Scent over-marking occurs when an animal deposits its scent mark on top of the scent mark of a conspecific; adjacent-marking occurs when an animal deposits its scent mark next to the scent mark of a conspecific. Given that male rodents usually scent mark more than females and that animals spend more time investigating the odor of the top-scent donor of an over-mark, I tested the following three hypotheses. First, male meadow voles deposit more scent marks than female meadow voles. Second, male meadow voles will deposit more over-marks and adjacent-marks in response to the scent marks of a same-sex conspecific than females would. Third, meadow voles spend more time investigating the odor of the second vole placed in the arena than that of the first vole placed in the arena. To test these hypotheses, two age-matched, like-sex conspecifics (first vole and second vole) were placed successively into an arena in which they were allowed to freely explore and scent mark for 15 min. The first hypothesis was not supported. The first and second vole, independently of sex, deposited a similar number of scent marks. The second hypothesis was also not supported by the data: more conspecific scent marks were over-marked by the second female than by the second male. The third hypothesis was supported by the data. After investigating a scented arena, males and females spent more time investigating the odor of the second vole than that of the first vole. Sex differences in scent-marking behaviors of meadow voles are unlike those reported for other species of rodents.     

Olfactory Experience Affects the Response of Meadow Voles to the Opposite‐Sex Scent Donor of Mixed‐Sex Over‐Marks

Scent marking and over‐marking are important forms of communication between the sexes for many terrestrial mammals. Over the course of three experiments, we determined whether the amount of time individuals investigate the scent marks of opposite‐sex conspecifics is affected by 4 d of olfactory experience with those conspecifics. In Experiment 1, female meadow voles, Microtus pennsylvanicus, spent more time investigating the scent mark of the novel male conspecific than that of the familiar male donor, whereas male voles spent similar amounts of time investigating the scent mark of the familiar female and a novel female conspecific. In Experiment 2, voles were exposed to a mixed‐sex over‐mark in which subjects did not have 4 d of olfactory experience with either the top‐scent donor or the bottom‐scent donor. During the test phase, male and female voles spent more time investigating the scent mark of the opposite‐sex conspecific that provided the top‐scent mark than that of a novel, opposite‐sex conspecific. Male and female voles spent similar amounts of time investigating the scent mark of the bottom‐scent donor and that of a novel opposite‐sex conspecific. In Experiment 3, voles were exposed to a mixed‐sex over‐mark that contained the scent mark of an opposite‐sex conspecific with which they had 4 d of olfactory experience. During the test phase, male voles spent more time investigating the mark of the familiar, top‐scent female than the scent mark of a novel female donor but spent similar amounts of time investigating the mark of the familiar, bottom‐scent female and that of a novel female donor. In contrast, female voles spent more time investigating the mark of a novel male donor than that of either the familiar, top‐scent male or that of the familiar, bottom‐scent male. The sex differences in the responses of voles to scent marks and mixed‐sex over‐marks are discussed in relation to the natural history and non‐monogamous mating system of meadow voles.     

Male and Female Meadow Voles,Microtus pennsylvanicus,Differ in Their Responses to Heterospecific/Conspecific Over‐Marks

Voles use runways, paths, and trails that may also be used by rabbits and mink. These shared areas could contain the scent marks of conspecifics and heterospecifics. Thus, it is likely that the scent marks of heterospecifics may overlap or be overlapped by those of voles, forming over‐marks. Much is known about how voles respond to over‐marks of two different conspecifics. However, we do not know how they would respond to an opposite‐sex conspecific whose scent marks are in an over‐mark with the scent marks of predator or the scent marks of a non‐predator heterospecifics. We tested the hypothesis that meadow voles, Microtus pennsylvanicus, differ in their response to the scent mark of the opposite‐sex conspecific if the scent mark was overlapped by that of a mink, a vole predator, or rabbit, a vole non‐predator. We found that female but not male voles showed a preference for the scent marks of the opposite‐sex conspecifics that were part of the mink‐vole over‐mark when compared to those of opposite‐sex conspecifics that were not part of the over‐mark. This preference by female voles was independent of whether the male vole was the top‐scent donor or bottom‐scent donor of the over‐mark. Male and female voles showed no preference between the scent marks of the opposite‐sex conspecifics whose marks were part of or not part of the rabbit‐vole over‐mark. Sex differences in the manner that meadow voles respond to rabbit‐vole and mink‐vole over‐marks are discussed.     

Self-Grooming as a Tactic Used by Prairie Voles Microtus ochrogaster to Enhance Sexual Communication

Observations of numerous mammals suggest males self-groom more than females in response to the odours of opposite-sex conspecifics. Two experiments tested the hypothesis that self-grooming may be a tactic used by males to attract mates in prairie voles Microtus ochrogaster . In the first experiment, we measured the amounts of time voles self-groomed during exposure either to male-scented cotton bedding, female-scented cotton bedding, or clean cotton bedding. Results from this experiment support the hypothesis and also show that female prairie voles self-groom in response to odours of males. In addition, male prairie voles groom more in response to male odours than to female odours, suggesting that self-grooming also serves a role in male–male competition. In the second experiment, male and female voles spent more time investigating scent marks of opposite-sex conspecifics that recently self-groomed at a higher rate than those of opposite-sex conspecifics that self-groomed at a lower rate. Female, but not male prairie voles, spent more time investigating scent marks of opposite-sex conspecifics that self-groomed at a high rate than those of same-sex conspecifics that self-groomed at a high rate. For prairie voles, self-grooming may increase the detection of their scent marks by conspecifics. By self-grooming, prairie voles may be attempting to attract opposite-sex conspecifics, and males may also be attempting to deter encounters with male conspecifics.     

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.     

基于交叉抚育的雄性根田鼠对异性同胞尿气味的识别

通过交叉抚育建立室内繁殖种群,在断奶后（80日龄）分别取这些供体的新鲜尿气味作刺激物,在行为观察箱中观察和记录雄性根田鼠对雌鼠气味的行为反应,以研究根田鼠同胞识别的化学通讯机制。结果表明：①在不同的发育时期（2～70日龄）,雄性同巢同胞与异巢同胞的体重没有显著差异。②雄性根田鼠对雌性同巢非同胞气味的接近潜伏期显著长于对异巢非同胞的接近潜伏期（P〈0．05）,其对异巢非同胞气味的访问时间和嗅舔时间都显著高于同巢非同胞气味（P〈0．05）。③雄性根田鼠对雌性异巢同胞和异巢非同胞气味的不存在明显偏好。其对两者的接近潜伏期、访问频次、访问时间、嗅舔频次和嗅舔时间等行为响应均无显著差异（P〈0．05）。这些结果表明,80日龄时,雄性根田鼠能够识别熟悉和陌生的无亲属关系雌性尿气味,但不能区分陌生的亲属和非亲属,因此,其异性同胞识别的机制为共生熟悉模式。     

Meadow Voles (Microtus pennsylvanicus) and Prairie Voles (M. ochrogaster) Differ in Their Responses to Over-Marks from Opposite- and Same-Sex Conspecifics

Over‐marking occurs when one individual deposits its scent mark on the scent mark of a conspecific. Previous studies have shown that meadow voles (Microtus pennsylvanicus) and prairie voles (M. ochrogaster) that were exposed to an over‐mark of two same‐sex conspecifics, later responded similarly to the top‐scent mark but differed in their response to the bottom‐scent mark. In the present study, we examined the responses of meadow voles and prairie voles to same‐sex and mixed‐sex over‐marks to ascertain whether their responses reflect the different tactics which males and females in promiscuous (meadow voles) and monogamous (prairie voles) species use to attract opposite‐sex conspecifics and to compete with same‐sex conspecifics. Males and females of both species spent more time investigating the mark of the top‐scent donor than that of the bottom‐scent donor of an over‐mark. Meadow voles exposed to a mixed‐sex over‐mark spent more time investigating the mark of the opposite‐sex conspecific independently of whether it was from the top‐ or bottom‐scent donor. In contrast, prairie voles spent more time investigating the mark of the opposite‐sex donor if it was from the top‐scent donor. These results suggest that: (i) over‐marking serves a competitive function; (ii) the scent marks of individuals attract multiple mates in promiscuous species such as the meadow vole; and (iii) the scent marks of individuals establish and maintain pair bonds between familiar opposite‐sex conspecifics in monogamous species such as the prairie vole.     

Effects of food availability on proceptivity: A test of the reproduction at all costs and metabolic fuels hypotheses

Proceptive behaviours are used by animals to indicate interest in opposite-sex conspecifics. These behaviours can be affected by an individual's nutritional status. Two mutually exclusive hypotheses have been proposed to account for the effects of food availability on reproduction. These are the metabolic fuels hypothesis and the reproduction at all costs hypothesis. It is not known if food availability affects proceptive behaviours such as scent marking, over-marking, and self-grooming. In this study, we tested the hypothesis that food-deprived and nonfood-deprived meadow voles, Microtus pennsylvanicus, differ in the number of scent marks they deposit, the proportion of over-marks they deposit, and the amount of time they spend self-grooming when they encounter the scent marks of opposite-sex conspecifics. We tested this hypothesis by exposing meadow voles that either had continuous access to food or were food-deprived for either 6hours or 24hours to the scent marks of an opposite-sex conspecific. Due to differences in the natural history of male and female meadow voles, we predicted that female voles' behaviour will best be explained by the metabolic fuels hypothesis whereas males' behaviour will best be explained by the reproduction at all costs hypothesis. We found that both male and female voles deprived of food for either 6hours or 24hours spent less time self-grooming compared to nonfood-deprived voles. However, food availability did not affect the scent marking and over-marking behaviour of male and female voles. Differences in the effects of food availability on these proceptive behaviours are discussed within the context of the natural history of meadow voles.     

Dietary protein content affects the response of meadow voles, <Emphasis Type="Italic">Microtus pennsylvanicus</Emphasis>, to over-marks

The response to signals, including scent marks, from opposite-sex conspecifics can be affected by the nutritional state of both the sender and receiver of these signals. Protein content of the diet affects how meadow voles (Microtus pennsylvanicus) respond to single scent marks, but it is unknown how it affects an individual’s response to the overlapping scent marks of two donors (an over-mark). In experiment 1, we tested the hypothesis that protein content of the diet affects the amount of time voles spend investigating the marks of the top- and bottom-scent donors of an over-mark. Males and females fed a 22% protein diet spent more time investigating the scent mark of the top-scent donor than that of the bottom-scent donor; voles fed 9% and 13% protein diets spent similar amounts of time investigating the top- and bottom-scent donors. In experiment 2, we tested the hypothesis that protein content of the diet of the top- and bottom-scent donors affects the amount of time conspecifics spend investigating their scent marks. Female voles spent more time investigating the mark of the top-scent male than that of the bottom-scent male, independent of the differences in protein content of the diets of the top- and bottom-scent donors. Male voles, however, spent more time investigating the top-scent female when she was fed a diet higher in protein content than that of the bottom-scent female. Our results are discussed within the context of the natural history of voles.     

Response of Prairie Voles, Microtus ochrogaster (Rodentia, Arvicolidae), to Scent Over-marks of Two Same-sex Conspecifics: A Test of the Scent-masking Hypothesis

Previous work shows that after investigating a same-sex over-mark, two nonmonogamous species, meadow voles and golden hamsters, preferred the odor of the top-scent donor to that of the bottom-scent donor, and behaved as the odor of the bottom-scent donor was not familiar. This finding supported the scent-masking hypothesis; one of three hypotheses suggested previously to account for how an animal responds to the overlapping scent marks of two same-sex conspecifics. The present experiments tested whether one of these hypotheses, either scent-masking, scent-bulletin-board, or scent-blending, predicts how a monogamous species, the prairie vole, responds to such over-marks. Our data show that none of the three hypotheses adequately describes the way in which prairie voles respond to conspecific over-marks. Although prairie voles preferred the top scent to the bottom scent, they behaved as if the latter scent was familiar and less important than a novel scent (a scent not part of the over-mark). Overall, the data suggest that the manner in which males and females respond to same-sex over-marks reflects the different tactics they may use to attract and compete with conspecifics in monogamous and nonmonogamous species.     

Age Affects Over-Marking of Opposite-Sex Scent Marks in Meadow Voles, Microtus pennsylvanicus

Models of age-related effects on behavior predict that among short-lived species younger adults are more attractive and attracted to opposite-sex conspecifics than are older adults, whereas the converse is predicted for long-lived species. Although most studies of age-related effects on behavior support these predictions, they are not supported by many studies of scent marking, a behavior used in mate attraction. Over-marking, a form of scent marking, is a tactic used by many terrestrial mammals to convey information about themselves to opposite-sex conspecifics. The present study tested the hypothesis that the age of meadow voles, Microtus pennsylvanicus ; a microtine rodent, affects their over- and scent-marking behaviors when they encounter the marks of opposite-sex conspecifics. Sex differences existed in the over-marking behavior of adult voles among the three different age groups that were tested. Male voles that were 5–7 and 10–12 mo olds over-marked a higher proportion of the marks of females than did 2–3 mo old male voles. Female voles that were 2–3, 5–7, and 10–12 mo old over-marked a similar number of marks deposited by male voles. Overall, the data were not consistent with models predicting the behavior of short-lived animals such as rodents when they encounter the opposite sex. The differences in over-marking displayed by older and younger adult male voles may be associated with life history tradeoffs, the likelihood that they will encounter sexually receptive females, and being selected as mates.     

Self‐Grooming Response of Meadow Voles to the Odor of Opposite‐Sex Conspecifics in Relation to the Dietary Protein Content of Both Sexes

Many animals self‐groom when they encounter the scent marks of opposite‐sex conspecifics. Self‐grooming transmits odiferous substances that contain information about the groomer’s condition, which is affected by its nutritional state. We tested the hypothesis that the amount of time that individuals self‐groom to opposite‐sex conspecifics is affected by the amount of protein in their diet and that of the scent donor. We did so by feeding meadow voles (Microtus pennsylvanicus) a diet containing 9%, 13%, or 22% dietary protein for 30 d and observing their self‐grooming behavior when they were exposed to bedding scented by an opposite‐sex conspecific (odor donor) fed one of the three diets, or fresh cotton bedding (control). The hypothesis was partially supported. We found that the protein content of the diet of male and female groomers did not affect the amount of time they self‐groomed. However, the protein content of the diet of male odor donors affected the amount of time that female voles spent self‐grooming. Female voles self‐groomed more in response to male odor donors fed a 22% protein‐content diet than to those produced by male odor donors fed either a 9% or a 13% protein‐content diet. Interestingly, the amount of time males self‐groomed was not affected by the protein content of the diet of the female odor donor. These results may, in part, be explained by the natural history of free‐living meadow voles, sex differences in costs associated with mate attraction and reproduction, and the direct or indirect benefits that females receive from males fed a diet high in protein content.     

Persistence of the Attractiveness of Two Sex-specific Scents in Meadow Voles,Microtus pennsylvanicus

The function of an odour may be reflected in its fade-out time in the environment. In this study, we investigated fade-out times of two specific odours, the anogenital area scent and that of the posterolateral region. These two odours support opposite-sex preferences in male and female meadow voles, Microtus pennsylvanicus, but convey nonidentical information to conspecifics during the breeding season. The first experiment tested whether meadow voles respond preferentially to scents that were aged for 15 min (fresh) to 30 d. Males preferred female anogenital area scent to male anogenital area scent if both scents were ≤ 10 d old. By comparison, females preferred male anogenital area scent to female anogenital area scent if the scents were ≤ 25 d old. However, male and female voles preferred the posterolateral scent of males to that of females if the scents were ≤ 1 d old. Thus, fade-out times for these two scents differ for males and females, suggesting different functions. In the second experiment, male and female voles preferred fresh anogenital area scent and fresh posterolateral region scent compared with those same scents that were older. This result suggests that older scents may have lost information over time about the sex of the donor. Overall, data from both experiments indicate that voles may use specific scents for communication in different social contexts.     

Meadow voles and prairie voles differ in the percentage of conspecific marks they over-mark

Many terrestrial mammals scent mark in areas containing the scent marks of conspecifics, and thus, may deposit their own scent marks on top of those that were deposited previously by conspecifics. This phenomenon, known as over-marking appears to play a role in same-sex competition or mate attraction. The present study determines whether meadow and prairie voles avoid over-marking the scent marks of conspecifics, target the scent marks of conspecifics and over-mark them, or randomly over-mark the scent marks of conspecifics. The data show that meadow and prairie voles adjust the number and location of scent marks that they deposit in areas marked previously by particular conspecifics. Male and female meadow and prairie voles target the scent marks of opposite-sex conspecifics and over-mark them. Female meadow and prairie voles also target the scent marks of female conspecifics. In contrast, male meadow and prairie voles over-mark the scent marks of male conspecifics in a random manner. By differentially over-marking the scent marks of conspecifics, voles may be able to communicate particular information to a variety of conspecifics.     

Olfactory Communication and Neighbor Recognition in Giant Kangaroo Rats

We hypothesized that olfactory communication facilitates neighbor recognition in the giant kangaroo rat, Dipodomys ingens , and is therefore influential in coordinating social interactions in this solitary, desert rodent. We tested whether (i) D. ingens can discriminate between odors of same- and opposite-sex conspecifics; and (ii) the kangaroo rats exhibit scent preferences based on familiarity. In habituation-discrimination tests, we found that both genders distinguish differences between the scent of individuals of the same- and opposite-sex. In olfactory preference tests, both males and females spent significantly more time investigating the scent of their familiar cagemate than the scent of an unfamiliar conspecific. Giant kangaroo rats may be able to recognize familiar neighbors from olfactory cues, thus supporting a hypothesis of neighbor recognition. Neighbor recognition may be an important mechanism of social interactions in this endangered species.     

Meadow voles,Microtus pennsylvanicus,can discriminate between scents of individual house cats,Felis catus

Individual discrimination provides animals the opportunity to adjust their exposure and behavior when interacting with other animals, both conspecifics and heterospecifics. Meadow voles, Microtus pennsylvanicus, were exposed to scents of house cats, Felis catus. Our first experiment tested whether meadow voles could discriminate between caudal, interdigital, and facial scents produced by a cat with a habituation–dishabituation paradigm. Upon exposure to the familiar scent and a novel one, meadow voles did not investigate either scent more than the other. Our second experiment tested whether meadow voles discriminate between the facial scents of different cats. When exposed to a familiar scent of one cat and the unfamiliar scent of another cat, the meadow voles did discriminate and investigated the unfamiliar scent more than the familiar scent. The results suggest that meadow voles will discriminate between cats using any scent that the cat may inadvertently leave within the environment, thereby reducing the vole's risk of predation by that individual.     

Female meadow voles,Microtus pennsylvanicus,do not alter their over-marking in response to female conspecifics that were food deprived

Many terrestrial mammals will deposit scent marks and over-marks, the latter being the overlapping scent marks of two conspecifics. Studies have shown that male rodents that are exposed to the overlapping scent marks of two female conspecifics later spend more time investigating the mark of the top-scent female than that of the bottom-scent female. This suggests that over-marking is a form of competition and that the top-scent female is more likely than the bottom-scent female to be chosen as a potential mate. Thus, females should over-mark the scents of neighboring females at a rate that will maximize their chances of attracting males. However, meadow voles live in areas that may contain patchy food availability and residents may differ in their nutritional status. Females in a better nutritional state may be more likely than those in poorer nutritional states to indicate their presence in an area, signal possession of a territory, and to attract mates. Thus, we tested the prediction that female meadow voles, Microtus pennsylvanicus, that were not food deprived would deposit more over-marks than female voles that were food deprived for 6 h. Food-deprived female voles and female voles that had continuous access to food deposited a similar number of scent marks and used a similar proportion of those marks as over-marks when they encountered the scent marks of female conspecifics. These findings suggest that the nutritional status of female voles does not affect their ability to signal their presence in an area marked by a female conspecific.     

Behavioural development of conspecific odour preferences in bank voles,Clethrionomys glareolus

Biological odours of conspecifics are known to have strong influences on behavioural interaction in bank voles Clethrionomys glareolus. This experiment tested two hypotheses. (1) Olfactory cues from familiar and unfamiliar mature opposite-sex conspecifics differ in their attractiveness to males and females, and their behavioural reactions change with age. (2) A genetically based mechanism is involved in female recognition of kin.In a two-choice preference test, prepubertal males and females were more attracted to familiar than to unfamiliar odours of opposite-sex conspecifics, as manifested by more time spent sniffing familiar voles. As the young reached sexual maturity they shifted their odour preferences. Mature males and females preferred the novel odour of unrelated opposite-sex conspecifics to that of relatives. The results of experiments testing the second hypothesis indicate that females use a genetically based mechanism to recognise their kin. Young and mature females were able to recognise the odour of their biological but socially unknown fathers, and showed the same pattern of behaviour as females in previous experiments.The possible biological functions of kin recognition in bank voles are discussed.     

Food Deprivation Suppresses a Preference for the Top-Scent Mark of an Over-Mark in Meadow Voles (Microtus pennsylvanicus)

Food availability affects whether mammals communicate their interest in interacting with opposite‐sex conspecifics. This study examined the responses of voles to over‐marks, and factors that influence the formation and maintenance of a preference for the top‐scent in an over‐mark. Specifically, we investigated how food deprivation affected the amount of time male and female voles exposed to an over‐mark, later responded to the marks of the top‐ and bottom‐scent donors when subsequently presented with the two scents side by side. Males and females that were not food deprived and males that were food deprived 6 h before exposure to an over‐mark later maintained a preference for the donor of the top‐scent mark compared with the donor of the bottom‐scent mark of the over‐mark. Females that were food deprived for 6 h before or after exposure of the over‐mark and males food deprived 6 h after the exposure to the over‐mark showed no preference for the top‐scent mark donor. Re‐feeding females that were food deprived for 6 h before exposure to an over‐mark was sufficient to restore their preference for the mark of the top‐scent male over that of the bottom‐scent male. The different responses of food‐deprived male and female voles to over‐marks of opposite‐sex conspecifics may be associated with differences in their tactics for interacting with potential mates and the higher energetic costs of reproduction in female voles than in male voles.     

Time course of androgenic modulation of odor preferences and odor cues in male meadow voles, Microtus pennsylvanicus.

During the breeding season, male meadow voles prefer female over male odors and females prefer male over female odors. Testosterone control of males' odor preferences and production of odors attractive to females differ. A male meadow vole's preference for female versus male odor was still evident 1 week after castration, but not 1 week later. This preference was reinstated in testosterone-treated male voles 2 weeks after the onset of hormone replacement. The attractiveness of male odors to females did not disappear until 3 weeks after castration. The attractiveness of male odors was reinstated 1 week after castrated males were treated with testosterone. The time course for the androgenic modulation of production of odors attractive to females may facilitate breeding. For example, at the end of the breeding season males may emit an odor that is still attractive to females. Similarly, at the beginning of the breeding season males may emit an odor that is attractive to females.