Female Richardson's Ground Squirrels Research Articles

Call-specific patterns of neural activation in auditory processing of Richardson's ground squirrel alarm calls.

IntroductionRichardson's ground squirrels use alarm calls to warn conspecifics about potential predatory threats. Chirp calls typically indicate high levels of threat from airborne predators, while whistle calls are associated with lower levels of threat from terrestrial predators. These types of calls primarily elicit escape behaviors and increased vigilance in receivers, respectively. While much is known about the neural mechanisms involved in the production of vocalizations, less is known about the mechanisms important for the perception of alarm calls by receivers, and whether changes in perceived risk are associated with unique patterns of neuronal activation. Thus, to determine whether alarm calls associated with different levels of predation risk result in differential neuronal activation, we used immunohistochemistry to identify and quantify c‐Fos immunopositive cells in brain regions important in stress, fear, danger, and reward, following alarm call reception.MethodsWe exposed 29 female Richardson's ground squirrels (10 control, 10 whistle receivers, and 9 chirp receivers) to playbacks of whistles, chirps, or a no‐vocalization control. We then assessed neuronal activation via c‐Fos immunohistochemistry in 12 brain regions.ResultsGround squirrels receiving high‐threat “chirp” vocalizations had reduced neuronal activation in the medial amygdala and superior colliculus compared with controls. It is likely that changes in activity in these brain regions serve to alter the balance between approach and avoidance in turn promoting escape behaviors.ConclusionsThus, we conclude that in Richardson's ground squirrels, these brain regions are important for the perception of risk resulting from receiving alarm calls and allow for appropriate behavioral responses by receivers.

Like mother, like daughter: heritability of female Richardson's ground squirrel Urocitellus richardsonii cortisol stress responses.

Activation of the hypothalamic–pituitary–adrenal (HPA) axis liberates glucocorticoids, which provides an acute indication of an individual’s response to stressors. The heritability of the stress response in wild mammals, however, remains poorly documented. We quantified the cortisol stress response of female Richardson’s ground squirrels (RGSs) to handling and physical restraint, testing for: (1) the effects of individual age, time of day, and sample latency; (2) repeatability within individuals; (3) narrow-sense heritability; and (4) differences among individuals owing to potential genetic and/or environmental effects. We detected a positive linear relationship between baseline plasma cortisol (BL-cortisol) concentration and stress-induced plasma cortisol (SI-cortisol) concentration that defined each individual’s cortisol stress response. BL-cortisol, SI-cortisol, and stress response did not differ according to the time the sample was taken, or by subject age. Cortisol stress response was highly repeatable within individuals, had a mother–offspring heritability of h2 = 0.40 ± 0.24 (mean ± SE), full-sibling heritability of , and half-sibling heritability of . Stress responses of sibling groups, immediate-family groups, and squirrels within a given area did not differ, whereas those of individuals from more distantly related matrilines did. Our results highlight the natural variability in HPA axis reactivity among individuals by quantifying both BL- and SI-cortisol levels, demonstrate partial heritability of the stress response that is not attributable to environmental variation, and suggest that at least part of an individual’s stress response can be accounted for by differences in matrilineal history.

Age‐specific resource investment strategies: evidence from female Richardson's ground squirrels (Spermophilus richardsonii)

AbstractTo avoid a possible cost to their future survival and/or reproduction, individuals must balance their somatic and reproductive investments. The van Noordwijk and De Jong model of resource investment predicts that investments into reproduction and soma can vary among individuals of a population based on the variation in the total amount of energy that individuals acquire. With principal components analysis (PCA), we created two axes of life history for female Richardson's ground squirrels Spermophilus richardsonii: an index of total energy investment (PC1) and an index of investment tactic (PC2). Using these indices, we examined patterns of resource allocation to reproductive and somatic investments. Because yearling female Richardson's ground squirrels complete growth to adult size during pregnancy and early lactation, their somatic needs exceed those of older, fully grown females. Therefore, we predicted that yearlings would show more evidence of a tradeoff between reproductive and somatic investments compared with older females. Both yearling and older females invested four to five times more mass into their litters than into their own body mass. With increasing total investment, yearling females increased investment in both reproduction and themselves, whereas older females invested relatively more in reproduction than themselves. Regardless of age, females that emerged heavier from hibernation invested fewer resources into themselves and more into their litters. Variation in total energy investment and investment tactic indices was similar for yearling and older females. Contrary to our prediction, however, yearling females showed positive associations between reproductive and somatic investments, whereas older females exhibited showed no significant association between reproductive and somatic investments.

Somatic senescence: evidence from female Richardson's ground squirrels

We studied reproductive and somatic investments in >700 female Richardson's ground squirrels (Spermophilusrichardsonii) of known age over a 14‐year period to evaluate three hypotheses, restraint, senescence, and residual reproductive value, proposed to explain age‐specific life history patterns in iteroparous vertebrates. We found that reproductive investment, measured as litter mass at first emergence from the natal nest, did not differ among age classes. Although yearling female Richardson's ground squirrels made a greater somatic investment during reproduction than older females, they produced similar numbers and mass of offspring as older females. Reproductive investment did not decline with age, though active season somatic investment was lowest in the oldest females. Somatic investment during reproduction was highest in yearlings. This combination of age‐related changes in somatic investment unaccompanied by changes in reproductive investment was not well explained by any of the hypotheses examined, though the senescence hypothesis best explained the combination of declining somatic investment and declining survival of the oldest females. Our results supported the ideas that reproductive and somatic senescence evolve independently, and that somatic senescence may be more common in relatively smaller species.

Sexual Differences in Reproductive Effort of Richardson's Ground Squirrels

Male and female Richardson's ground squirrels exhibit differences in a constellation of behavioral, ecological, and physiological characteristics related to a fundamental sexual difference in reproductive effort, viz. males primarily expend energy on mate acquisition whereas females primarily expend energy on parenting. Male Richardson's ground squirrels emerge from hibernation earlier than females, at a heavier body mass, and with larger fat reserves. Once females emerge, males reduce time foraging and they compete aggressively and intensively for access to estrous females with resultant physical wounding, loss of body mass, depletion of fat reserves, and high mortality. Females retain post-hibernation fat reserves during gestation and even increase in personal body mass. Although mass of the litter exceeds the mother's own mass by late lactation, mothers are largely able to meet the demands of milk production through foraging, and their body mass remains fairly constant through lactation. Adult males immerge into hibernation earlier than adult females, and are heavier and fatter on immergence. In their first active season, juvenile males complete growth to adult size, whereas juvenile females attain only 80% of adult size; females then complete growth during pregnancy the following spring. Juvenile males attain adult size by delaying entry into hibernation until 7-9 weeks later than juvenile females. During hibernation, both juvenile and adult male Richardson's ground squirrels spend substantially less time than females in the physiological state of torpor. In particular, males tenninate torpor> I week before emergence, during which time they subsist on seeds cached in the hibernaculum, replenish fat, and initiate spennatogenesis in preparation for the forthcoming mating season. In contrast, female Richardson's ground squirrels do not store food in the hibernaculum, they emerge from hibernation <2 days after termination of torpor, and they are impregnated 2-4 days after' emergence from hibernation when at their lowest annual body mass. On an annual basis, adult females have a higher survival rate than adult males, largely because females are more likely to survive through the reproductive period.

Maternal Traits and Reproduction in Richardson's Ground Squirrels

Differences among conspecifics in body mass result from underlying differences in structural size and physiological condition. To determine whether the structural or physiological component of body mass has a stronger influence on reproductive traits at parturition, we studied the body composition (lean dry mass and fat content), structural size (1st principal component scores computed from 10 skeletal measurements), and body condition (residuals from regression of body mass on structural size) of yearling and older female Richardson's ground squirrels (Spermophilus richardsonii). At parturition, differences among yearlings in body mass primarily reflected differences in structural size associated with continuing structural growth. Older females appeared to reach a deterministic adult structural size, and body mass of older females was most strongly associated with body condition. Structural size of yearling females and body condition of older females had significant positive effects on litter mass. For older females, date of parturition had a significant negative influence on litter size. Both yearling and older females exhibited significant positive effects of parturition date and body condition on neonate mass. In older females, trade—off resulted in smaller litters of heavier neonates as the breeding season progressed, perhaps reflecting the need for rapid growth of offspring before hibernation. Maternal size, maternal condition, and seasonal timing were important aspects of reproduction in Richardson's ground squirrels, but these characteristics are seldom considered concurrently in studies of life histories.

Differential Costs of Reproductive Effort for Male and Female Richardson's Ground Squirrels

The costs of reproductive effort for adult male and female Richardson's ground squirrels were compared to determine whether these costs differed in timing or magnitude in a manner related to sexual differences in mating and parental effort. Reproductive effort was assessed from 1982 to 1986 for a population of Richardson's ground squirrels in southern Alberta, Canada, by monitoring seasonal mortality schedules, fecundity, and changes in body mass and fat content. Although the adult sex ratio was female—biased, the operational sex ratio was male—biased. Males lost mass and sustained injuries as a result of male—male conflict during the mating season. From 50 to 79% of males disappeared annually during reproduction (between spring emergence and the end of the mating season), whereas &lt;20% of females disappeared during reproduction (between spring emergence and litter emergence). Overwinter mortality rates were similar for adult males and females. Active seasons of adult males and females were of similar durations, but because reproductive effort finished earlier for males, they had a longer period in which to prepare for hibernation, and they entered hibernation (immerged) with larger fat stores. Juvenile males had a longer active season and attained a greater proportion of adult structural size than juvenile females (90 vs. 75%). Although males emerged from hibernation with more residual fat than females, fat stores were rapidly depleted during mating 2—4 wk postemergence, whereas females did not deplete residual fat until late lactation 7—8 wk postemergence. Survival rates of females that did and did not wean litters did not differ significantly, and survival rates of mothers were not significantly or negatively correlated with litter size or litter mass. Although litter size tended to regress toward the mean in consecutive years of reproduction, neither size nor mass of litter weaned negatively influenced litter size or mass in the subsequent year. Depletion of larger stored fat reserves and lower survival rate during reproduction indicate that, from both energetic and survival perspectives, mating effort is more costly for male Richardson's ground squirrels than parental effort is for females.

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.

Lipid synthesis and deposition by adult Richardson's ground squirrels in the natural environment.

Adult male Richardson's ground squirrels, Spermophilus richardsonii, were estimated to have emerged from hibernation in late February to early March, and adult females in mid to late March. Half of the females trapped in late March were not pregnant, as against 10% after that time. In late March males and all females had similar WAT (white adipose tissue) deposits. Between late March and early June, WAT deposits in males increased from 14 g to 64 g (a rate of 5.6 g per week). In non-parous females WAT deposits increased from 13 g to 48 g from late March to late May (4.2 g per week). Fat deposits decreased during lactation but thereafter increased from 8 g to 29 g (a rate of 6.0 g per week) between early May and early June. In males the rate of fatty acid synthesis in BAT (brown adipose tissue), liver and WAT did not change from late March to late May, and rates in the corresponding tissues of non-pregnant females were similar to those in males. Fatty acid synthesis decreased during late pregnancy and lactation. After lactation, the rate of fatty acid synthesis in all tissues increased to that in males and non-pregnant females. Males initiated fattening 5-7 weeks earlier than females. It is concluded that compared with adult males, the later immergence of adult female Richardson's ground squirrels into hibernation is due primarily to later initiation of fattening and less to differences in rate of lipid synthesis after the reproductive period. Rates of fatty acid synthesis in liver and BAT were several times greater than that in WAT. The former tissues may contribute fatty acids for prehibernatory fattening.

Chronology of Reproductive Events for Female Richardson's Ground Squirrels

Timing of reproductive events for adult (≥ 1-year old) female Spermophilus rich-ardsonii in southern Alberta was determined from 1979 to 1984 by daily monitoring of squirrels following emergence from hibernation until litters emerged from the natal burrow. Females typically mated 3 to 5 days after emergence from hibernation and gave birth 22 to 23 days later. Juveniles were usually 28 to 30 days old when they first left the natal burrow. Thus most litters (130/175) appeared 53 to 58 days after the mother had emerged from hibernation. The reproductive chronologies of yearling and older females were virtually identical. The 22.5-day gestation period of S. richardsonii is the shortest documented for the genus. Interspecific comparison of reproductive chronologies of ground squirrels indicated that at least five species in the subgenus Spermophilus typically wean litters ca. 8 weeks after the mother's emergence from hibernation, whereas for several species in other subgenera the mother emergence-to-litter emergence interval exceeds 10 weeks.

Kin selection and adult female Richardson's ground squirrels: a test

A population of adult female Richardson's ground squirrels (Spermophilus richardsonii) was experimentally manipulated so that on one half of the study area each of the 9 females had 2 or 3 closely related females (mother, daughter, or littermate sister) as neighbours (the "kin cluster group," KC), while the 10 females on the other half of the area did not have closely related females as contiguous neighbours (the "no kin cluster group," NKC). In the previous year, breeding success and behaviour of females on both halves of the study area were similar. Following the manipulation, KC females spent a greater proportion of their aboveground time feeding, were less vigilant, shared a greater proportion of their core area with their nearest neighbour, were less likely to be involved in interactions that led to chasing and fleeing, and had a much better breeding success compared with females in the NKC group. These results provide a preliminary demonstration that the association of adult female kin to Richardson's ground squirrels can be advantageous, and as such, the observed behavioural asymmetries based upon kinship could be maintained by kin selection.

Differential reproduction among female Richardson's ground squirrels and its relation to sex ratio

The reproductive success of ten female Richardson's ground squirrels resident on a grassland pasture in southern Alberta in 1975 was determined by noting the number of their descendants present in 1976, 1977, and 1978. The two most successful females were the progenitors of 67% of the females resident in 1977 and of 57% of the females resident in 1978. None of the other eight females had descendants in the population in 1978. The two most successful females produced more daughters than did the other females and they did so, not by rearing larger litters, but by producing female-biased litters. The daughters of the two most successful females lived slightly longer than did the daughters of other females. Although the adult sex ratio was strongly female biased each breeding season, ranging between 0.26 and 0.42 males per female, typically all females became pregnant. Adult female offspring inherited their mother's home range and, if the mother or any female sibs were present, shared this area with them. Sons rarely remained resident in or near the natal area and adult males rarely remained resident in the same area for two consecutive years. Thus, post-weaning investments were greater in daughters than in sons. There were no conclusive correlations between sex ratio of litters and size of litters, age of the mother, previous reproductive success of the mother, population density, or the length of the overwinter period. More studies spanning several generations are required to elucidate the effects of the sex ratio of litters on the likelihood of an animal being represented by descendants in subsequent generations.

Field observations on the social relationships between adult female and juvenile Richardson's ground squirrels

Field observations were conducted in southern Saskatchewan in 1969 and 1971. Adult female Richardson's ground squirrels and their own young engaged predominantly in nasal and cohesive contacts while adults and young from other litters engaged predominantly in agonistic contacts. Identification sometimes occurred at a distance based on the location and behavior of the other animal.Newly emerged juveniles remained close to the home burrow and engaged mainly in non-agonistic interactions with both their mothers and other adults. Not until juveniles were 6–7 weeks old and were familiar with the area used by the mother did they correctly identify adults regardless of where the interaction occurred.

Social behavior between adult female Richardson's ground squirrels (Spermophilus richardsonii) and their own and alien young

Adult female Richardson's ground squirrels were paired at intervals with their own and unrelated young in a neutral cage. Little agonistic behavior occurred between related animals but such behavior was common when the adult and young were unrelated. Conversely, cohesive behavior was common between related animals but not between unrelated animals. A tendency for the adults to treat male and female young differently was noted. With only four exceptions (out of 48 tests) the first contact between adult and young was neutral, nose–nose being most common. The frequency of neutral behavior declined on the second contact and remained at the lower level. Implications of the study with regard to recognition, dispersal, and territory learning are discussed.