Hibernation effects on memory in European ground squirrels (Spermophilus citellus).

Effects of hibernation on memory were tested in European ground squirrels (Spermophilus citellus). The animals were trained in summer to successfully accomplish two tasks: a spatial memory task in a maze and an operant task on a feeding machine. One group hibernated normally, and the other was prevented from hibernation by maintaining ambient temperature at 22 degrees C. In spring, the same tasks were repeated for both groups and their individual performances compared to the initial training phase. The experimental groups differed significantly in both tasks. The nonhibernating animals had higher levels of retention and needed significantly fewer trials to relearn the tasks than the group that had hibernated. In addition to testing the retention of conditioned tasks, social memory was also studied. The ground squirrels were given a social recognition test in spring with one familiar and one unfamiliar conspecific. In contrast to the conditioned tasks, social memory did not seem to be affected by hibernation. The results indicate negative effects of hibernation on the retention of conditioned tasks, which could produce important constraints on animals. A potential explanation for this memory loss might be changes in neuronal activity, which occur during hibernation.     

Behavioural development of conspecific odour preferences in bank voles,Clethrionomys glareolus

Biological odours of conspecifics are known to have strong influences on behavioural interaction in bank voles Clethrionomys glareolus. This experiment tested two hypotheses. (1) Olfactory cues from familiar and unfamiliar mature opposite-sex conspecifics differ in their attractiveness to males and females, and their behavioural reactions change with age. (2) A genetically based mechanism is involved in female recognition of kin.In a two-choice preference test, prepubertal males and females were more attracted to familiar than to unfamiliar odours of opposite-sex conspecifics, as manifested by more time spent sniffing familiar voles. As the young reached sexual maturity they shifted their odour preferences. Mature males and females preferred the novel odour of unrelated opposite-sex conspecifics to that of relatives. The results of experiments testing the second hypothesis indicate that females use a genetically based mechanism to recognise their kin. Young and mature females were able to recognise the odour of their biological but socially unknown fathers, and showed the same pattern of behaviour as females in previous experiments.The possible biological functions of kin recognition in bank voles are discussed.     

Kin recognition and the 'armpit effect': evidence of self-referent phenotype matching

In species with multiple paternity or maternity, animals may best assess their relatedness to unfamiliar conspecifics by comparing their own phenotype(s) with those of unidentified individuals. Yet whether animals can recognize kin through self-matching is controversial. Because golden hamsters (Mesocricetus auratus) mate multiply and can produce multiply sired litters, they were tested for their ability to use self-matching for kin recognition. Hamsters that were reared only with non-kin since birth responded differentially to odours of unfamiliar relatives and non-relatives. Postnatal association with kin was not necessary for this discrimination. Prenatal learning was unlikely because of delayed production and perception of social odours. To our knowledge, this is the first demonstration that a vertebrate can use its own phenotype for kin-recognition purposes without prior experience with kin. By using itself as a referent, rather than its siblings or parents, a golden hamster may be better able to direct nepotism towards the most appropriate individuals. Kin discrimination via self-inspection may be especially important in nepotistic contexts (to identify most closely related conspecifics), whereas inclusion of the phenotypes of close kin as referents may be favoured in mate-choice contexts (to identify all related individuals).     

Social Interaction is Necessary for Discrimination between and Memory for Odours of Close Relatives in Golden Hamsters

The role of social experience in recognition of individuals and their odours is not well understood. In a previous study, hamsters discriminated between the odours of their familiar litter mates, but they did not discriminate between the odours of two males or two females from a different litter that were unfamiliar to them. In this paper the role of social experience in discrimination between odours of male litter mates is examined using habituation techniques. Males, tested 1.5–2 mo after separation from their litter mates, discriminated between the flank gland odours of their foster brothers, but they did not discriminate between flank odours from their unfamiliar brothers that had been reared by another mother (Expt. 1). In Expt. 2, adult males did not discriminate between the flank gland odours of two males from a different litter after a week of exposure across a barrier to their sights, sounds, and odours, but subjects did discriminate between the odours of these same males after five brief encounters with them. A month after the encounters, however, subjects no longer discriminated between these odours. In contrast, adult males discriminated between the flank odours of their brothers 9 mo after separation from them (Expt. 3). These results suggest that hamsters must have direct interactions with closely related individuals to discriminate between their odours because the odours of close kin are so similar. Experience with nest mates results in long-lasting memories for their odours.     

Preferences of newborn mice for odours indicating closer genetic relatedness: is experience necessary?

Evidence from studies with adult rodents indicates that individual recognition enables distinctions between familiar individuals irrespective of relatedness (but including close kin) and a separate mechanism enables discriminations based on genetic relatedness without prior familiarity. For example, adult mice could assess the extent of their genetic relatedness to unfamiliar individuals using perceptual similarities between their individual odours. The ontogeny of this genetic relatedness assessment mechanism, however, had not been investigated. Here, in two-choice tests, newborn mice differentially preferred odours of more genetically similar lactating females (paternal aunts to unrelated conspecific and conspecific to heterospecific) even without prior direct exposure to adults with the tested genotypes. The results provide a direct demonstration of genetic relatedness assessment abilities in newborns and show that experience with parental odours is not necessary for genetic relatedness distinctions. Future studies will be necessary to determine whether exposure to odours of other foetuses in the womb or littermates shortly after birth affects this genetic relatedness assessment process.     

Kin recognition by tadpoles and froglets of the wood frog Rana sylvatica

Summary We investigated kin recognition by the wood frog Rana sylvatica in blind laboratory experiments using spatial proximity as a recognition assay. Tadpoles were tested for the ability to discriminate between: 1) familiar full-sibs and unfamiliar non-kin, 2) unfamiliar paternal half-sibs and unfamiliar non-kin, and 3) familiar and unfamiliar full-sibs. Tadpoles discriminated full- and paternal half-sibs from unrelated conspecifics, but did not discriminate between familiar and unfamiliar full-sibs. Froglets from the same laboratory population were tested for the ability to discriminate between 1) familiar full-sibs and unfamiliar non-kin, and 2) unfamiliar paternal half-sibs and unfamiliar non-kin. Froglets preferentially associated with full- and half-sibs over unrelated conspecifics. Our results show that familiarity, i.e., prior association, is not necessary for kin recognition in tadpoles and froglets. The ability of tadpoles and froglets to recognize unfamiliar paternal half-sibs demonstrates that a common maternal factor is not necessary for kin recognition, and indicates that the recognition cue has a genetic component. Our results add to the increasing evidence that a variety of vertebrate and invertebrate animals have the ability to recognize unfamiliar kin by using genetically specified recognition cues.     

Size-Dependent Chemosensory Responses to Familiar and Unfamiliar Conspecific Faecal Pellets by the Iberian Rock-Lizard, Lacerta monticola

We conducted a field study to analyse the social relationships between males of the Iberian rock lizard (Lacerta monticola). The degree of familiarity was determined based on the degree of overlap between their home ranges. We then designed a laboratory experiment to test whether the same males were able to discriminate between familiar and unfamiliar conspecifics using faecal pellet odours. Differential tongue‐flick rates suggest that large males (snout‐to‐vent length, SVL > 75 mm), at least, may discriminate between odours of familiar and unfamiliar males. The behavioural responses were dependent on relative differences in body size between the responding male and the male that donated the faecal pellet. Thus, as responding small males increased in size relative to their corresponding familiar male, their rate of tongue‐flicking significantly decreased; this was not the case in response to unfamiliar males. In contrast, there were no significant correlations between the response of large males to familiar or unfamiliar male stimuli, regardless of size differences. These results suggest that chemical cues contained in faecal pellets allow individual recognition in male L. monticola, and that the response depends on body size. We suggest that faecal pellets might be used to scent‐mark home ranges, which would contribute to lowering the costs of aggressive interactions.     

Interactions between Males of the Lizard Liolaemus tenuis: Roles of Familiarity and Memory

For territorial organisms, recognition of familiar individuals can reduce the frequency and intensity of aggressive encounters (‘dear enemy’ phenomenon), stabilize social systems, and reduce the cost of territory maintenance. Here, we investigated the behavioural events displayed during contests between familiar and unfamiliar individuals in the lizard Liolaemus tenuis (Liolaemidae), a species in which males are territorial. The behaviours recorded were attack, warning, evasion, and submission, and the latencies to the first aggressive (attack or warning) behaviour. Additionally, we assessed the ability of individuals to remember a familiar conspecific after a period without social interaction. Individual males reduced and delayed aggressive behaviour directed towards socially familiar individuals compared with unfamiliar ones. These results suggest that males distinguished between familiar and unfamiliar conspecific males and are in agreement with the ‘dear enemy’ phenomenon. Other behaviours were similar in the contests between familiar and unfamiliar individuals. Recognition of familiar conspecifics was lost after 20 d without social interactions. This may be relevant for interactions with floater males or with neighbours that lose their territory and subsequently attempt to fight for their ex‐neighbour's territory.     

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.     

Selection of odorants for memory tests on the basis of familiarity,perceived complexity,pleasantness, similarity and identification

In a procedure for the selection of two equivalent sets of familiar and two equivalent sets of unfamiliar odours for use in odour memory studies, 24 na?ve subjects were first asked to rate the familiarity, perceived complexity and pleasantness of 54 a priori unfamiliar odours and 57 a priori familiar odours and to identify the latter. After selection of the 40 most familiar and the 40 least familiar odours, the subjects sorted each of these two sets into groups of similar odours. Their results were analysed by multidimensional scaling and cluster analysis and each set was divided into two recognition sets that had the same degree of similarity between target and distractor odours and that had similar values of familiarity, pleasantness, perceived complexity (familiar and unfamiliar sets) and identifiability (familiar sets). Finally, recognition tasks were performed in order to check the equivalence in memory performance of both the two familiar and the two unfamiliar recognition sets.     

Kin discrimination in sticklebacks is mediated by social learning rather than innate recognition

Theory predicts several advantages for animals to recognize kin. These include inbreeding avoidance and an increase in inclusive fitness. In shoaling species, kin recognition may lead to an increased amount of altruism among shoal members. Adult, non‐reproductive three‐spined sticklebacks, Gasterosteus aculeatus, prefer to shoal with kin. This preference was shown for familiar as well as for unfamiliar individuals. However, whether it is based on learned cues of familiar individuals or on innate mechanisms like self‐referent phenotype matching or ‘true’ kin recognition through recognition alleles remains unknown. In our experiments, juvenile fish were given the choice between shoals that differed in relatedness and familiarity. The number of testfish who joined each group indicated that sticklebacks prefer to shoal with familiar kin when the alternative shoal was composed of unfamiliar non‐kin. When one shoal consisted of familiar kin while the second consisted of familiar non‐kin testfish did not show any preference. Kin recognition in sticklebacks is thus most likely mediated by social learning.     

Kin-recognition abilities and nepotism as a function of sociality

Despite widespread interest in kin selection and nepotism, relatively little is known about the perceptual abilities of animals to recognize their relatives. Here I show that a highly nepotistic species, Belding's ground squirrels (Spermophilus beldingi), produces odours from at least two sources that correlate with relatedness ('kin labels'), and that ground squirrels can use these odours to make accurate discriminations among never before encountered ('unfamiliar') kin. Recognition odours appear to vary linearly with relatedness, rather than in an all-or-none fashion, allowing precise estimates of kinship even among distant relatives. Thus S. beldingi are able to recognize their distant kin and male kin, even though they do not treat them preferentially. I also show that a closely related species (S. lateralis) similarly produces kin labels and discriminates among kin, although it shows no evidence of kin-directed behaviour. Thus, contrary to a commonly held assumption, kin favouritism and recognition abilities can evolve independently, depending on variation in the costs and benefits of nepotism for a given species.     

Discrimination of family‐specific odours by juvenile coho salmon: roles of learning and odour concentration*

Free‐swimming coho salmon fry Oncorhynchus kisutch of some families showed preference (relative to the behaviour of naïve sibs) for the odours of similarly aged non‐sibs to whom they had been exposed during the post‐hatch (alevin) stage and the early free‐swimming (fry) stage, but not the embryo (egg) stage, indicating that odour‐learning had occurred during the later developmental periods. Recognition (i.e. preference) of sib‐ pecific odours was evident after a month, and in one case 5 months, of separation from those odours. Thus, young salmon incubating in their gravel nests in streams appear to have the capacity to learn the chemical characteristics of conspecifics and retain this memory for at least several months without reinforcement. However, in addition to the general attractiveness of sibs and familiar non‐sibs over unfamiliar non‐sibs, some non‐sibs were consistently more attractive than others. Preference between two different non‐sib odours could be reversed by changing their relative concentrations, indicating that relative attractiveness is a function of both familiarity and odour concentration. Therefore, although juvenile coho salmon learn, remember, and are subsequently attracted by sib‐specific odours in early life, familiar odours are not always preferred over unfamiliar conspecific odours. Preference in dyadic assays is therefore an insensitive measure of recognition.     

Intraspecific differences in the pattern of hibernation in the ground squirrelSpermophilus beldingi

Summary Intraspecific differences in the patterns of heterothermy were found in captive Belding's ground squirrels that hibernated undisturbed at ambient temperatures of 5°C, 10°C, and 15°C. The timing of all entrances into and arousals from hibernation was determined from records of copper-constantan thermocouples that were mounted on the floor of each animal's nest box and connected to continuously recording potentiometers. In the absence of food, large adult males terminated hibernation spontaneously in the spring. In contrast, females and small non-breeding males (yearlings) did not stop hibernating but instead they shortened their bouts of torpor in the spring so that they aroused every three or four days. This interval of frequent arousals, termed the emergence period, lastel until the squirrels became emaciated, and it was only in the 2 or 3 weeks preceeding death (starvation period) that arousal frequency once again decreased towards midwinter values (Fig. 3). These animals terminated hibernation when fed during the emergence or starvation periods, but they were able to resume torpor if that feeding lasted less than a week.Termination of hibernation and reproductive development in males were related to the size of the animals, not their age. Males two years and older which did not deposit normal quantities of fat were like yearlings in that they had open-ended hibernation seasons and showed little testicular enlargement. Likewise, juvenile males that grew to near adult size in their first summer spontaneously terminated hibernation and had well developed testes like most older individuals. In addition, both the frequency and duration of arousals in the emergence period were related, in part, to the extent of the animals' fat reserves, such that large squirrels spent more time at high body temperatures than small individuals (Figs. 5, 6). This trend was most pronounced at high ambient temperatures.These intraspecific differences in hibernation physiology are consistent with the sex and agerelated differences in the timing of emergence above ground in nature. The increase in the time spent euthermic in the spring isinterpreted as an adaptation for increasing the opportunities for environmental assessment. The intraspecific differences in the extent of this euthermia appear to be associated with differences in the balance between the energy supplies available to an animal and its need to accelerate the use of that energy (i.e., arouse) in order to achieve an early and accurately-time emergence from the hibernaculum.     

Kin recognition by larval wood frogs (Rana sylvatica): effects of diet and prior exposure to conspecifics

Summary We investigated kin recognition by larval wood frogs (Rana sylvatica) in blind laboratory experiments using spatial affinity as a recognition assay. Tadpoles reared with full-sibs displayed a significant preference for familiar full-sibs over unfamiliar non-kin, but failed to discriminate between unfamiliar full-sibs and unfamiliar paternal half-sibs. Tadpoles reared in social isolation (with or without maternal egg jelly) from the two-celled embryonic stage displayed a significant preference for unfamiliar full-sibs over unfamiliar non-kin. Tadpoles reared on a meat diet with their full-sibs: 1) exhibited a significant preference for unfamiliar full-sibs fed meat over unfamiliar non-kin fed meat, 2) failed to discriminate between unfamiliar full-sibs fed lettuce and unfamiliar non-kin fed meat, 3) exhibited a significant preference for unfamiliar non-kin fed meat over unfamiliar non-lin fed lettuce, 4) failed to discriminate between unfamiliar full-sibs fed meat and unfamiliar full-sibs fed lettuce, and 5) displayed a significant spatial preference for odors associated with meat (a familiar food) over odors associated with lettuce (an unfamiliar food). Our results, together with those of Cornell et al. (1989), indicate that the recognition cue of larval R. sylvatica has both genetic and environmental (dietary) components. Our findings establish that previous exposure to maternal egg jelly, kin, or conspecifics is not necessary for the development of kin recognition ability in larval R. sylvatica. Our results are more consistent with the self-learning of recognition cues (a form of phenotype matching) than with a recognition mechanism that involves a genetically fixed recognition template. Finally, our results indicate that increasing similarity between the recognition template and perceived cue does not necessarily result in increasing spatial affinity for kin.     

Fine‐scale kin recognition in the absence of social familiarity in the Siberian jay,a monogamous bird species

Kin recognition is a critical element to kin cooperation, and in vertebrates, it is primarily based on associative learning. Recognition of socially unfamiliar kin occurs rarely, and it is reported only in vertebrate species where promiscuity prevents recognition of first‐order relatives. However, it is unknown whether the recognition of socially unfamiliar kin can evolve in monogamous species. Here, we investigate whether genetic relatedness modulates aggression among group members in Siberian jays (Perisoreus infaustus). This bird species is genetically and socially monogamous and lives in groups that are formed through the retention of offspring beyond independence, and the immigration of socially unfamiliar nonbreeders. Observations on feeders showed that genetic relatedness modulated aggression of breeders towards immigrants in a graded manner, in that they chased most intensely the immigrant group members that were genetically the least related. However, cross‐fostering experiments showed that breeders were equally tolerant towards their own and cross‐fostered young swapped as nestlings. Thus, breeders seem to use different mechanisms to recognize socially unfamiliar individuals and own offspring. As Siberian jays show a high degree of nepotism during foraging and predator encounters, inclusive fitness benefits may play a role for the evolution of fine‐scale kin recognition. More generally, our results suggest that fine‐graded kin recognition can evolve independently of social familiarity, highlighting the evolutionary importance of kin recognition for social species.     

Direct Familiarity Does Not Alter Mating Preference for Sisters in Male Pelvicachromis taeniatus (Cichlidae)

In social species, individuals who grew up together are usually relatives. Therefore, direct familiarity is normally a reliable kin recognition mechanism that is used in many species to discriminate kin from non‐kin. It has been shown in animals and in humans that familiar individuals are rejected as mating partners in order to circumvent potential costs of inbreeding. Here, we tested whether direct familiarity also leads to inbreeding avoidance behaviour in male Pelvicachromis taeniatus, a small socially monogamous cichlid with biparental brood care. In mate choice experiments, reproductively active males were given the choice between familiar sisters and unfamiliar, unrelated females. In a previous study, both sexes of P. taeniatus had preferred unfamiliar full‐sibs over unfamiliar unrelated individuals as mating partners. Here, we show that direct familiarity does not alter the male preference for closely related females. This result is in accordance with theoretical predictions, that inbreeding can be advantageous under certain conditions, and confirms previous findings, that active inbreeding is an adaptive strategy in P. taeniatus.     

基于交叉抚育的雄性根田鼠对异性同胞尿气味的识别

通过交叉抚育建立室内繁殖种群,在断奶后（80日龄）分别取这些供体的新鲜尿气味作刺激物,在行为观察箱中观察和记录雄性根田鼠对雌鼠气味的行为反应,以研究根田鼠同胞识别的化学通讯机制。结果表明：①在不同的发育时期（2～70日龄）,雄性同巢同胞与异巢同胞的体重没有显著差异。②雄性根田鼠对雌性同巢非同胞气味的接近潜伏期显著长于对异巢非同胞的接近潜伏期（P〈0．05）,其对异巢非同胞气味的访问时间和嗅舔时间都显著高于同巢非同胞气味（P〈0．05）。③雄性根田鼠对雌性异巢同胞和异巢非同胞气味的不存在明显偏好。其对两者的接近潜伏期、访问频次、访问时间、嗅舔频次和嗅舔时间等行为响应均无显著差异（P〈0．05）。这些结果表明,80日龄时,雄性根田鼠能够识别熟悉和陌生的无亲属关系雌性尿气味,但不能区分陌生的亲属和非亲属,因此,其异性同胞识别的机制为共生熟悉模式。     

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.     

Influence of energy stores on activation of reproductive function in male golden-mantled ground squirrels

Summary Male golden-mantled ground squirrels were captured in the field in late summer and placed on either unlimited or restricted (80% normal) food rations in the laboratory until each animal began to hibernate. At entrance into hibernation mean body mass was 274.5 g for the unlimited group and 224.5 g for the restricted group. Only six of 21 males subsequently underwent reproductive maturation during winter. Each of these six received the unlimited ration prior to hibernation, and these six included the five heaviest animals in the experiment. In addition to activating their reproductive systems, these heavier squirrels began hibernation later and ended hibernation earlier than the lighter squirrels. Squirrels that remained reproductively quiescent averaged 25.5% body mass as fat in early spring and thus were not severely limited in energy stores during winter.In another experiment a group of 13 male and female squirrels were housed together in a common outdoor enclosure in order to examine the possible relationship between reproductive condition and social standing of males. Although there appeared to be a social hierarchy among males, each male fattened substantially in fall and became reproductively active during winter.These results suggest that the level of energy stores accumulated as fat prior to hibernation in fall affects the potential of male ground squirrels to breed in spring. This dependence of reproductive development on energy stores may reflect the high energetic costs associated with breeding in males when they emerge from hibernation in spring when food availability is low.