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.     

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.     

Re‐Feeding Food‐Deprived Male Meadow Voles Affects the Sperm Allocation of Their Rival Males

An individual's nutritional status affects the manner in which same‐ and opposite‐sex conspecifics respond to that individual, which may affect their fitness. Male meadow voles, Microtus pennsylvanicus, increase their sperm allocation if they encounter the scent mark of an unfamiliar male that is not nutritionally challenged. If, however, the scent mark comes from a male that has been food deprived for 24 h, stud male voles do not increase their sperm allocation. Food‐deprived males may be viewed as being lower quality and a reduced risk of sperm competition by rival males. We hypothesized that stud males in promiscuous mating systems tailor their sperm allocations depending on whether rival males have been food deprived and then re‐fed. We predicted that newly re‐fed males will be considered a strong risk of sperm competition because of the potentially high fitness and survival costs associated with food deprivation in males, and that they will cause stud males to increase their sperm allocation. Our results, however, showed that the recovery period from 24 h of food deprivation was a relatively slow process. It took between 96 and 336 h of re‐feeding male scent donors that were food deprived for 24 h to induce stud males to increase their sperm allocation to levels comparable to when scent donors were not food deprived. Stud male voles may be conserving the amount of sperm allocated until the male scent donors have recovered from food deprivation and subsequent re‐feeding.     

Food Deprivation and Restriction During late Gestation Affect the Sexual Behavior of Postpartum Female Meadow Voles,Microtus pennsylvanicus

In many species of small mammals, including meadow voles, Microtus pennsylvanicus, females come into postpartum estrus (PPE) within 12–24 h of giving birth, allowing them to mate and become pregnant while raising the current litter. PPE females show increases in attractivity, proceptivity, and receptivity, the three components of sexual behavior, relative to females not in PPE. Several studies have shown that food deprivation and restriction reduce attractivity, proceptivity, and receptivity of females not in PPE. We tested the hypothesis that food deprivation and restriction during late gestation cause deficits and decrease the attractivity, proceptivity, and receptivity of females when they enter PPE. Our data support the hypothesis. On day 1 of lactation, females that were food deprived and food restricted produced scent marks that were significantly less attractive as those produced by control PPE females. Food deprivation but not food restriction caused females to no longer display significant preferences for the scent marks of males over those of females (proceptivity). Food deprivation and food restriction were sufficient to induce females to become significantly less sexually receptive than control females. Eleven of 12 control PPE females mated, 4 of 12 food‐restricted females mated, and 3 of 12 food‐deprived females mated. Dams facing food deprivation or restriction during late gestation may have to balance the benefits of mating during PPE with the increased costs associated with getting pregnant while they are lactating.     

Adaptive immune responses are linked to the mating system of arvicoline rodents

ABSTRACT Males generally exhibit reduced immune responses and greater susceptibility to disease than females. The suppressive effect of testosterone on immune function is hypothesized to be one reason why males have lower immune responses than females. Presumably, this effect of testosterone should be more pronounced among polygynous than monogamous species because circulating testosterone is higher among polygynous than monogamous males. The present study examined the extent to which sex differences in specific humoral immunity are related to the endocrine status and mating system of two arvicoline rodents. Humoral immunity was evaluated among polygynous meadow voles (Microtus pennsylvanicus) and monogamous prairie voles (Microtus ochrogaster) by challenging them with the novel antigen keyhole limpet hemocyanin (KLH) and assessing specific immune responses 5, 10, and 15 d following immunization. Overall, meadow voles mounted higher anti-KLH IgM and IgG responses than prairie voles did. Sex differences were also apparent for anti-KLH IgM responses; male meadow voles mounted higher antibody responses than conspecific females, whereas female prairie voles mounted greater responses to KLH than did conspecific males. Male meadow voles had significantly higher testosterone concentrations and reproductive organ mass than male prairie voles did but had elevated immune responses, suggesting that testosterone may not be the primary factor involved in the observed sex and species differences in immune responses. Species and sex differences in corticosterone concentrations were also evident and may contribute to the observed differences in immune function. The influence of extrinsic factors on immune function is also discussed. Taken together, these data provide evidence that the mating system may influence endocrine-immune 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.     

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.     

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.     

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.     

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.     

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.     

The behavior of female meadow voles,Microtus pennsylvanicus,during postpartum estrus and the responses of males to them

For numerous species of terrestrial mammals, postpartum estrus, PPE, is a period of heightened attractivity, proceptivity, and receptivity that occurs shortly after the female delivers her litter. Many mammals mate almost exclusively during PPE. However, we know little about the behavior of PPE females and how male conspecifics behave toward them. This review focuses on the results of recent studies that tried to examine systematically the behavior of PPE female meadow voles, Microtus pennsylvanicus, and the responses of males to them. Our review is divided in five parts. First, we introduce the topic of PPE in rodents. Second, we discuss the outcome of studies showing that PPE female voles were more attractive to males, directed more proceptive behaviors toward males, and were more sexually receptive and likely to get pregnant compared to females that were not in PPE. Third, we discuss studies that examined how male voles respond and adjust their behavior when they encounter PPE females. Males increase the likelihood of mating with PPE females by recalling the reproductive state of females and the location of their nests, and by anticipating how long or when each of these females would be in PPE. Fourth, we focus in how food availability, an ecological constraint facing gestating female voles, affected their attractivity, proceptivity, and receptivity postpartum. Fifth, we revisit the benefits of seeking out and mating with PPE females and introduce the costs of doing so for both males and PPE females. We close our review with a list of questions that can be used to formulate testable hypotheses surrounding the behavior of PPE females and the responses of male conspecifics to them.     

Male copulatory behavior and the induction of ovulation in female voles: a quest for species specificity.

Two experiments were conducted to investigate species specificity in the neuroendocrine responsiveness of female prairie voles to the copulatory patterns of males. In Experiment 1, prairie vole males mated for one ejaculatory series were not significantly more effective in inducing ovulation in prairie vole females than montane voles mated with prairie vole females for one series, two series, or to satiety. Mating with conspecific males did result in significantly more implanted embryos than did heterospecific matings. In Experiment 2, it was found that, when the amount of vaginal stimulation was both low and equated across groups, prairie vole males were significantly more effective in triggering ovulation in female prairie voles than were either meadow voles or montane voles. Although there appears to be some species specificity to the “vaginal codes” of these congeneric species, its biological significance is unclear.     

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.     

Pre-implantation Pregnancy Disruption in Female Meadow Voles Microtus pennsylvanicus (Rodentia: Muridae): Male Competition or Female Mate Choice?

I investigated alternative hypotheses concerning the functions of pre-implantation male-induced pregnancy disruption in meadow voles. Disruptions may be viewed as: 1. Postcopulatory male competition; 2. A mechanism for postcopulatory mate choice by females; and 3. A means of benefitting females by terminating investment in litters that may be harmed by new males. Female voles were paired with a second male 3 d after mating with their first mate. Behavioural interactions between the female and each male were compared for females that disrupted or retained the pregnancy sired by the first male. Whether they were the females' first or second mates, males siring litters showed similar high levels of approach and moderately high aggression, behaviour that differed from the females' other mates. Disrupted females huddled sooner with their second mates than females that retained their original pregnancies, and females tended to approach males that approached them. These results suggest that females influence whether a disruption occurs by the amount of contact they initiate with the second male, and thus pregnancy disruption may facilitate postcopulatory mate choice by females. This pre-implantation disruption did not enhance female reproductive success: pup survival was the same whether or not a disruption occurred, and males living with pups they had sired (after a disruption) spent as much time with them as males with unrelated pups (females did not disrupt).     

Meadow Voles and Prairie Voles Differ in the Length of Time They Prefer the Top-Scent Donor of an Over-Mark

Scent over-marking occurs when one individual places its scent mark on top of one deposited by a conspecific. Studies have shown that animals investigating an over-mark later behave as if the top-scent mark is more important than the bottom-scent mark. Differences in response to over-marks may reflect differences in social and mating systems. Here, we ascertained the length of time that meadow voles ( Microtus pennsylvanicus ) and prairie voles ( Microtus ochrogaster ), exposed to an over-mark, maintain a preference for the mark of the top-scent donor compared with that of the bottom-scent donor. If voles had no previous sexual experience with their top-scent and bottom-scent donors, male and female meadow voles maintained a preference for their top-scent donor's mark over their bottom-scent donor's mark for 48 h. In contrast, male and female prairie voles maintained such preferences for 24 h and 12 h, respectively. If voles had prior sexual experience with either their top- or bottom-scent donor, such experience did not affect the length of time meadow voles and male prairie voles maintained a preference for their top-scent donor. Female prairie voles maintained a 12-h preference for the top-scent mark if it belonged to the mate. If the mate was the bottom-scent donor, female prairie voles showed no preference for it or the top-scent mark. These findings are discussed within the framework that an association may exist between the manner in which voles respond to over-marks and their social and mating systems.     

Sexual Competition,Coercive Mating and Mate Assessment in the One‐Sided Livebearer,Jenynsia multidentata: Are They Predictive of Sexual Dimorphism?

We investigated the mechanisms of sexual selection operating on body size in the one‐sided livebearer (Jenynsia multidentata), a small fish characterized by male dwarfism. Mating in the one‐sided livebearer is coercive: males approach females from behind and try to thrust their copulatory organ at the female genital pore. Females counter males' mating attempts by either swimming away or attacking them. We tested the hypothesis that the components of sexual selection favouring small size in males (sexual coercion) were more effective than those favouring a large size (male competition and mate choice). When alone, small males had a significantly higher success in their mating attempts than large males. The proportion of successful attempts was also positively correlated with female size. When two males competed for the same female, the large male had a significant mating advantage over the small one. With a 1 : 1 sex ratio, the large‐male mating advantage vanished because each male tended to follow a different female. Large males, however, preferentially defended large females, thus compelling small males to engage with smaller, less fecund females. Males did not discriminate between gravid and non‐gravid females, but preferred mating with larger females. This preference disappeared when males were much smaller than the female, probably in relation to the risk for the male of being eaten or injured by the female. In a choice chamber, male‐deprived females that had their sperm storage depleted remained close to males and showed a preference for large individuals, a behaviour not observed in non‐deprived females. Nonetheless, when placed with males in the same aquarium, all females showed avoidance and aggression. Struggling may represent a way by which the female assesses the skill and endurance of males.     

Scent Counter-marking by Male Meadow Voles: Females Prefer the Top-scent Male

Scent counter-marking, in which one individual deposits scent in close proximity to the scent of another individual, is a widespread but poorly understood aspect of olfactory communication. Recent work with golden hamsters suggests that animals may have specially evolved mechanisms for determining which individual has marked most recently, and this work emphasizes the need for studies with other species. In Experiment 1 it was shown for the first time that male meadow voles, Microtus pennsylvanicus, scent mark with urine and anogenital scents and probably also counter-mark with these scents. Female meadow voles, after investigation of an area marked by two males, preferred the whole-body odours of the male that had marked the arena most recently (Experiment 2). After females investigated a male's home cage that had just been marked by another male, they again preferred the whole-body odours of the male that had marked in the cage most recently (Experiment 3). These results demonstrate that female voles, like male hamsters, can distinguish the top or most recent individual's scent from the bottom or older scent in places marked by two males, and further indicate that female voles may prefer the individual that deposited the top scent. Taken together, the results suggest that counter-marking by male voles may be a type of competitive advertising and that females may base mate-choice decisions on information from the pattern of such counter-marks.     

Effect of prenatal stress on the hypothalamo-hypophyseal-adrenal system activity and fat metabolism in the male water vole Arvicola terrestris

The HPA axis function and the fat metabolism were studied in adult male water voles born to intact mothers and mothers deprived of food on the 15th and 18th days of their pregnancy. The HPA response to emotional stress was relatively low in experimental males in winter. The hormonal response to a 24-hrs food deprivation diminished in experimental group only in February. The blood level of free fatty acids was increased in experimental group as compared to the control one. The short maternal food deprivation modified adaptive abilities of their male progeny.     

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.