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.     

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.     

The Equivocal Relationship Between Territoriality and Scent Marking in Wild Saddleback Tamarins (<Emphasis Type="Italic">Saguinus fuscicollis</Emphasis>)

Researchers have often assumed that scent marking serves a territorial function in callitrichines, although some controversy exists. To fulfill such a function, scent marks should 1) prevent intrusions, 2) ensure access to feeding resources, 3) enable avoidance of intergroup encounters, or 4) play an important role in the aggressive encounters between groups. We studied 13 saddleback tamarins (Saguinus fuscicollis) belonging to 3 free-ranging groups, which formed mixed-species troops with moustached tamarins (S. mystax) in the Amazonian rain forest of Peru. None of the predictions were confirmed. The tamarins used a border-marking strategy, marking more on the periphery of their territory. However, feeding trees in overlap and encounter areas received more scent marking but were still visited by neighboring groups. Intergroup encounters occurred more often than expected, and scent-marking frequency was not higher during them than when no other group was present. It appears that instead of defending a territory in the classic sense, the tamarins are optimizing signal transmission by depositing their scents where the probability of detection by neighbors is higher. Saddleback tamarins may use shared areas of their home ranges to exchange information with neighboring groups, perhaps regarding reproductive opportunities.     

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 and intrasexual competition in a cooperative carnivore with low reproductive skew

Most mammals scent-mark and a variety of hypotheses have been put forward to explain this behaviour. Differences in the main function of scent-marking between species are likely to be related to differences in social systems. Here, we investigate the functions of scent-marking in a cooperatively breeding carnivore. In the banded mongoose ( Mungos mungo ), individuals of both sexes commonly breed in their natal group and reproductive skew within groups is low. Using experimental scent-mark presentations, we tested predictions of the intrasexual competition, self-advertisement to potential mates and dominance assertion hypotheses. Both males and females responded more intensely to scent marks of same-sexed than of opposite-sexed individuals. Dominant individuals counter-marked more than subordinate ones and males showed higher counter-marking rates than females, but only marginally so. During oestrus, responses to scent marks were increased by both sexes. Our findings strongly indicate that scent-marking in the banded mongoose primarily serves a purpose in intrasexual competition both between and within groups. Unlike in other social herpestids and some solitary rodents, we found little evidence for self-advertisement. We suggest that the peculiar social system of the banded mongoose results in self-advertisement losing importance in this species, shifting the main function of scent-marking to intrasexual competition.     

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.     

Cheetah behaviour at scent-marking sites indicates differential use by sex and social rank

Scent-marking is an important form of communication for solitary species, as the information remains for the receiver after the sender has left the area. Individuals of different demographic or dominance classes (ranks) need to provide different information to conspecifics. Therefore, the use of scent-marking sites is of particular value for solitary species, but their functional role may vary between demographic classes. Using camera traps, we video-recorded the behaviour of cheetahs at scent-marking sites, assessing how individuals of different sex and social rank use the sites for different roles. We tested hypotheses that these sites are for territorial marking, reproductive signalling and information gathering. We found that females visit the sites infrequently, apparently to signal oestrous events, while males visit the sites frequently for territorial marking and information gathering. Among males, dominant individuals scent-marked the most and reacted to female visitation by vocalizing. In contrast, subordinate males, although also visiting the sites, were not recorded scent-marking nor vocalizing. These differences in the functional use of scent-marking sites among sex and social rank support the hypotheses that cheetah s use these scent-marking sites for both territorial and reproductive signalling, as well as to gather information.     

Scent‐Marking Behaviour in a Pack of Free‐Ranging Domestic Dogs

Most mammals scent‐mark, and a variety of hypotheses have been put forward to explain this behaviour. Most of our knowledge about scent marking in domestic dogs comes from studies carried out on laboratory or companion dogs, while few studies have been carried out on free‐ranging dogs. Here, we explored the functional significance of different scent‐marking behavioural patterns in a pack of free‐ranging domestic dogs by testing two non‐exclusive hypotheses: the indirect territorial defence and the dominance/threat hypotheses. Through direct observation, we recorded the locations of dog scent marks (urination, defecation and ground scratching) and information regarding the identity and posture of the marking animal. We found evidence that markings are used by dogs to form a ‘property line’ and to threaten rivals during agonistic conflicts. Both males and females utilized scent marking to assert dominance and probably to relocate food or maintain possession over it. Raised‐leg urination and ground scratching probably play a role in olfactory and visual communication in both males and females. Urinations released by females, especially through flexed‐leg posture, may also convey information about their reproductive state. Finally, our observations suggest that defecation does not play an essential role in olfactory communication among free‐ranging dogs and that standing and squat postures are associated with normal excretion. Our results suggest that many of the proposed functions of marking behaviours are not mutually exclusive, and all should be explored through detailed field and laboratory studies.     

Interspecific variation of scent-marking behaviour in wild tamarins, Saguinus mystax and Saguinus fuscicollis.

The scent-marking behaviour of sympatric moustached, Saguinus mystax, and saddle-back tamarins, Saguinus fuscicollis, was compared in order to explore interspecific differences and potential sources of variation. The author examined basic patterns of scent marking (types, intensity, complexity), substrate use (type, orientation, height), and social patterning of scent marking in three groups of S. mystax and one group of S. fuscicollis at the Estación Biológica Quebrada Blanco, Peruvian Amazonia. S. mystax and S. fuscicollis differed significantly in the relative frequency of different types, and in the intensity and complexity of scent marking. Only S. fuscicollis showed allomarking. They also differed significantly in the type, orientation and height of substrates used for scent marking which corresponded to general differences in substrate use. In S. fuscicollis, but very rarely in S. mystax, two or more group members marked the same site sequentially or simultaneously. 'Collective scent marking', i.e. simultaneous scent marking by most or all group members, occurred only in S. fuscicollis. Since both tamarin species live sympatrically in mixed-species groups, ecological factors are unlikely to account for the differences found in scent-marking behaviour (except for differences in substrate use). They probably relate to as yet unknown differences in social and reproductive strategies of the two species.     

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.     

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.     

Spatial patterns of scent marking in wild moustached tamarins, Saguinus mystax: no evidence for a territorial function

I investigated whether scent marking has a territorial function in wild moustached tamarins. I examined the spatial distribution of scent marking within the home ranges of four groups of this neotropical primate and tested predictions from Gorman & Mills' (1984, Journal of Zoology,202, 535-547) model for border and 'hinterland' marking. Although home ranges were economically defensible, no evidence was found for increased marking along the territorial boundary or in areas of home range overlap, but there was also no evidence for hinterland marking. Observed distributions of scent marking in exclusively used and overlapping areas of the home range did not deviate from distributions that would be expected if scent marking occurred at random (expectation based both on size of area and on frequency of quadrat occupation), and there was a strong correlation between frequency of quadrat occupation and frequency of scent marking per quadrat. These results indicate that scent marking has no territorial function in moustached tamarins. This is in line with mainly qualitative findings from the majority of other studies on wild marmosets and tamarins. These and other findings on scent marking in moustached tamarins suggest that this behaviour functions mainly in intersexual communication. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

Olfactory demarcation of territorial but not home range boundaries by Lemur catta

Over 350 h of observations were collected using focal animal sampling of scent-marking behavior by 2 troops of ring-tailed lemurs (Lemur catta) in the field in Madagascar. Although they did not mark any branch species preferentially, they did have preferred marking sites. Significantly more scent marks were deposited in the area of home range overlap between troops than in the area of exclusive use. However, few marks were deposited at the periphery of the area of overlap. Instead, the majority of the marks were in a narrow band within the area of overlap that coincided with the positions of intertroop confrontations. Female genital marks and male arm marks, as well as the accompanying male shoulder rubs thus appear to demarcate territorial borders.     

Red foxes (Vulpes vulpes) use rabbit (Oryctolagus cuniculus) scent marks as territorial marking sites

One of the functions of chemical communication is territorial signalling. To achieve this, animals should mark their territories in a manner that increases the detectability of the marks, thereby maximising the probability that other animals detect the scent marks. In this study, we focused on the scent-marking behaviour of red foxes in relation to the abundance of their main prey, the European rabbit, in a suburban forest in Madrid, Spain. Our results reveal that foxes scent-marked more and increased the detectability of their marks in areas of higher rabbit density. It would appear that foxes defend food resources from competitors by increasing the number and the detectability of their scent marks.     

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 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.     

Optimal patterns of scent marks in klipspringer (Oreotragus oreotragus) territories

The distribution of preorbital gland scent marks and dung middens within three territories of wild klipspringers in Zimbabwe are described. Nearest-neighbour analyses revealed that scent marks were distributed non-randomly and in a rough ring some distance within the territory boundary. Marking densities were greatest at about half the territory radius. In two territories, marking densities were shown to be sensitive to intrusion pressure at the periphery, being higher along contested boundaries than where territories were not contiguous. Marks were placed on branches facing neighbouring territories, where they are more likely to be detected, along contested boundaries but not in other areas. An analytical model is developed which tests the efficacy of scent-marking strategies along the continuum between extreme hinterland and extreme perimeter marking. This shows that the optimal position for a ring of scent marks is at 0.78 of the territory radius and is the product of a trade-off between maximizing the probability of mark detection by intruders and minimizing the cost of intrusion.     

Scent marking in mammals

This paper reviews experimental and field studies on scent marking behaviour. The occurrence and effects of scent marking are considered in particular, and a number of areas for further research are made apparent. Marking behaviour in mammals is often stated to be ‘territorial’ or, more specifically, to play a role in territorial defence. In fact there is a shortage of evidence to support this view; many of the relevant observations are anecdotal or interpreted with preconceived notions of function in mind. While marking is clearly associated with aggressive behaviour in many species and may therefore be related in some way to territorial behaviour, its role in aggression is not understood. Moreover, there is evidence to support a number of other theories of function some of which are unrelated to territory. It seems that, as with any other mode of communication, scent marking has become adapted for use in a variety of contexts. It probably has more than one function in any one species and different functions in different species.     

The predation risks of interspecific eavesdropping: weasel–vole interactions

Competing species benefit from eavesdropping on each other's signals by learning about shared resources or predators. But conspicuous signals are also open to exploitation by eavesdropping predators and should also pose a threat to other sympatric prey species. In western Finland, sibling voles Microtus rossiameridionalis and field voles M. agrestis compete for food and space, and both species rely upon scent marks for intraspecific communication. Both vole species are prey to a range of terrestrial scent hunting predators such as least weasels, however, the competitively superior sibling voles are taken preferentially. We tested in large out‐door enclosures whether field voles eavesdrop on the signals of its competitor, and whether they behave as though this eavesdropping carries a risk of predation. We presented field voles with scent marks from unknown conspecifics and sibling voles and measured their visitation, activity and scent marking behaviours at these scents under high (weasel present) and low (weasel absent) predation risk. Field voles readily visited both field and sibling vole scents under both high and low predation risk; however their activity at sibling vole scent marks declined significantly under increased predation risk. In contrast, predation risk did not affect field voles’ activity at conspecific scents. Thus, field voles were compelled to maintain eavesdropping on heterospecific scents under an increased risk of predation, however they compensated for this additional risk by reducing their activity at these risky scents. Scent marking rates declined significantly under high predation risk. Our results therefore reveal a hidden complexity in the use of social signals within multi‐species assemblages that is clearly sensitive to the potential for increased predation risk. The predation risks of interspecific eavesdropping demonstrated here represents a significant generalisation of the concept of associational susceptibility.