A test of the dear enemy phenomenon in the Eurasian beaver

We tested the hypothesis that Eurasian beavers, Castor fiber, display the dear enemy phenomenon; that is, they respond less aggressively to intrusions by their territorial neighbours than to intrusions by nonterritorial floaters (strangers). This ability could be advantageous in facilitating differential treatment of wandering strangers versus established neighbours. Territorial beavers were presented with scent from neighbouring and stranger adult males. Thirty-nine different active beaver families, 18 in 1998 and 21 in 1999, were presented with a two-way choice between two pairs of experimental scent mounds; mounds with castoreum from a neighbour and a stranger, and mounds with anal gland secretion from a neighbour and a stranger. Direct observations of the families during evenings showed that: (1) beavers sniffed both castoreum and anal gland secretion from a stranger significantly longer than from a neighbour, and (2) beavers responded aggressively (stood on the mound on their hind feet, pawing and/or overmarking) significantly longer to castoreum, but not to anal gland secretion, from a stranger than from a neighbour. When experimental scent mounds were allowed to remain overnight and the beavers' responses were measured the following morning, the beavers' responses were significantly stronger to both castoreum and anal gland secretion from a stranger than from a neighbour. These findings indicate that Eurasian beavers can use scent to discriminate between neighbours and strangers, thereby supporting existence of the dear enemy phenomenon in this species. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

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.     

EVOLUTIONARY RELATIONSHIPS AMONG COLONIES OF COLUMBIAN GROUND SQUIRRELS AS SHOWN BY MITOCHONDRIAL DNA

Mitochondrial DNA (mtDNA) from 71 Columbian ground squirrels (Spermophilus columbianus) collected in 12 locations in western Canada were assayed for restriction-site variation with 10 endonucleases. Five of these endonucleases revealed variant patterns, and the composite genotypes were used to develop a linear transformation series among the mtDNA genotypes. Two of the four clones had a wide distribution, while the remaining two clones were geographically restricted. The mtDNA of Columbian ground squirrels was also compared to two other species of Sciuridae: Richardson's ground squirrels (S. richardsonii) and Arctic ground squirrels (S. parryii). Calculation of divergences from fragment length and restriction-site data indicated that Arctic ground squirrels and Richardson's ground squirrels were more closely related to each other than either was to Columbian ground squirrels. The transformation series among clones within the Columbian ground squirrels was rooted using Richardson's and Arctic ground squirrels as out-groups. From these data, we conclude that the colonization by female founders of Columbian ground squirrel populations occurred after deglaciation along the eastern ranges of the Rocky Mountains, while colonies on the western ranges may have been present before extensive deglaciation occurred, having existed in refugia in northwestern Alberta.     

Effect of kinship on social behaviors in Brandt's voles (<Emphasis Type="Italic">Microtus brandti</Emphasis>)

The roles of kinship in agonistic behavior and mate choice were evaluated in Brandt's voles (Microtus brandti). In chambers bedded with familiar or unfamiliar substrates, the aggressive behavior and social investigation towards adult unfamiliar same-sex siblings and non-siblings were examined, and no significant kin bias was found. Males sniffed and followed unfamiliar unrelated females significantly more than unfamiliar sibling sisters, but males did not show significant preferences in copulatory behavior and agonistic behavior. Females spent significantly more time copulating with unfamiliar unrelated males than with their unfamiliar sibling brothers, while they did not show a significant preference in social investigation between them. Our study shows that kinship might play a role in the inbreeding avoidance based on preweaning familiarity or/and phenotype matching, but the role of kinship in agonistic behavior remains unclear.     

Oestrous females investigate the unfamiliar male more than the familiar male in both commensal and non-commensal populations of house mice

We studied female preferences for familiar and unfamiliar males. The subjects were laboratory-born house mice: (1) non-commensal Mus musculus domesticus from the eastern part of Syria along the Euphrates River; and (2) commensal M. m. musculus from the Czech Republic. Pair-choice preference tests have revealed that oestrous females of both populations sniffed towards unfamiliar males more than familiar males. In the case of females exhibiting postpartum oestrus, this preference was less pronounced and statistically not significant. Thus, our mice clearly exhibited the behavioural pattern known from commensal populations of polygynous and/or promiscuous M. m. domesticus. We found no inverse tendency to seek proximity to the familiar male that has been previously reported from closely related and presumably monogamous aboriginal mouse Mus spicilegus. We conclude that neither commensal M. m. musculus, nor non-commensal M. m. domesticus, are likely to share a monogamous mating system with mound-building mice.     

Sex differences in olfactory social recognition memory in meadow voles,Microtus pennsylvanicus

Terrestrial mammals, like rodents, use odors, and scent marks to indicate their presence in an area to conspecifics. These odors convey information about the scent donor's genotype, sex, condition, and age. The ability to discriminate among the scent marks of conspecifics and later recollect the identity of the donor is essential for choosing between familiar and unfamiliar mates. We tested the hypothesis that the promiscuous meadow vole (Microtus pennsylvanicus) can recollect the odor of a familiar, opposite-sex conspecific and distinguish it from that of an unfamiliar, opposite-sex conspecific. We also hypothesized that because reproductive success is highly skewed among male meadow voles and competition for mates is intense, males will be more likely than females to recollect the odor of a familiar, opposite-sex conspecific and distinguish it from that of an unfamiliar, opposite-sex conspecific, for a longer period of time. Using a habituation task, we first exposed the voles, 4 times successively, to the anogenital area scent of an opposite-sex conspecific. Then, 1 hr, 24 hrs, 72 hrs, or 96 hrs after the fourth exposure, voles were presented with the odor of the donor from the exposure phase (familiar donor) and that of an unfamiliar, opposite-sex conspecific. Female meadow voles spent similar amounts of time investigating the scent of the familiar male donor and that of an unfamiliar male donor after the 1-hr and 24-hr intervals. Male meadow voles, however, spent more time with the scent of an unfamiliar female donor than that of the familiar female donor after the 1-hr, 24-hr, and 72-hr intervals, suggesting that male voles could recollect the scent mark of a familiar female for at least three days. The implications of these sex differences in social memory may reflect the different strategies male and female meadow voles use in the recognition of previous and potential mates. Recognition of an individual's scents may enhance fitness by allowing animals to direct appropriate behaviors toward those individuals.     

Hibernating patterns of free-ranging Columbian ground squirrels

Summary The patterns of torpor and euthermy during hibernation was documented for 28 free-ranging Columbian ground squirrels (Spermophilus columbianus) fitted with temperature-sensitive radio transmitter collars. Adult males began hibernation earlier, were euthermic for a greater proportion of the hibernating season and emerged earlier than other age and sex classes. The patterns of hibernation of adult females did not differ significantly from those of juveniles. Emergence from the hibernaculum was preceded by a long (3–12 d) euthermic interval in adult males but not in adult females or juveniles. Changes in soil temperature did not appear to initiate emergence. The greater time spent euthermic by adult males is interpreted as a significantly greater energy cost of hibernation for adult males than for other age and sex classes. The benefits offsetting these costs may be increased reproductive potential in spring and avoidance of predation in late summer.     

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.     

Why do river otters scent-mark? An experimental test of several hypotheses

We tested several alternative hypotheses about the function of scent marking by the North American river otter, Lontra canadensis. Otters may mark at latrine sites with spraints (faeces) to (1) signal species identity, (2) advertise their reproductive status, (3) establish and maintain territories, and (4) communicate social status and identity to group members. Olfactory preference tests were conducted at the Alaska Sealife Center in Seward, Alaska, on a group of 15 wild-caught male otters in February 1999. We found that male otters investigated otter scent more than sealion faeces. The male otters also showed a preference for male scent over the scent of anoestrous females. No preference for the scent of unfamiliar males, compared with the scent of familiar males, was observed, and no preference for the scent of close kin was detected. However, an investigation of dominant relationships of the captive otters showed that dominant males spent more time investigating male scent than did subordinate males. Thus, spraints deposited at latrine sites may function to communicate social status of males.     

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.     

Managing anabolic steroids in pre-hibernating Arctic ground squirrels: obtaining their benefits and avoiding their costs

Androgens have benefits, such as promoting muscle growth, but also significant costs, including suppression of immune function. In many species, these trade-offs in androgen action are reflected in regulated androgen production, which is typically highest only in reproductive males. However, all non-reproductive Arctic ground squirrels, irrespective of age and sex, have high levels of androgens prior to hibernating at sub-zero temperatures. Androgens appear to be required to make muscle in summer, which, together with lipid, is then catabolized during overwinter. By contrast, most hibernating mammals catabolize only lipid. We tested the hypothesis that androgen action is selectively enhanced in Arctic ground squirrel muscle because of an upregulation of androgen receptors (ARs). Using Western blot analysis, we found that Arctic ground squirrels have AR in skeletal muscle more than four times that of Columbian ground squirrels, a related southern species that overwinters at approximately 0°C and has low pre-hibernation androgen levels. By contrast, AR in lymph nodes was equivalent in both species. Brain AR was also modestly but significantly increased in Arctic ground squirrel relative to Columbian ground squirrel. These results are consistent with the hypothesis that tissue-specific AR regulation prior to hibernation provides a mechanism whereby Arctic ground squirrels obtain the life-history benefits and mitigate the costs associated with high androgen production.     

Age-dependent use of local and global landmarks during escape: experiments using Columbian ground squirrels

How animals utilize their space often changes during ontogeny, perhaps resulting from alternative use of orientation mechanisms. This study investigated whether landmark-based navigation mechanisms were age-dependent in Columbian ground squirrels (Spermophilus columbianus). In field tests, young (1-2 years old) and adult (3-6 years old) animals had to find an escape burrow when either local, global, or both types of landmarks were obstructed. The comparison of escape times between age groups revealed that adult squirrels found escape burrow faster than young animals if global landmarks were available. However, if only local landmarks were present, young squirrels outperformed older animals. The comparison of escape time within each age group showed that obstruction of global or local landmarks lengthened escape time of adult squirrels. In contrast, young animals had longer escapes only when local landmarks were obstructed. The results suggested that the use of different types of landmarks was age specific.     

Rival recognition in the territorial tawny dragon (Ctenophorus decresii)

The ability to discriminate between familiar and unfamiliar conspecifics is important in territorial animals as it allows animals to distinguish neighbours from non-neighbours. This prevents wasting time and energy in unnecessary aggressive interactions. I investigated the ability of adult males of a territorial lizard, the tawny dragon (Ctenophorus decresii), to distinguish familiar from unfamiliar rivals in a laboratory setting. Males significantly reduced their aggression levels in repeat interactions with familiar rivals and increased their aggression levels towards unfamiliar males. The time taken for interactions to be settled was also significantly lower towards familiar than unfamiliar males. The results of this study suggest that adult male tawny dragons can discriminate familiar from unfamiliar conspecifics. Furthermore, animals were presented with three new rivals in succession and showed a robust ability to discriminate between familiar and unfamiliar males.     

Retention of social recognition after hibernation in Belding's ground squirrels

The retention of social memory during long periods of separation, such as hibernation or migration, has not been well documented, despite evidence for long-term social relationships in migrating species or in long-lived sedentary species. We investigated the ability of captive Belding's ground squirrels, Spermophilus beldingi, to remember previously familiar individuals as well as littermates after 9 months of isolation. Before hibernation, young ground squirrels discriminated between odours of familiar and unfamiliar individuals, as shown by greater investigation of a novel individual's odour. The following spring, these yearlings did not respond differentially to odours of previously familiar and unfamiliar individuals, suggesting that memory for familiar conspecifics was lost during hibernation. In contrast, both female and male yearlings continued to discriminate between odours of littermates and previously familiar nonlittermates. Thus, recognition of close kin was maintained during prolonged social isolation, but recognition of familiar, unrelated individuals was not. If re-establishment of familiarity is not costly or if adults rarely interact with the same individuals in successive years, then selection may not favour retention of individual memories of particular conspecifics over the winter. Even though males rarely encounter kin after dispersal, yearling males did recognize their siblings, suggesting that the relative costs of maintaining kin-recognition abilities year-round may be low. Possible mechanisms underlying the formation and maintenance of individual and kin recognition are discussed. Copyright 2000 The Association for the Study of Animal Behaviour.     

Chemical communication of reproductive status in female cotton-top tamarins (Saguinus oedipusoedipus)

Among Callitrichids, scent secretions have been identified as carrying information regarding species, subspecies, gender, social status, individuality, hormonal status, and timing of ovulation. We propose that information regarding familiarity and reproductive status is also communicated. Seven male–female pairs of cotton-top tamarins (Saguinus oedipus oedipus) were presented with several drops of distilled water, a scent secretion from the female of that pair, scent secretions from unfamiliar, reproductively mature but noncycling females, and scent secretions from unfamiliar, reproductively cycling females. Behavioral responses from both males and females were recorded over a 10 min period. Differences in behavioral response for both males and females were significant across all four conditions. This indicates that cotton-top tamarins are capable of discriminating a familiar scent from an unfamiliar scent as well as the reproductive status of an unfamiliar female. The communication of this information may play an important role in regulating mate selection, reducing reproductive competition, and stabilizing transfers in and out of groups in the wild. Am. J. Primatol. 45:337–349, 1998. © 1998 Wiley-Liss, Inc.     

Olfactory communication and the importance of different odour sources in the ferret (Mustela putorius f. furo)

Olfactory communication has a major role in solitary carnivores, particularly during the breeding season. Scent-marking behaviour in ferret (Mustela putorius f. furo) has been well studied, but not the significance of the deposited odours for the animal. We compared the interest in urogenital, anal and body odours of opposite-sex conspecifics between male and female ferrets and investigated both sexes’ discrimination ability (familiar vs. unfamiliar) for these three opposite-sex odours and the use of its ability by females during the breeding season. Males are more interested than females in the urogenital odour of the opposite sex. Male body odour probably did not interest females and males are somewhat interested in the female one. However, anal odour of the opposite sex is as interesting for males as for females and both sexes are able to discriminate familiar anal odour from an unfamiliar one. Moreover, females could use this ability when they must choose to have some sensory contact between olfactory familiar and unfamiliar males since they prefer to be in contact with the former. These results are coherent with behavioural differences observed between male and female solitary mustelids in the field and in captivity, and the consortship success of resident males compared to roaming males.     

Donning your enemy's cloak: ground squirrels exploit rattlesnake scent to reduce predation risk

Ground squirrels (Spermophilus spp.) have evolved a battery of defences against the rattlesnakes (Crotalus spp.) that have preyed on them for millions of years. The distinctive behavioural reactions by these squirrels to rattlesnakes have recently been shown to include self-application of rattlesnake scent-squirrels apply scent by vigorously licking their fur after chewing on shed rattlesnake skins. Here, we present evidence that this behaviour is a novel antipredator defence founded on exploitation of a foreign scent. We tested three functional hypotheses for snake scent application--antipredator, conspecific deterrence and ectoparasite defence--by examining reactions to rattlesnake scent by rattlesnakes, ground squirrels and ectoparasites (fleas). Rattlesnakes were more attracted to ground squirrel scent than to ground squirrel scent mixed with rattlesnake scent or rattlesnake scent alone. However, ground squirrel behaviour and flea host choice were not affected by rattlesnake scent. Thus, ground squirrels can reduce the risk of rattlesnake predation by applying rattlesnake scent to their bodies, potentially as a form of olfactory camouflage. Opportunistic exploitation of heterospecific scents may be widespread; many species self-apply foreign odours, but few such cases have been demonstrated to serve in antipredator defence.     

Maternal Diet Influences Offspring Feeding Behavior and Fearfulness in the Precocial Chicken

Background

In chicken, oils in the maternal diet confer a specific scent to the yolk. Embryos are known to perceive and memorize chemosensory signals of the surrounding environment; however, the potential impact of the maternal diet has not previously been investigated. In the present study, we hypothesized that chicken embryos memorize the chemical signals of the maternal diet and that this perceptual learning may orient subsequent feeding behavior of the hatchlings.

Methodology/Principal Findings

Laying hens were fed standard food enriched with 2% menhaden oil (MH group) or 2% soybean oil (controls). The scent of menhaden was significantly more detected in MH egg yolks than in control yolks by a human panel. We analyzed the development and behavior of offspring towards different types of food, bearing or not bearing the menhaden scent. When chicks were exposed to a 3-min choice test between the familiar food bearing the menhaden scent and the familiar food without menhaden, no effect of treatment was observed. In a 3-min choice test with unfamiliar food (mashed cereals) MH chicks showed a clear positive orientation toward the unfamiliar food bearing the menhaden scent. By contrast, control chicks showed a preference for the non-odorized unfamiliar food. MH chicks expressed higher emotional reactivity level than control chicks as expressed by food neophobia and longer immobility in a restraint test.

Conclusion/Significance

Chicks exposed in ovo to menhaden oil via the maternal diet preferentially oriented their feeding behavior towards food containing menhaden oil, but only when the food was unfamiliar. We propose that oil in the maternal diet engenders maternal effects and contributes to the development of behavioral phenotype in the offspring. In ovo chemosensory learning may have evolved to prepare precocial offspring for their environment. This suggests a common principle of embryonic chemosensory learning across vertebrate taxa.     

Responses to Femoral Gland Secretions by Visually Adept Male and Female Collared Lizards

Although visually transmitted social signals are well documented in many diurnal iguanians, including collared lizards, secretory femoral glands also suggest a role of chemical signals in intraspecific communication. We conducted laboratory trials to test the extent to which male and female collared lizards responded by tongue‐flicking femoral gland secretions, neutral (water), and odoriferous (cologne) control substances, males distinguished self‐secretions from those produced by unfamiliar rival males, and females distinguish secretions from unfamiliar vs. familiar males. Both males and females spent similar amounts of time in four arena quadrants each with a Petri dish treated with one of the four test compounds. Males gave more tongue flicks/trial to secretions produced by unfamiliar rivals and cologne than they tongue‐flicked their own secretions and water. By contrast, the number of tongue flicks by females on control substances and familiar and unfamiliar males was similar. Results support the hypothesis that femoral gland secretions function in intrasexual signaling among male collared lizards, perhaps allowing them to distinguish unfamiliar rivals. Females tongue‐flicked secretions from familiar and unfamiliar males with similar frequency that was high relative to that of males, suggesting a possible role of secretions in assessment of males. Ours is the first evidence of a signaling role of femoral gland secretions in collared lizards and adds to a growing body of evidence that chemical signaling has evolved in diurnal lizards that also have highly developed visual‐based signaling.     

鳄蜥对熟悉和陌生个体气味的辨别

个体辨别对于减少同种争斗以及配偶选择具有重要意义。我们用棉棒粘取鳄蜥(Shinisaurus crocodilurus)尿液作为气味源,以香水作为对照,测定鳄蜥对熟悉个体气味、陌生个体气味以及香水的舔舌次数和舔舌潜伏期,来探讨鳄蜥通过化学信息辨别熟悉和陌生个体的能力。结果显示,不论是雌性还是雄性,对不同个体尿液的舔舌次数均显著高于对香水的,舔舌潜伏期显著短于香水的;尽管雄性对陌生同性个体气味与熟悉同性个体气味的舔舌次数无显著差异,但对前者的舔舌潜伏期显著短于后者;雄性对陌生雌性气味的舔舌次数显著多于熟悉雌性气味的,对前者的舔舌潜伏期显著短于后者;雌性对陌生雄性气味的舔舌潜伏期显著短于对熟悉雄性气味的;雄鳄蜥对陌生雌性气味的舔舌次数显著多于雌鳄蜥对陌生雄性的。结果表明,鳄蜥能辨别同种个体的化学信息,并能通过化学信息来辨别熟悉和陌生个体,推测鳄蜥的这种辨别能力对其领域分配以及繁殖交配有重要作用。