Thermal versus tactile stimuli and audible vocalization in rat pups

The influences of thermal and tactile stimuli on the audible vocalization in pup rats,Rattus norvegicus were investigated. Mother rats and their litters were exposed to ambient temperature (AT) depression by 5°C for 2 hours every other day from 3 to 11 days postpartum. Nearly all audible calls emitted by pups were recorded during tactile contact with the mother. AT depression alone neither prolonged the total duration of pup-licking by mother nor intensified audible vocalization. It was found, however, that the frequency (No./h.) of nest exiting by the dam doubled during the cooling and that the sum of audible peeps emitted by cooled pups in 4 cooling days was higher than sum of peeps emitted by the control pups. This difference is apparently related to an increase in the mother's motor activity, especially nest-building activity, during cooling. Analysis of circumstances accompanying peep emission supports the hypothesis that the tactile stimuli delivered by mother play the predominant role in causing audible vocalization in pup rats. This investigation was supported by Project CPBP-04.01. of the Polish Academy of Science     

Prolactin levels and maternal behavior induced by ultrasonic vocalizations of the rat pup.

The relationship among ultrasonic vocalization (USV), prolactin and maternal behavior was investigated in lactating rat mothers and their pups. The lactating mother had a cannula inserted into the external jugular vein, and was exposed to USVs emitted from a pup immediately. Changes of prolactin and maternal behavior were determined. Prolactin increased dramatically during exposure to USVs, when maternal search, retrieving and nest building behavior appeared significantly. These results suggested that the relationship among USV, prolactin and maternal behavior was included in communication between lactating mother and pup.     

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.     

Dopamine receptor D2 deficiency reduces mouse pup ultrasonic vocalizations and maternal responsiveness

Dopamine signalling facilitates motivated behaviours, and the D2 dopamine receptor (D2R) is important in mother–infant interactions. D2R antagonists disrupt maternal behaviour and, in isolated rat pups, reduce ultrasonic vocalizations (USVs) that promote maternal interaction. Here, we examined the effects of genetic D2R signalling deficiency on pup‐dam interaction with Drd2 knockout (D2R KO) mice. Using heterozygous (HET) cross littermates, the effect of pup genotype on isolation‐induced USVs was quantified. Independent of parental genotype, D2R‐deficient pups emitted fewer USVs than wild type (WT) littermates in a gene dose‐dependent manner. Using reciprocal D2R KO‐WT crosses, we examined how parental genotype affects pup USVs. Heterozygous pups from D2R KO dams produced fewer USVs than HET pups from WT dams. Also, exposure to USV‐emitting pups increased plasma prolactin levels in WT dams but not in D2R KO dams, and KO dams showed delayed pup retrieval and nest building. These findings indicate the importance of the interaction between pup and dam genotypes on behaviour and further support the role of D2R signalling in maternal care.     

VOCAL INDIVIDUALITY IN MOTHER AND PUP SOUTH AMERICAN FUR SEALS, ARCTOCEPHALUS AUSTRALIS

South American fur seals breeding in Peru are subjected to levels of maternal aggression, and subsequent pup mortality, that are higher than has been reported for any other otariid species. For mothers and pups to maintain contact with each other, a mutual recognition system should exist to facilitate reunion and avoid misdirection of maternal effort. We recorded vocalizations of mothers and pups at Punta San Juan, Peru, during the 1994 and 1995 breeding seasons. Sixteen acoustic variables were measured from a total of 560 calls from 15 mothers and 13 pups. Multivariate analysis showed that calls were variable in several acoustic dimensions. While calls of both mothers and pups showed low variability within and high variability among individuals, mothers' calls were more individualistic. On average, discriminant-function analysis correctly assigned 60% of pup calls and 70% of mother calls to the individual that produced them. Characteristics of the fundamental frequency were most important for distinguishing among mothers, while pup calls, which typically contained less harmonic structure, could be differentiated by formant-like frequency ranges. Thus, calls of mother and pup South American fur seals appear to exhibit sufficient stereotypy to allow for recognition and discrimination among individuals.     

How mothers find their pups in a colony of Antarctic fur seals

In Antarctic fur seals, Arctocephalus gazella, mothers must identify their own young among hundreds or even thousands of pups, if they are to invest in their own offspring and avoid misdirecting their parental care. When returning to their breeding colony from a foraging trip of several days at sea, mothers have to find and identify their young before suckling can occur. There appears to be little confusion about which pup belongs to a mother, and adoption is absent or rare. Using behavioral observations, we investigated the means by which female Antarctic fur seals identified their pups in a breeding colony of about 750 mother-pup pairs on Kerguelen Island. We evaluated the importance of vision, scent communication, vocalizations, and rendezvous locations as possible explanations of how mothers find their pups. Every pup that a mother examined, whether her own or not, exchanged naso-nasal inspection with her, suggesting a strong role for olfactory communication in individual recognition. Both mothers and pups called to each other, and mothers that searched for pups over a longer period gave more calls and encountered more pups. Thus, vocalizations may have been used to attract pups that might be offspring. Nursing usually occurred in the same place from the end of one maternal visit to the colony and the arrival at the beginning of the next visit, suggesting that nursing locations may serve as a meeting place, or rendezvous, for mothers and pups. These results suggest that finding pups is a two-stage process for females, in which pups for sampling are attracted by calls or examined at the previous nursing location, and then individual identification is made by olfactory cues.     

ATYPICAL PUP REARING STRATEGIES BY SEA OTTERS

Eight tagged sea otter (Enhydra lutris) pups in central Prince William Sound, Alaska, weighed 6–15 kg at the time of separation from their mother. Four pups weighing 15 kg were able to forage successfully on their own. Three pups weighing ≤9 kg had negligible chances of survival and apparently were abandoned by sick females. Abandonment of a pup may reduce the burden on a sick female, enabling recovery and subsequent reproduction. One of the three sick females that abandoned a pup in this study recovered and pupped again. Abandonment of pups should occur most often in populations where females are stressed by poor food resources. Reassociation with a previous offspring, as observed once in this study, also may occur most frequently in food-limited populations where reproductive failures are most common and pup survivorship is significantly increased by additional maternal assistance.     

Preclinical Reproductive and Developmental Toxicity Profile of a Glycine Transporter Type 1 (Glyt1) Inhibitor

Bitopertin is a glycine type 1 (GlyT1) inhibitor intended for the treatment of psychiatric disorders. The principle adverse effect in the regulatory reproductive toxicity studies was peri‐natal pup death when rat dams were treated during parturition at a dose resulting in five‐times the human therapeutic exposure (AUC). Cessation of dosing two days before parturition prevented the pup deaths. Investigatory experiments and pharmacokinetic modelling suggested that the neonatal mortality was related to transplacental passage of bitopertin leading to high systemic levels in the newborn pups. Brain levels of bitopertin in the rat fetus and neonate were two‐fold higher than in the mother. As illustrated by knock‐out mice models, GlyT1 function is essential for neonatal pup survival in rodents, but is not necessary for normal prenatal morphological development. The glycine transport systems are immature at birth in the rat, but are functionally well‐developed in the human newborn. While the relevance to humans of the neonatal mortality seen in rats following late gestational exposure is unknown, bitopertin would not be recommended for use during late pregnancy unless the anticipated benefit for the mother outweighs the potential risk to the newborn.     

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.     

Within-litter variance in rat maternal behaviour

As a first step in determining the influence of maternal behaviour on sibling behavioural variance, we tested whether rat mothers differentially interact with neonates within the same litter. We also tested whether fading of an ink-mark on individual pups could provide an index of within-litter variance in maternal licking in laboratory rats. In Study 1, during the first postnatal week we distinguished individual Sprague-Dawley rat pups across 4 litters by placing an ink-mark on the skin and quantified variance in maternal licking frequency toward each pup and compared fading of individual pup marks to the frequency of maternal licks received and to four pup characteristics that could influence mark-fading. In Study 2, neonate mark-fading (a proxy for maternal licking) was compared to adolescent and adult offspring behaviour across 8 litters. Results indicated that: (1) there are substantial and consistent differences in how much rat mothers lick same-sex siblings within a litter, (2) differential licking rates can be documented with a non-observational method (ink-mark-fading), and (3) within-litter variance in maternal behaviour may relate to sibling behavioural variance. The findings indicate a viable research model for future experimental studies on causes and consequences of differential maternal investment within families.     

Sensory processes in the discrimination of pups by female mice (Mus musculus)

Maternal pup retrieval by house mice (Mus musculus) was studied in an investigation of sensory processes in the discrimination of ‘own’ from ‘alien’ pups. In a control condition, mothers were able to discriminate their own from alien young. This ability seemed to be based on olfactory cues, while visual and auditory cues did not seem to be involved. Furthermore, it is suggested that retrieval consists of: elicitation (probably mediated by auditory cues); location of the pup (auditory and olfactory cues); and recognition of the pup (initially olfactory cues, with subsequent gustatory and tactile cues).     

Dog Pups’ Attractiveness to Humans Peaks at Weaning Age

The domestic dog (Canis lupus familiaris) is characterized by greatly reduced parenting investment compared with the wild type wolf (C. l. lupus) from which it is descended. Unlike wolf pups, which are reared by both parents into their second year of life, dog pups are abandoned by their mother at weaning around eight weeks of age. This relatively small parental involvement may contribute to the high pup mortality observed in dogs not living as pets. We hypothesized that people would find dog pups most attractive around weaning age when conspecific parental care is significantly reduced and pup mortality rate is high. Younger and older pups would benefit less from human intervention because in the former case the mother is providing care, and in the latter their survival is already compromised. To test this hypothesis, 51 participants rated the attractiveness of 39 black and white headshot photographs presented on a computer screen of dog pups from three breeds (Jack Russell Terrier, Cane Corso, and White Shepherd), from birth to 7 months old. In line with our hypothesis, attractiveness of Cane Corsos peaked at 6.3 weeks of age; Jack Russell Terriers’ attractiveness peaked at 7.7 weeks; and White Shepherds were most attractive at 8.3 weeks. There were also differences in attractiveness between the breeds, with Cane Corsos rated less attractive than the other two breeds. If this attractiveness motivates humans to care for the dog pups and thereby improves pup survival, this could confer significant advantages to dogs, and may contribute to our understanding of the process of domestication.     

Maternal buffering of stress response in free‐ranging Pacific harbor seal pups in Alaska

We examined the effects of maternal buffering in free‐ranging Pacific harbor seal pups during capture and handling research procedures. We predicted that pups held with their mother would benefit from social buffering and exhibit lower cortisol concentrations resulting from capture and handling than dependent pups caught without their mothers and weaned pups. We expected that pups captured with their mother that experienced a short separation would exhibit increased stress‐induced vocal behavior and activity level compared to dependent weaned pups caught alone. The results showed that the presence of the mother significantly buffered the stress response, as measured by reduced serum cortisol concentrations, in pups captured with their mothers as compared to dependent pups captured alone. Cortisol concentrations of mothers with pups initially were higher than nonlactating females, then diminished. Pups showed a significantly higher rate of vocalization soon after maternal separation compared to single pups separated for a longer period of time. Newly separated pups, especially males, showed a high level of activity compared to the other pups. The results provide unique quantitative evidence of the physiology underlying the maternal‐pup bond in a marine mammal, and the role that maternal buffering may play on the stress response of the offspring.     

Mechanisms of Change in the Ontogeny of Black-tailed Prairie Dog Time Budgets

This study examines the behavioral mechanisms underlying changes in the time allocation patterns of black-tailed prairie dog (Sciuridae: Cynomys ludovicianus) pups. Previous analyses of time budgets had revealed substantial differences between pups (young of the year) and adults, and that pup time budgets changed significantly over time. This paper shows that these differences were due to two mechanisms: pups generally differed from adults in the frequency of performance of different behaviors; however, changes in pup behavior over time were due to changes in both bout frequencies and durations. Other influences on bout durations were also examined. Time of day dramatically affected the duration of most behaviors, with vigilance bouts longest in the morning and feeding bouts longest in the evening. The presence of a pup's mother above ground and the height of the vegetation a pup was in had much less influence on bout durations. Multiple regression analyses were used to identify other potential influences (e.g., weather and social conditions) on bout lengths. Of these, the distance of a pup from the nearest burrow produced the strongest relationships.     

Offspring kidnapping with subsequent shared nursing in Antarctic fur seals

Non-offspring maternal care should be common in phocids, but their occurrence would be uncommon among otariids due to the high costs of raising offspring, particularly lactation, and an efficient recognition system that allow for accurate recognition during the frequent mother–pup re-associations. However, non-offspring maternal care has been documented in some otariid species. While the phenomenon in general is not novel among the colonially breeding seals, the exclusive care to a single pup by two lactating females for an extended time is a behavior scarcely documented in natural population. In an extension of this allonursing care, we document the first case of the kidnapping of a pup with subsequent shared nursing in Antarctic fur seal including data on the effect of this interaction on the pup’s growth. While all other lactating females nursed exclusively their own pups, the shared nursing was advantageous for the pup because he grew noticeably larger (in weight and axillary girth) than other of his cohort, particularly after 50 days. This advantage would have been influenced by the asynchrony of the foraging cycle of the biological and foster mother, which resulted in a higher attendance on shore than any other male pups. Although several explanations have been hypothesized for allolactation in mammals, our observations suggest a misguided parental care, associated with recognition errors by the foster mother whose pup was stillborn.     

Accumbal dopamine function in postpartum rats that were raised without their mothers

Postpartum rats that had been previously raised in an artificial rearing (AR) apparatus, without their mothers or siblings during the preweaning period, show altered maternal responses towards their own offspring in adulthood. In mother-reared (MR) rats, nucleus accumbens (NAC) dopamine (DA) responses to pups evoke a robust sustained rise during the postpartum period and following treatment with estrogen/progesterone parturient-like hormones (Afonso et al., 2009). These MR females had siblings that received AR rearing with varying amounts of preweaning tactile stimulation (ARmin; ARmax). The present study examined NACshell DA responses to pup and food stimuli in these AR rats, and statistically compared them to their MR siblings. Microdialysis samples were collected from adult (90 days postnatal) AR females in different parity states (cycling vs. postpartum, Exp. 1), or after ovariectomy with different hormone treatments (sham vs. hormone, Exp. 2. After basal sample collection, pup and then food stimuli were individually presented to the females in the dialysis chamber. As with their MR siblings, basal DA concentrations were lower and pup-evoked DA responses greater in hormonally-primed AR females than in non-primed AR controls. Compared to their postpartum MR sisters (Exp. 1), AR rats had increased basal DA levels, reduced pup related DA elevations, and disrupted maternal behavior. The postpartum AR impairment in pup-evoked DA was reversed by additional pre-weaning tactile stimulation. Exogenous hormones (Exp. 2) eliminated AR impairments on pup-evoked DA responses. Although MR and AR siblings had comparable DA responses to food stimuli, upon reanalyzing MR data it was found that only postpartum dams had DA responses to pups greater than to food. These data suggest that that the hormonally induced suppression of basal DA levels may reflect saliency of pups which was greater in MR than in AR dams. Preweaning tactile stimulation could partially reverse these effects only in naturally cycling or parturient animals.     

Accumbal dopamine function in postpartum rats that were raised without their mothers

Postpartum rats that had been previously raised in an artificial rearing (AR) apparatus, without their mothers or siblings during the preweaning period, show altered maternal responses towards their own offspring in adulthood. In mother-reared (MR) rats, nucleus accumbens (NAC) dopamine (DA) responses to pups evoke a robust sustained rise during the postpartum period and following treatment with estrogen/progesterone parturient-like hormones (Afonso et al., 2009). These MR females had siblings that received AR rearing with varying amounts of preweaning tactile stimulation (ARmin; ARmax). The present study examined NACshell DA responses to pup and food stimuli in these AR rats, and statistically compared them to their MR siblings. Microdialysis samples were collected from adult (90 days postnatal) AR females in different parity states (cycling vs. postpartum, Exp. 1), or after ovariectomy with different hormone treatments (sham vs. hormone, Exp. 2. After basal sample collection, pup and then food stimuli were individually presented to the females in the dialysis chamber. As with their MR siblings, basal DA concentrations were lower and pup-evoked DA responses greater in hormonally-primed AR females than in non-primed AR controls. Compared to their postpartum MR sisters (Exp. 1), AR rats had increased basal DA levels, reduced pup related DA elevations, and disrupted maternal behavior. The postpartum AR impairment in pup-evoked DA was reversed by additional pre-weaning tactile stimulation. Exogenous hormones (Exp. 2) eliminated AR impairments on pup-evoked DA responses. Although MR and AR siblings had comparable DA responses to food stimuli, upon reanalyzing MR data it was found that only postpartum dams had DA responses to pups greater than to food. These data suggest that that the hormonally induced suppression of basal DA levels may reflect saliency of pups which was greater in MR than in AR dams. Preweaning tactile stimulation could partially reverse these effects only in naturally cycling or parturient animals.     

Behavioral budgets of captive sea otter mother–pup pairs during pup development

Instantaneous sampling of eight behavior categories for a captive mother sea otter (Enhydra lutris) and her four pups was conducted continuously during the first three months following each pup's birth. Initially, pup-grooming and rest occupied the largest proportion of the mother's time. Despite a steady decline in the amount of time the mother spent pup-grooming, the mother continued to groom the pup a substantial amount of time three months after the pup's birth. The proportion of time the mother spent resting, self-grooming, or swimming did not change significantly over the study period, suggesting that these behaviors are important to the mother's self-maintenance. The newborn pups' behaviors were initially limited to rest, active, and nursing, with large proportions of time spent resting and nursing. A significant increase in self-grooming occurred regularly by week 2, followed by increases in swimming (week 3), diving (week 6), and feeding (week 7). Three months after birth, the pups' behavior budgets were similar to their mother, with the exception that pups self-groomed substantially less than their mother self-groomed. The lower proportion of pup self-grooming may be due to the continued close proximity to their mother in captivity, which afforded extended association, and allowed the mother to continue to perform this complex behavior for the pup. © 1993 Wiley-Liss, Inc.     

Paternal behavior increases testosterone levels in offspring of the California mouse

Paternal care during early development influences pup survivorship in the monogamous and biparental California mouse, Peromyscus californicus. Moreover, paternal pup retrievals impact development of adult offspring aggression and the neuropeptide vasopressin, yet little is known about the underlying mechanisms of these developmental changes. Because testosterone can increase arginine vasopressin and aggression, we hypothesized that paternal pup retrievals increase testosterone levels in prepubertal male P. californicus pups. Male pups were assigned to one of three groups: hormonal baseline, nonretrieval control, or retrieval. On postnatal days 18-21, all pups and the mother were removed from the cage, and the focal male pup was placed either outside of the nest to elicit paternal retrievals (retrieval group) or in the nest to discourage paternal retrievals (nonretrieval group). Testosterone was elevated at 45-min, but not 90-min, post-manipulation in retrieved compared to nonretrieved pups. Moreover, there was a significant positive correlation between pup retrievals and testosterone in the 45-min group. This rapid testosterone rise in response to paternal retrievals may facilitate an increase in aggression and vasopressin in adult offspring. Therefore, this period of development previously viewed as hormonally quiescent may be more active in response to paternal behavior than previously thought.     

Endogenous 24-hour cycle of core temperature and oxygen consumption in week-old Zucker rat pups

Summary Experiments were designed to test whether or not the 24-h core temperature fluctuations in week-old rat pups are of endogenous origin. Lean (Fa/-) Zucker rat pups born on the same day to mothers maintained in two different colonies with light/dark cycles 12 h out of phase with each other were mother-reared through the first 3–4 days of life and then artificially reared simultaneously in constant dim light. Continuous, automatic measurement of core temperature and oxygen consumption during artificial rearing showed clear 24-h rhythms in 5- to 8-day-old pups. Each rhythm reached a daily minimum at a time corresponding to the beginning of the light period in the colony of origin. The amplitude of these rhythms did not diminish during artificial rearing, nor did the phase difference between the rhythms of pups originating in the two colonies systematically change. The persistent 12-h phase differences between these two groups of pups prove that the observed rhythms are not caused by exogenous stimuli. We conclude that the rat pup possesses an endogenous time-keeping mechanism that permits the expression of overt rhythmicity at the age of 1 week.Abbreviations Tc core temperature - LD-pups born to a mother entrained to a 7:00 to 19:00 light cycle, then artificially reared in constant dim light - DL-pups born to a mother entrained to a 19:00 to 7:00 light cycle, then artificially reared in constant dim light - SCN suprachiasmatic nucleus