Private heat for public warmth: how huddling shapes individual thermogenic responses of rabbit pups

Background

Within their litter, young altricial mammals compete for energy (constraining growth and survival) but cooperate for warmth. The aim of this study was to examine the mechanisms by which huddling in altricial infants influences individual heat production and loss, while providing public warmth. Although considered as a textbook example, it is surprising to note that physiological mechanisms underlying huddling are still not fully characterised.

Methodology/Principal Findings

The brown adipose tissue (BAT) contribution to energy output was assessed as a function of the ability of rabbit (Oryctolagus cuniculus) pups to huddle (placed in groups of 6 and 2, or isolated) and of their thermoregulatory capacities (non-insulated before 5 days old and insulated at ca. 10 days old). BAT contribution of pups exposed to cold was examined by combining techniques of infrared thermography (surface temperature), indirect calorimetry (total energy expenditure, TEE) and telemetry (body temperature). Through local heating, the huddle provided each pup whatever their age with an ambient “public warmth” in the cold, which particularly benefited non-insulated pups. Huddling allowed pups facing a progressive cold challenge to buffer the decreasing ambient temperature by delaying the activation of their thermogenic response, especially when fur-insulated. In this way, huddling permitted pups to effectively shift from a non-insulated to a pseudo-insulated thermal state while continuously allocating energy to growth. The high correlation between TEE and the difference in surface temperatures between BAT and back areas of the body reveals that energy loss for non-shivering thermogenesis is the major factor constraining the amount of energy allocated to growth in non-insulated altricial pups.

Conclusions/Significance

By providing public warmth with minimal individual costs at a stage of life when pups are the most vulnerable, huddling buffers cold challenges and ensures a constant allocation of energy to growth by reducing BAT activation.     

Sex Differences in Thermogenesis Structure Behavior and Contact within Huddles of Infant Mice

Brown adipose tissue (BAT) is a thermogenic effector abundant in most mammalian infants. For multiparous species such as rats and mice, the interscapular BAT deposit provides both an emergency “thermal blanket” and a target for nestmates seeking warmth, thereby increasing the cohesiveness of huddling groups. Sex differences in BAT regulation and thermogenesis have been documented in a number of species, including mice (Mus musculus)–with females generally exhibiting relative upregulation of BAT. It is nonetheless unknown whether this difference affects the behavioral dynamics occurring within huddles of infant rodents. We investigated sex differences in BAT thermogenesis and its relation to contact while huddling in eight-day-old C57BL/6 mouse pups using infrared thermography, scoring of contact, and causal modeling of the relation between interscapular temperature relative to other pups in the huddle (T_IS ^rel) and contacts while huddling. We found that females were warmer than their male siblings during cold challenge, under conditions both in which pups were isolated and in which pups could actively huddle in groups of six (3 male, 3 female). This difference garnered females significantly more contacts from other pups than males during cold-induced huddling. Granger analyses revealed a significant negative feedback relationship between contacts with males and T_IS ^rel for females, and positive feedback between contacts with females and T_IS ^rel for males, indicating that male pups drained heat from female siblings while huddling. Significant sex assortment nonetheless occurred, such that females made more contacts with other females than expected by chance, apparently outcompeting males for access to each other. These results provide further evidence of enhanced BAT thermogenesis in female mice. Slight differences in BAT can significantly structure the behavioral dynamics occurring in huddles, resulting in differences in the quantity and quality of contacts obtained by the individuals therein, creating sex differences in behavioral interactions beginning in early infancy.     

Triadic Positions of Tibetan Macaques Huddling at a Sleeping Site

We studied huddling of Tibetan macaques (Macaca thibetana) at a sleeping site in Huangshan, China, during the mating and birth seasons. Tibetan macaques in a free-ranging group made physical contact with each other and formed huddling groups on the ledge of a steep cliff at night. We analyzed the size and composition of huddling groups and the frequencies of dyadic huddles—two individuals in physical contact—in the huddling group to determine the social influences on huddling behavior. Affiliated dyads that frequently groomed in the daytime frequently formed dyadic huddles in night-time huddling groups. Female–male dyads formed dyadic huddles less frequently than expected. In addition, Tibetan macaques chose 2 partners with which they initiated contact when they approached a huddling group. The frequencies with which some combinations of 3 individuals contacted each other and formed triangular huddles are not consistent with the expected frequencies. For example, female–male–male triads frequently formed triangular huddles in the birth season but did so infrequently in the mating season because of male competition for estrous females. When all 3 dyads within a certain triad formed dyadic huddles frequently, the triad was more likely to form a triangular huddle. The choices of approaching individuals might make a systematic, rather than random, positioning of individuals in huddling groups at their sleeping site.     

Modeling Huddling Penguins

We present a systematic and quantitative model of huddling penguins. In this mathematical model, each individual penguin in the huddle seeks only to reduce its own heat loss. Consequently, penguins on the boundary of the huddle that are most exposed to the wind move downwind to more sheltered locations along the boundary. In contrast, penguins in the interior of the huddle neither have the space to move nor experience a significant heat loss, and they therefore remain stationary. Through these individual movements, the entire huddle experiences a robust cumulative effect that we identify, describe, and quantify. This mathematical model requires a calculation of the wind flowing around the huddle and of the resulting temperature distribution. Both of these must be recomputed each time an individual penguin moves since the huddle shape changes. Using our simulation results, we find that the key parameters affecting the huddle dynamics are the number of penguins in the huddle, the wind strength, and the amount of uncertainty in the movement of the penguins. Moreover, we find that the lone assumption of individual penguins minimizing their own heat loss results in all penguins having approximately equal access to the warmth of the huddle.     

Coordinated movements prevent jamming in an Emperor penguin huddle

For Emperor penguins (Aptenodytes forsteri), huddling is the key to survival during the Antarctic winter. Penguins in a huddle are packed so tightly that individual movements become impossible, reminiscent of a jamming transition in compacted colloids. It is crucial, however, that the huddle structure is continuously reorganized to give each penguin a chance to spend sufficient time inside the huddle, compared with time spent on the periphery. Here we show that Emperor penguins move collectively in a highly coordinated manner to ensure mobility while at the same time keeping the huddle packed. Every 30-60 seconds, all penguins make small steps that travel as a wave through the entire huddle. Over time, these small movements lead to large-scale reorganization of the huddle. Our data show that the dynamics of penguin huddling is governed by intermittency and approach to kinetic arrest in striking analogy with inert non-equilibrium systems, including soft glasses and colloids.     

Dominance and huddling behaviour in Bronze Mannikin Lonchura cucullata flocks

Bronze Mannikins Lonchura cucullata form flocks of up to 30 birds at the end of the breeding season and huddle in communal nests during winter. Assuming there are thermoregulatory benefits associated with huddling for these small endotherms, particularly during winter, we predicted that dominant individuals in flocks would obtain the central locations within the huddles. We tested this prediction by determining the dominance hierarchies of six captive flocks of five individuals by examining interactions at a feeder. Mannikins were observed to huddle when cold-stressed. Although mannikins do not naturally form linear huddles, for ease of observation we recorded the positions of individually marked birds in linear huddles at 5 °C before and after disturbances every half hour for 3 h. Captive flocks of mannikins established linear dominance hierarchies and dominant individuals obtained the central location within the huddle. The central position in the huddle may be beneficial in thermodynamically challenging environments through reduced energy expenditure.     

Emperor penguin mates: keeping together in the crowd

As emperor penguins have no breeding territories, a key issue for both members of a pair is not to be separated until the egg is laid and transferred to the male. Both birds remain silent after mating and thereby reduce the risk of having the pair bond broken by unpaired birds. However, silence prevents finding each other if the pair is separated. Huddles—the key to saving energy in the cold and the long breeding fast—continuously form and break up, but not all birds are involved simultaneously. We studied the behaviour of four pairs before laying. Temperature and light intensity measurements allowed us to precisely detect the occurrence of huddling episodes and to determine the surrounding temperature. The four pairs huddled simultaneously for only 6 per cent of the time when weather conditions were harshest. Despite this asynchrony, the huddling behaviour and the resulting benefits were similar between pairs. By contrast, the huddling behaviour of mates was synchronized for 84 per cent of events. By coordinating their huddling behaviour during courtship despite the apparent confusion within a huddle and its ever-changing structure, both individuals save energy while securing their partnership.     

Dynamic thermal balance in the leaf-eared mouse: the interplay among ambient temperature,body size,and behavior

Endotherms maintain constant body temperature through physiological and behavioral adjustments. Behavioral thermoregulation is an important factor influencing energy balance. We exposed the leaf-eared mouse, Phyllotis darwini, to temperatures corresponding to its natural thermal range and studied two forms of behavioral thermoregulation: diminishing surface to volume ratio by huddling and heat dissipation by increasing physical contact with the substrate (flattening). We predicted that at low ambient temperatures (T(a)) huddling would be used as a heat conservation mechanism and at high T(a) flattening would be used for heat loss. We simultaneously measured oxygen consumption (VO2) and flattening, in response to three independent factors: huddling, T(a), and body mass. Each experiment was a 6-h VO2 trial where five virgin females were measured at constant T(a). We performed this protocol for two body mass groups, small (ca. 40 g) and large (ca. 70 g), in a metabolic chamber. Treatments were groups with and without the ability to huddle at five different T(a), ranging from 5 degrees to 35 degrees C. A significant interaction between all three factors was found. Huddling and flattening were used as strategies for conserving or dissipating heat, respectively, and the shift between both strategies occurred at the lower limit of thermoneutrality. At T(a) below thermoneutrality, huddling was a more effective way of reducing metabolic requirements and was more efficient (H(E)) in small individuals than large individuals. So, by huddling, small individuals save more energy. At high T(a), flattening appeared to be an equally useful mechanism for heat loss, for both large and small animals.     

The developmental emergence of coupled activity as cooperative aggregation in rat pups.

Rat pups (Rattus norvegicus) are born blind and deaf yet manage to wriggle about in a huddle, dynamically adjusting their positions and thereby displaying thermoregulation and energy conservation at the level of the group. As pups develop, their activity and mobility outpace the development of their visual and auditory systems making it increasingly difficult to aggregate and maintain aggregation while still blind and deaf. The developmental emergence of coupled activity may be one mechanism that facilitates aggregation. Our previous research has shown that the activity of a seven-day-old pup is independent of the activity of the litter mates it contacts. However, we hypothesized that, by day 10, more active and mobile pups will exhibit coupled activity, becoming increasingly quiescent when in contact with other behaviourally quiescent pups. In order to test this hypothesis, we used individual-based modelling. Because the structure of the model was complex, we used a Darwinian algorithm for evolving a model that behaved like ten-day-old pups aggregating in an arena. Sensitivity to quiescent individuals was manifested in some litters by the transitory spreading of quiescence across aggregates of both real and virtual pups (a contagion effect). As pups develop, individual behaviour becomes increasingly contingent on the behaviour of others revealing what may be a basic component in the development of cooperative behaviour.     

Oxytocin mediates the acquisition of filial, odor-guided huddling for maternally-associated odor in preweanling rats

The present study was designed to examine possible roles of oxytocin (OT) in the acquisition of a filial huddling preference in preweanling rats. We used a procedure in which a scented, foster mother can induce an odor-guided huddling preference in preweanling pups, following a single, 2-h-long co-habitation ( [Kojima and Alberts, 2009] and Kojima and Alberts, 2011). This single, discrete period for preference learning enables us to observe the mother–pup interactions that establish the pups' preferences and to intervene with experimental manipulations. Four, 14-day-old littermates interacted with a scented foster mother that provided maternal care during a 2-h session. Two of the pups were pretreated with an intracerebroventricular injection of OT or an oxytocin antagonist (OTA), and the others received a vehicle injection. Filial preference for a maternally-paired odor was measured in a huddling test the next day. OT is necessary for acquisition of the filial preference: The preference learning was blocked in the pups treated with OTA, but not in their vehicle-treated littermates who experienced the same mother at the same time. Injection with exogenous OT did not augment the pups' preference. Manipulating pups' central OT also altered the contact interactions of the mother and pups. When some pups received OT, mother–litter aggregations formed as frequently and with similar combinations of bodies, but contact aggregations were significantly more cohesive than when some pups in the litter received OTA. We discuss dual, behavioral and neuroendocrine roles of OT in social learning by preweanling rats.     

Oxytocin mediates the acquisition of filial,odor-guided huddling for maternally-associated odor in preweanling rats

The present study was designed to examine possible roles of oxytocin (OT) in the acquisition of a filial huddling preference in preweanling rats. We used a procedure in which a scented, foster mother can induce an odor-guided huddling preference in preweanling pups, following a single, 2-h-long co-habitation (Kojima and Alberts, 2009, Kojima and Alberts, 2011). This single, discrete period for preference learning enables us to observe the mother–pup interactions that establish the pups' preferences and to intervene with experimental manipulations. Four, 14-day-old littermates interacted with a scented foster mother that provided maternal care during a 2-h session. Two of the pups were pretreated with an intracerebroventricular injection of OT or an oxytocin antagonist (OTA), and the others received a vehicle injection. Filial preference for a maternally-paired odor was measured in a huddling test the next day. OT is necessary for acquisition of the filial preference: The preference learning was blocked in the pups treated with OTA, but not in their vehicle-treated littermates who experienced the same mother at the same time. Injection with exogenous OT did not augment the pups' preference. Manipulating pups' central OT also altered the contact interactions of the mother and pups. When some pups received OT, mother–litter aggregations formed as frequently and with similar combinations of bodies, but contact aggregations were significantly more cohesive than when some pups in the litter received OTA. We discuss dual, behavioral and neuroendocrine roles of OT in social learning by preweanling rats.     

Causes and predictors of nest mortality in a European rabbit population

We conducted a study on nest mortality of an individually marked population of European rabbits (Oryctolagus cuniculus L., 1758) living in a field enclosure. Over 4 years, we determined maternities and quantified pup mortality during the nest period of 703 pups born in subterranean breeding burrows. Overall, pup mortality occurred in 42.7% of the litters, whereas 32.4% of all born pups were affected. Mortality was highest during the first few postnatal days. In about 50% of the cases, we managed to quantify different causes of mortality such as malnutrition, flooding, cooling of the pups, infanticide, or predation. The pups’ body mass on postnatal day 1, the thermal environment and the number of litter mates were the most important predictors of nest mortality. Litter mortality risk decreased with increasing soil temperature around the subterranean nests. A comparatively higher average pup body mass lowered the nest mortality risk of a litter, whereas this effect was more pronounced when soil temperatures were low. Furthermore, mortality was lowest in medium-sized litters, most probably due to the balance between the thermal benefits of huddling with litter siblings and the costs of having them due to the lower share of milk obtained by the individual pups in larger litters. In addition, nest mortality depended on characteristics of the mother; mortality was increased in litters of low-ranking females and of mothers with lower body mass. In conclusion, our study highlights multiple causes and the effects of different environmental and social factors on nest mortality of this small mammal.     

Shape of,and body direction in,huddles of Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>) in Arashiyama,Japan

We studied huddles of Japanese macaques (Macaca fuscata) in the Arashiyama E troop at the “Arashiyama Monkey Park, Iwatayama” of Kyoto, central Japan. The macaques made physical contact with other individuals and formed huddles when the air was cold. The 99–101 adult females and 26–36 adult males in the study troop formed 345 huddles during 42 scan samples in the winter of 2001 and 376 huddles during 52 scan samples in the winter of 2002. The average size of huddles was 2.3 (range 2–7) individuals. Males huddled less frequently than females. Maternal kin-related dyads formed 2-female huddles more frequently than unrelated dyads. Choice of huddling partners might restrict the size of huddles. The most frequently observed 3 and 4-member huddles were triangular and diamond-shaped. Macaques usually huddled ventro–ventrally, ventro–laterally, and ventro–dorsally. A third individual frequently placed the ventral part of its body against the first individual and simultaneously put the lateral part of its body against the second individual, so that the 3 individuals formed a triangular huddle. This behaviour indicates that Japanese macaques choose their position and body direction in the huddle to reduce the area of body surface exposed to the air, thereby conserving body heat.     

Huddling relationships in night sleeping groups among wild Japanese macaques in Kinkazan Island during winter

Huddling groups at sleeping sites, and allogrooming and proximity in the daytime during winter, were examined in a wild Japanese macaque (Macaca fuscata) troop on Kinkazan Island in the non-snowy district of northern Japan. All sleeping groups, defined as a cluster in which individuals huddle at sleeping sites, were formed on the ground. Their sizes tended to increase when the temperature was lower. The number of adults with mutual physical contact in sleeping groups increased when the size of sleeping groups increased. These results suggest that the physiological function of huddling is protection from low temperatures, and that macaques select the ground as sleeping sites to form large sized groups. Huddling was performed most frequently among kin dyads. Non-related dyads which appeared to be affiliative in the daytime also huddled frequently at sleeping sites. Even non-related dyads which showed affiliative behavior less frequently in the daytime exhibited huddling, at night, however, they did so less often than those of kin dyads and affiliated dyads. It appears that huddling at night by pairs that did not normally affiliate in the daytime was made possible by the increased tolerance of individuals responding to colder temperatures at night in winter. Furthermore, huddling, grooming, and proximity were exhibited at greater frequency between kin dyads, and between high-ranking males and specific females of kin groups, although the dyads of individuals older than 15 years often were involved only in huddling. These results suggest that two types of social bonds exist at sleeping sites in winter. One is the social bond common to both the daytime and nighttime, the other is peculiar to nighttime. Consequently, the social function of huddling is that, troop integration might increase at sleeping sites in winter as close social relationships among adults are extended more widely than those in daytime.     

The development of locomotor kinematics in neonatal rats: an agent-based modeling analysis in group and individual contexts

An agent-based model of infant rat (pup) locomotion and aggregation was developed by modifying a previous model of pup aggregation [Schank, J.C., Alberts, J.R., 2000a. The developmental emergence of coupled activity as cooperative aggregation in rat pups. Proc. R. Soc. London B 267, 2307-2315]. The main difference between the earlier and current models is the incorporation of whole-body kinematics of directional locomotion. Data on locomotion and aggregation are presented for individuals and groups of 7- and 10-day-old pups and the data were used to evolve models (with a genetic algorithm) that fit these data. Aggregation between 7- and 10-day-old pups was considerably different and could be explained by agent-based models, in particular, models with directional-kinematic matrices specifying the probabilities of moving to adjacent cells. The directional kinematics of whole-body movement differed between the two age classes and differed between group and individual contexts for 10-day-old pups. This may indicate a developmental transition (by day 10) to more central control of behavior and the ability to change patterns of movement based on social context. The behavior analyzed with agent-based models may provide a precise way to measure motor and nervous system development in rats and other rodents.     

Role of huddling on the energetic of growth in a newborn altricial mammal

Huddling is considered as a social strategy to reduce thermal stress and promote growth in newborn altricial mammals. So far, the role of huddling on the allocation of saved energy has not been quantified nor have the related impacts on body temperature rhythms. To determine the energy partitioning of rabbit pups either raised alone or in groups of eight, four, or two individuals, when thermoregulatory inefficient (TI) and efficient (TE), we first investigated their total energy expenditure and body composition. We then monitored body temperature and activity rhythms to test whether huddling may impact these rhythms, centered on the suckling event. Pups in a group of eight utilized 40% less energy for thermogenesis when TI than did pups alone and 32% less energy when TE. Pups in groups of eight and four had significantly lower thermoregulatory costs in the TI period, whereas pups in groups of two, four, and eight had lower costs during the TE period. Huddling pups could therefore channel the energy saved into processes of growth and accrued more fat mass (on average 4.5 +/- 1.4 g) than isolated pups, which lost 0.7 g of fat. Pups in groups of four and eight had a body temperature significantly higher by 0.8 degrees C than pups in groups of two and one when TI, whereas no more differences were noted when the TE period was reached. Moreover, pups alone showed an endogenous circadian body temperature rhythm that differed when compared with that of huddling pups, with no rise before suckling. Thus huddling enables pups to invest the saved energy into growth and to regulate their body temperature to be more competitive during nursing, particularly at the early time when they are TI.     

Nursing Behavior in Mexican Free-tailed Bat Maternity Colonies

The nursing behavior of Mexican free-tailed bats (Tadarida brasiliensis mexicana) was examined in two large maternity cave roosts during six nursing seasons. After depositing pups in large creches, adults return to these creches two or more times daily to nurse. Densities, movements, and roosting associations of pups in creches were documented, and a night-vision device and infrared-sensitive video system were used to observe female-pup reunions and nursing affiliations. Densities of young (< 15 d) pups in creches averaged 4000 pups/m². Pups moved independently of one another between milk meals. Stable roosting associations among pups were absent, and females evidently could not predict where a given pup would be relocated. Upon returning to the creche, females searched for and relocated pups using vocal and olfactory cues. Experiments with marked individuals demonstrated that females nursed the same pups on subsequent nights. These same experiments indicated that female/pup recognition was mutual and that the pup participated in reunions by moving toward its putative mother. However, pups also attempted to suckle from other females and 35 instances of apparently successful milk “theft” were observed. Observed milk theft was insufficient to account for the frequency of alloparental nursing that was estimated independently using genotype tests. The high densities of bats within roosts and the lack of stable roosting associations among individuals argue against selection for shared nursing via kin selection and/or reciprocity. Errors in pup recognition, milk-dumping by females, and adoption by mothers whose own pup had died may occur, but high pup survival to weaning suggests that adoption is rare. The estimate of alloparental nursing obtained from genotype tests may be inflated as a result of increased opportunities for milk theft caused by our disturbance of adults. Current evidence suggests that energetic costs to females of alloparental nursing and searching for pups are compensated by mutualistic benefits obtained from aggregative roosting.     

Social Cognition in Individuals at Ultra-High Risk for Psychosis: A Meta-Analysis

Objective

Treatment in the ultra-high risk stage for a psychotic episode is critical to the course of symptoms. Markers for the development of psychosis have been studied, to optimize the detection of people at risk of psychosis. One possible marker for the transition to psychosis is social cognition. To estimate effect sizes for social cognition based on a quantitative integration of the published evidence, we conducted a meta-analysis of social cognitive performance in people at ultra high risk (UHR).

Methods

A literature search (1970-July 2015) was performed in PubMed, PsychINFO, Medline, Embase, and ISI Web of Science, using the search terms ‘social cognition’, ‘theory of mind’, ‘emotion recognition’, ‘attributional style’, ‘social knowledge’, ‘social perception’, ‘empathy’, ‘at risk mental state’, ‘clinical high risk’, ‘psychosis prodrome’, and ‘ultra high risk’. The pooled effect size (Cohen’s D) and the effect sizes for each domain of social cognition were calculated. A random effects model with 95% confidence intervals was used.

Results

Seventeen studies were included in the analysis. The overall significant effect was of medium magnitude (d = 0.52, 95% Cl = 0.38–0.65). No moderator effects were found for age, gender and sample size. Sub-analyses demonstrated that individuals in the UHR phase show significant moderate deficits in affect recognition and affect discrimination in faces as well as in voices and in verbal Theory of Mind (TOM). Due to an insufficient amount of studies, we did not calculate an effect size for attributional bias and social perception/ knowledge. A majority of studies did not find a correlation between social cognition deficits and transition to psychosis, which may suggest that social cognition in general is not a useful marker for the development of psychosis. However some studies suggest the possible predictive value of verbal TOM and the recognition of specific emotions in faces for the transition into psychosis. More research is needed on these subjects.

Conclusion

The published literature indicates consistent general impairments in social cognition in people in the UHR phase, but only very specific impairments seem to predict transition to psychosis.     

Olfactory and Thermal Influences on Ultrasonic Vocalization During Development in Rodents

Ultrasounds are emitted by developing rodents, and changes withage in several parameters of vocalization have been reportedfor numerous myomorphs. In this paper I integrate with ultrasonicvocalization several behaviors which change during development.Included are studies controlling stimulation by olfactory, thermal,and tactile cues as well as detailed studies of specific responsessuch as movement, suckling, grooming, and huddling. Developmentis analyzed in well-known species, such as the rat (Rattus norvegicus),and in less familiar species, especially the pine vole (Microtuspinetorum). Lacking the capacity for physiological thermoregulation, altricialrodent pups with their mother use several behavioral strategieswhich facilitate thermoregulation. Inside the nest, pups adjustthe temperature by changing their huddling. The mother regulatesthe length of suckling bouts according to her body temperature.When a pup is removed from the warm nest, vocalizations of thepup can increase the likelihood of retrieval by the mother andthereby indirectly facilitate thermoregulation. In several species which have been studied, vocalization ratesare highest when pups begin to move into and out of nests andexhibit olfactory-directed movement. As olfactory preferencesbecome established and movement is coordinated, a decline invocalization appears in rat, mouse, hamster, spiny mouse, andpine vole. In the gerbil, however, the decline precedes competencein olfactory-directed movement. In the presence of home shavings, young rats emit low ratesof vocalization, while pine vole young emit calls at a highrate. This contrast may relate to the intensive attachment ofyoung pine voles to the mother in early life.     

Interactions of partners in family pairs,care of the offspring,and the role of tactile stimulation in formation of parental behavior of the Mongolian gerbil (<Emphasis Type="Italic">Meriones unguiculatus</Emphasis>) under laboratory conditions

The interactions of sexual partners and care of the offspring in male and female Mongolian gerbils reared in biparental and uniparental family groups (without an adult male) were compared. In individuals reared in biparental family groups, sexual differences related to the manifestation of parental care were small and statistically insignificant. In individuals reared in uniparental groups, the interactions of sexual partners related to grooming changed; the duration in males decreased threefold, as compared to the norm; indices of parental behavior of females and, especially of males, related to tactile stimulation of pups (huddling with pups in the nest and duration of licking pups) also decreased. The importance of the parental contribution of males, especially of tactile stimulation, in the evolution of the family-group mode of life is discussed.