Natal Emergence Research Articles

Early predictors of female lifetime reproductive success in a solitary hibernator: evidence for "silver spoon" effect.

Fitness consequences of early-life conditions remain unclear and poorly studied in mammals. Based on long-term observations of yellow ground squirrels (Spermophilus fulvus), we identified early determinants of female fitness by analyzing the effects of early-life individual and environmental characteristics (weaning weight, weight gain rate, date of natal emergence, natal litter size, location of the natal burrow, local density of juveniles, population density and precipitation in the post-weaning period) on lifetime reproductive success (LRS). We found high variation and right-skewed distribution in all five LRS components (survival to adulthood, adult lifespan, and lifetime numbers of weaned litters, weanlings, and yearling offspring). Numbers of litters, weanlings, and adult offspring were correlated with each other and increased with lifespan, confirming that longevity is a better predictor of LRS than fecundity. Survival to adulthood was the most sensitive fitness component to early conditions and was higher in females (a) with greater weaning weight, (b) born further from human settlement and (c) born at lower population density. Population density at birth was the best early predictor of all LRS components and negatively influenced adult lifespan and numbers of weanlings and yearling offspring. Early growth rate positively affected the probability of reproducing after the first hibernation and the number of offspring weaned. Such syndrome of high-quality (heavy and fast-growing) young born in a favourable environment ("a silver spoon effect") with downstream damping fitness consequences has been observed so far in only a few mammalian species.

Developmental patterns and body fat content of juvenile common hamsters (Cricetus cricetus l.)

Abstract The common hamster (Cricetus cricetus) is a facultative hibernator producing up to three litters per year. Juveniles born late in the season have less time to grow and prepare for the winter than early-born ones. We investigated a free-ranging population in an urban environment in Vienna, Austria. We compared body mass, proportion of body fat, as well as head, tibia and hind foot length between juveniles of first and second litters at natal emergence, four weeks post-emergence and shortly before onset of hibernation. In addition we tested for differences in growth rates during the first four weeks after emergence and for potential effects of sex and litter size. Capture-mark-recapture techniques were applied. Body fat content was calculated using a multiple regression model integrating morphometric parameters. At natal emergence, second litter offspring were larger and heavier than those of first litters. Litter size did not account for these differences. During the first week after natal emergence, first litter pups gained body mass faster, and during the first two weeks also showed faster head and tibia growth rates than second litter pups. Four weeks after natal emergence, however, second litter juveniles were still larger and heavier than first litter ones. Body fat content four weeks post-emergence did not differ between first and second litters but decreased with litter size. Shortly before onset of hibernation, however, first litter juveniles, which had more time to grow and accumulate body fat, exceeded second-litter ones in all measured parameters. In all litters investigated, we found no sex difference at natal emergence but males were heavier and larger than females four weeks thereafter demonstrating that the commonly known sexual dimorphism in this species developed during this period. Considering the time constraints late born juveniles face, the con ditional advance at natal emergence is assumed to be adaptive by increasing the chances for these individuals to survive overwinter despite the limited time to prepare for the hibernation period

Effects of birth date and natal dispersal on faecal glucocorticoid concentrations in juvenile Common hamsters

In seasonally breeding animals, timing of reproduction in females can influence offspring development and survival. Temporal and energetic constraints are often more pronounced in juveniles born late in the season, and could activate the stress axis. Common hamsters (Cricetus cricetus) are hibernating rodents, and adult females produce up to three litters during the active season. Birth dates range from May to September, and shortly after natal emergence pups are weaned and start to disperse. In this study, we used faecal cortisol metabolites (FCM) as a non-invasive measure of recent glucocorticoid exposure. We compared FCM levels between early- (June/July) and late- (August/September) born juvenile Common hamsters during their first weeks after natal emergence. We further compared FCM levels in juveniles born in the study area and individuals that immigrated either early or late in the season. Additionally, we investigated potential effects of human disturbances on cortisol secretion patterns. FCM levels in late-born juveniles increased during the first weeks post-emergence and were significantly higher than those in early-born individuals during the post-weaning period. Late-immigrating juveniles had significantly higher FCM levels than early immigrants and residents during the same time period. Individuals that inhabited areas frequently used by humans had higher FCM levels than those in low-impact areas. These results indicate that the seasonal timing of birth and dispersal affect cortisol secretion patterns in juvenile Common hamsters. As all juveniles immerged into their hibernacula during early October, we assume that late-born and late-immigrated individuals have less time to prepare for hibernation. This could elevate energetic demands and increase exposure to predators and/or humans during food caching. These factors might lead to increased adrenal activity and thus, elevated FCM concentrations in these individuals. Potential consequences of these time constraints and associated physiological effects could be reflected in the lower overwinter survival rates of juveniles born late in the season.

The causal role of odours in the development of recognition templates and social preferences

Despite decades of theoretical interest in the role of kin recognition in mate choice and nepotism, data on both the mechanisms and functions of recognition are available for only a few species. Even less common are demonstrations of direct causal links between the production and perceptual components of recognition and subsequent social preferences. Belding's ground squirrels, Spermophilus beldingi, produce odours that vary with kinship and can be used to discriminate classes of kin. However, the links between odours, recognition templates and differential treatment of conspecifics have not been shown empirically. Here I examined whether the manipulation of odour recognition templates influences juvenile behaviours. I induced recognition errors by exposing young to odours from a foreign mother before natal emergence. According to phenotype-matching mechanisms, developing young should incorporate all encountered odours into their kin template and later treat individuals matching the template as kin. As in previous studies, the most preferred play partners were littermates, but young also interacted preferentially with juveniles from the foreign family, whose odours were similar to the foreign mother and therefore matched their templates, compared with unfamiliar, unrelated juveniles. This preference for juveniles of the foreign family could not be due to relatedness or direct familiarity prior to emergence. Patterns of nasal investigations mirrored those of play bouts. This is a novel demonstration of a causal link between recognition cues, recognition templates and ‘kin’-differentiated behaviours, and highlights the potency of social odours during development on later social dynamics.

Inverted-U shape relationship between cortisol and learning in ground squirrels

Adrenal hormones regulate glucose levels, responses to unpredictable stressors and modulate cognition. Glucocorticoids can have an inverted-U shape relationship with cognition, as very low or high levels impair, whereas moderate elevations facilitate, acquisition and retention of memories. To date these relationships have been tested with humans and rodents in laboratory settings rather than with wild animals in biologically relevant contexts. This study examined whether the elevated cortisol observed in juvenile Belding’s ground squirrels ( Spermophilus beldingi) at natal emergence might promote both acquisition of adaptive responses to this species’ two alarm calls warning of predators and memory of the spatial configuration of mothers’ territories. Both experimentally increased and decreased basal cortisol levels interfere with acquisition and retention of an association between a warning call and the appropriate response compared with naturally occurring moderately elevated cortisol. Further, decreased cortisol impairs learning of a novel, complex spatial maze. Thus in the field the brief elevation of cortisol at emergence might facilitate acquisition of spatial memory of a three-dimensional environment and responses to alarm calls during a sensitive period of learning. This novel demonstration of the inverted-U shape function in a wild animal suggests that natural selection has favored a hormonal profile facilitating rapid acquisition of important survival behaviors.

Effects of nutritional factors on juvenile development in male European ground squirrels ( Spermophilus citellus)

In European ground squirrels ( Spermophilus citellus) as in other obligate hibernators, physiological processes underlie strict time constraints. Especially for the juveniles growth and prehibernatory fattening are temporally very limited. The aim of this study was to determine the effects of specific nutritional factors on development in juvenile males. Male ground squirrels were investigated for a 7-week period starting at natal emergence. Individuals were assigned to 1 of 3 experimental groups and were provided with a diet either high in proteins or polyunsaturated fatty acids (PUFAs). The third group was used as a control and was fed with a standard rat diet. Food quality affected growth in that males of the high-protein group had significantly larger head lengths in week 4, 5, and 6 after natal emergence than those of the other 2 groups. However, body mass did not differ significantly between the groups. All juvenile males showed an increase in plasma testosterone levels from week 1–2 to week 3–4 post-emergence, thereafter testosterone secretion remained stable until week 5–6. The daily testosterone increase after the first 2 weeks was significantly higher in the PUFA group compared to the other 2 groups. The results underline the importance of diet composition for growth rates and the timing of gonadal activation during early development in this species.

Development of individually distinct recognition cues

Despite extensive research on the functions of kin recognition, little is known about ontogenetic changes in the cues mediating such recognition. In Belding's ground squirrels, Spermophilus beldingi, secretions from oral glands are both individually distinct and kin distinct, and function in social recognition across many contexts. Behavioral studies of recognition and kin preferences suggest that these cues may change across development, particularly around the time of weaning and emergence from natal burrows (around 25 days of age). I used an habituation-discrimination task with captive S. beldingi, presenting subjects with odors collected from a pair of pups at several ages across early development. I found that at 21 days of age, but not at 7 or 14, young produce detectable odors. Odors are not individually distinct, however, until 28 days of age, after young have emerged from their burrows and begun foraging. In addition, an individual's odor continues to develop after emergence: odors produced by an individual at 20 and 40 days of age are perceived as dissimilar, yet odors produced at 28 and 40 days are treated as similar. Developmental changes in odors provide a proximate explanation for why S. beldingi littermate preferences are not consolidated until after natal emergence, and demonstrate that conspecifics must update their recognition templates as young develop.

The adaptive utility of Richardson’s ground squirrel (Spermophilus richardsonii) short-range ultrasonic alarm signals

Richardson’s ground squirrels ( Spermophilus richardsonii (Sabine, 1822)) produce audible (ca. 8 kHz) and (or) ultrasonic (ca. 48 kHz) alarm vocalizations that warn conspecifics of impending danger. Audible calls have a larger active space than ultrasonic calls because they travel farther, are louder, and contain frequencies to which conspecific and allospecific recipients are more sensitive. In our first experiment, we presented an alarming stimulus to 103 squirrels to examine the effect of threat proximity on signal type. The ratio of ultrasonic to audible alarm calls increased with increasing distance from the stimulus. We conclude that the size of the active space influences signalling strategy and that squirrels emitting ultrasonic calls can signal conspecifics to the exclusion of distant predators. As recipients of ultrasonic calls must be close to the signaler, one context in which ultrasonic calling may be most adaptive is during natal emergence when juveniles are particularly abundant, highly vulnerable to predation, and clustered in space. In our second experiment, we broadcast ultrasonic alarm signals to emerging juveniles and found that they, like older individuals, responded to calls by increasing vigilance. We discuss the adaptive utility of multiple signalling strategies in light of our findings.

Developmental and geographic variation in stress hormones in wild Belding's ground squirrels ( Spermophilus beldingi)

Extensive research has been conducted on the role of glucocorticoids in regulating growth, mobilizing energy, responding to stressors and modulating learning and memory. However, little is known about the production of corticoids during early development in free-living animals, particularly during sensitive periods of acquisition of important behaviors. In a four-year study of Belding's ground squirrels, Spermophilus beldingi, a non-invasive assay of glucocorticoids was used to quantify age and population differences among juveniles from three California locations. Fecal–cortisol metabolites are elevated during a short period when juveniles first emerge aboveground from their natal burrows at about 4 weeks of age. This period of cortisol elevation coincides with when young are learning survival behaviors such as anti-predator responses and foraging strategies. Population differences in juvenile cortisol levels, which may reflect local variation in habitat quality and predator environments, were not evident until 2 weeks after emergence. Elevated cortisol at the age of emergence was also observed in juveniles born and reared in captivity without exposure to typical stressors that occur around the age of emergence. These results indicate that corticoids are regulated during early development, and the possible functions of age-related corticoid levels are discussed, including mobilization of glucose for natal emergence and later facilitation of growth and energy storage during the short summer before hibernation. In some species, elevated corticoids can also facilitate learning and memory, and current work is exploring whether the higher cortisol observed in all three S. beldingi populations just after emergence function to promote rapid acquisition of survival behaviors.

Endocrine profiles and reproductive output in European ground squirrels after unilateral ovariectomy

In the course of a long-term study on reproductive physiology and behaviour in female European ground squirrels ( Spermophilus citellus) we investigated interactions among reproductive timing, maternal effort and hibernation. To gain information on the state of follicular development shortly before hibernation, histological investigations of ovaries were carried out. To collect the ovaries, unilateral ovariectomy was chosen as the least invasive method. The aim of this study was to monitor patterns of hormone secretion, behavioural parameters and reproductive output in females after unilateral ovariectomy, and compare them with intact individuals to assess potential effects of the treatment. Reproductive performance including duration of gestation and lactation, litter size, and offspring mass at natal emergence were similar in treated and untreated individuals. Before weaning, plasma estradiol levels were higher in the hemicastrated group than in intact females. Progesterone concentrations tended to be lower in unilaterally ovariectomized females during gestation and postlactation. In both groups we measured cortisol metabolites in fecal samples to estimate basal adrenal activity. Untreated individuals had significantly higher cortisol levels than hemicastrated females during lactation. In all other phases no significant differences in patterns of cortisol excretion were found between the two groups. Prehibernatory body-mass did not differ between treated and untreated females. These results indicate that unilateral ovariectomy had no significant negative effects on reproductive timing and output in female European ground squirrels. Compensatory activity of the remaining ovary does occur, concerning estradiol secretion even a kind of overcompensation was reported. These elevated estradiol levels in unilaterally ovariectomized females could play a role in limiting the degree of follicular compensation.

Paternal effort and its relation to mating success in the European ground squirrel

The necessity for parental care is a driving force for determining mating systems and social organization. The European ground squirrel, Spermophilus citellus, is a polygynous, gregarious species in which male parental behaviour would not be expected. We had observed males digging in litter burrows that were later occupied by females and their offspring. Males never stayed overnight within these burrows. To determine whether this was some kind of paternal effort we tested the following hypotheses: (1) that male burrowing behaviour was directed towards the male's own offspring or towards the pregnant or lactating mother of the male's offspring; (2) that this behaviour had costs in terms of condition, decreased survival or fecundity; and (3) that it benefited offspring condition or survival. All three assumptions were met. Males worked on the litter burrow of their copulatory partners. Thus, this behaviour was directed towards the male's potential offspring. Male burrowing costs were seen in decreased foraging time and increased body mass loss. Offspring benefits were evident in increased mass at natal emergence. We conclude that male digging at litter burrows can be considered as paternal effort. Lastly, we considered the effects of polygyny on this male parental effort by comparing mating effort, mating success and paternal effort. High mating success was associated with high mating effort and low paternal effort. Moderate to low mating success was associated with lower mating effort and higher paternal effort, indicating a trade-off between the two.

Explaining the seasonal decline in litter size in European ground squirrels

In European ground squirrels Spermophilus citellus as in many ground squirrel species, late born litters are composed of fewer young than early born litters. Two alternative though not mutually exclusive hypotheses may explain this seasonal pattern of change in litter size. On the one hand, the production of few large young late in the season may be an adaptation to time limitations on the offspring, that have to complete growth and fattening prior to hibernation. Then one would expect a trade‐off between offspring number and size as the breeding season progresses. At its extreme, this hypothesis would predict that total maternal effort should be equal independent of litter size. Alternatively, litter size may be determined by physiological limitations on the mother, in that highly constrained mothers breed later and produce smaller litters. Then one would expect reduced overall maternal effort in highly constrained mothers of smaller litters. In this case, a trade‐off between litter size and offspring size would not be expected. We found that total maternal effort in terms of gestation length and the duration of lactation increased with increasing litter size, thus supporting the second hypothesis. Lactation was not terminated at natal emergence. It extended a relatively long period of time beyond the time of first litter emergence depending on litter size. During prolonged lactation, individual young of large litters made up body mass to young of small litters. As a consequence, juvenile weaning body mass was unaffected by litter size although offspring body mass at natal emergence was inversely related to litter size. This additional weight gain in young of large litters compensated for initial survival disadvantages and presumably affected fecundity at yearling age.

Temporal aspects in the development of Belding's ground squirrels’ litter-mate preferences

Four experiments were conducted to determine how experience around the time of natal emergence affected the development of litter-mate preferences in juvenile Belding's ground squirrels,Spermophilus beldingiSocial preferences were ascertained by observing six captive groups, each housed in outdoor enclosures beginning at natal emergence, and recording the frequency of dyadic play. Juveniles preferred their litter-mates as play partners on day 1 above-ground, demonstrating that pre-emergent interactions influenced social development. Whether cross-fostered young displayed play-partner preferences based on relatedness and rearing history depended on when young were exchanged with respect to natal emergence, which suggests that social development is especially sensitive to experience shortly before natal emergence. Juveniles do not display litter-mate preferences if they emerge into an environment from which dams have been removed, but in the present study, if juveniles interacted for 1 week before dams were withdrawn from enclosures, then litter-mate preferences were manifested both before and after dams were withdrawn. These results suggest that a foundation for litter-mate preferences is laid before natal emergence, and that preferences are solidified by interactions between litter-mates on their first few days above-ground. Finally, non-litter-mates that interacted with each other shortly after natal emergence were preferred social partners during later encounters compared with non-litter-mates denied the opportunity to interact shortly after emergence. Collectively, the four experiments demonstrate that social experience around the time of natal emergence is crucial to the developmental process that generates litter-mate preferences inS.beldingi1997 The Association for the Study of Animal Behaviour

The development of alarm-call response behaviour in free-living juvenile Belding's ground squirrels

The production of and responses to alarm calls by adult ground-dwelling squirrels has been widely documented, yet the development of alarm-call behaviours has not been systematically addressed. The responses of free-living Belding's ground squirrels,Spermophilus beldingi, to playbacks of conspecific (three alarm calls and juvenile squeals) and heterospecific (wren song) vocalizations were observed from natal emergence until the age of dispersal. Discrimination of the five auditory stimuli was not present at emergence but developed within the next 5 days, with responsivity to whistle alarm calls, indicative of fast-moving predators, developing earlier than to trill alarm calls, associated with slow-moving predators. Response patterns (response duration, vigilant postures and initial responses) changed throughout the following 4 weeks, and approximated adult responses before juveniles dispersed. Juvenile responses were indirectly influenced by conspecifics, particularly the dam, as well as by the physical environment, including distance from the natal burrow and location within the meadow. Alarm-call responses appeared to be adapted to the juvenile's current stage of development, with younger juveniles making a trade-off between information gathering and escape responses. The development of appropriate responses to each alarm call is hypothesized to be facilitated by observations of experienced ground-squirrels' responses. Despite their vulnerability, juveniles may not emerge with fully formed associations between alarm calls and responses if the local predator context changes over time, thus favouring plasticity in the response repertoire.

Early auditory experience and the ontogeny of alarm-call discrimination in Belding's ground squirrels (Spermophilus beldingi).

Because young ground squirrels are vulnerable to predation, selection would favor the early ability to respond to alarm calls. This requires discrimination of classes of alarm calls from each other as well as from non-alarm calls. Pre-emergent auditory experience may influence the development of discrimination. As a means of determining when Belding's ground squirrels (Spermophilus beldingi) can discriminate among calls, cardiac responses to alarm calls and control stimuli were recorded from 2 rearing groups that differed in the frequency of alarm-call exposure. Results suggest that before natal emergence, young can discriminate between 2 classes of alarm calls but they may not discriminate these calls from control stimuli. No differences in responses were found between the rearing groups; thus experience with calls may not influence the onset of discrimination. Early discrimination may facilitate the rapid development of post-emergent behavioral alarm-call responses.

Reproductive effort during gestation and lactation by Richardson's ground squirrels.

Reproductive effort by yearling and older female Richardson's ground squirrels was studied over a 4-year period in southern Alberta by obtaining serial weight records from marked individuals to compare the mother's mass at critical points in the annual cycle (emergence from hibernation, estrus, parturition, and litter emergence) with her litter's mass at birth and weaning. Yearlings weighed only 80% of older adults at emergence from hibernation, but they mated at the same time as older females, attained adult mass coincident with pregnancy, and weaned litters that were not significantly smaller in size or mass than those of older females. Age and maternal mass were weak predictors of litter size and litter mass. Of the net increase in mass of the combined mother-litter unit during gestation, over half (60% of 139 g for yearlings; 52% of 127 g for older females) was attributable to an increase in the mother's own mass, whereas during lactation almost all of the net increase (93% of 545 g for yearlings; 96% of 567 g for older females) was attributable to an increase in the litter's mass. On a daily basis, deposition of mass in the litter was 6 times greater during lactation than gestation. On average, neonates weighed 2.3% (6.5 g) of maternal mass at birth and 23.1% (81 g) at emergence from the natal burrow; offspring masses at birth and at emergence were significantly negatively correlated with litter size. On average, litters weighed 16.3% (48 g) of maternal mass at birth and 157.5% (578 g) at emergence from the natal burrow. Compared with other hibernating sciurids, Richardson's ground squirrels have a similar offspring mass relative to maternal mass both at birth and at emergence from the natal burrow. However, because of the large litter size (typically 6-8), absolute reproductive effort, measured either as litter mass at birth or at natal emergence, is large for the body size of the species.