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.     

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.     

The amount of time that a meadow vole, Microtus pennsylvanicus, self-grooms is affected by its reproductive state and that of the odor donor

Many hypotheses have been put forth to account for differences in the amount of time that animals engage self-grooming when exposed to conspecifics or their odors, but most ignore the possibility that self-grooming may be associated with olfactory communication between groomers and conspecifics. As yet, we do not know the function of self-grooming and why animals do so when they encounter the odors of conspecifics. The present experiment tests the hypothesis that the amount of time that a meadow vole, Microtus pennsylvanicus, self-grooms is affected by the reproductive state of the odor donor and its own reproductive state. The findings support the hypothesis. Male voles spent more time self-grooming when they were exposed to bedding scented by female voles in postpartum estrus (PPE) compared to that of female voles in other reproductive states and female mice. PPE female voles spent more time self-grooming when they were exposed to bedding scented by testosterone-treated male voles than either to that of gonadectomized male voles and male mice. PPE female voles spent more time than OVX+E and more time than OVX females self-grooming when they were exposed to bedding scented by testosterone-treated male voles. GX+T male voles spent more time than GX male voles self-grooming when they were exposed to bedding scented by PPE female voles. The results suggest that individuals self-groom more in the presence of an odor of a highly receptive potential mate than that of a less receptive mate.     

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.     

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.     

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.     

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.     

Self-grooming induced by sexual chemical signals in male root voles (Microtus oeconomus Pallas)

Sniffing is one-way animals collect chemical signals, and many males self-groom when they encounter the odor of opposite-sex conspecifics. We tested the hypothesis that sexual chemical signals from females can induce self-grooming behavior in male root voles (Microtus oeconomus Pallas). Specifically, we investigated the sniffing pattern of male root voles in response to odors from the head, trunk, and tail areas of lactating and non-lactating females. The self-grooming behavior of males in response to female individual odorant stimuli was documented, and the relationship between self-grooming and sniffing of odors from the head, trunk, and tails areas were analyzed. Sniffing pattern results showed that males are most interested in odors from the head area, and more interested in odors from the tail as compared to the trunk area. Males displayed different sniffing and self-grooming behaviors when they were exposed to odors from lactating females as compared to non-lactating females. Males also spent more time sniffing and engaged in more sniffing behaviors in response to odors from the lactating females’ tail area as compared to the same odors from non-lactating females. Similarly, males spent more time self-grooming and engaged in more self-grooming behaviors in the presence of individual odors from lactating females as compared to individual odors from non-lactating females. Partial correlation analyses revealed that the frequency of self-grooming was significantly correlated with the frequency of tail area sniffs. Results from this experiment suggest that sexual attractiveness of lactating females is stronger than that of non-lactating females. Furthermore, the partial correlation analysis demonstrated that self-grooming in males is induced by odors from the tail area of females. Collectively, these results support the hypothesis that sexual chemical signals from females can induce self-grooming behavior in male root voles. Self-grooming may also reflect the groomer's sexual motivation and facilitate sexual interactions.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

The Reproductive State of Female Voles Affects their Scent Marking Behavior and the Responses of Male Conspecifics to Such Marks

During the breeding season, the reproductive condition of female mammals changes. Females may or may not be sexually receptive. We conducted a series of experiments to determine whether reproductive condition of female meadow voles affects their scent marking behavior as well as the scent marking behavior of male conspecifics. In expt 1, females in postpartum estrus (PPE females) deposited more scent marks than females that were neither pregnant nor lactating (REF females) or ovariectomized females (OVX females). In expt 2, male voles scent marked more and deposited more over‐marks in areas marked by PPE females than by REF and OVX females. In expt 3, PPE females deposited more scent marks and over‐marks in areas marked by males than did females in the other reproductive states. The results of these experiments showed that male and female voles may vary in the number, type and location of scent marks they deposit in areas scented by particular conspecifics.     

不同社会等级雄性根田鼠对自身和同性陌生气味的辨别

采用两两遭遇法确定雄性根田鼠的社会等级,然后以新鲜尿作气味源,在行为选择箱中观察不同社会等级雄性根田鼠对自身气味和非自身气味的行为响应模式,结果表明:种群中从属个体对自身尿液存在明显偏好,其对自身尿液的接近潜伏期显著短于非自身尿液,而访问时间、自我修饰频次都显著高于非自身尿液;种群中优势个体则优先访问非自身尿液,其对非自身尿液的访问时间、嗅舔时间、自我修饰及反标记均显著高于自身尿液;对非自身尿液,不同社会等级雄性个体之间存在明显不同的行为反应模式。这说明,不同社会等级雄性根田鼠具有自我识别的能力且模式不同,同时其对非自身尿气味响应模式的差异也与自身的社会等级有关。     

Use of olfaction for sexual recognition in the subterranean rodent<Emphasis Type="Italic">Ctenomys talarum</Emphasis>

The ability of the tuco-tucoCtenomys talarum Thomas, 1898 to recognize sex by olfactory cues contained in urine, faeces and soiled shavings was tested by using preference tests. Nonbreeding tuco-tucos selected odours from opposite-sex rather than same-sex conspecifics. This pattern differed between sexes: females spent more time sniffing male than female odours for all scent sources whereas males did not show any difference in the time they spent investigating odours of each sex for each tested odour sources. Dissimilarities in odour selections between sexes may be attributed to a different combination of factors involved in olfactory interest for each sex. The function of gender cues recognition is discussed.     

Scent marking and mate choice in the prairie vole, Microtus ochrogaster

Scent marking is common among male and female rodents and might be used in male-male competition and as a mechanism for mate attraction. I tested the hypotheses that females would choose males based on their frequency and placement of scent marks, and that a female would advertise interest in a particular male by placing her scent marks on or near those of a preferred mating partner. In a series of experiments conducted with prairie voles, Microtus ochrogaster, females did not choose mates based on the frequency or placement of scent marks by males nor did they advertise their interest in a particular male through the frequency or placement of scent marks. The number of males chosen that scent-marked more than their opponents did not differ significantly between females exposed (11 of 15) and not exposed (10 of 15) to scents of males. Females exposed and not exposed to scents of males preferred seven of the same males that had scent-marked more than their opponents. When a third group of females was exposed to four times more scent of the less preferred than preferred males, they still chose the preferred males. Thus, the frequency and placement of scent marks by males were not used to assess males for mate choice nor did female prairie voles use scent to advertise their preference for a mating partner. In that scent marking is common in male and female mammals, scent quality might be more important than quantity in male-male competition and mate attraction.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

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.