Female Columbian Ground Squirrels Research Articles

Born with an advantage: early life and maternal effects on fitness in female ground squirrels.

Lifetime fitness and its determinants are an important topic in the study of behavioral ecology and life-history evolution. Early life conditions comprise some of these determinants, warranting further investigation into their impact. In some mammals, babies born lighter tend to have lower life expectancy than those born heavier, and some of these life-history traits are passed on to offspring, with lighter-born females giving birth to lighter offspring. We investigated how weight at weaning, the relative timing of birth in the season, maternal weight, and maternal age affected the longevity and lifetime reproductive success (LRS) of female Columbian ground squirrels (Urocitellus columbianus). We hypothesized that early life conditions such as offspring weight would not only have lifetime fitness consequences but also intergenerational effects. We found that weight at weaning had a significant impact on longevity, with heavier individuals living longer. The relative timing of an individual's birth did not have a significant association with either longevity or LRS. Individuals born to heavier mothers were found to have significantly higher LRS than those born to lighter mothers. Finally, maternal age was found to be significantly associated with their offspring's LRS, with older mothers having less successful offspring. Our results provide evidence that early life conditions do have lifelong fitness and sometimes intergenerational consequences for Columbian ground squirrels.

Phenotypic plasticity in reproductive and somatic efforts of female Columbian ground squirrels

Phenotypic plasticity of life-history traits is well known among vertebrate species. We estimated reproductive and somatic efforts of female Columbian ground squirrels ( Urocitellus columbianus (Ord, 1815)) to test for plasticity of these important resource allocations. We examined a 27-year dataset of life-history traits on these long-living (8–10 years), hibernating, montane-living mammals. Environmental variation was estimated from two important traits of mothers, their relative timing of breeding and spring maternal body mass (initial “capital” for use in subsequent reproduction). Results from 183 known-aged mothers and 508 litters revealed considerable variation in the relative timing of breeding, initial maternal mass, and reproductive and somatic efforts, as well as significant variation among ages and years. Results from 125 mothers that reproduced more than once (and 450 litters) revealed significant plasticity of reproductive and somatic efforts with respect to relative timing of breeding and spring maternal mass. A within-subject centering statistical approach showed that phenotypically plastic reproductive and somatic efforts were due to variation within individuals, but were not always reflected by the pattern of responses among individuals in the population. The plastic responses of different mothers appeared to be similar in strength.

Telomere dynamics in female Columbian ground squirrels: recovery after emergence and loss after reproduction.

Telomeres are specialized non-coding DNA sequences locatedat the end of chromosomesand that protect genetic information. Telomere loss over lifespan is generally viewed as a phenomenon associated with aging in animals. Recently, telomere elongation after hibernation has been described in several mammals. Whether this pattern is an adaptation to repair DNA damage caused during rewarming from torpor or if it coevolved as a mechanism to promote somatic maintenance in preparation for the upcoming reproductive effort remains unclear. In a longitudinal study measuring telomere length using buccal swabs, we tested if telomere elongation was related to reproductive success in wild adult female Columbian ground squirrels (Urocitellus columbianus) that were monitored from emergence from hibernation to the end of the reproductive season. We found three key results. First, female telomere length increased at the start of the breeding season, both in breeding and non-breeding individuals. Second, post-emergence telomere lengthening was unrelated to female future reproductive output. Third, telomere length decreased in breeding females during lactation, but remained stable in non-breeding females over a similar period. Within breeders, telomeres shortened more in females producing larger and heavier litters. We concluded that telomere lengthening after hibernation did not constrain immediate female reproductive capacities. It was more likely to be part of the body recovery process that takes place after hibernation. Telomere erosion that occurs after birth may constitute a physiological cost of female reproduction.

Territorial scent-marking effects on vigilance behavior, space use, and stress in female Columbian ground squirrels

Social environments can profoundly affect the behavior and stress physiology of group-living animals. In many territorial species, territory owners advertise territorial boundaries to conspecifics by scent marking. Several studies have investigated the information that scent marks convey about donors' characteristics (e.g., dominance, age, sex, reproductive status), but less is known about whether scents affect the behavior and stress of recipients. We experimentally tested the hypothesis that scent marking may be a potent source of social stress in territorial species. We tested this hypothesis for Columbian ground squirrels (Urocitellus columbianus) during lactation, when territorial females defend individual nest-burrows against conspecifics. We exposed lactating females, on their territory, to the scent of other lactating females. Scents were either from unfamiliar females, kin relatives (a mother, daughter, or sister), or their own scent (control condition). We expected females to react strongly to novel scents from other females on their territory, displaying increased vigilance, and higher cortisol levels, indicative of behavioral and physiological stress. We further expected females to be more sensitive to unfamiliar female scents than to kin scents, given the matrilineal social structure of this species and known fitness benefits of co-breeding in female kin groups. Females were highly sensitive to intruder (both unfamiliar and kin) scents, but not to their own scent. Surprisingly, females reacted more strongly to the scent of close kin than to the scent of unfamiliar females. Vigilance behavior increased sharply in the presence of scents; this increase was more marked for kin than unfamiliar female scents, and was mirrored by a marked 131% increase in free plasma cortisol levels in the presence of kin (but not unfamiliar female) scents. Among kin scents, lactating females were more vigilant to the scent of sisters of equal age, but showed a marked 318% increase in plasma free cortisol levels in response to the scent of older and more dominant mothers. These results suggest that scent marks convey detailed information on the identity of intruders, directly affecting the stress axis of territory holders.

Social stress in female Columbian ground squirrels: density-independent effects of kin contribute to variation in fecal glucocorticoid metabolites

Social interactions among conspecifics can have marked effects on individual physiology, especially through their modulation of the stress axis by affecting the production of adrenal glucocorticoids (GCs). Previous research has focused on how individual GC levels may be influenced by social status, but few studies have considered how the balance between positive (e.g. cooperation) and negative (e.g. competition) social interactions shape individual GC levels. A lack of association between individual GC levels and social factors may be confounded by opposite effects of social competition on the one hand and social cooperation on the other. We tested for these effects in the Columbian ground squirrel (Urocitellus columbianus), a colonial rodent. During the breeding season, females are exposed to territorial unrelated neighbors and to territorial, but more tolerant, close kin. On one hand, territoriality and competition for resources led us to predict a positive association between local colony density and female GC levels. On the other, higher tolerance of philopatric kin females and known fitness benefits led us to predict a negative association between kin numbers and female GC levels. We compared levels of fecal cortisol metabolites (FCMs) in females at two different spatial scales during lactation: local (a female’s core territory during lactation, 30-m radius about her nest burrow) and colony-wide. At the local scale, female FCM levels were neither related to colony density nor to the number of co-breeding female kin, but FCM levels increased with age. At the colony scale, female FCM levels varied in a quadratic fashion with female kin numbers. FCM levels decreased by 15% from 0 to 1 co-breeding kin present and increased with > 1 kin present. Among females that had only one co-breeding kin present, daughters (and littermate sisters and mothers, but not significantly) led to a 14% reduction in FCM levels compared with females that had no kin. Our results reject the idea that local colony density is associated with increased GC levels this species, but indicate subtle (positive and negative) effects of kin on individual GC secretion. They further call into question the importance of the nature of social relationships in modulating the stress experienced by individuals. Few studies have tested how the balance between positive (e.g. cooperation) and negative (e.g. competition) social interactions shapes individual stress and glucocorticoid (GC) levels in group-living animals. In colonial Columbian ground squirrels, breeding females are exposed to territorial neighbors and to more tolerant close kin. We show that kin numbers have subtle (positive and negative) effects on female GC levels. Compared with breeding females with no kin, female GC levels decrease by 15% with the presence of a single co-breeding close relative, but increase with the presence of more than one co-breeding related female. Among females that have only one co-breeding kin, the presence of daughters (and littermate sisters and mothers, but not significantly) leads to a 14% reduction in female GC levels. Our results highlight how GC levels may be influenced by the specific nature of social relationships in group-living animals.

Testing the reproductive and somatic trade-off in female Columbian ground squirrels.

Energetic trade‐offs in resource allocation form the basis of life‐history theory, which predicts that reproductive allocation in a given season should negatively affect future reproduction or individual survival. We examined how allocation of resources differed between successful and unsuccessful breeding female Columbian ground squirrels to discern any effects of resource allocation on reproductive and somatic efforts. We compared the survival rates, subsequent reprodction, and mass gain of successful breeders (females that successfully weaned young) and unsuccessful breeders (females that failed to give birth or wean young) and investigated “carryover” effects to the next year. Starting capital was an important factor influencing whether successful reproduction was initiated or not, as females with the lowest spring emergence masses did not give birth to a litter in that year. Females that were successful and unsuccessful at breeding in one year, however, were equally likely to be successful breeders in the next year and at very similar litter sizes. Although successful and unsuccessful breeding females showed no difference in over winter survival, females that failed to wean a litter gained additional mass during the season when they failed. The next year, those females had increased energy “capital” in the spring, leading to larger litter sizes. Columbian ground squirrels appear to act as income breeders that also rely on stored capital to increase their propensity for future reproduction. Failed breeders in one year “prepare” for future reproduction by accumulating additional mass, which is “carried over” to the subsequent reproductive season.

Ectoparasites and fitness of female Columbian ground squirrels.

Parasites play an important role in the evolution of host traits via natural selection, coevolution and sexually selected ornaments used in mate choice. These evolutionary scenarios assume fitness costs for hosts. To test this assumption, we conducted an ectoparasite removal experiment in free-living Columbian ground squirrels (Urocittelus columbianus) in four populations over three years. Adult females were randomly chosen to be either experimentally treated with anti-parasite treatments (spot-on solution and flea powder, N = 61) or a sham treatment (control, N = 44). We expected that experimental females would show better body condition, increased reproductive success and enhanced survival. Contrary to our expectations, body mass was not significantly different between treatments at mating, birth of litter or weaning of young. Further, neither number nor size of young at weaning differed significantly between the two treatments. Survival to the next spring for adult females and juveniles was not significantly different between experimental and control treatments. Finally, annual fitness was not affected by the treatments. We concluded that females and their offspring were able compensate for the presence of ectoparasites, suggesting little or no fitness costs of parasites for females in the different colonies and during the years of our experiments.

Scream of Death: Responses of Female Columbian Ground Squirrels to Anti-Infanticide Pup Distress Calls

Parents sometimes discriminate offspring from non-offspring while responding to vocalizations, ensuring that parental care is directed towards their progeny exclusively. This discrimination may result from differences in acoustic characteristics across individuals. However, recognition capabilities specific to individuals may not occur when parents differentiate offspring via location because litters are segregated spatially. Offspring discrimination is important during “distress calls” emitted by young-of-the-year for imminent danger because mothers that respond to non-offspring reduce the time available for protecting their litter, and failure to respond may result in offspring mortality. Columbian ground squirrel (Spermophilus columbianus) pups sometimes emit a scream-like distress call near their mothers when attacked by marauding conspecifics. With field observations of infanticide and playback experiments that manipulated the identity and location of the caller, I examined whether a location-based rule or vocal recognition per se mediate female responses to distress calls. Mothers became vigilant and approached the speaker in response to playbacks of distress calls broadcast on their territory, regardless of whether the recording was an offspring or non-offspring. However, mothers approached distress call recordings originating on their territory more often than those occurring on adjacent territories. Thus, female Columbian ground squirrels respond to distress calls based on a location-based rule (viz., on or off their territory) rather than true vocal recognition. This strategy seems appropriate, since lactating females are territorial and pups rarely mix between litters during the 1–5 day period just after emergence from their natal burrow when they are susceptible to infanticide.

Variation in reproductive success of male and female Columbian ground squirrels (Urocitellus columbianus)

The imbalanced reproductive success of polygynous mammals results in sexual selection on male traits like body size. Males and females might have more balanced reproductive success under polygynandry, where both sexes mate multiply. Using 4 years of microsatellite DNA analyses of paternity and known maternity, we investigated variation in reproductive success of Columbian ground squirrels, Urocitellus columbianus (Ord, 1815); a species with multiple mating by both sexes and multiple paternity of litters. We asked whether male reproductive success was more variable than that of females under this mating system. The overall percentage of confirmed paternity was 61.4% of 339 offspring. The mean rate of multiple paternity in litters with known fathers was 72.4% (n = 29 litters). Estimated mean reproductive success of males (10.27 offspring) was about thrice that of females (3.11 offspring). Even after this difference was taken into account statistically, males were about three times as variable in reproductive success as females (coefficients of variation = 77.84% and 26.74%, respectively). The Bateman gradient (regression slope of offspring production on number of successful mates) was significantly greater for males (βM = 1.44) than females (βF = 0.28). Thus, under a polygynandrous mating system, males exhibited greater variation in reproductive success than females.

Kin selection in Columbian ground squirrels: direct and indirect fitness benefits

Empirical and theoretical studies have supported kin selection by demonstrating nepotism or modelling its conditions and consequences. As an alternative, we previously found that female Columbian ground squirrels had greater direct fitness when more close kin were present. Extending those results, we used population matrix methods to calculate minimum estimates of individual fitness, estimated direct and indirect components of fitness, estimated inclusive fitness by adding the direct fitness (stripped of estimated influences of the social environment) and indirect fitness components together, and finally looked for inclusive fitness benefits of associations with close kin who seem to be 'genial neighbours'. We examined the estimated fitness of a sample of 35 females for which complete lifetimes were known for themselves, their mothers and their littermate sisters. Six of these females had no cosurviving adult close kin, and their direct fitness was significantly lower than 29 females with such kin (λ = 0.66 vs. λ = 1.23). The net fitness benefit of the presence of close kin was thus 0.57. The estimated indirect component of fitness through benefits to the direct fitness of close kin was 0.43. Thus, estimated inclusive fitness for females with cosurviving close kin (λ = 1.09) was significantly greater than that for females without surviving close kin (viz., λ = 0.66). The presence of closely related and philopatric female kin appeared to result in considerable fitness benefits for female ground squirrels, perhaps through the behavioural mechanisms of lowered aggression and other forms of behavioural cooperation.

Scent communication by female Columbian ground squirrels, Urocitellus columbianus

Scent-marking is a frequent behaviour of highly social ground squirrels and might play an important role in their social dynamics. Female Columbian ground squirrels exhibit considerable scent-marking during the reproductive period. We examined how gestating and lactating females responded to jugal gland scent-marks of same-sexed and opposite-sexed conspecifics with attention to genetic relatedness and the geographical location of the territory of individuals. We tested the dear-enemy, threat-level and kin-discrimination hypotheses to explain patterns of scent-marking. Females sniffed the scent of non-neighbouring males significantly longer than other types of scent categories and tended to over mark the scent of females more than the scent of males. Furthermore, females sniffed significantly longer at scents during gestation than during lactation. We concluded that scent-marking mainly functioned in the defence of female territories and for protection of pups against infanticidal females (threat-level hypothesis). Our results were also in accordance with the kin-discrimination hypothesis, because greater attention was paid to the marks of non-kin females. Kin females might not pose an infanticidal threat, perhaps explaining greater tolerance among related reproductive females. We concluded that scent-marking may be a relatively low-cost means of territorial defence, as well as a means of communication of aspects of individual identity.

Why do female Columbian ground squirrels (Spermophilus columbianus) give an estrus call?

Female Columbian ground squirrels ( Spermophilus columbianus (Ord, 1815)) sometimes emit a repetitive vocalization after copulation. We examined two possible explanations for why sexual selection would favor expression of these “estrus calls”: to encourage sperm competition through mating with additional males and to increase mate guarding by the consort male as a mechanism of postcopulatory female mate choice. During three annual mating periods, we observed mating behaviour, estrus calls, and postcopulatory behavioural interactions of free-ranging individuals. Predictions of the advertisement hypothesis were supported, as females typically solicited courtship interactions with nonconsort males directly after emitting an estrus call. Thus, females that emitted an estrus call were more likely to acquire additional matings than noncalling females, particularly if calls were emitted after the female’s first mating. These results were not consistent with predictions of the postcopulatory female mate choice hypothesis, as calling females should initiate social contact with the consort male and stay proximate to the copulatory site after copulation if they are encouraging mate guarding. For reasons that remain unclear, the probability that an estrus call would follow mating increased linearly with the age of the consort male. However, our results taken together suggest that estrus advertisement is the most likely social context of female postcopulatory calling.

Previous Experience and Reproductive Investment of Female Columbian Ground Squirrels

Reproductive success of females in iteroparous species usually increases early in life, then remains constant or declines. The restraint hypothesis suggests that primiparous females limit their 1st reproduction in order to avoid future costs to survival, reproduction, or both, whereas constraint indicates that primiparous females are limited in their 1st reproductive attempt either because they lack sufficient resources (measured by body mass) or lack experience at weaning a litter. To evaluate these alternatives, we examined age- and experience-related patterns of reproduction in female Columbian ground squirrels (Spermophilus columbianus) with data from a long-term study and by experimentally altering age at 1st reproduction. In the results of the long-term study, experienced females had significantly higher reproductive investment and reproductive success (number of offspring surviving to yearling age) compared to inexperienced females. Annual survival of females was not affected by their level of previous weaning experience or current reproductive investment. Additionally, subsequent reproductive success was not impaired by earlier reproduction. In the experimental results, experienced females had significantly higher reproductive investments compared to inexperienced females. Constraint in terms of previous weaning experience best explained the differences in reproductive investment and reproductive success between primiparous and multiparous females.

Causes and consequences of sex-biased dispersal in Columbian ground squirrel, Spermophilus columbianus

AbstractDispersal is a fundamental process with wide ranging evolutionary consequences. In birds and mammals, members of one sex typically disperse more frequently, sooner and/or further than members of the other sex. The aim of this study was to examine factors affecting dispersal by yearling male and female Columbian ground squirrels (Spermophilus columbianus), and to determine whether inbreeding avoidance, competition or other factors can explain why inter-colony dispersal is more common in males than in females. Males who stayed in their natal colony as adults emerged as yearlings heavier and later from hibernation than males who disappeared in their yearling year, whereas for females, this was not the case. Males who had sisters emerging as yearlings in the same colony were not more likely to leave the colony than males who were alone or with brothers. Further, there was no significant difference in the probability that females would mate with an immigrant compared to a natal male. Finally, three-year-old males who stayed in the colony moved significantly further away from their natal burrow than females of the same age.I conclude that sex differences in inter-colony dispersal, while promoting outbreeding, are not directly due to inbreeding avoidance, but that inbreeding avoidance may play a role in governing intra-colony dispersal distances. Further, resource competition seems to play a minor role. Aggression by adults against yearling males and the acceptance of yearling females by their mothers may be the proximate cause for male bias in inter-colony dispersal in Columbian ground squirrels. To conclusively demonstrate this effect, however, we need to look at aggression in more detail.

The effects of capital on an income breeder: evidence from female Columbian ground squirrels

To maximize fitness, organisms must optimally allocate resources to reproduction, daily metabolic maintenance, and survival. We examined multiple years of live-trapping and observational data from a known-aged population of female Columbian ground squirrels, Spermophilus columbianus (Ord, 1815), to determine the influences of stored resources and daily resource income on the reproductive investments of females. We predicted that because yearling females were not fully grown structurally while producing their first litter, they would rely exclusively on income for reproduction, while reproductive investment in older females (≥2 years of age) would be influenced by both stored resources (capital) and daily income. Results from path analysis indicated that both yearlings and older females were income breeders. However, initial capital indirectly influenced investment in reproduction of yearling and older females. Females with the greatest initial capital maintained high body masses while investing relatively more income in reproduction. By considering influences of both capital and income, important relationships can be revealed between these resources and their influence on life histories.

Age of primiparity and implications of early reproduction on life history in female Columbian ground squirrels

Summary Factors leading to differences in age of primiparity and possible life‐history implications arising from these differences were studied in a population of Columbian ground squirrels (Spermophilus columbianus; Ord, 1815). We used data collected from 1992 to 2000 on two neighbouring colonies of ground squirrels in south‐eastern Alberta, Canada. Earlier born females were more likely to wean successfully a litter at the age of 2. Among 2‐year‐old females, those who emerged earlier and heavier from hibernation were more likely to wean offspring than those females who emerged later and lighter from hibernation. The presence of the mother had a significant positive impact on reproductive output in 2‐year‐old females. Although there was a positive correlation between lifetime reproductive success and age at death, there was no difference in lifetime reproductive success or in age at death, depending on age of primiparity. For individual females, litter size at weaning at 2 years old did not differ from that at 3 years old. We conclude that body condition, presence or absence of the mother and environmental conditions are the main factors leading to differences in age of first successful reproduction in Columbian ground squirrels. Previous breeding experience does not seem to play a role in determining reproductive success. Finally, differences in age of first successful reproduction do not seem to have an effect on lifetime reproductive success or longevity.

Senescence and age‐related reproduction of female Columbian ground squirrels

Summary Three hypotheses have been proposed to explain age‐structured patterns of reproductive investment and somatic investment: residual reproductive value, senescence and evolutionary restraint. We evaluated these hypotheses for female Columbian ground squirrels (Spermophilus columbianus) by examining age‐related patterns of somatic and reproductive investment. Females were designated as successful (those that weaned litters) and unsuccessful (those that did not wean litters). Somatic investment varied among both successful and unsuccessful females of different ages, with yearlings having the highest investment. Considering all females, reproductive investment varied among age classes with yearlings and the oldest (6–9‐year‐olds) having the lowest investments. However, when only successful females were considered, reproductive investment was lowest in the yearlings and not significantly different among older females. The highest proportion of successful females occurred in the middle adult age classes, while yearlings and the oldest females displayed the lowest proportion of successful females. During the breeding season, somatic investments of successful and unsuccessful females differed significantly only in the yearling age class, with unsuccessful females having the highest investment. Evolutionary restraint or constraint explained patterns of reproduction in the yearling age class, where both reproductive investment and proportion of reproductive females were low. There was evidence for senescence of reproduction by some of the oldest females.

Mortality in relation to season, age, sex, and reproduction in Columbian ground squirrels (Spermophilus columbianus)

We investigated the timing of and age at mortality in Columbian ground squirrels (Spermophilus columbianus) in relation to sex and reproductive status. Life-history data were collected from 1994 to 1999 in the foothills of the Rocky Mountains, Alberta, Canada. We predicted increased mortality for males during mating and for females during lactation. Further, we expected reproductively successful females to have higher mortality than females that did not reproduce successfully. Finally we assumed that at some age reproductive success of females would decrease and mortality increase because of old age. For both sexes, survival over winter was high (ca. 90%) for adults. While there was a significant increase in mortality of adult males during the mating season, females did not have higher mortality during lactation than during the rest of the active season. Reproductive status influenced mortality in females: non-reproducing females had a higher chance of surviving than reproducing females. Females that weaned young were more likely to die after the weaning period than females that lost their litter during lactation. There was a positive correlation between maternal survival and survival of offspring to yearling age. Our results showed evidence of trade-offs between reproduction and survival of male and female Columbian ground squirrels.

Timing of Hibernation and Molt in Female Columbian Ground Squirrels

Timing of Hibernation and Molt in Female Columbian Ground Squirrels

Effect of brief exposure to a potential predator on cortisol concentrations in female Columbian ground squirrels (Spermophilus columbianus)

We examined the effect of exposure to a potential predator on cortisol concentrations in captive female Columbian ground squirrels (Spermophilus columbianus) and determined if lactation mitigated this cortisol response. Lactating and nonlactating females were exposed to a dog (Canis familiaris) for 5 min once a week over a 8-week period. Blood was collected 5 min and 2.5 and 4.5 h after exposure to the dog. Females exposed to the dog had higher concentrations of total (but not free) cortisol than unexposed females only in the 5-min blood sample. Over the active season, total- and free-cortisol levels were 37-47% higher in females exposed to the dog than in unexposed females in early to mid-July when young were being weaned. The cortisol response to the dog was suppressed during lactation. Cortisol levels were, on average, 41-59% lower during lactation than during nonlactation 5 min (but not 2.5 or 4.5 h) after exposure to the dog.