Altricial Mammals Research Articles

Precocious Torpor in an Altricial Mammal and the Functional Implications of Heterothermy During Development.

Most mammals and birds are altricial, small and naked at birth/hatching. They attain endothermic thermoregulation at a fraction of their adult size at a vulnerable stage with high heat loss when many could profit from using torpor for energy conservation. Nevertheless, detailed data on the interrelations between torpor expression and development of endothermic thermoregulation are currently restricted to <0.1% of extant endotherms. We investigated at what age and body mass (BM) desert hamsters (Phodopus roborovskii), wild-caught in Inner Mongolia and born in autumn/early winter when environmental temperatures in the wild begin to decrease, are able to defend their body temperature (Tb) at an ambient temperature (Ta) of ∼21°C and how soon thereafter they could express torpor. Measurements of surface temperatures via infrared thermometer and thermal camera show that although neonate hamsters (BM 0.9 ± 0.1 g) cooled rapidly to near Ta, already on day 15 (BM 5.5 ± 0.2 g) they could defend a high and constant Tb. As soon as day 16 (BM 5.8 ± 0.2 g), when their maximum activity metabolism (measured as oxygen consumption) approached maxima measured in vertebrates, animals were able to enter torpor for several hours with a reduction of metabolism by >90%, followed by endothermic arousal. Over the next weeks, torpor depth and duration decreased together with a reduction in resting metabolic rate at Ta 30–32°C. Our data show that development of endothermy and torpor expression in this altricial hamster is extremely fast. The results suggest that precocious torpor by juvenile hamsters in autumn and winter is an important survival tool in their vast and harsh Asian desert habitats, but likely also for many other small mammals and birds worldwide.

Coordinated Emergence of Hippocampal Replay and Theta Sequences during Post-natal Development

SummaryHippocampal place cells encode an animal’s current position in space during exploration [1]. During sleep, hippocampal network activity recapitulates patterns observed during recent experience: place cells with overlapping spatial fields show a greater tendency to co-fire (“reactivation”) [2], and temporally ordered and compressed sequences of place cell firing observed during wakefulness are reinstated (“replay”) [3, 4, 5]. Reactivation and replay may underlie memory consolidation [6, 7, 8, 9, 10]. Compressed sequences of place cell firing also occur during exploration: during each cycle of the theta oscillation, the set of active place cells shifts from those signaling positions behind to those signaling positions ahead of an animal’s current location [11, 12]. These “theta sequences” have been linked to spatial planning [13]. Here, we demonstrate that, before weaning (post-natal day [P]21), offline place cell activity associated with sharp-wave ripples (SWRs) reflects predominantly stationary locations in recently visited environments. By contrast, sequential place cell firing, describing extended trajectories through space during exploration (theta sequences) and subsequent rest (replay), emerge gradually after weaning in a coordinated fashion, possibly due to a progressive decrease in the threshold for experience-driven plasticity. Hippocampus-dependent learning and memory emerge late in altricial mammals [14, 15, 16, 17], appearing around weaning in rats and slowly maturing thereafter [14, 15]. In contrast, spatially localized firing is observed 1 week earlier (with reduced spatial tuning and stability) [18, 19, 20, 21]. By examining the development of hippocampal reactivation, replay, and theta sequences, we show that the coordinated maturation of offline consolidation and online sequence generation parallels the late emergence of hippocampal memory in the rat.

Developmental delay in shivering limits thermogenic capacity in juvenile high-altitude deer mice (Peromyscus maniculatus)

Many endotherms native to cold and hypoxic high-altitude (HA) environments have evolved a highly vascularized and aerobic skeletal muscle. This specialized muscle phenotype contributes via shivering to an enhanced capacity for aerobic thermogenesis (cold-induced V̇ O2,max). However, it is unclear how selection at HA for shivering thermogenesis acts early in the development of small altricial mammals, which are born with immature skeletal muscles and without the capacity for homeothermic endothermy. We have previously shown that postnatal maturation of brown adipose tissue and non-shivering thermogenesis is delayed in HA native deer mouse pups (Peromyscus maniculatus). To assess whether HA adaptation has also altered the developmental program of skeletal muscle and shivering thermogenesis, we used laboratory-reared descendants of deer mice native to low altitude (LA, 430 m a.s.l.) and HA (4350 m a.s.l.) and a LA congeneric outgroup (P. leucopus). We found that LA juveniles were able to shiver robustly at 2 weeks after birth. However, HA juveniles were unlikely able to shiver at this point, resulting in a 30% lower capacity for thermoregulation compared with lowlanders. It was only at 27 days after birth that HA juveniles had established the aerobic muscle phenotype characteristic of HA adults and a superior cold-induced V̇ O2,max compared with LA mice of the same age. The capacity for shivering may be delayed in HA mice to allow energy to be allocated to other important processes such as growth.

The evolution of ontogenetic allometric trajectories in mammalian domestication.

Morphological divergence of domesticated as compared to wild forms must result from changes in the ontogenetic process. Species-specific tests for heterochrony have rejected a single explanation of domestic forms representing juveniles of their wild relatives. Ontogenetic allometric trajectories for 12 pairs of wild and domestic mammals were examined using skull growth data for 1070 specimens, including representatives from all lineages in which domestication has occurred. A suite of tests were performed to quantify allometric disparity in wild and domestic forms and assess the extent and patterning of modification to allometric trajectories. Domestication has modified postnatal ontogenetic allometric trajectories in mammals, and has generated disparity, achieved through lengthening of trajectory slopes and alteration to slope angles. Allometric disparity was similar for domestic forms compared to their wild relatives, whereas the magnitude of dispersion along allometric vectors differed between precocial mammals and altricial mammals, underscoring the importance of life history and shared evolutionary history in patterns of ontogenetic variation. The results verify the importance of scaling in the morphological changes associated with domestication. The response to domestication for all measured trajectory parameters was variable across species, suggesting multiple pathways of change.

Understanding mammary activity in red-rumped agouti and implications for management and conservation of this Neotropical game species.

The red-rumped agouti (Dasyprocta leporina) produces precocial young and is the most hunted and farmed game species in several Neotropical countries. An understanding of the reproductive biology, including the relationship between litter size and teat functionality is crucial for conservation management of this animal. In precocial mammals, as the red-rumped agouti, maintaining maternal contact to learn foraging patterns may be more important than the energy demands and nutritional constraints during lactation and suckling may not play important roles when compared to altricial mammals. Therefore, in this study we evaluated the relationship between mammary functionality with litter size, litter birth weight, and parturition number in captive red-rumped agouti. Functionality was assessed by manual palpation of teats from un-sedated females (N=43). We compared the average birth weight of all newborns, male newborns and female newborns among agoutis with different litter sizes and different parturitions by one way ANOVA's, while Pearson's Chi-squared tests were used to detect relationships between teat functionality, litter size, and parturition number. Parturition number had no effect on the mean birth weight of all young (F0.822, P > 0.05), male young (F0.80, P > 0.05) or female young (F0.66, P > 0.05) in the litters. We found (i) no significant correlations (P > 0.05) between teat functionality and litter size and (ii) no significant correlations (P > 0.05) between teat functionality and parturition number. This suggests that whilst all teat pairs were functional, functionality was a poor indicator of litter size; suggesting that female agouti young may not have a high dependency on maternal nutrition; an possible evolutionary strategy resulting in large wild populations; hence its popularity as a game species.

Body mass modulates huddling dynamics and body temperature profiles in rabbit pups

Altricial mammals typically lack the physiological capacity to thermoregulate independently during the early postnatal period, and in litter-bearing species the young benefit strongly from huddling together with their litter siblings. Such litter huddles are highly dynamic systems, often characterized by competition for energetically favorable, central positions. In the present study, carried out in domestic rabbits Oryctolagus cuniculus, we asked whether individual differences in body mass affect changes in body temperature during changes in the position within the huddle. We predicted that pups with relatively lower body mass should be more affected by such changes arising from huddle dynamics in comparison to heavier ones. Changes in pups' maximum body surface temperature (determined by infrared thermography) were significantly affected by changes in the number of their neighbors in the litter huddle, and indeed these temperature changes largely depended on the pups' body mass relative to their litter siblings. Lighter pups showed significant increases in their maximum body surface temperature when their number of huddling partners increased by one or two siblings whereas pups with intermediate or heavier body mass did not show such significant increases in maximum body temperature when experiencing such changes. A similar pattern was found with respect to average body surface temperature. This strong link between changes in the number of huddling partners and body surface temperature in lighter pups might, on the one hand, arise from a higher vulnerability of such pups due to their less favorable body surface area-to-volume ratio. On the other hand, as lighter pups generally had fewer neighbors than heavier ones and thus typically a comparatively smaller body surface in contact with siblings, they potentially had more to gain from increasing their number of neighbors. The present findings might help to understand how individual differences in body mass within a litter lead to the emergence of individual differences in sibling interactions during early postnatal life in different species of altricial and litter-bearing mammals.

Chemical Identification of "Maternal Signature Odors" in Rat.

Newborn altricial mammals need just after birth to locate their mother's nipples for suckling. In this precocious behavior, including for the human baby, maternal odor via the olfactory process plays a major role. Maternal odor emitted by lactating females or by amniotic fluid (AF) attracts pups, but the chemical identity of this attractant has not yet been elucidated. Here, using behavioral tests and gas chromatography coupled with mass spectrometry (GC-MS) techniques, we show that AF extracts from rat pregnant female, nipples, ventral skin, milk, and nest extracts of mother contained 3-6 active substances. AF extracts contained 3 active compounds: ethylbenzene, benzaldehyde, and benzyl alcohol, and their mixture in similar proportions to those found in AF extracts, in a ratio, respectively, of 1:1:12 (700 ng), attracts pups as putative maternal attractant substances (MAS). These 3 AF substances have already been identified in milk, nipples, ventral wash, and nest extracts of mother, but not in feces. Moreover, anethole flavor incorporated in pregnant rat and mother's diet is also detected in AF, nipples, milk, and nest extracts and the pups are attracted to anethole odor, but not in the case of the no-anethole pups. MAS, combined with diet flavors present in the AF bath, represent olfactory signals as "maternal signature odors" (MSO) that are learned by fetus and pups. These findings open the way to improved understanding of the neurobiology of early olfactory learning and of the importance of evolutionarily conserved survival behavior in many mammal species.

Breathing while altricial: the ontogeny of ventilatory chemosensitivity in red-winged blackbird (Agelaius phoeniceus) nestlings.

Altricial bird species, like red-winged blackbirds, hatch at an immature state of functional maturity with limited aerobic capacity and no endothermic capacity. Over the next 10-12 days in the nest, red-winged blackbirds develop increased metabolic capacity before fledging. Although ontogeny of respiration has been described in precocial birds, ontogeny of ventilatory chemosensitivity is unknown in altricial species. Here we examined developmental changes in chemosensitivity of tidal volume (Vt), breathing frequency (ƒ), minute ventilation (V̇e), and whole animal oxygen consumption (V̇o2) from hatching to just before fledging in red-winged blackbirds on days 1, 3, 5, 7, and 9 posthatching (dph) in response to hypercapnia (2 and 4% CO2) and hypoxia (15 and 10% O2). Under control conditions, there was a developmental increase in V̇e with age due to increased Vt Hypercapnic and hypoxic chemosensitivities were present as early as 1 dph. In response to hypoxia, 1, 3, and 9 dph nestlings increased V̇e at 10% O2, by increasing ƒ with some change in Vt in younger animals. In contrast to early neonatal altricial mammals, the hypoxic response of nestling red-winged blackbirds was not biphasic. In response to hypercapnia, 3 dph nestlings increased V̇e by increasing both ƒ and Vt From 5 dph on, the hypercapnic increase in V̇e was accounted for by increased Vt and not ƒ. Chemosensitivity to O2 and CO2 matures early in nestling red-winged blackbirds, well before the ability to increase V̇o2 in response to cooling, and thus does not represent a limitation to the development of endothermy.

Development of an altricial mammal at sea: II. Energy budgets of female sea otters and their pups in Simpson Bay, Alaska

Lactation is a critical and energetically expensive period of reproduction, especially for female sea otters (Enhydra lutris) and their pups, both of which have resting metabolic rates that are ca. 2.5-fold higher than terrestrial mammals of similar size. The simultaneous energy budgets for female Alaskan sea otters and their pups during the first three months postpartum were calculated based on published activity budgets for wild animals and metabolic rates for specific behaviors of captive sea otters. Pups were classified into three behavioral/size categories: Category 1 (C1) 0–<4wk. old; Category 2 (C2) 4–<8wk. old; and Category 3 (C3) 8–12wk. Energy for growth (Energygrowth) averaged 0.0416MJday−1 for all pups. The combined daily energy expenditure to support resting metabolism and activity (Energyr+a) for C1 and C2 pups was 1.31 and 2.61MJday−1, respectively, of which most (C1: 99%; C2: 84%) was associated with resting-equivalent behaviors (i.e., resting, nursing and being groomed by the female). Energyr+a for C3 pups was 4.62MJday−1 of which 49% was associated with resting-equivalent behaviors, while 35% was associated with active behaviors (i.e., feeding, swimming and grooming). The underlying resting metabolic rate for all behaviors represented 100% of Energyingest for C1, 94% for C2 and 85% for C3 pups. Energyr+a for all females was similar regardless of pup age and averaged 10.88MJday−1 (range 10.79–11.03). Energyr+a for C1 females was associated mainly with self-grooming and pup grooming (30%) and swimming (25%), while only 10% was associated with feeding. Energyr+a for C3 females was mainly associated with feeding (37%) with less energy devoted to swimming (10%) and grooming (14%). Lactation energy (Energylactation) in C3 females was 3.5-fold greater than in C1 females. Ingested energy for C1 females was 19.55MJday−1, which increased to 22.13MJday−1 for C2 females and 26.53MJday−1 for C3 females. As with pups, the underlying resting metabolic rate for all female behaviors represented 70% of Energyingest for C1 females and 72% for C2 and C3 females. Hence, thermogenesis dominated the metabolism of female sea otters as with their pups. These results provide a quantitative picture of the energetics of Alaskan female sea otters and their pups during early pup rearing in a species that has one of the highest mass specific resting metabolic rates of any mammal and the most altricial neonate born at sea.

Contribution of within-litter interactions to individual differences in early postnatal growth in the domestic rabbit

Interactions with littermates are an important component of the early environment of altricial mammals, frequently with major consequence for individual development, growth and survival. Early differences in starting mass within litters are often predictive of individual differences in behaviour and development, although to what extent such differences are independent of (epi)genetic factors is not always clear. In our study on domestic rabbits, Oryctolagus cuniculus, we created experimentally mixed litters consisting of either heavier or lighter pups obtained from different litters at birth and raised by foster mothers. We hypothesized that pups' body mass relative to their new littermates would determine the nature of their social interactions with consequences for their early growth, largely independent of their absolute or relative body mass in their litters of origin. As predicted, pups with a higher starting mass on postnatal day 1 compared to members of their new litter consistently had more neighbours in the litter huddle, thus reflecting their more central position. In turn, pups with more neighbours had relatively higher body temperatures, greater milk intake and a higher milk conversion ratio, resulting in relatively greater growth during the first critical postnatal week. Relative body mass in the litter of origin or absolute body mass had no notable effect, indicating that the observed developmental patterns were truly driven by pups' body mass relative to their current littermates rather than being a consequence of (epi)genetic effects potentially associated with their birth mass. In conclusion, our study underlines the importance of interactions among siblings in shaping individual differences in early growth and development largely independent of genetic factors.

Development of an altricial mammal at sea: I. Activity budgets of female sea otters and their pups in Simpson Bay, Alaska

Parental care is necessary for the survival of most mammalian offspring. However, this is especially true for neonatal sea otters (Enhydra lutris), which are the most altricial of marine mammals born at sea. The female not only feeds the pup but also protects it from environmental and predatory threats while maintaining the insulating properties of its fur for thermoregulation. We studied the behavior of female sea otters and their pups during the first three months postpartum in Simpson Bay, Alaska. Six behaviors for females and seven behaviors for pups were recorded to produce 24-h activity budgets. Pups were classified into three behavioral/size categories: Category 1 (C1) 0 – <4 wks old; Category 2 (C2) 4 – <8 wks old; Category 3 (C3) 8–12 wks. The percentage of time females spent feeding increased from 9% (C1) to 32% (C3) reflecting the increased nutritional requirements of the maturing pups. C1 females spent 21% of their time swimming in a meandering manner, possibly to protect young pups from predation, which decreased to 8% for females with C3 pups. The time spent resting by females (ca. 50%) was independent of pup category. C1 pups spent 83% of their day resting which decreased to 48% for C3 pups. Time spent nursing remained constant (ca. 8%) for all pup categories, but feeding on solid food provided mainly by the female increased to 17% (C3 pups). The percentage of time that pups spent swimming increased to 17% (C3 pups) as they developed strength and coordination. Our results provide a quantitative picture of the changes in female and pup behavior and activity patterns during the early and critical developmental stages of altricial pups at sea.

Mild effects of gestational stress and social reactivity on the onset of mother–young interactions and bonding in sheep

Consequences of prenatal stress on mother–young relationships are well-documented in altricial mammals but less so in precocial mammals. In this study, we investigated the effects of unpredictable aversive events on maternal behavior and mutual mother–young recognition in pregnant ewes while accounting for modulatory effects of ewe reactivity. From a population of 120 Romane-breed ewes, we selected 20 high-responsive (HR) and 20 low-responsive (LR) ewes according to pre-mating reactivity assessed in isolation tests. Over the final third of pregnancy, 10 HR ewes and 10 LR ewes were exposed daily to various aversive events such as social isolation, mixing and transport (stressed ewes), while the other 20 ewes were not exposed to aversive events (control ewes). Although the treatment induced chronic stress, physiologically confirmed by an increase in salivary cortisol following transport and sham shearing, maternal behavior of stressed ewes observed during the first 30 min postpartum and in the selectivity test 1 h 30 min later did not differ from controls. However, in a maternal motivation test performed 48 h postpartum, stressed ewes vocalized less than controls when separated from their lambs, and walked less readily past an unknown object to reach their lambs. Lambs of stressed ewes spent more time near their dam in a preference test performed 15 h after birth compared to control-ewe lambs. HR ewes spent more time grooming their lambs than LR ewes. We posit that domestication could have selected animals displaying robust expression of maternal behavior related to social reactivity and producing offspring that are better adapted to challenging situations.

Temporal modulation of the canonical clockwork in the suprachiasmatic nucleus and olfactory bulb by the mammary pheromone 2MB2 in pre-visual rabbits

During the early stages of development, the olfactory system plays a vital role in the survival of altricial mammals. One remarkable example is the Oryctolagus cuniculus, whose mother–young interaction greatly depends on the 2-methylbut-2-enal (2MB2) pheromone that triggers nipple search and grasping behaviors. Olfactory stimulation with 2MB2 regulates the expression of the core body temperature and locomotor activity rhythms in rabbit pups, indicating the modulation of the circadian system by this volatile cue. To address this issue, in the present study, we determined the effect of stimulation with pulses of 2MB2 on the molecular circadian clockwork in the suprachiasmatic nucleus (SCN) and in the main olfactory bulb (MOB). For this purpose, 7-day-old rabbits were stimulated with distilled water (CON), with ethyl isobutyrate (ETHYL) or with the pheromone (2MB2) at different times of the cycle, and 1h later, the expression of the activity marker C-FOS and of the clock proteins PER1, CRY1 and BMAL1 was evaluated in the SCN and in the three layers of the MOB.The clock proteins were abundantly expressed in both structures; nevertheless these showed diurnal rhythmicity only in the MOB, confirming that central pacemakers exhibit a heterochronical development of the molecular clockwork. C-FOS expression in the SCN and in the MOB was modulated by exposure to ETHYL and to 2MB2 only when these stimulants were presented at ZT00 and at ZT18. In contrast, the clock proteins were essentially modulated by 2MB2 at ZT00 and at ZT06 in both structures. In addition, the PER1 and CRY1 proteins exhibited differential responses to stimulation in the three layers of the MOB. For the first time, we report a modulatory and time-dependent effect of the mammary pheromone 2MB2 on the expression of the core clock proteins in the SCN and in the MOB in rabbits during pre-visual stages of development.

Thermoregulatory development and behavior of Ctenomys talarum pups during brief repeated postnatal isolation

In altricial mammals, the role of the mother and siblings throughout pup's early ontogeny is critical to determine “normal” development in neonates. It has been reported that variations in parental investment during pups' development affect thermoregulatory capacity, growth patterns, brain development and behavior during lifetime, such as spatial learning and memory in adults. Ctenomys talarum (tuco-tuco) is a solitary subterranean rodent, who inhabits complex burrows and exhibits developed spatial orientation abilities. Tuco-tuco's pups display an altricial development, spending more than 80% of the time in contact with the mother. Throughout weaning period, pups display active exploratory behavior and improvements in their spatial capabilities. Then, we determined the effect of repeated brief postnatal isolations on the acquisition of physiological thermoregulation and the development of spatial learning capabilities in tuco-tuco's pups. As it occurs in wild animals, daily brief isolations (30min) did not affect the acquisition of adult's body temperature nor resting metabolic rate's development pattern. Moreover, behavioral response and adult spatial abilities of isolated pups were similar to that observed in non-isolated ones. Then, during periods of mother's absence, minor physiological and behavioral adjustments, such as shivering and postural changes, are required to keep C. talarum pups within allostasis.

Evidence of a nesting psychology during human pregnancy

In altricial mammals, “nesting” refers to a suite of primarily maternal behaviours including nest-site selection, nest building and nest defense, and the many ways that nonhuman animals prepare themselves for parturition are well studied. In contrast, little research has considered pre-parturient preparation behaviours in women from a functional perspective. Reports in the popular press assert that women experience “nesting” urges, in the form of cleaning and organizing behaviours. Anthropological data suggest that having control over the environment is a key feature of childbirth preparation in humans, including decisions about where birth will take place, and who will be welcome in the birthing environment. Here, we describe the results of two studies, a large online study comparing pregnant and non-pregnant women, and a longitudinal study tracking women throughout pregnancy and into the postpartum period and comparing non-pregnant women at similar time intervals, using a nesting questionnaire that we developed. We found that women exhibit nesting behaviours, including space preparation and social selectivity, which peak in the third trimester of pregnancy. As is the case with nonhuman mammals, nesting in women may serve a protective function.

Transport Response is a filial-specific behavioral response to maternal carrying in C57BL/6 mice

BackgroundA mother carries her young in many altricial mammals, such as cats, lions, rats and mice. During maternal carrying, the transported young assume a compact posture. We have recently shown that, in both humans and mice, the carried infants immediately calmed down and showed reductions in heart rate, distress vocalizations, and voluntary movement. The loss of the calming response in mouse pups hindered maternal retrieval efficacy. These findings suggested that the infant calming response functioned to reduce the maternal burden of carrying and was therefore conserved in a variety of mammalian species. However, it remains unclear how and when each component of this calming response develops and whether it is a filial-specific behavior.ResultsWe dissected various components of the carrying-induced responses in mouse pups, collectively called the “Transport Response” herein. We showed that during the second postnatal week, pups exhibited characteristic compact posture with limb ventroflexion. The body trunk remained paradoxically pliable, suggesting complex neural regulation throughout the body. Pups also showed an increased pain tolerance to a tail pinch during the Transport Response. Analyses of the developmental courses of distinct components of the Transport Response revealed the independent regulation of each component: in the first postnatal week, the cessation of ultrasonic vocalizations was exhibited prominently; in the second postnatal week, immobilization reached its peak; and toward the third postnatal week, the postural component became fully matured. At the end of the third postnatal week, when the pups are able to transport by themselves, the pups no longer exhibited the Transport Response.ConclusionsThis study has revealed the mouse Transport Response as a complex set of behavioral and physiological components, each of which has a specific postnatal time window but is orchestrated in a well-matched manner with the maturation of ambulatory ability in the pups. These findings collectively indicate that the Transport Response is a filial-specific, innate behavioral reaction and is distinct from a simple reflex or defensive freezing response. The Transport Response could be a novel index of primitive filial attachment behaviors, acting to smooth mother-infant interaction.

Development of retinal projections and response to photic input in the suprachiasmatic nucleus of New Zealand White Rabbits

In rabbit pups, nursing by the mother is the prevailing entraining signal for their circadian rhythms during at least the first two weeks of life. Therefore, they are considered a natural model of food anticipatory activity. However, the photic entrainment of the circadian system in rabbit pups during this developmental stage is not well understood. The present study examined the retinal projections to the suprachiasmatic nucleus (SCN) and the functional responses of the SCN to light exposure. Using the anterograde tracer cholera toxin-B, we examined the retinal projections to the SCN at postnatal days (PD) 1, 9, 19 and in adult animals. The results revealed that the retinal projections were present at PD1 with a bilateral symmetry, and with a contralateral tendency at PD19 and adults. We also explored the response of the SCN to a light pulse by assessing the induction of FOS protein, a marker of neuronal activation, at PD1, 12, 19 and in adults. Light-induced FOS was observed during day and night at PD1, but mainly during night at PD12, 19 and adults. We conclude that in the SCN there is a “gating” mechanism to FOS induction by light that develops several days after birth, as in other mammals, and in the rabbit is already present at PD12. Moreover, in contrast to other altricial mammals, the circadian visual system, although not essential for entraining the rhythm during first two weeks of life, is present and functional in rabbit pups from birth.

The Pattern of Nipple Use Before Weaning Among Littermates of the Domestic Dog

AbstractSuckling provides a well‐defined and functionally significant context in which to study mammalian sibling competition and the possible consequences of this for long‐term differences in individual behavior, physiology, and life histories. There have, however, been surprisingly few studies of suckling behavior, even in species as accessible as the domestic dog. In a first approach, we filmed the suckling behavior of 10 litters (47 puppies) of various dog breeds in their owners' homes during the first postnatal month before the start of weaning. The pattern of nipple use was very similar across litters but very different to that of the better‐studied pig or cat. Puppies showed only weak preference for particular (central) nipple rows, they often switched nipples during nursing sessions and showed no evidence of teat consistency in which each littermate uses primarily one or two particular nipples. They also showed very little agonistic behavior that could be interpreted as contesting access to nipples. The present findings provide a reminder of the diversity of suckling patterns among altricial mammals and of the need for more comparative information to better understand the reasons for and functional significance of such differences.

Private Heat for Public Warmth: How Huddling Shapes Individual Thermogenic Responses of Rabbit Pups

BackgroundWithin 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 FindingsThe 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/SignificanceBy 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.

Differential maturation of the molecular clockwork in the olfactory bulb and suprachiasmatic nucleus of the rabbit

Recent studies suggest that the main olfactory bulb (OB) represents a functional circadian pacemaker. In many altricial mammals, during pre-visual stages of development the olfactory system plays a vital role in their survival. One remarkable example is the European rabbit; the newborns are normally raised in a dark nursery burrow, and the lactating female briefly visits her young approximately once every 24 h. Under these conditions, newborn rabbits depend on the circadian system to anticipate the arrival of the lactating doe as well as on pheromonal cues on the mother's ventrum to locate nipples and suckle efficiently. To investigate the development of the rabbit's circadian system, we characterized the 24-h pattern of expression of clock genes in the OB and suprachiasmatic nucleus (SCN) of pre-visual week-old rabbits and compared this with the pattern of expression in visual juvenile rabbits several weeks after weaning. We report for the first time that Per1, Cry1, and Bmal1 are expressed in the OB of newborn and juvenile rabbits. In addition, the diurnal pattern of clock gene expression develops earlier in the OB than in the SCN of newborn rabbits. Given the early maturation of the molecular clockwork and the biological relevance of this structure during development, it is possible that the OB plays an important role in temporal regulation during pre-visual life in rabbits.