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.     

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.     

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.     

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.     

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.     

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.     

Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles

Stressful social conditions, such as isolation, that occur during sensitive developmental periods may alter present and future social behavior. Changes in the neuroendocrine mechanisms closely associated with affiliative behaviors and stress reactivity are likely to underlie these changes in behavior. In the present study, we assessed the effects of post-weaning social housing conditions on the neuropeptides arginine vasopressin (AVP) and oxytocin (OT), and components of the hypothalamic-pituitary-adrenal axis (corticotropin releasing factor: [CRF], and corticosterone: [CORT]) in the prairie vole (Microtus ochrogaster), a socially monogamous bi-parental rodent. Following weaning at 21 days of age, prairie voles were maintained in one of three housing conditions: social isolation (isolate), paired with a same sex sibling (sibling) or paired with a stranger (stranger) of the same sex and age. Housing conditions were maintained for either 4 or 21 days. Central CRF, AVP and OT immunoreactivity (ir) were quantified and circulating plasma CORT, AVP and OT were assayed. Isolated voles had higher CRF-ir in the paraventricular nucleus of the hypothalamus (PVN) compared with sibling and stranger housed voles. Plasma CORT was significantly higher in isolates. AVP-ir was significantly lower in the PVN of isolate females compared to either sibling females or stranger females. However, AVP-ir was significantly higher in the supraoptic nucleus (SON) of isolates compared to siblings. There were no differences in central OT-ir or plasma OT. These results identify neuroendocrine mechanisms which respond to isolation and potentially modulate behavior.     

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.     

Over-marking and Adjacent Marking are Influenced by Sibship in Male Prairie Voles,Microtus ochrogaster

Scent over-marking occurs when an animal deposits its scent mark on top of the scent mark of a conspecific. Over-marking may provide advantages in the transfer of information to the individual whose scent is on top but not to the individual whose scent is on the bottom. We tested the hypothesis that over-marking is a competitive form of olfactory communication and that male prairie voles would over-mark the scent marks of same-sex conspecifics more than those of same-sex siblings. Two age-matched male voles (first male and second male) were placed successively into an arena in which they were allowed to explore freely and scent mark for 15 min at age 12, 20, 28, 36, 44, and 52 d. The first male was placed into a clean arena, whereas the second male was placed into an arena containing either the scent marks of an age-matched male sibling or nonsibling. Age affected the total number of scent marks deposited by the voles; 12-20-d-old voles deposited fewer scent marks, over-marks and adjacent marks than did 28-52-d-old voles. Sibship did not affect the total number of scent marks deposited by the first and second voles but did affect the number of over-marks and adjacent marks deposited by the second vole. Siblings received significantly fewer over-marks and adjacent marks than did nonsiblings; this effect was most dramatic after the voles reached 28 d of age, a time coincident with the onset of puberty. Males separated from siblings and housed singly at 44-d-old and tested at 52-d-old, deposited significantly more over-marks and adjacent marks in arenas if the first vole was a nonsibling than if it was a sibling. This differential scent-marking supports the hypothesis that over-marking and adjacent marking are used as competitive forms of olfactory communication by male prairie voles.     

Adult female prairie voles and meadow voles do not suppress reproduction in their daughters

Reproductive suppression of young females by conspecific females has been reported from laboratory studies on several species of rodents, including the prairie vole, Microtus ochrogaster, but not meadow voles, M. pennsylvanicus. We exposed female prairie voles and meadow voles to two treatments: a mother and one 23-26-day-old daughter paired with a strange male and a 23-26-day-old daughter paired with a different strange male. We found no differences in the proportion of daughters breeding or the time to sexual maturation for daughters raised in the two treatments for either species. Thus, we have no indication that mothers had any adverse effect on reproductive efforts of their daughters. These results differ from previous studies that concluded young female prairie voles were reproductively suppressed by female relatives. The difference between our and previous studies on reproductive suppression is that we examined breeding in young females rather than proximate measures of growth and reproductive development. We question the evolutionary significance of reproductive suppression among related female microtine rodents, especially in that it has not been documented from field populations.     

Sibling recognition in the prairie vole, Microtus ochrogaster

Since mating is seldom observed between sibling prairie voles, Microtus ochrogaster, this, behavioural discrimination was used to investigate sibling recognition in this species. Cross-fostering of 1–3-day-old pups demonstrated that unrelated pups reared together did not breed, whereas siblings reared apart bred readily when paired at weaning. When unrelated voles were paired at 14 days of age, prior to sexual maturity, significantly fewer pairs bred than when strangers were paired at 21 days of age. Separation of 21-day-old siblings for 8 days before pairing overcame incest avoidance; a 15-day separation was required for breeding by siblings that had remained together until they were 50 days old. These results indicate that sibling recognition and, consequently, incest avoidance depend on association prior to weaning.     

社会关系和性关系中的自我理毛行为

有很多观点解释了动物自我理毛的作用。例如,动物通过自我理毛可以清除在与附近的同种异性接触期间传播来的寄生虫,当嗅出同种异性的气味时也可能自我理毛,因为自我理毛是一种动物在逃避还是战斗之间所面临的进退两难选择时表现出来的改向行为。动物可以通过自我理毛缓解紧张,因而是一种缓解冲动的方式。在其它情况下,动物自我理毛可能表示对同种个体的反应,它们在不同场合下普遍存在自我理毛行为,表明这种行为有多种功能。因此,在这篇综述中,作者尽量避免自我理毛具有其它功能的争议,我们无意把自我理毛看成一种仅仅是对焦虑和紧张的反应、降低体温的机制,或者是一种护理体表的行为,我们也感到这种观点没有新意,这种有局限性的观点不支持自我理毛行为具有多种功能。我们在本文中更多关注的是自我理毛的特定背景,即当一个个体遇到同种个体的气味而出现的自我理毛行为[动物学报5l（5）：772-779,2005]。     

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.     

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.     

The integrated processing response of voles to fibre content of natural diets

1. Two species of voles were fed high fibre (barnyard grass) and low fibre (alfalfa) diets to test the integrated processing response (IPR) hypothesis. This hypothesis states that many herbivores are able to maintain their required intake of digestible nutrients and energy on diets with very different fibre content because of compensatory changes in intake of food, size of gastro-intestinal (GI) tract, passage rates of fibre and absorptive capacity of the GI tract.
2. As predicted by the IPR hypothesis, each species of vole maintained a similar intake of digestible dry matter on the two different diets. Both species also had greater intake, larger GI size, shorter mean retention times and greater GI mass (an indicator of epithelial mass and absorptive capacity) when fed grass than when fed alfalfa.
3. The two species differed in that meadow voles, the more active species, had greater total intake and obtained a greater amount of digestible dry matter from either diet than did prairie voles. Meadow voles also consume more grass in the field than do prairie voles, and they digested grass better than did prairie voles. Prairie voles, which consume more dicots in the field, digested alfalfa better than did meadow voles.
4. Meadow voles had longer GI tracts, particularly small intestines, than did prairie voles, which may be linked to their greater ability to digest grass. However, meadow voles did not have larger caeca than prairie voles, even though caecal size increased on grass diets for both species. The GI size of prairie voles fed grass increased more than did the GI size of meadow voles, and this may have enabled prairie voles to utilize a grass diet, though they prefer to eat dicots. Greater selection of leaves, which have less fibre than stems, and longer mean retention times of food may account for better digestion of alfalfa by prairie 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.     

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.     

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.     

Social isolation impairs adult neurogenesis in the limbic system and alters behaviors in female prairie voles

Disruptions in the social environment, such as social isolation, are distressing and can induce various behavioral and neural changes in the distressed animal. We conducted a series of experiments to test the hypothesis that long-term social isolation affects brain plasticity and alters behavior in the highly social prairie vole (Microtus ochrogaster). In Experiment 1, adult female prairie voles were injected with a cell division marker, 5-bromo-2′-deoxyuridine (BrdU), and then same-sex pair-housed (control) or single-housed (isolation) for 6 weeks. Social isolation reduced cell proliferation, survival, and neuronal differentiation and altered cell death in the dentate gyrus of the hippocampus and the amygdala. In addition, social isolation reduced cell proliferation in the medial preoptic area and cell survival in the ventromedial hypothalamus. These data suggest that long-term social isolation affects distinct stages of adult neurogenesis in specific limbic brain regions. In Experiment 2, isolated females displayed higher levels of anxiety-like behaviors in both the open field and elevated plus maze tests and higher levels of depression-like behavior in the forced swim test than controls. Further, isolated females showed a higher level of affiliative behavior than controls, but the two groups did not differ in social recognition memory. Together, our data suggest that social isolation not only impairs cell proliferation, survival, and neuronal differentiation in limbic brain areas, but also alters anxiety-like, depression-like, and affiliative behaviors in adult female prairie voles. These data warrant further investigation of a possible link between altered neurogenesis within the limbic system and behavioral changes.