Juvenile Belding's Ground Research Articles

Play behavior and responses to novel situations in juvenile ground squirrels

Play is a characteristic behavior of mammals, occurring among juveniles across a wide range of mammalian species. We evaluated the hypothesis that play helps prepare young animals to cope with unfamiliar situations. We observed play behavior in juvenile Belding's ground squirrels (Urocitellus beldingi) during the developmental period in which play primarily occurs in this species, and conducted behavioral tests in unfamiliar arenas at the beginning and toward the end of the play interval. Measures of social but not nonsocial play were associated with the outcomes of behavioral tests. Rates of social play and the duration of social play bouts were reliable predictors of increases in boldness and exploration across behavioral tests, as well as decreases in the time required to escape from an unfamiliar arena. In particular, juveniles who engaged in social play at intermediate to high rates and who had intermediate to long-lasting social play bouts had greater increases in boldness–exploration scores and greater decreases in escape times in behavioral tests than did juveniles who engaged in social play at the lowest rates and had the shortest social play bouts. These results support the idea that social play behavior in juvenile U. beldingi helps prepare juvenile squirrels to successfully navigate challenges during the juvenile period, and raise the possibility that minimum thresholds of social play may be sufficient for juvenile U. beldingi to gain some of the potential benefits of play behavior.

Alarm calls elicit predator-specific physiological responses

Glucocorticoids regulate glucose concentrations and responses to unpredictable events, while also modulating cognition. Juvenile Belding's ground squirrels (Urocitellus beldingi) learn to respond to whistle and trill alarm calls, warning of aerial and terrestrial predators, respectively, shortly after emerging from natal burrows at one month of age. Alarm calls can cause physiological reactions and arousal, and this arousal, coupled with watching adult responses, might help juveniles learn associations between calls and behavioural responses. I studied whether young show differential cortisol responses to alarm and non-alarm calls, using playbacks of U. beldingi whistles, trills, squeals (a conspecific control vocalization) and silent controls. Trills elicited very high cortisol responses, and, using an individual's response to the silent control as baseline, only their response to a trill was significantly higher than baseline. This cortisol increase would provide glucose for extended vigilance and escape efforts, which is appropriate for evading terrestrial predators which hunt for long periods. Although whistles do not elicit a cortisol response, previous research has shown that they do result in bradycardia, which enhances attention and information processing. This is a novel demonstration of two physiological responses to two alarm calls, each appropriate to the threats represented by the calls.

Functions and consequences of play behaviour in juvenile Belding's ground squirrels

We evaluated hypotheses suggesting that play behaviour in free-living juvenile Belding's ground squirrels, Spermophilus beldingi, helps to regulate energy balance and promotes development of motor skills. We also examined the possibility that play behaviour and motor development influence important early life events in S. beldingi. We regularly measured body fat of juveniles using nondestructive methods, observed their behaviour, conducted motor skills tests, monitored dispersal status of males, and evaluated weaning success of females during their first effort to reproduce as yearlings. Rates of feeding were greater among juveniles who engaged in both social and nonsocial play behaviour at low compared to high rates, suggesting that play does not help young animals expend excess energy that they consume. By contrast, body fat was greater among juveniles who engaged in social play at high compared to low rates, supporting the idea that energetic variables such as body fat limit the expression of play behaviour. Motor skills of juvenile S. beldingi improved throughout the period in which juveniles engaged in play behaviour. Improvement in motor skills was greater in juveniles who engaged in social play at high compared to low rates, suggesting a link between social play and motor development. Motor skill levels at the end of the play period were greater among males who dispersed by the end of the juvenile summer than among males still residing in their natal areas. Rates of social play and improvement in motor skills over the course of the play period were greater in females who successfully weaned a litter as yearling than in females who did not. These last two results raise the possibility that play behaviour and motor development during the play period influence important events in the early lives of S. beldingi, which may ultimately influence long-term reproductive success.

Seasonal effects of food provisioning on body fat, insulin, and corticosterone in free-living juvenile Belding's ground squirrels (Spermophilus beldingi)

We evaluated the relationship between body fat and the metabolic hormones insulin and corticosterone in free-living juvenile Belding's ground squirrels (Spermophilus beldingi). Some free-living juveniles were provisioned with extra food high in fat and calories, and unprovisioned juveniles were used as controls. Body fat (as a percentage of body mass) of squirrels was regularly evaluated using non-invasive methods. Blood samples were also regularly collected from juveniles and assayed for plasma concentrations of insulin and corticosterone. Provisioned juveniles were fatter than unprovisioned juveniles during most of the active season, but differences in body fat disappeared near the end of summer as juveniles began fattening for hibernation. Thus, our data indicate that although body fat may fluctuate with energy availability early in the active season, it is regulated at precise levels as squirrels prepare for winter. Plasma corticosterone concentrations did not differ between provisioned and unprovisioned juveniles. However, plasma insulin concentrations were greater in provisioned than in unprovisioned juveniles early in the summer. Differences in insulin concentrations disappeared later in the active season, just prior to the disappearance of differences in body fat. Moreover, plasma insulin concentrations were significantly correlated with subsequent changes in body fat. Thus, our data suggest a link between insulin and seasonal regulation of body fat in juvenile S. beldingi.

Endocrine and Energetic Mediation of Play Behavior in Free-Living Belding's Ground Squirrels

Many juvenile mammals play, and rates and patterns of play behavior often differ between young males and females. The sexual dimorphisms typical of mammalian play suggest that it might be influenced by gonadal hormones. Moreover, because play competes with growth, physical development, and acquisition of fat reserves for available energy, play behavior should theoretically be influenced by energetic variables. We examined patterns of social play behavior and endocrine and energetic mediation of social play in free-living juvenile Belding's ground squirrels (Spermophilus beldingi). Bouts of social play in young S. beldingi resembled adult copulation and fighting, and young males initiated sexual play but not play fighting at much higher rates than did young females. To elucidate the proximal causes of play, we altered early androgen exposure by treating females with testosterone (T) at birth and used females treated with oil vehicle as controls. We concurrently manipulated energy availability by provisioning with extra food and used unprovisioned squirrels as controls. Hourly rates of play behavior were highest near the time of weaning and declined thereafter among both experimental and control groups of juveniles. Thus, we observed no influence of either T treatment or food provisioning on the temporal patterning of play behavior. Perinatal T treatment had no effect on play fighting, but caused rates of sexual play behavior initiated by young females to increase to near those observed for young males, suggesting that T organizes a masculine tendency to initiate sexual play behavior but not play fighting. Food provisioning increased rates of play among males and females from both T-treated and control litters, suggesting that energy availability limits play behavior.

How mothers influence the development of litter-mate preferences in Belding's ground squirrels

We performed three experiments to examine the role of mothers in the development of litter-mate preferences in captive juvenile Belding's ground squirrels,Spermophilus beldingi. First, when observed in the absence of mothers, juveniles did not play preferentially with litter-mates, which suggests that mothers somehow influence the ontogeny of litter-mate preferences. Second, when mothers were present but unable to intervene in social interactions, juveniles displayed litter-mate preferences, which suggests that mothers do not influence their offsprings’ social development by directly intervening in social interactions. In another group, mothers were removed daily, a few hours before nocturnal immergence, and returned the following morning. Juveniles in this group did not display litter-mate preferences and at night they occupied burrows with many more non-litter-mates than litter-mates. These results suggest that associating with non-litter-mates can compromise the development of litter-mate preferences, and implies that mothers indirectly influence social development by affecting the identities of sleeping partners. Third, newly emergent juveniles that interacted only with litter-mates for 3 days in the absence of mothers subsequently preferred litter-mates over non-litter-mates as play partners. This result demonstrates that once litter-mate preferences are instilled, due in part to social experiences during juveniles’ initial days above-ground, the preferences are expressed even in the absence of mothers. Collectively, the results demonstrate that the presence ofS.beldingimothers is important to juvenile social development, but that mothers do not actively direct the ontogeny of their offsprings’ social relationships.

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.

The development of littermate preferences in juvenile Belding's ground squirrels

Abstract. Kin favouritism has been documented widely in free-living ground squirrels (genus Spermophilus), but the development of kin favouritism has not been explained. To investigate the development of littermate preferences in captive Belding's ground squirrels, S. beldingi, groups composed of four dams and 16 juveniles (young-of-the-year) were observed in outdoor enclosures for a period of 5-11 days, beginning when juveniles first emerged aboveground from natal burrows (buried nestboxes). Social play was the most frequently observed social interaction. Littermates played together about twice as often as non-littermates on a per pair basis and juveniles were also more likely to share a burrow at night with their littermates than non-littermates. Independently of relatedness, the sex of a pair also affected play-bout frequencies (m-m>m-f>f-f), as did body-weight differences between juveniles. It was concluded that juveniles displayed social preferences for littermates shortly after they emerged from natal burrows, which suggests that interactions between littermates prior to or just after emergence affected the development of social preferences. Dams indirectly affected the development of social preferences: when dams were not placed in enclosures littermate preferences were not observed. The results of this study support the hypothesis that kin favouritism develops from early social interactions involving dams and littermates. However, it remains to be determined whether the preferences manifested by recently emerged juveniles are maintained throughout the summer and whether such preferences provide the foundation for kin favouritism in adults.