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.     

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 .     

Variations in scent-marking behaviour of European badgers<Emphasis Type="Italic">Meles meles</Emphasis> in the vicinity of their setts

For European badgersMeles meles (Linnaeus, 1758), the importance of olfactory signals located at home-range borders in the context of territoriality has been widely accepted. Badgers, however, also scent mark far from their borders, often in the vicinity of their communal sett. Little is known about the significance of these marks in intraspecific communication. Here, we investigated the patterns of object-marking with subcaudal gland secretions close to the sett. Using remote-controlled, battery-powered infra-red video equipment, we recorded 442 incidences of object-marking between April 1996 and June 1997. The frequency of object marking varied significantly in relation to season, sex, age and reproductive status. In both sexes, relative object-marking rates were highest during the mating season, when individuals in reproductive condition marked significantly more often than non-reproductive animals. During the cubrearing season females marked at a significantly higher rate than males, and in both sexes adults scent-marked significantly more frequently than younger individuals. Approximately 30% of all scent-marks received an over-mark within 24 h of their deposit. In males over-marking behaviour was recorded only during the mating season, whereas females over-marked in all seasons at equal rates. Overall, our results suggest that in addition to their territorial functions, subcaudal scent-marks also serve as individual-specific advertisement signals directed at other group-members.     

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 age, sex, and reproductive status on scent marking frequencies in the golden lion tamarin, Leontopithecus rosalia

This study reports on the longitudinal changes in scent marking frequencies of male and female lion tamarins in relation to age, reproductive status, and group composition. Juvenile males and females in family groups and subordinate males in trios (2 males, 1 female) scent marked infrequently. Juvenile females scent marked less than juvenile males and began scent marking later. Adult pair-bonded males and females scent marked with similar frequencies. Females showed scent marking increases during mid-pregnancy, but their scent marking decreased both before and again after parturition. Both males and females exhibited decreases in scent marking while transporting dependent infants.     

Scent Marking in Female Prairie Voles: a Test of Alternative Hypotheses

We conducted three experiments with females in different stages of reproductive condition to test alternative hypotheses for the function of scent marking in female prairie voles, Microtus ochrogaster . The three reproductive categories were isolated females prior to sexual stimulation (anoestrous), sexually stimulated (oestrous) and lactating. Females in different reproductive condition were given the opportunity to scent mark clean unmarked substrate or areas that had previously been marked by adult females or adult males. The numbers of scent marks deposited by females did not differ statistically for females in different reproductive condition. However, there was a trend for anoestrous females to mark the most, oestrous females less, and lactating females the least. The lack of scent marking by lactating females might be to reduce conspicuousness to conspecifics or predators. Oestrous females tended to mark the most in the area marked previously by males, although the difference was not statistically significant.
Our results provide some support for a mate-attraction hypothesis and a territorial-defense hypothesis, but were most consistent with a self-advertisement hypothesis. Over marking was uncommon and did not differ by experiment or sex of previous donor. Our results suggest that the number and placement of scent marks by females are highly variable and function primarily to convey individual identity.     

Scent marking as resource defense by female Lemur catta

Because ring-tailed lemurs (Lemur catta) are a female-dominant, female-philopatric species in which the females provide the majority of parental care and troop defense, resource defense is a possible function of female lemur scent marking. To test this hypothesis, I conducted three studies. First, I presented captive, individually housed females with a series of samples of female scent, each from a different female, to determine whether they would respond to those samples and discriminate between them. Second, I reanalyzed data from a focal animal study of four females in two adjacent troops in Berenty Reserve, Madagascar, to determine female marking rates before, during, and after the mating season, and to clarify the relationship among positions of feeding, intertroop defense, and scent marking. The third study was based on ad libitum observations of the sniffing and marking behavior of a troop in Berenty Reserve during a year when they traveled far out of their home range. The females in study 1 investigated female scent samples but provided no evidence that they discriminated between them. In study 2 the wild females marked throughout the study and did not limit their marking to the mating season. They deposited significantly more of their marks in a zone of confrontation with adjacent troops, where they also did the majority of their feeding, and they increased their rate of marking during agonistic intertroop confrontations. The females determined the positions of their scent marks and deposited the first mark in the majority of countermarking sequences. When the females traveled out of their defended range in study 3, they significantly decreased their rate of marking and increased their rate of sniffing spots but not marking them. All evidence gathered so far supports the hypothesis that one function of female ring-tailed lemur scent marking is to provide intergroup information that is then used to reinforce the border of the defended resource.     

A comparison of scent marking between a monogamous and promiscuous species of peromyscus: pair bonded males do not advertise to novel females

Scent marking can provide behavioral and physiological information including territory ownership and mate advertisement. It is unknown how mating status and pair cohabitation influence marking by males from different social systems. We compared the highly territorial and monogamous California mouse (Peromyscus californicus) to the less territorial and promiscuous white-footed mouse (P. leucopus). Single and mated males of both species were assigned to one of the following arenas lined with filter paper: control (unscented arena), male scented (previously scent-marked by a male conspecific), or females present (containing females in small cages). As expected, the territorial P. californicus scent marked and overmarked an unfamiliar male conspecific's scent marks more frequently than P. leucopus. Species differences in responses to novel females were also found based on mating status. The presence of unfamiliar females failed to induce changes in scent marking in pair bonded P. californicus even though virgin males increased marking behavior. Pair bonding appears to reduce male advertisement for novel females. This is in contrast to P. leucopus males that continue to advertise regardless of mating status. Our data suggest that communication through scent-marking can diverge significantly between species based on mating system and that there are physiological mechanisms that can inhibit responsiveness of males to female cues.     

A preliminary study of olfactory behavior of captiveLemur coronatus during the breeding season

The olfactory behavior of a captive population of crowned lemurs (Lemur coronatus)was studied during their annual breeding season in order to investigate its possible role in the fine-tuning of mating synchrony after photoperiodic initiation of reproductive activity. The frequencies of five stereotyped olfactory behavior patterns were recorded in four male-female groups during 315 1-hr observation sessions between October and March. The mean total scent-marking frequency of all males was positively correlated with their mean testicular size. Male anogenital-, head-, and allomarking frequencies decreased during the breeding season, whereas hand-marking frequencies remained constant. Male head-marking increased significantly in the 5 days preceding female vaginal estrus. Furthermore, males responded to many female scents by olfactory investigation and/or overmarking, whereas females never showed an observable behavioral response to male scent marks. The marking frequencies of two females did not change significantly during the breeding season, while those of two others decreased significantly. These results suggest qualitative changes of female scents during estrus and a less important role of male scents in intersexual communication in the context of reproduction than previously thought.     

Patterns of male scent-marking in Propithecus edwardsi of Ranomafana National Park, Madagascar

Scent-marking behavior has been well documented in many primate species. Three common functions attributed to scent-marking in males of multi-male/multi-female lemur species include: 1) advertisement of individual identity, 2) territorial defense, and 3) reproductive suppression. We examined the average number of scent-marks per hour exhibited daily by adult male sifakas (Propithecus edwardsi) and found that patterns of scent-marking changed with season, natal status, and dominance status. Males in single-male groups scent-marked at the highest rate, followed by dominant males, males of equal status, and subordinate males. Non-natal males generally scent-marked at higher rates than natal males, and adult males living in a natal group without a parent marked at higher rates than males living with a parent. All males scent-marked at higher rates in the migration season compared to the other seasons. These patterns were consistent with territorial defense and advertisement to females, and the suggestion that these chemical signals impart information concerning status. Since scent-marking behavior tracked seasons and varied with both dominance and natal status, it may serve multiple functions in males.     

Sociosexual development,pair bond formation,and mechanisms of fertility suppression in female cotton-top tamarins (Saguinus oedipus oedipus)

The effect of various social environments on sociosexual behavior was examined in six young female cotton-top tamarins (Saguinus oedipus oedipus) and in three established breeding females. Behavioral observations and hormonal samples were collected on young females while they were living with their families, when they were isolated from conspecifics, and after they were paired with an unrelated male. While living with the family, all females showed a suppression of fertility and low frequencies of sociosexual behavior. Following removal from the family, isolated females displayed an increase in rate of scent marking and an increase in hormonal levels. When young females were paired with males, they were exposed to scent secretions from their natal families, from an unfamilar family, and from a control for a total of 24 weeks. After pairing, hormonal levels increased dramatically, and ovarian cyclicity began. An increase in sociosexual behavior and elevated levels of scent marking accompanied this physiological change. Newly paired females had higher rates of affiliative behavior and scent marking than did established breeding females. However, both newly paired and established breeding males were more likely to initiate contact, grooming bouts, and social sniffing than were females. Time to first ovulation was later in females who were exposed to scent secretions from their natal families than it was in those females given a control for the first 8 weeks following pairing. No female conceived during exposure to scent secretions. However, once normal ovarian cycling had begun or a pregnancy was established, exposure to scent secretions had no effect. Thus, the social environment influences the fertility, sociosexual behavior, and pair bond formation of cotton-top tamarins. In addition, chemical stimuli found in the scent secretions produced by the natal family are most likely involved in reproductive suppression.     

Reproductive Strategies in Lemur catta: Balance Among Sending,Receiving, and Countermarking Scent Signals

Our goal is to go deep into behavioral olfactory strategies possibly used by ring-tailed lemurs in reproductive competition and to shed some light on the function of female scent marks deposited outside the breeding season. We followed 16 captive adults at the Pistoia Zoo (Tuscany, Italy) for > 1,500 h from May 1997 to March 1999. Male direct and indirect olfactory investigation on females showed complementary distributions, the former peaking during the breeding and the latter during the birth season. Males are thus able to monitor female reproductive conditions throughout the whole year. During the birth season there was an increase of female genital marking. The olfactory advertisement probably guarantees that the extremely brief estrus does not remain unnoticed and allows male intrasexual competition a long period to operate. Male indirect olfactory monitoring and countermarking on female signals peaked during the birth season, which suggests that male intrasexual competition is achieved both by getting female chemical messages and by concealing them from other males. Female countermarking on other female genital marks peaked during the breeding season. High-ranking females had higher frequencies of countermarking than those of low-ranking females, which suggests that the advantage of obliterating scent signals of other females is greater than the disadvantage of revealing one's own reproductive condition.     

Discrimination between males and females by scent in Lemur fulvus.

Two captive male Lemur fulvus were presented with scents of conspecific males and females, outside the mating season. Both subjects sniffed male scents significantly more than female scents. Male and female scents did not elicit significantly different amounts of scent marking. None of the responses of either subject suggested any discrimination of sub-species by scent.     

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.     

Scent marking in a territorial African antelope: II. The economics of marking with faeces

Faeces may be ideal substances for scent marking because they have a minimal energetic cost to the signaller. However, marking with faeces is also constrained by the animal's ability to produce faeces. This study examined whether limits on the volume of faeces produced by oribi Ourebia ourebi, in Serengeti National Park, Tanzania, caused territorial males to regulate their output and prioritize the placement of faecal marks. Territorial males marked with faeces more often, and with a smaller volume per defecation, than did juvenile males and females. Territorial males also defecated only on established dung middens along borders shared with other territorial males or on top of a female's urine and faeces. In contrast, juvenile males and females defecated randomly with regard to their location in territories. Territorial males with larger harems marked with faeces at higher rates and less volume than males with few or no females. This difference suggests that when males overmark female excretions they reduce the amount of faeces available for marking other preferred sites, such as along territory borders shared with other males. Dominant males with adult subordinates marked with faeces less often, and with a greater volume per mark, than males that defended territories without the aid of subordinates. Dominant males also reduced the volume of marks less as the number of females on their territory increased than did males without subordinates. Territories occupied by more than one adult male also were marked with faeces at higher rates, and with marks of greater volume, than territories held by single males. These results suggest that the presence of subordinate males reduced the demand on dominant males to regulate the volume and placement of faecal marks. Overall, these results suggest that territorial male oribi regulate their faecal marking behaviour in response to a limited supply of faeces. Copyright 1999 The Association for the Study of Animal Behaviour.     

Can overmarking be considered as a means of chemical mate guarding in a wild callitrichid?

Mate guarding is a male strategy to monopolize matings and thus to ensure paternity. Since in callitrichids female reproductive status is advertised by scent marks, one may expect mate guarding by chemical means. We addressed this question during an episode of consortship observed in a polyandrous trio of wild saddleback tamarins (Saguinus fuscicollis). During consortship, the consort male was the only one to allomark the female. Scent marking frequency decreased for all individuals, although the consort male marked more than the other male during consortship, while there was no difference in the previous period. During consortship, almost 50% of female scents were overmarked by the consort, and more than 56% of the consort's scent marks were employed to overmark the female's scents. Therefore, the other male had limited access to female scent marks. Mate guarding may thus have a chemical component in tamarins, and olfactory communication may play an important role in mating competition.     

Do cavity‐nesting primates reduce scent marking before retirement to avoid attracting predators to sleeping sites?

The largest population of endangered golden lion tamarins (Leontopithecus rosalia, GLTs) decreased from approximately 330 to 220 individuals between 1995 and 2000 due to a dramatic increase in predation at sleeping sites. We used behavioral data from eight social groups in this population to test two hypotheses: First, if GLTs attempt to mitigate the risk of predation at sleeping sites, they should reduce their rates of scent marking just prior to retirement. Second, if the benefits of scent marking prior to entering the sleeping site merit an increase in the rate of marking, then tamarins should increase their rate of pre-retirement scent marking during the breeding season, when such behavior would have its greatest impact on reproductive fitness. We used a generalized linear model (GLM) repeated-measures analysis to compare rates of daytime scent marking with rates of marking just prior to retirement for males and females. In addition, we compared scent marking prior to retiring in the nonbreeding season to marking rates before retirement in the breeding season for males and both sexes considered concurrently. Contrary to our expectations, GLTs significantly increased their rates of scent marking during the 30 min prior to entering their sleeping site-an observation driven by an increase in male (but not female) rates of marking. Rates of marking before entering the sleeping site were greater in the nonbreeding season compared to the breeding season, when both sexes were considered concomitantly and when males were evaluated alone. We conclude that GLTs do not attempt to minimize predation risk by decreasing scent marking in the period before they enter their sleeping site, and that tamarins do not scent mark at this time of day in order to transmit information about reproductive status or to control reproduction of subordinates. We speculate that scent marking in the 30 min prior to entering sleeping sites may serve to reduce predation risk by enabling tamarin groups to return quickly to favored sleeping sites in the evening when crepuscular predators are active.     

Female prairie voles do not choose males based on their frequency of scent marking

We conducted an experiment to test three alternative hypotheses for the function of frequency of scent marking in male prairie voles, MICROTUS OCHROGASTER: (1) sexual attraction (to advertise male quality for mating); (2) reproductive competition; and (3) self-advertisement or individual identity. In laboratory experiments, males deposited scent on all areas of a bare substrate, and more in an area next to a stimulus animal than other areas, regardless of the stimulus animal's sex. Females did not choose mates based on their frequency of scent marking and scent marking did not antagonize or stimulate aggression between males. The frequency of scent marking by males supports the individual identity hypothesis, and is less consistent with the sexual attraction or reproductive competition hypotheses. Mate choice is likely based on a complex suite of characters, but at least in prairie voles, the frequency of scent marking by males does not appear to be one of them.     

Scent marking in two western Amazonian populations of woolly monkeys (Lagothrix lagotricha)

We describe patterns of scent marking observed in two wild populations of lowland woolly monkeys that were the subjects of long-term studies in the westernmost portion of the Amazon basin. The woolly monkeys engaged primarily in two types of scent marking: chest rubbing and anogenital rubbing. In both study populations, males and females performed both types of scent marking, but males chest-rubbed more commonly than females, while females engaged in more anogenital rubbing. We evaluated two nonexclusive hypotheses for the function of scent marking by woolly monkeys: 1) that scent marking is used in sociosexual contexts, and 2) that scent marking is used to convey information about occupancy of or willingness to defend an area from conspecifics in other social groups. We found no association between the occurrence of scent-marking behavior and location within the home range, but did find that scent marking occurred more commonly than expected on days when copulations, mating solicitations, and intergroup encounters were observed. Additionally, mating activity and chest rubbing were highly correlated across the yearly cycle, even when the potentially confounding variable of ripe fruit availability was controlled for. In woolly monkeys, overt male-male competition is rare and female choice is an important part of the mating system. Our results are most consistent with the idea that scent marking plays a role in advertising male quality or competitive ability, and perhaps in coordinating mating activity.     

Scent marking in a territorial African antelope: I. The maintenance of borders between male oribi

Scent marking is ubiquitous among the dwarf antelope and gazelles of Africa, but its function has been the subject of debate. This study examined preorbital gland scent marking in the oribi, Ourebia ourebi, a territorial African antelope. Several hypotheses for the function of scent marking by territorial antelope were tested with observational data. Of these, the hypotheses that scent marking is driven by intrasexual competition between neighbouring males, and that marks serve as an honest advertisement of a male's ability to defend his territory from rivals, were supported best. Thirty-three territorial male oribi on 23 territories marked most at borders shared with other territorial males, and territorial males marked more often at borders shared with multimale groups than at borders shared with a single male. This suggests that males perceived neighbouring male groups as a greater threat to territory ownership than neighbouring males that defended their territories without the aid of adult subordinates. Marking rate was unrelated to territory size or the number of females on adjacent territories, but males with many male neighbours marked at higher rates than those with fewer male neighbours. These results suggest that the presence of male neighbours has a greater effect on the scent marking behaviour of territorial antelope than has been considered previously. Copyright 1999 The Association for the Study of Animal Behaviour.