SCENT-MARKING, DOMINANCE AND FLEHMEN BEHAVIOR IN DOMESTIC RABBITS IN AN ARTIFICIAL LABORATORY TERRITORY

The olfactory exploratory and scent-marking behavior of domesticrabbits were observed in an artificial laboratory enclosure.The rabbits tended to mark certain objects more frequently thanothers with their chin gland secretion (chinning), apparentlyguided by visual characteristics; however, they preferred tosniff and chin objects which had been chinned previously overthose that had never been chinned. They chinned more frequentlywhen faecal pellets were present. Dominant male rabbits chinnedobjects more frequently, and subordinate male rabbits less frequently,in a freshly marked environment than in a clean one; similarlydominant males chinned more frequently and subordinates lessfrequently when urine from another rabbit was present. Rabbitspreferentially chinned urine and faecal pellets from other rabbitsover their own. The dominance relations of the rabbits were determined by analyzingthe behavior patterns correlated with chasing and fleeing. Oneof the most characteristic features of encounters between tworabbits was a complete sexual display. Long periods of sniffing of certain substances, usually urine,by the rabbits were analyzed and found to be basically similarto sniffing and flehmen patterns shown by cats. The data supportthe hypothesis that the whole flehmen pattern including lickingand headshaking is involved with transporting substances insolution to the vomeronasal organ. ^* Present Address: Laboratory of Neurophysiology, UCLA MentalRetardation Center, Los Angeles, California 90024. ^** Present address: Laboratory of Animal Physiology, Kruislaan320, Amsterdam, The Netherlands.     

The age of olfactory cues functioning in chemocommunication among male domestic cats

In a simulated open-field situation we tried to obtain information about the ability of tomcats to distinguish between urine marks of differing ages. Reactions to these marks were sniffing, sniffing intensively and “Flehmen”. The variables we chose to demonstrate a possible discriminatory ability between urine marks of different ages were: (1) latency, i.e. the time that elapses between the cat's release in the observation arena and the finding of a urine mark, (2) the number of occurrences of Flehmen after sniffing, (3) the frequency of sniffing and Flehmen, (4) the duration of the first sniffing bout and (5) the occurrence of a return to the same scent source during an observation.Our most striking observation was that fresh urine marks (maximum age, 4 hours) were explored first, before marks more than one day old; the other variables did not differ dramatically although we observed a general decline in the intensity of the reaction with increasing age of the urine marks.We also found that the visual characteristics of a urine mark play an important role, particularly in the occurrence of returns. Furthermore we found that the reactions of sniffing and Flehmen are linked with an attempt to identify the donor.All results, including the possible influence upon marking behaviour of the presence or absence of fresh marks, are discussed in the light of the use of a “time plan” spacing mechanism by the domestic tomcat as had been suggested in earlier literature.     

Seasonal changes of reproductive behavior and fecal steroid concentrations in Père David's deer.

From July 1997 to September 1997 and from March 1998 to July 1998, we studied reproductive behaviors of Père David's deer in Dafeng, China. During the field behavioral observations, we collected fresh voided fecal samples from the Père David's stags and hinds periodically and kept those samples under -20 degrees C until laboratory analysis. We analyzed the fecal testosterone, estradiol, and progesterone concentrations in those samples using radioimmunoassay. During this study, we also recorded 17 types of male reproductive behaviors and nine types of female reproductive behaviors. Reproductive behaviors and the fecal steroid concentrations showed overt seasonal fluctuations. There were statistically significant correlations between some male reproductive behaviors, such as anogenital sniffing, urine sniffing, urine spraying, wallowing, bellowing, antler adorning, Antler swags mud, chasing, herding hinds, chin resting, mounting and copulating, with the fecal testosterone concentrations. These results suggested that seasonal reproductive behaviors in stags are strongly associated with circulating testosterone. We also found that some female reproductive behaviors fluctuate corresponding with changes in fecal estrogen concentrations. Although there was no direct evidence to confirm the correlations between female reproductive behaviors and fecal estrogen in our experiment, we could not rule out that reproductive activities of hinds were largely related to ovarian estrogen secretion, and estrogen is necessary for inducing female reproductive behaviors.     

Seasonal Changes of Reproductive Behavior and Fecal Steroid Concentrations in Père David's Deer

From July 1997 to September 1997 and from March 1998 to July 1998, we studied reproductive behaviors of Père David's deer in Dafeng, China. During the field behavioral observations, we collected fresh voided fecal samples from the Père David's stags and hinds periodically and kept those samples under −20°C until laboratory analysis. We analyzed the fecal testosterone, estradiol, and progesterone concentrations in those samples using radioimmunoassay. During this study, we also recorded 17 types of male reproductive behaviors and nine types of female reproductive behaviors. Reproductive behaviors and the fecal steroid concentrations showed overt seasonal fluctuations. There were statistically significant correlations between some male reproductive behaviors, such as anogenital sniffing, urine sniffing, urine spraying, wallowing, bellowing, antler adorning, Antler swags mud, chasing, herding hinds, chin resting, mounting and copulating, with the fecal testosterone concentrations. These results suggested that seasonal reproductive behaviors in stags are strongly associated with circulating testosterone. We also found that some female reproductive behaviors fluctuate corresponding with changes in fecal estrogen concentrations. Although there was no direct evidence to confirm the correlations between female reproductive behaviors and fecal estrogen in our experiment, we could not rule out that reproductive activities of hinds were largely related to ovarian estrogen secretion, and estrogen is necessary for inducing female reproductive behaviors.     

根田鼠气味识别的性二型

以新鲜尿和粪作气味源,在行为选择箱中观察根田鼠的行为识别模式,结果表明：雌鼠对陌生同性尿、粪气味源行为识别的差异不显,雄鼠对陌生同性尿、粪气味源的行为识别在多个指标上存在显差异;根田鼠对陌生异性尿、粪的行为响应模式无明显差异;除嗅舔时间外,雌、雄鼠对粪气味的行为识别在其他指标上不存在明显差异;比较雌、雄鼠对尿刺激的行为识别发现,雄鼠对尿刺激的访问频次和反标记显大于雌鼠,雌性嗅舔时间显大于雄性,其他方面二之间并无显差异。因此,雌、雄性根田鼠对粪气味的行为识别模式不存在性别差异;对尿气味的行为识别模式存在性别差异。     

Individual Odours in Two Chromosomal Species of Blind,Subterranean Mole Rat (Spalax ehrenbergi): Conspecific and Cross-species Discrimination

Mole rats from two chromosomal species (2n = 58 and 2n = 60) of the Spalax ehrenbergi superspecies of Israel were tested to determine whether they were able to discriminate differences in the odour of urine from same-sex individuals of their own and of the other chromosomal species. An habituation-discrimination apparatus was designed for use with these solitary and blind subterranean rodents. Animals habituated to the odour of urine from one individual presented for 10 min at a centre sniffing area in the roof of a 50 cm long Perspex tunnel. The odour of urine from the original donor and from a second individual were presented at two other sniffing areas in the tunnel roof during a 5 min discrimination phase. Significant differences in the time spent investigating the two odours demonstrated successful discrimination between them. The results indicate that male and female mole rats of both species can discriminate between the individual-specific odour cues in urine from pairs of conspecifics and pairs of heterospecific mole rats.     

An olfactory recognition system in the ferret Mustela furo L. (Carnivora: Mustelidae)

This study demonstrates that ferrets can use variations in odours from anal sac secretions as a communication system. Odour preference tests showed that ferrets can discriminate between male and female ferret anal sac odours, between strange and familiar, familiar and their own, and fresh and 1-day-old odours. They did not discriminate between fresh and 2-h-old odours, nor did male ferrets discriminate between the odours of oestrous and anoestrous females. Ferrets were more attracted to the odours of the opposite sex than to those of their own sex. When faced by an opponent, male ferrets were more aggressive in the presence of their own rather than their opponent's odour, and less aggressive with their opponent's odour than with that of a known, dominant animal's odour. These results are consistent with both a sex attraction role and a territorial defence role for anal sac odours. A scent-matching mechanism for territorial defence is supported, although a neighbour-neighbour recognition/avoidance mechanism cannot be rejected. Gas chromatography revealed sexually and individually distinct profiles of volatile compounds in anal sac extracts, but no consistent seasonal trends. Females had high concentrations of 2,3-dimethylthietane and/or 3,4-dimethyl-1,2-dithiolane. Males usually had high concentrations of indole. 2-Propylthietane was an important constituent in most individuals. These differences in concentration were significant and could provide an olfactory recognition system of sex and individual identity.     

Responses to urine odor in the tufted capuchin (Cebus apella)

When the tufted capuchin urinates, it frequently performs “urine-washing”. Previous studies have proposed several hypotheses about this behavior. This study investigated 1) whether the tufted capuchin can distinguish the urine odor of conspecific individuals from other groups, and 2) whether the capuchins can distiguish conspcific urine odor of from that of other species. When an odor bar that had been prepared in conspecific other group's cage was presented, the response (sniffing, licking, or biting) was significantly greater than that to any other odors, including that of the home group, 5 other species, or a neutral odor. This tendency was stronger in males than in females. and suggests that the tufited capuchin is able to discriminate its home group's urine odor from that of the other groups. This monkey may also discriminate its own species from others by urine odor. The sex difference of the response to the odor bar may be the result of differences in social role between males and females. These results support the idea that the tufted capuchin may use olfaction for social communication.     

Kin recognition in golden hamsters: evidence for kinship odours

Differential treatment of kin and non-kin has been well documented, but much remains unclear about how kin are recognized. If kin are recognized by a phenotype-matching mechanism, there must be a correlation between genetic relatedness and the similarity of cues used for recognition. A habituation technique was used with golden hamsters,Mesocricetus auratus, to investigate the relative similarity of the odour quality of flank gland secretions from siblings and unrelated individuals. Hamsters discriminated between the odours of their own, same-sex siblings but also treated these odours as similar compared to odours of non-siblings (experiment 1). They did not discriminate between the flank gland odours of unfamiliar siblings from another family (experiment 2). They also did not discriminate between the flank gland odours of unfamiliar, paternal half-siblings from another family (experiment 3). These results indicate that subjects perceived odours from genetically similar individuals as similar and provide evidence for kinship odour cues. The discrimination between the flank gland odours of subjects’ own siblings, however, indicates that hamsters learn the subtle differences between the odours of their close kin, probably through experience with siblings in the nest. When only volatile components from flank gland secretions were available to subjects (experiment 4), they again discriminated between the odours of their own siblings, suggesting that the volatile components from the flank gland secretion were sufficient for recognition of individual litter-mates.     

Discrimination of individuals by odor in male Mongolian gerbils, Meriones unguiculatus

The ability to discriminate among individuals plays a fundamental role in the establishment of social relationships in animals. We examined how Mongolian gerbils (Meriones unguiculatus) discriminate among individuals using odor. In the first experiment, the ability of male gerbils to discriminate among five odor sources from different individuals was investigated using a habituation-dishabituation paradigm. After male gerbils had been habituated to a scent from one individual, they were exposed to familiar and unfamiliar scents from different donors simultaneously. Where urine and ventral gland secretions were used, the subjects spent more time investigating novel odors than familiar ones, suggesting that they were able to discriminate individual differences in these odor sources. However, with the scents of feces and saliva, they could detect, but could not discriminate individual differences; with scent from inside the pinnae, they could not even detect. In the second experiment, we tested whether cross-habituation occurred between the scents of urine and ventral gland secretions. A male was exposed repeatedly to urine from one of two familiar donor males during four habituation trials, and was then exposed to the ventral gland secretions from two donors simultaneously. The subject males spent more time investigating scents of ventral gland secretions, but there was no difference in the investigation time between ventral gland scents from the two donors. These results suggest that male gerbils discriminate among individuals using odors from urine and ventral gland secretions and that cross-habituation may not occur between these scents during social-memory formation.     

Chemosensory discrimination of male age by female Psammodromus algirus lizards based on femoral secretions and feces

Chemical communication plays an essential role in several social and reproductive behaviors of many animals. In lizards, the main sources of semiochemicals are femoral or pre‐anal gland secretions and feces. In male lizards Psammodromus algirus, there are age‐related differences in the chemical composition of femoral gland secretions and in the reproductive strategies, with older males defending territories and females, while younger males adopting sneak‐mating strategies. Females flee more often from mating advances of young males than from those of old males, which are more successful in obtaining matings. This suggests that age discrimination of males may be important for females. We tested here whether females showed differential chemosensory responses to chemical cues (femoral gland secretion and feces) of males of two age classes, and whether females use information from substrate scent marks of males of different ages to select where to stay. We found that females elicited more tongue‐flicks to the secretion and feces of old males than to control or secretion and feces of young males. Also, the time spent by females on a scented paper depended on the treatment, suggesting that females tended to spend more time on scent marks made with femoral secretions of old males. Adult females seemed capable to discriminate between young and old males based on chemical cues alone and showed more interest in scents of old males. However, substrate scent marks did not seem to entirely determine site selection by females, suggesting that females might need additional cues to perform the choice. These results can be explained by the different age‐dependent reproductive strategies of males, which can affect differentially to females.     

Discrimination of chemical stimuli in conspecific fecal pellets by a visually adept iguanid lizard,Crotaphytus collaris

Iguanid lizards are known for visual acuity and a diminished vomeronasal organ, which has led to mixed conclusions on whether iguanids use chemical cues. The collared lizard, Crotaphytus collaris, is a territorial iguanid that lives in open rocky habitats. Fecal pellets placed prominently on open rocky perches may provide an ideal mechanism for intraspecific chemical signaling. In order to determine whether collared lizards can discriminate between chemical stimuli found in conspecific fecal pellets, we collected 24 males and 25 females to analyze sex-specific behavioral responses via tongue-flicks and a newly observed behavior for the species, gular pumps, to cotton swabs containing water, cologne, chemical stimuli from conspecific male and female fecal pellets, and the lizard’s own fecal pellet. Both sexes were able to discriminate chemical stimuli from water via at least one behavior. Male collared lizards exhibited greater rates of response (tongue-flick and gular pumps) toward male fecal pellets when compared to the negative water control. Our results also suggest individuals may be able to discriminate between fecal pellets, as indicated by generally greater (but non-significant) counts of male tongue-flick responses to male fecal pellets when compared to their own. Collared lizard chemical discrimination appears to utilize tongue-flick and gular pump behaviors, possibly associated with distinct chemosensory modes (vomerolfaction and olfaction). Based on this study, we suggest that chemical signals may play a greater role in intraspecific communication than previously thought in this highly visual lizard.     

布氏田鼠在不同光周期下对陌生个体尿液和粪便的气味辨别

研究了成年布氏田鼠在10min内,对不同光照周期下（长光照：LD;短光照：SD）陌生雌／雄个体尿液和粪便两种单一个体气味源的气味行为反应,实验发现：所有雌雄被试鼠对LD气味源比SD气味源表现出更多的嗅闻行为。LD和SD被试鼠对同性／异性尿液气味的嗅闻行为没有表现出明显的差别,但LD被试雄鼠对陌生雌鼠粪便的嗅闻频次显多于SD被试雄鼠,从嗅闻行为特征量（嗅闻行为占所有行为的百分比）来看,所有LD和SD被试雌,雄鼠对尿液的嗅 明显多于粪便,除SD粪便气味外,被试鼠对异性气味源的嗅闻明显多于同性,实验结果表明：作为两种个体气味源,尿液和粪便都带有季节性信息,而且是具有性别特性的。异性的个体气味源比同性的个体气味源更具吸引力;长光照动物的个体气味比短光照动物的气味更具吸引力。     

Responses to oral gland scents from different males in Columbian ground squirrels

Acrylic cubes carrying oral gland scents from strange, neighbouring, and resident male Columbian ground squirrels (Spermophilus columbianus), plus a cube with no scent, were presented near the home burrows of squirrels in the field. Adult males and adult females sniffed scented cubes longer than unscented cubes, sniffed cubes with scent from other (strange and neighbouring) males longer than cubes with the resident male's own scent, and sniffed cubes with scent from strange males longer than cubes with scent from neighbouring males. Males also scent-marked the cubes on a number of occasions; differences in the frequency with which the cubes were marked followed the same pattern. It thus appears that adult Columbian ground squirrels can recognize familiar as opposed to unfamiliar males, and may also be able to determine individual identity, through oral gland scent. An ability to distinguish familiar from unfamiliar males by scent could be advantageous in facilitating differential treatment of wandering strange males versus established neighbours.     

Observations of scent-marking and discriminating self from others by a domestic dog (Canis familiaris): tales of displaced yellow snow

Little is known about what stimuli trigger urinating or scent-marking in domestic dogs, Canis familiaris, or their wild relatives. While it is often suggested that the urine of other animals influences urinating and scent-marking patterns in canids, this has not been verified experimentally. To investigate the role of urine in eliciting urinating and marking, in this pilot study I moved urine-saturated snow ('yellow snow') from place-to-place during five winters to compare the responses of an adult male domestic dog, Jethro, to his own and others' urine. Jethro spent less time sniffing his own urine than that of other males or females, and that while his interest in his own urine waned with time it remained relatively constant for other individuals' urine. Jethro infrequently urinated over or sniffed and then immediately urinated over (scent-marked) his own urine. He marked over the urine of other males more frequently than he marked over females' urine. The method used here can be extended to other species for which experimental data are lacking. Though based on one dog, these novel data may further our knowledge of the role of scent-marking in territorial behavior and of sex differences in territory acquisition and maintenance.     

Flehmen: Its occurrence and possible functions in feral goats

Flehmen is a behaviour characterized by an open mouth and the upper lip curled back and up. It is given by feral goats of both sexes. Males give flehmen most often in response to the urine of females, but also to their own urine and to the urine of other males. Females give flehmen and a related behaviour, riech-gähnen, after sniffing their own and unrelated neonates. Flehmen in the feral goat may function in the olfaction of a number of compounds, enabling males to assess oestrus in females and the relative condition of other males, and females to differentiate between their own and unrelated neonates. Two functional classes can be recognized: monitoring processes, involving regular, frequent testing, and discriminatory learning processes, involving relatively rare decision-making. It is emphasized that the relative frequency of flehmen in different contexts may not reflect its biological significance.     

Mice recognize recent urine scent marks by the molecular composition

Male mice mark the territory with urine scent marks that are frequently renewed to maintain the territory ownership. We measured the response of male mice to small spots of urine deposed either 0, 5, 11, 22, 45, 90 min, or 24 h before testing and show that mice loose interest in sniffing scent marks as they become older and older. We asked what scent features tell a mouse how recent a scent mark is, and therefore, we studied the molecule-to-behavior relationship by correlating 6 behavioral variables--the number of sniffing acts, the latency to the first sniff, the number of urine marks, the latency to the first mark, the area of the marks, and the number of fecal pellets-to 2,4-dehydro-exo-brevicomin, linalool, 2-sec-butyl-4,5-dihydrothiazole, 2,4-dimethylphenol, 4-ethylphenol, and 6,10-dimethyl-5,9-undecadien-2-one released from urine spots over the time, identified, and quantified by gas chromatography and mass spectrometry. Canonical correlation between the molecular and the behavioral principal components was strong (R(1) = 0.96, P = 0.026). The principal component based on 2,4-dehydro-exo-brevicomin, linalool, and 2-sec-butyl-4,5-dihydrothiazole correlated negatively with countermarking and positively with the sniffing behavior, suggesting a semantic feature of fresh male mouse urine.     

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.     

Effects of prepubertal ovariectomy on the development of scent glands, scent marking, and aggressive behaviors of female tamarin monkeys (Saguinus fuscicollis)

The effects of prepubertal ovariectomy on scent gland development, scent marking behavior, and on social interactions with strange adult conspecifics were studied in adult females cohabiting with intact males. Eight females were ovariectomized and eight underwent control surgery at 6 months of age. All were returned to their families after surgery and allowed to reach sexual maturity. At 18 months of age, each female was permanently paired with an adult, intact male. When the subjects were 21 months old, the social interactions of all pairs with strange adults were tested in a situation analogous to a territorial encounter. The scent marking activities of the subjects and their mates were studied during “territorial encounters,” in trial-free control situations, and in the presence of novel objects. Ovariectomy prior to puberty retarded the development of the scent gland but did not inhibit it completely. Social interactions with strange conspecifics were also affected. Ovariectomized females showed fewer threat displays than did control females, but there was no significant difference in the amount of injurious aggression both female groups directed at the strangers. Under all testing conditions, ovariectomized females tended to scent mark less frequently with the circumgenital-suprapubic gland than did controls. This difference was statistically significant only under some of the testing conditions. Intact females scent marked more frequently than their males but ovariectomized females did so only under trial-free testing conditions. The sternal scent gland was used very infrequently by all subjects and there was no difference in marking activity between males and females or between ovariectomized and control females.     

Chemical communication in the lacertid lizard Podarcis muralis: the functional significance of testosterone

Chemical signals are essential for intersexual communication in many animals, including lizards. While faeces have been suggested to contain socially relevant chemical stimuli, epidermal gland secretions are generally believed to be the leading source of chemosignals involved in lizard communication. Early research has shown that sex hormones affect epidermal gland activity, with androgens stimulating gland/pore size and/or gland productivity. However, the functional significance of hormone‐induced glandular activity in lizard chemical communication remains unclear. In this study, we manipulated testosterone (T) concentrations in male Podarcis muralis lizards. While T‐supplementation did not change pore size, it did increase secretion production substantially. Chemosensory tests showed that female conspecifics tongue‐flick at a higher rate and more quickly towards the secretion of males with experimentally increased T levels than towards the secretion of control males, suggesting that females can discriminate between males with dissimilar T levels based on chemical cues of secretion alone. Based on the scent of faeces, however, females were unable to discriminate between males with differential T levels. Also, females reacted more quickly when offered larger amounts of secretion – irrespective of whether secretions were obtained from control or T‐increased males. This result indicates that secretion quantity affects chemosignal detectability in Podarcis muralis.