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 strategies of New World primates

This paper reviews recent findings on scent-marking behavior in wild New World primates. These findings are used to examine three functional hypotheses: territoriality, regulation of social and reproductive dominance, and mating competition/mate attraction. Available data provide little evidence for a territorial function of scent-marking behavior in New World primates. Evidence for a function in the regulation of social and reproductive dominance is ambiguous. The patterns of scent marking found so far (i.e., rates of scent marking according to sex and social or reproductive status, and the spatial distribution of scent marks), and the sparse information on responses to scent marks are consistent with a hypothesized function in intrasexual competition and intersexual mate choice. Suggestions for future research are made.     

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.     

The role of scent marking in the social communication of wild golden lion tamarins, Leontopithecus rosalia

The role of scent marking in the social communication of mammals is widely variable. One reason for this variation is that the function of scent marking may vary with different ecological and social conditions. The purpose of this study was to test four nonexclusive hypotheses explaining the role of scent-marking frequency in different ecological and social contexts for wild golden lion tamarins. Relative to ecological contexts, we compared scent-marking frequency during seasons of abundant and scarce food resources. Relative to social contexts, we compared scent-marking frequency when groups were isolated and when groups were in the presence of neighbouring groups. We found that the tamarins used scent marking to mark the location of food resources. Additionally, males used scent marking to communicate intrasexual dominance within their groups, while females did not. Our results also indicate that alpha females increased their scent-marking frequency to communicate to members of other groups, while the presence of members of other groups did not elicit a similar response by alpha males. We did not find evidence for a territorial function of scent marking in golden lion tamarins. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

Scent marking in sifaka: no one function explains it all

Various hypotheses to explain possible functions of scent-marking have been put forth and basically fall into five categories: territorial demarcation, ownership of resources, mate attraction, noncombative fighting, and self-advertisement. Verreaux's sifaka (Propithecus verreauxi verreauxi), like many prosimians, use scent-marking as one form of communication. The goal of this study was to determine the function of scent-marking in sifaka. All-occurrence of scent-marks, scent-mark context, and scent-mark style were collected on 23 sifaka in the Kirindy Forest of western Madagascar for 7 months (September 2001-March 2002). Scent-mark rates were collected using continuous focal animal sampling from November 2000-March 2002. Home range data were collected using monthly censuses and instantaneous focal sampling throughout the 17 months. Scent-marking behavior was exhibited almost exclusively by adults. Scent-mark rates were not related to the number of resident adult males, number of resident adult females, rank, or group size. The majority of scent-marks occurred in the perimeter of the home range; however, less than a quarter of the home range was used by only a single group. Sifaka did not preferentially mark food trees, mark during the mating season, or mark during intergroup encounters. The results from this study indicate that none of the five hypothesized functions best explains all scent-marking in Verreaux's sifaka. Rather, scent-marking may serve different functions for different individuals.     

'Nasty neighbours' rather than 'dear enemies' in a social carnivore

Territorial animals typically respond less aggressively to neighbours than to strangers. This 'dear enemy effect' has been explained by differing familiarity or by different threat levels posed by neighbours and strangers. In most species, both the familiarity and the threat-level hypotheses predict a stronger response to strangers than to neighbours. In contrast, the threat-level hypothesis predicts a stronger response to neighbours than to strangers in species with intense competition between neighbours and with residents outnumbering strangers, as commonly found in social mammals such as the banded mongoose (Mungos mungo). The familiarity hypothesis predicts reduced aggression towards neighbours also in these species. We exposed free-living banded mongoose groups to translocated scent marks of neighbouring groups and strangers. Groups vocalized more and inspected more samples in response to olfactory cues of the neighbours than to the strangers. Our results support the threat-level hypothesis and contradict the familiarity hypothesis. We suggest that increased aggression towards neighbours is more common in social species with intense competition between neighbours, as opposed to reduced aggression towards neighbours typical for most solitary species.     

Sex differences in scent marking in Propithecus edwardsi of Ranomafana National Park, Madagascar

In this study we compared the scent-marking rates of females with those of males. Specifically, we examined the ability of season, dominance status, and natal status to explain the frequency of scent marking in female sifakas living wild in Ranomafana National Park, Madagascar, and compared the results with those published for males [Pochron et al., American Journal of Primatology, in press]. We also sought to determine whether vulnerability to infanticide affects marking frequency in adults of either sex, and whether female reproductive status affects female marking behavior. We found that males marked at twice the rate of females, and like males, females in single-female groups marked at the highest rates. Dominant females and non-natal females marked at higher rates than did subordinate females and natal females, a pattern also seen in males. This suggests that scent marks may convey important information about status. Neither females nor males varied their marking frequency with the presence of vulnerable infants. Females did not alter marking frequency with reproductive state, and like males, they marked at higher rates in the period prior to the mating season than they did in the mating season itself. This implies that females may use scent marks more for intrasexual aggression or territoriality than for mate attraction.     

Scent marking by common volesMicrotus arvalis in the presence of a same-sex neighbour

Several vole species use scent marked runways radiating from their burrows for foraging and dispersion. These marks are probably used for social communication. This 4-day laboratory study investigated the environmental and social causations of marking inside pre-existing corridors in male and female common volesMicrotus arvalis (Pallas, 1778). Firstly I tested the novelty and the reinforcement hypotheses in isolated voles, predicting respectively a habituation or a continuous increase in mark deposition. I then confronted with each other two same-sex voles for two days to investigate the differences between males and females in the pattern of marks inside three corridors, one of which runs along the common partition with the neighbour. I tested the self-advertisement and territorial-defence hypotheses, respectively predicting in the presence of a neighbour either a similar marking between the three corridors or a greater marking in the corridor close to the neighbour than in the two other corridors. The results showed no habituation in marking, even in a familiar environment, confirming the reinforcement hypothesis. After the addition of a neighbour, only the females left more marks in the corridor that ran alongside the common border than in the two other corridors. The territorial-defence hypothesis was thus confirmed in (territorial) females while the self-advertisement was supported in (non-territorial) males. Finally, I tested the competitive-ability hypothesis in females, stating that the abundance of scent marks of an individual before a social interaction can predict its degree of intolerance in a future social interaction. The results from female pairs physically interacting for four days support the hypothesis.     

Sex differences in scent‐marking in sifaka: Mating conflict or male services?

Male and female interests can either be in conflict or serve as a basis for exchange. Communication is thus an important aspect of intersexual relationships. Verreaux's sifaka (Propithecus verreauxi verreauxi), like many prosimians, uses chemical signals as one form of communication. The goals of this study were to determine 1) if males and females exhibit sex differences in their scent-marking behavior, and 2) if scent-marking is an example of mating conflict or cooperation. All occurrences of scent-marks, scent-mark context, and scent-mark style were collected on 23 sifaka in the Kirindy Forest of western Madagascar for 7 months (September 2001-March 2002). Scent-mark rates were collected using continuous focal animal sampling from November 2000-March 2002. Home-range data were collected using monthly censuses and instantaneous focal sampling throughout those 17 months. The pressures of behavioral ecology seem to have shaped scent-marking in sifaka: the sexes exhibited significantly different scent-marking behavior. Results from this study are consistent with the hypotheses that 1) females scent-mark to advertise their presence and mark their resources, 2) clean-chested males use scent-marks as between-group communication to advertise their presence, and 3) stained-chested males use scent-marks as a form of olfactory mate-guarding. Scent-marking does not appear to be a "service" that males provide to females, because overmarking limits female communication rather than adding to the overall number of scent-marks. Scent-marking behavior is a crucial aspect of the mating conflict and for understanding intersexual relationships in sifaka.     

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.     

The effect of pair bonding in Cabrera vole’s scent marking

The Cabrera vole (Microtus cabrerae) is a rare rodent living in patchy grassy areas of the Iberian Peninsula where unpaired individuals of both sexes use scent marking primarily to increase their mate-finding likelihood. Cabrera voles establish long-term pair bonds with opposite-sex conspecifics constituting a breeding pair, which is expected to reduce the efforts in searching for a new mate. Under such circumstances, scent marking as a strategy to increase mate-finding likelihood became useless. Accordingly, we hypothesise that pair bonded Cabrera voles suppress mate-finding scent marking to reduce energetic costs and predation risk. To test this hypothesis, we compared scent-marking behaviour towards a clean substrate, in both paired and non-paired voles. No differences were found in the scent marks’ type and the amount of marks placed by voles in both conditions. We also analysed the scent-marking behaviour of both sex pair bonded voles when exposed simultaneously to a clean substrate, a substrate pre-marked by males and a substrate pre-marked by females. We found no significant differences in scent-marks (urine-marked area and number of faecal boli) across the three types of substrate types. In accordance with our prediction, these results suggest that pair bonded Cabrera voles did not use scent marking for mate finding, thus providing further support to the existence of a monogamous mating strategy. Furthermore, our results fail to support the use of scent marking for territorial defence purposes.     

Roles of Different Types of Excretions in Mediated Communication by Scent Marks of the Common Palm Civet, Paradoxurus hermaphroditus Pallas, 1777 (Mammalia, Carnivora)

We studied scent-marking behavior, olfactory response to various excretions (secretion of the perineal gland, urine, and feces), as well as the information content of these excretions in the common palm civet (Paradoxurus hermaphroditus Pallas, 1777). Six forms of scent-marking behavior have been described. The activity and proportion of forms of such behavior differ in males and females. Dragging the perineal gland and leaving the secretion on the substrate was most commonly observed in the animals of both sexes. The olfactory response of the palm civet varied in duration and depended both on animal sex and excretion type. The palm civet could distinguish animal species, sex, and familiar/unfamiliar individuals by the odor of the perineal gland secretion. Differences in the olfactory response of the palm civet to feces was observed only if they belonged to different species. The scent marks of the perineal gland were most significant in mediated communication by scent marks of the palm civet; they completely replicated the information of the urine marks.     

Scent marking within and between groups of wild banded mongooses

Scent marking is commonly described as a territorial behaviour, and scent marks might deter potential intruders from entering occupied areas. Conspecific neighbours present both a reproductive and a territorial threat, thus, determining which, if any, of these threats shapes scent-marking behaviour is difficult. Banded mongooses Mungos mungo provide a rare clear separation between reproductive rivals (found within groups) and territorial rivals (neighbouring groups), because immigration into social groups is extremely rare, and mating occurs almost exclusively within groups. This situation offers an opportunity to assess the relative importance of territorial defence and intra-group competition for mates in shaping scent-marking behaviour. We combined detailed behavioural observations of scent marking, chemical analyses of scent composition and discrimination experiments in the field, and found little evidence for higher rates of scent marking in overlapping areas, a lack of group specificity of scents and a failure of individuals to discriminate between the scents of different groups. Although scent may fulfill some role in territorial demarcation and defence, these results suggest that scent marks and scent-marking patterns are also involved in communicating within social groups.     

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.     

Sex and age-specific differences in ultraviolet reflectance of scent marks of bank voles (Clethrionomys glareolus)

Scent markings of voles are visible via their ultraviolet reflection. Kestrels, and possibly other diurnal raptors, may use this property when hunting. We performed a laboratory study on bank voles to determine whether UV-reflectance of scent marks differs in relation to sex, age and social status. When reflectance spectra of scent marks were measured with a spectroradiometer, we found UV reflectance to be strongest in mature males. There were no differences between mature females and immature juveniles, nor between sexes in juveniles or mature and immature individuals in females. Moreover, we did not find any difference in UV reflectance between dominant and subordinate mature males. The results of this study support earlier findings that UV sensitive predators may use UV reflectance of scent marks as a prey cue. Consequently, studies on differing vulnerability of voles to avian predators should take into account not only their space use and behaviour but also the UV reflectance of their scent marks. Accepted: 21 August 1999     

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.     

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 .     

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.     

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.     

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.