Olfactory preferences, scent marking, and "proceptivity" in female hamsters

Two appetitive sexual behaviors of female hamsters, attraction to odors of males and vaginal scent marking, were investigated and the correlations of each to reproductive states were determined. Both estrous and diestrous females were more attracted to the odors of intact males than to the odors of females or castrated males; this differential attraction was more pronounced for estrous females. Lactating females, but not pregnant females, were also preferentially attracted to odors of intact males. Thus, odors alone provided sufficient information to allow sexual discrimination by females, and estrous, diestrous, and lactating females were preferentially attracted to odors of intact males whereas pregnant females were not. Reproductive condition had no influence on responses to odors of castrated males or diestrous females. Vaginal scent marking was strongly influenced by reproductive state: Marking frequency was low in estrous, pregnant, and early lactation females, but high in late lactation and diestrous females, suggesting a function of advertisement of approaching receptivity. Thus sexual preferences based on olfactory cues and vaginal scent-marking frequency differed in their relationships to reproductive conditions. It is suggested that in other species such relationships between appetitive sexual behaviors and reproductive condition will depend on the species social organization, ecological niche, and taxonomic group, and consequently that the concept of preceptive behaviors should be broadened to include all appetitive sexual behaviors of females, not just those that are correlated with the hormonal state characterizing estrus.     

Peripubertal exposure to male odors influences female puberty and adult expression of male-directed odor preference in mice

Testosterone-dependent olfactory signals emitted by male are well known to accelerate female puberty in mice (Vandenbergh effect). However, it remains unclear whether these chemosignals also influence adult expression of male-directed odor preference. Therefore, we exposed female mice to intact or castrated male bedding (vs clean bedding as control) during the peripubertal period (postnatal day (PD) 21–38) and measured male-directed odor preference in adulthood. At PD45 or PD60, females exposed to intact male odors, and thus showing puberty acceleration, preferred to investigate odors from intact males over females or castrated males. Females exposed to castrated male odors did not show puberty acceleration but preferred male (intact or castrated) over female odors. Finally, control females did not show any odor preference when tested at PD45, although a preference for male odors emerged later (PD60). In a second experiment, females that were exposed to intact male odors after pubertal transition (PD36–53) also preferred intact male over castrated male odors. In conclusion, our results indicate that peripubertal exposure to male odors induced early expression of male-directed odor preference regardless of puberty-accelerating effect and that induction of male-directed odor preference is not specific to the peripubertal period.     

Scent-marking displays provide honest signals of health and infection

Males of many species produce scent marks and other olfactorysignals that function to intimidate rivals and attract females.It has been suggested that scent marks provide an honest, cheat-proofdisplay of an individual's health and condition. Here we reportseveral findings that address this hypothesis in wild-derivedhouse mice (Mus musculus domesticus). (1) We exposed males tofemale odor, which induces an increase in testosterone, andfound that sexual stimulation significantly increased the males'scent-marking and the attractiveness of their scent marks tofemales. (2) We challenged sexually stimulated males with anonreplicating strain of bacteria (Salmonella enterica C5TS)to activate immunity and found that this significantly decreasedthe males' scent-marking and the attractiveness of their scentmarks to females. (3) We collected scent marks from infectedand sham-infected males when they were sexually stimulated ornot, and we found that females could significantly discriminatethe scent marks of infected versus control males, but only whenthe males were sexually stimulated. Taken together, our resultsindicate that male mice modulate their scent-marking displaydepending on their health and perceived mating opportunities.Increased scent marking enhances males' attractiveness to females,scent marks provide an honest indicator of bacterial infection(and perhaps immune activation), and females are able to assessthe health of males more easily when males mark at a high rate.     

Scent marking by voles in response to predation risk: a field-laboratory validation

Predators use scent to locate their prey, and prey animals oftenalter their behavior in response to predation risk. I testedthe hypothesis that voles would decrease their frequency ofscent marking in response to predation risk. I conducted trialsin which prairie voles, Microtus ochrogaster, and woodland voles,M. pinetorum, were allowed to scent mark ceramic tiles placedin their runways in the field. The tiles were subjected to oneof three treatments: scented with odor from mink, Mustela vison(a rodent predator); rabbit, Oryctolagus cuniculus (a nonpredatormammal control); and no odor (control). No significant differenceswere found in the frequency of scent marking in response tothe three treatments for either species. To validate that volesdid not decrease their scent marking in response to predationrisk, I brought male prairie voles from the field site intothe laboratory and allowed them to scent mark white paper substratetreated with mink odor, rabbit odor, or no odor. No significantdifferences were found in the frequency of scent marks in responseto the three treatments. These results differ from what waspredicted based on laboratory studies with other species ofrodents that show avoidance, reproductive suppression, decreasedactivity, and reduced scent marking in response to odors ofpredators. Voles appear to scent mark different substrates andunder a wide variety of social and environmental situations,and this is not influenced by the presence of odor from a predator.     

Scent-marking behaviour by male prairie voles,Microtus ochrogaster,in response to the scent of opposite- and same-sex conspecifics

We conducted an experiment using the prairie vole (Microtus ochrogaster) to test predictions associated with the proposed functions of scent marking as a sexual attractant, in reproductive competition, and as a self-advertisement. We allowed an oestrous female, an anoestrous female, and an adult male to scent mark three portions of a clean substrate and then exposed a second male to this substrate for secondary marking. We did not support a sexual attraction hypothesis in that males did not place more scent marks in response to oestrous than anoestrous females. Similarly, we did not support a reproductive competition hypothesis in that males did not place more scent marks in response to marks of males than to those of females or bare substrate. Males did not overmark the scent of males or females and thus we did not support a scent-masking or scent-blending hypothesis. In that males deposited scent similarly in response to males, females, and on bare substrate, our results suggest that the frequency and placement of scent marks by males function primarily to advertise individual identity in an area.     

Effects of sex hormones and gender on attraction thresholds for volatile anal scent gland odors in ferrets

Body odors contribute to mate recognition and sexual partner preference in many mammals, including ferrets. We used a habituation/dishabituation procedure to test whether sex steroid hormones influence whether ferrets will approach and investigate different concentrations of volatile anal scent gland odors from male and female conspecifics. When tested with high concentrations of anal scent gland secretions in oil vehicle, gonadectomized male and female ferrets that received no sex steroids reliably discriminated anal scents from male and female conspecifics. This discrimination most likely reflects gender recognition rather than individual recognition because gonadectomized, sex steroid-treated ferrets discriminated between anal scents of males and females but not between anal scents of individual males or females. Treatment with either the estrogen receptor agonist, estradiol benzoate (EB), or the androgen receptor agonist, 5-alpha dihydrotestosterone proprionate (DHTP), increased investigation of low concentrations of anal scent by gonadectomized ferrets. These data suggest that ferrets could use anal scent gland secretions in mate recognition and that seasonal increases in circulating sex steroid hormones increase ferrets' responsiveness to low concentrations of these odors.     

Scent-marking by male mice under the risk of predation

The use by predators of scent marks made by potential prey isa largely unexplored potential cost of olfactory signaling.Here we investigate how animals that differ in their investmentin scent-marking respond to simulated predation risk, by comparingthe willingness to approach and counter-mark the scent marksof a competitor in the presence or absence of predator odor.We aimed to test whether animals that invest heavily in scent-marking,and which may thus be more vulnerable to eavesdropping predators,will either (1) take greater risks to counter-mark the competitor'sscent or (2) reduce or abandon scent-marking. Using outbredmale laboratory mice, Mus musculus, we show that, in the absenceof predators, individuals which initially scent-mark at highfrequency (high markers) approach the competitor's scent marksmore quickly and spend more time in counter-marking than thosewhich initially invest relatively little (low markers). Ina sib-sib experimental design, simulated presence of predationrisk (urine of ferrets, Mustela putorius furo) caused bothkinds of individual to approach the competitor's marks moreslowly, but high markers approached more quickly than low markersand spent more time in the vicinity of the competitor's marks.Only high markers significantly reduced their overmarking ofthe competitor's scent. These results suggest (1) that thereis a unique danger inherent to scent-marking at high frequenciesand (2) that high-marking males were prepared to accept increasedcosts of intrasexual competition in order to reduce the riskof predation. Further tests using the scent of naked mole-rats, Heterocephalus glaber, showed that these effects were not elicited simply by an unfamiliar odor. We discuss reasons for the observeddifference in response to predation risk between the groups,and the implications of these results for counter-selectionon scent-marking strategies.     

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 .     

Memorisation des marques olfactives chez la Genette (Genetta genetta L.): durée de reconnaissance par les femelles de marques olfactives de males

Memorization of Scent Marks in Genets (Genetta genetta L.): Duration of Female Memory of Male Scent Marks The aim of this work was to study the memorization of scent marks of known males by females in genets (Genetta genetta L.). An attempt was made to determine how long, after separation from a given male, females could discriminate between his scent marks and those of strange males. Significant differences in sniffing duration at the scent marks were observed nine weeks after separation. These results showed that olfactory cues could permit individual recognition in genets, and that memorizing the scent marks could also act in the regulation of aggressive behaviour in free-living animals.     

Scent wars: the chemobiology of competitive signalling in mice

Many mammals use scent marks to advertise territory ownership, but only recently have we started to understand the complexity of these scent signals and the types of information that they convey. Whilst attention has generally focused on volatile odorants as the main information molecules in scents, studies of the house mouse have now defined a role for a family of proteins termed major urinary proteins (MUPs) which are, of course, involatile. MUPs bind male signalling volatiles and control their release from scent marks. These proteins are also highly polymorphic and the pattern of polymorphic variants provides a stable ownership signal that communicates genome-derived information on the individual identity of the scent owner. Here we review the interaction between the chemical basis of mouse scents and the dynamics of their competitive scent marking behaviour, demonstrating how it is possible to provide reliable signals of the competitive ability and identity of individual males.     

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。     

Temporal and Spatial Distribution of Male Scent Marks in the Polygynous Greater Sac-Winged Bat

Scent marks are relatively long-lived signals that can be perceived by conspecifics when the producer is absent. Therefore, it is often not obvious to whom the signal is directed. In daytime roosts of the polygynous greater sac-winged bat, males scent mark territories with facial gland secretions. Territories are a valuable resource for males, as they offer exclusive courtship opportunities, which results in increased male reproductive success and, consequently, increased male–male competition over territories. The information encoded in male scent marks could, therefore, be either directed at females as part of an olfactory courtship display or at male competitors as part of territorial behaviour. We expected territorial males to scent mark in the morning, shortly before females return to the territory and close to female roosting sites, if scent marks are directed at females as part of the courtship display. And we expected harem males to scent mark at the territory boundaries, where male–male encounters are most likely to occur, if scent marks are directed at male competitors. We found that males marked more frequently in the afternoon, at a time when all females have already left the territory, and harem males marked at the territory boundaries and not inside their territory in the area where females roost. At boundaries males fan volatiles from specialised wing sacs towards competitors outside the territory. Scent marking of male Saccopteryx bilineata might therefore be congruent with the assessment-hypothesis, which states that scent marks offer intruders the possibility to make an olfactory assessment of the territory owner without direct physical interaction. Thus, scent marks of male S. bilineata are most likely influenced by male–male competition and not by female choice.     

Female marmoset monkeys (Callithrix jacchus) can be identified from the chemical composition of their scent marks.

The present study analyzed 42 organic solvent extracts of scent mark pools from five dominant female common marmosets by gas chromatography (GC) and combined GC and mass spectrometry. We determined whether there were qualitative or quantitative differences between the chemical composition of scent marks from individual females. Gas chromatography and mass spectral analysis detected the same 162 chemicals in 86% (36/42) of scent mark pools from five dominant females. This near identical chemical composition of scent marks suggested there were few, if any, qualitative differences between the chemical composition of scent marks from individual females. Instead, quantitative differences in scent may provide the key factor distinguishing individual females. Using the relative concentration of highly volatile chemicals detected by GC in scent marks, linear discriminant analysis classified scent mark pools to their correct donor approximately 91% of the time. Such highly reliable statistical matching of scent to donor suggested that each individual female common marmoset has a unique ratio of highly volatile chemicals in their scent marks which may permit individual identification of females from odors in their scent alone.     

The ownership signature in mouse scent marks is involatile

Male house mice advertise their territory ownership through urinary scent marks and use individual-specific patterns of major urinary proteins (MUPs) to discriminate between their own scent and that of other males. It is not clear whether recognition occurs through discrimination of the non-volatile proteins or protein-ligand complexes (direct model), or by the detection of volatile ligands that are released from MUPs (indirect model). To examine the mechanism underlying individual scent mark signatures, we compared investigatory and countermarking responses of male laboratory mice presented with male scent marks from a strain with a different MUP pattern, when they could contact the scent or when contact was prevented by a porous nitrocellulose sheet to which proteins bind. Mice investigated scent marks from other males whether these were covered or not, and biochemical analysis confirmed that the porous cover did not prevent the release of volatiles from scent marks. Having gained information through investigation, mice increased their own scent marking only if they had direct contact with another male's urine, failing to do this when contact was prevented. Individual signatures in scent marks thus appear to be carried by non-volatile proteins or by non-volatile protein-ligand complexes, rather than by volatiles emanating from the scent.     

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.     

A Comparison of Spontaneous and Odor-induced Chin Marking in Male and Female Domestic Rabbits (Oryctolagus cuniculus domestica)

Chin marking by the European rabbit (Oryctolagus cuniculus) is one of the classic but still little understood examples of mammalian chemical communication. To investigate whether the sexes differ in performance of this behavior, we compared the frequency of spontaneous chinning and chinning in response to the chin marks of conspecifics in 20 intact male and 20 intact female chinchilla-breed rabbits, and in five gonadectomized animals of each sex. Contrary to the expectation of greater chinning activity in males, no significant sex differences were found. Frequencies of spontaneous chinning were similar in the two sexes, large and stable individual differences were observed in both, chinning increased in both when marks from unfamiliar conspecifics were present, and both directed chin marks to objects marked by conspecifics more than to unmarked objects. Individual chinning frequencies correlated positively with urination but not defecation in both sexes, and spontaneous and odor-induced chinning were significantly reduced both in castrated and ovariectomized animals. The findings suggest that chinning is an equally significant part of the communication system of male and female rabbits and that its expression may be regulated by similar olfactory, hormonal, and social mechanisms.     

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.     

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.     

Hormonal regulation of chemosignal-stimulated precopulatory behaviors in male housemice (Mus musculus)

Five experiments examined the hormonal regulation of the precopulatory reproductive behavior of male housemice of two genotypes (DBA/2J inbreds and C57BL/6J X AKR/J hybrids). The two precopulatory behaviors examined were preferences for female urinary odors and ultrasonic courtship vocalizations to anesthetized females. The preferences were then used to make inferences about odor attractiveness. Gonadally intact hybrid males were highly attracted to the airborne urinary odors of female mice but were either indifferent to, or exhibited less attraction to, male urinary odors. Castration decreased male attraction to female odor such that castrated males were equally attracted to male and female odors. Normal levels of attraction could be maintained in castrated hybrid males by Silastic implants of either testosterone or estradiol. While Silastic implants of dihydrotestosterone (DHT) were also effective in maintaining attraction in hybrids, this hormone was ineffective in inbreds. The effectiveness of estradiol, DHT, and testosterone in maintaining attraction following castration was paralleled in castrated hybrids by the effects of these hormones in maintaining courtship vocalizations to females. In contrast to the genotype-specific effects of DHT upon behavior, DHT was effective in both genotypes in maintaining seminal vesicle weight. Estradiol, on the other hand, which was quite effective in maintaining both precopulatory behaviors in hybrids, had little effect upon seminal vesicle weight. Thus these experiments dissociate the behavioral effects of steroids from their effects upon peripheral morphology. We suggest that testosterone can activate precopulatory behaviors following either aromatization or 5-alpha reduction but that genetic variability somehow gives rise to strain differences in DHT responsiveness.     

Social influences on estrogen excretion and ovarian cyclicity in saddle back tamarins (Saguinus fuscicollis)

The effects of different social living conditions on estrogen excretion and on the ovarian cycle of saddle back tamarins were investigated. Urinary estrogens were monitored as indices of ovarian cyclicity in groups of adult females living under the following experimental conditions: (1) five parous females, each living with an adult castrated male (in one of the females plasma estradiol and progesterone were also measured); (2) five adult daughters living with their families. Each daughter was then removed from her family and paired with a vasectomized male. After pairing, scent marks collected from the family were introduced daily to one of the daughters and her mate. Scent exposure was then discontinued and hormone excretion measured for several weeks. The remaining four daughters were not exposed to family scent. The females living with castrated males showed urinary estrogen cycles of an average length of 17.5 ± 1.0 days. The plasma estrogen cycle was of the same length. The females studied under condition 2 showed low, noncycling estrogen levels while living in their families. They responded to pairing with an increase in the level of urinary estrogens, and four out of five showed regular estrogen cyclicity. The fifth female exposed to family scent marks after pairing also showed an increase in urinary estrogens. However, as long as scent transfer was maintained, no cycle was observed. Estrogen excretion increased again, and cyclicity commenced when scent transfer was discontinued. It is concluded that ovarian estrogen production is suppressed and cyclicity does not occur as long as daughters live in their families. Release from suppression and perhaps stimulation by the male cause a rapid increase in estrogen levels and the onset of cyclicity. Chemical stimuli produced by the family, perhaps particularly by the mother, may be involved in reproductive suppression.