Weight comparisons and litter size manipulation in Columbian ground squirrels (Spermophilus columbianus) show evidence of costs of reproduction

I studied reproductive costs in the female Columbian ground squirrel (Spermophilus columbianus) using individually marked animals. I compared weight changes during the active season and over winter, and mortality for females that did and did not wean young. Females raising young were heavier at emergence in that spring than unsuccessful ones. Females that did not raise young gained more weight during summer, were heavier than successful females at the time of entry into hibernation, and were heavier emerging from hibernation the following spring. Over-winter mortality was higher for females that reared young compared to reproductively unsuccessful females. A food supplementation experiment showed that energy-rich food can accelerate individuals’ weight gain. Interactions between litter size, birth weight, weight at emergence from the natal burrow, survival of young to yearling age, and maternal fitness were also studied. Litter sizes were experimentally manipulated to evaluate how females cope with costs of rearing one additional young. Birth weight of juveniles was positively correlated with survival to emergence from the natal burrow and with survival to yearling age. Partial litter loss was higher in experimentally enlarged litters than in either experimentally decreased or control litters. Total litter loss, survival of adult females or the probability of weaning young the following year were not affected by the litter size manipulation. Females appear to adjust the size of their litter before birth, and to some extent during lactation, to their ability to wean young. Received: 20 January 2000 / Received in revised form: 12 March 2000 / Accepted: 18 March 2000     

Inheritance of nest sites in female Columbian ground squirrels

Summary Home ranges, areas of intensive use, and locations of nest sites were determined for female Columbian ground squirrels and their daughters over seven years from a low-density population in southwestern Alberta. Adult females usually retained similar home ranges from year to year. However, they moved their nest sites more often than expected in years when a yearling daughter was present. Core areas and centres of activity also changed when the nest site was moved. Most daughters settled on their natal areas. The relinquishing of nest sites by females to their daughters is seen as a form of parental investment.     

Natal dispersal in Belding's ground squirrels (Spermophilus beldingi)

Summary Dispersal from the natal site was documented in two populations of Belding's ground squirrels (Spermophilus beldingi) living at different altitudes in the Sierra Nevada of North America. Distance dispersed and age at dispersal were monitored by a combination of observation, trapping, radio telemetry, and examination of road kills. Dispersal was sexually dimorphic in both populations (Tables 1 and 2). All surviving males emigrated before they were 55 weeks of age, with most dispersing midway through the juvenile summer (Fig. 1). By contrast, most females remained within the boundaries of their mothers' home range (Fig. 2 and 3). Those very few females that did emigrate moved distances from their natal burrows similar to those travelled by dispersing males (200–450 m; Table 2), but females tended to disperse at a slightly older age. Significant differences between the study populations were found in distances moved by juveniles of both sexes (Fig. 2). Body weights of juvenile male dispersers were significantly greater than were those of juvenile males of equivilent ages that had not yet dispersed (Fig. 4). The results were considered in light of Shields' (1982) discussion of dispersal and inbreeding. I concluded that if dispersal is related to reproductive success, then dispersal distances selected for use in tests of evolutionary hypotheses should be measured just prior to the subject animals' first reproduction. Finally, although not tested in the present study, the evolutionary hypothesis most consistent with my data suggests that dispersal in S. beldingi may function to minimize nuclear family incest.     

Sibling recognition in Richardson's ground squirrels (Spermophilus richardsonii)

Summary Young from 10 litters of Richardson's ground squirrels were crossfostered within 24 h of birth. Litters, composed then of uterine-sibs and fostered non-sibs, were caged together until 37 days of age (1 week after weaning), at which time the juveniles were separated and caged individually. At a mean age of 110 d squirrels were tested for recognition during 10-min trials in an arena using the following pair-types: sibs reared together (SRT), sibs reared apart (SRA), non-sibs reared together (NSRT), and non-sibs reared apart (NSRA). Juvenile S. richardsonii displayed an ability, determined prenatally or soon after birth, to recognize their biological siblings. Familiarity, based upon association before and at the time of weaning, also affected discrimination between conspecifics, although this effect was less apparent.     

The association of female kin in the arctic ground squirrel Spermophilus parryii

Summary The association of kin in arctic ground squirrels (Spermophilus parryii) was studied near Haines Junction, Yukon Territory, during the summers of 1977, 1978, and 1979. Males dispersed in this population, thus only females were likely to live near relatives.Close female kin (sisters, mothers/daughters) had greater overlap of home ranges and interacted more amicably and less agonistically than did less closely related females. Closely related females clumped their young at emergence, whereas more distantly related females did not; there was little indication of clumping of pre-emerged young. The overlap of home ranges of distant relatives (known genetic relatives that had not associated in a natal burrow) was intermediate to that of close relatives and non-relatives. The types of interactions between distant relatives were more similar to those between non-relatives than between close relatives.I conclude that female arctic ground squirrels exhibit nepotism. Females may benefit from associations with relatives by sharing watching for predators once juveniles become conspicuous. Male arctic ground squirrels commit infanticide and several females may be more effective at protecting their young from infanticidal males than females living alone. I suggest that clumping of young by close relatives may provide a mechanism allowing distantly related females to identify each other.Address for offprint requests     

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.     

The functional significance of infanticide in a population of California ground squirrels (Spermophilus beecheyi)

Naturally-occurring infanticide was observed in a population of California ground squirrels (Spermophilus beecheyi). In four seasons, 40 infanticides were observed. All victims were post-emergent pups. Of 37 killings in which the killer was sexed 36 were by females. All infanticidal females were mothers at the time they killed, but in no case was a mother seen to kill or harm her own young. The victim was cannibalized in 22 cases and taken immediately into the killer’s burrow in 16 others. In no case did killers gain access to the victimized mother’s burrow or territory and female pups were not killed preferentially over males. In light of evolutionary explanations, infanticide in this population may best fit the resource exploitation hypothesis, in which killers commit infanticide to gain a nutritional benefit. Resource competition is a possible auxiliary explanation, since any time a female kills unrelated young she is eliminating possible competitors to her own offspring. This behavior could confer a fitness advantage on killers or it could be an adaptively neutral, alternative feeding strategy. More data are necessary to distinguish between these hypotheses. Received: 26 January 1995/Accepted after revision: 9 September 1995     

Ecological and hormonal correlates of antipredator behavior in adult Belding’s ground squirrels (Spermophilus beldingi)

Predator–prey relationships provide an excellent opportunity to study coevolved adaptations. Decades of theoretical and empirical research have illuminated the various behavioral adaptations exhibited by prey animals to avoid detection and capture, and recent work has begun to characterize physiological adaptations, such as immune reactions, metabolic changes, and hormonal responses to predators or their cues. A 2-year study quantified the activity budgets and antipredator responses of adult Belding’s ground squirrels (Spermophilus beldingi) living in three different California habitats and likely experiencing different predation pressures. At one of these sites, which is visually closed and predators and escape burrows are difficult to see, animals responding to alarm calls remain alert longer and show more exaggerated responses than adults living in two populations that likely experience less intense predation pressure. They also spend more time alert and less time foraging than adults at the other two sites. A 4-year study using noninvasive fecal sampling of cortisol metabolites revealed that S. beldingi living in the closed site also have lower corticoid levels than adults at the other two sites. The lower corticoids likely reflect that predation risk at this closed site is predictable, and might allow animals to mount large acute cortisol responses, facilitating escape from predators and enhanced vigilance while also promoting glucose storage for the approaching hibernation. Collectively, these data demonstrate that local environments and perceived predation risk influence not only foraging, vigilance, and antipredator behaviors, but adrenal functioning as well, which may be especially important for obligate hibernators that face competing demands on glucose storage and mobilization.     

The squirrel that cried wolf: reliability detection by juvenile Richardson's ground squirrels (Spermophilus richardsonii)

Where alarm signals function to warn others of the presence of threat, variation is likely to exist in the reliability of alarm signalers. Some signalers, with too low a threshold of excitation, will issue false alarms and should be ignored if potential alarm recipients are to maximize energy gains. We exposed juvenile Richardson's ground squirrels to reliable signalers, whose alarm calls were paired with the presentation of a predator model, and unreliable signalers, whose alarm calls were played when no potential predator was present. Call recipients discriminated among individual alarm callers, and reduced responsiveness to callers that had been unreliable. Thus, like primates, squirrels are capable of forming a concept of reliability by associating an individual's identity with that individual's past performance.     

Development of food preferences: social learning by Belding's ground squirrels Spermophilus beldingi

Summary The mechanisms by which food selection behavior develops may constrain the evolution of optimal foraging, yet these mechanisms have received relatively little attention in recent optimal foraging studies. We used cafeteria-style feeding trials to examine the role of social learning in the development of food preferences by a generalist mammalian herbivore, Spermophilus beldingi. Naive young spent relatively little time feeding and showed no preferences among five plant species offered in their feeding trials. This random pattern persisted for one set of young during two subsequent trials in the absence of their mother. A second group of young squirrels was tested initially alone, once with their mothers, and then once more alone. These squirrels fed more than those in the control group during their final trials, and showed significant preferences among plant species. These paralleled the preferences of their mothers. These results suggest that social learning may be important in the development of feeding behavior in ground squirrels, and provide a possible mechanism for cultural differences in food preferences among populations.     

Why do female Belding's ground squirrels disperse away from food resources?

We examined the effects of food provisioning on the natal dispersal behavior of Belding's ground squirrels (Spermophilus beldingi). We provided extra food to adult and yearling females in their maternal territories during pregnancy and lactation, and to offspring of these females in their natal areas for 6 weeks after weaning. We used unprovisioned young of unprovisioned mothers as controls. Provisioning influenced the probability of dispersal from the natal area by female but not male S. beldingi. All surviving male S.␣beldingi dispersed by 55 weeks of age, regardless of whether they and their mothers received extra food. By contrast, we observed a significant trend, beginning 3 weeks after weaning and continuing through the yearling year, for a greater proportion of provisioned than control female S. beldingi to emigrate from the natal area. Competition for food did not appear to influence natal dispersal of females. However, overall population density, density of females weaning litters, and rates of aggression and vigilance among these females, were higher in provisioned than control areas, suggesting that competition for non-food resources was unusually intense in provisioned areas. We propose that juvenile female, but not juvenile male, S. beldingi may emigrate from the natal site to increase access to areas with low densities of conspecifics. Together with findings of earlier workers, our results suggest that spatial and temporal distributions of environmental resources are important influences on the dispersal behavior of female ground squirrels. Received: 28 February 1996 / Accepted after revision: 16 October 1996     

Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta)

When agonistic interventions are nepotistic, individuals are expected to side more often with kin but less often against kin in comparison with non-kin. As yet, however, few mammal studies have been in a position to test the validity of this assertion with respect to paternal relatedness. We therefore used molecular genetic kinship testing to assess whether adult female rhesus macaques (Macaca mulatta) from the free-ranging colony of Cayo Santiago (Puerto Rico) bias their interventions in ongoing dyadic aggressive interactions towards maternal and paternal half-sisters compared with unrelated females. It turned out that females supported maternal half-sisters significantly more often than paternal half-sisters or non-kin regardless of the costs associated with such interventions. Similarly, females targeted maternal half-sisters significantly less often than non-kin when this was associated with high costs. Unrelated females provided significantly higher mean rates of both high- and low-cost support to each other than did paternal half-sisters. However, females targeted paternal half-sisters significantly less often than non-kin when targeting was at low cost, suggesting that females refrain from intervening against paternal half-sisters. Our data confirm the general view that coalition formation in female mammals is a function of both the level of maternal relatedness and of the costs of intervention. The patterns of coalition formation among paternal kin were found to be more complex, and may also differ across species, but clear evidence for paternal kin discrimination was observed in female rhesus as predicted by kin selection theory.     

Levels of social behaviors and genetic structure in a population of round-tailed ground squirrels (Xerospermophilus tereticaudus)

Ground-dwelling sciurids exhibit a continuum of sociality and several models predict levels of sociality within this taxon. Models of ground squirrel sociality predict round-tailed ground squirrels (Xerospermophilus tereticaudus) to be solitary; however, previous behavioral studies suggest round-tailed ground squirrels have a matrilineal social structure. To resolve this discrepancy, we combined behavioral observations with genetic analyses of population structure. We assessed levels of agonistic and amicable behaviors combined with fine-scale population genetic structure of round-tailed ground squirrels in a multi-year study in AZ. Only 45 agonistic and 40 amicable interactions were observed between adults in over 137 h of observations. Overall rates of agonistic or amicable interactions between adults were low (≤0.69/h), with no relationship between relatedness of individuals and rates of either amicable or agonistic interactions. Interactions between juvenile littermates were predominantly amicable. Population substructure was not evident with Bayesian analyses, global or pairwise F _ST values; average relatedness among females was not different from males. However, in 2006, the year after a population reduction through targeted animal elimination, a population bottleneck was detected within at least five of seven loci. Contrary to previous behavioral studies, this population of round-tailed ground squirrels, although aggregated spatially, did not exhibit high levels of social behavior nor subpopulation genetic structure. Analyses of the genetic relationships and sociality along a continuum, particularly within aggregates of individuals, may lead to insights into the origin and maintenance of social behaviors by elucidating the mechanisms by which aggregates with intermediate social levels are formed and maintained.     

Mating competition in an asocial ground squirrel,Spermophilus tridecemlineatus

Summary Male thirteen-lined ground squirrels (Spermophilus tridecemlineatus) are subject to three forms of intrasexual competition: competition over location of spatially scattered females, overt conflict over access to those females, and sperm competition. The likelihood of both overt conflict and sperm competition varies between seasons; changes in male density, female density, and breeding synchrony were investigated as possible sources of that variability. Male density was artificially reduced mid-way through one mating season. The results of that experiment, as well as subsequent between-season comparisons, indicate that fluctuations of male density have hardly any effect on levels of overt conflict and sperm competition. By contrast, those forms of intrasexual competition are influenced strongly by female density and/or breeding synchrony.     

Alarm calling behavior of the thirteen-lined ground squirrel,Spermophilus tridecemlineatus

Summary Alarm calling in a population of thirteenlined ground squirrels, Spermophilus tridecemlineatus, was studied over a three-year period. Data on ground squirrel reactions to human and canine approaches and to the approach or presence of avian predators were used to quantify alarm calling behavior.The results support the hypothesis that alarm calling in this species functions to warn genetic relatives. Human and canine approach-elicited calls were most frequently given by mothers and their recently emerged young; adult males and nonparous females rarely called. The onset of maternal calling coincided with the aboveground appearance of a mother's own litter, and both juvenile and maternal calling were terminated at approximately three weeks post-emergence. Alarm calls were rarely emitted during encounters with avian predators.Alarm calling behavior in S. tridecemlineatus thus appeared to be dependent upon the presence of newly emerged juvenile relatives. To investigate whether the population structure of S. tridecemlineatus was perhaps incompatible with the evolution of alarm calling directed toward adult relatives, the distance between the home ranges of adult relatives and the distance over which the alarm vocalization is audible to ground squirrels were measured. The results revealed that females were likely to have adult relatives relatives residing within audible range of the call.     

Variation in litter size: a test of hypotheses in Richardson's ground squirrels

We studied litter size variation in a population of Richardson's ground squirrels (Spermophilus richardsonii) in Alberta, Canada, from 1987 to 2004. Litter size at first emergence of juveniles from the natal burrow ranged from 1 to 14; the most common litter sizes, collectively accounting for 41.0% of 999 litters, were 6 and 7. The number of offspring surviving to adulthood (attained on emergence from hibernation as yearlings) increased with increasing litter size, a result that was not predicted by Lack's "optimal litter size" hypothesis, Mountford's "cliff-edge" effect, or the "bad-years" effect. Contrary to the negative effects predicted by the "cost of reproduction" hypothesis, litter size had no significant influence on survival of mothers to the subsequent year or on the size of the subsequent litter. Rather, our results best fit the predictions of the "individual optimization" hypothesis, which suggests that litter size is determined by the body condition and environmental circumstances of each mother. Supporting this hypothesis, survival of individual offspring was not significantly associated with litter size. Additionally, year-to-year changes in maternal body mass at mating were positively associated with concurrent changes in litter size (r = 0.56), suggesting that litter size depends on the body condition of the mother. Because the mean number of recruits to adulthood increased as litter size increased (r2 = 0.96) and litter size increased with maternal condition, offspring productivity was greater for mothers in better body condition.     

Functional aspects of the pair bond in winter in Bewick's swans (Cygnus columbianus bewickii)

Summary The benefits to partners of monogamous pairs of maintaining continual spatial proximity in the non-breeding season were studied in Bewick's swans wintering in Norfolk, UK.When separated from their mates, females were less successful in aggressive encounters, were threatened more frequently and spent less time feeding than when close to them. Males also suffered reduced success in encounters and a higher frequency of threats by other flock members, though the effect was less pronounced than for females. This sex difference in effect of separation may be associated with the greater weight of males and the fact that success in encounters is related to weight.Partners appeared to assist each other by joining in aggressive encounters, as well as by inhibiting other birds from threatening their mates. However, the precise manner in which the female assisted the male is still obscure, since the highest intensity aggressive encounters — physical fights — involved only male partners. It is suggested that the male may fight harder in his mate's presence.Proximity of partners varied with situation and between different pairs. Partners maintained greater proximity in dense flocks than in dispersed flocks and showed a tendency to stay closer when feeding on winter wheat than on waste potatoes. Partners where the male was high-ranking spent more time together than those where the male was low-ranking.     

Male reproductive tactics to increase paternity in the polygynandrous Columbian ground squirrel (<Emphasis Type="Italic">Urocitellus columbianus</Emphasis>)

In polyandrous and polygynandrous species where females mate with multiple partners, males are expected to maximize their fitness by exhibiting an array of reproductive behaviors to ensure fertilization success, such as competing for the best mating order within a mating sequence, optimizing their investment in copulation, and mate guarding. Though there is genetic evidence of a first-male precedence in siring success for many mammalian species, the causes of this effect are poorly understood. We studied influences on first-male precedence in Columbian ground squirrels (Urocitellus columbianus). We found that the time a male spent consorting and mate guarding declined with his mating order (both the highest for the first male to mate). Mate guarding by the first male significantly reduced, but did not exclude, the number of additional males a female accepted. Later mating males reduced the time spent consorting, suggesting a perceived decreased chance of fertilization success. Consortship and mate guarding durations were positively related to the male’s siring success and to each other, suggesting that males adjusted these behaviors strategically to increase their chances of fertilization success. Our results suggest that besides being the first male to consort, first-male sperm precedence is further enhanced through longer mating bouts and by suppressing the chances and/or efforts of later mating males.     

Alarm calls of Belding's ground squirrels to aerial predators: nepotism or self-preservation?

Summary Belding's ground squirrels (Spermophilus beldingi) give acoustically distinct alarm calls to aerial and terrestrial predators. The animals typically give multiple-note trills to predatory mammals, and single-note whistles to flying hawks. During a 9-year study of free-living S. beldingi at Tioga Pass, California, the adaptive significance of the whistle call was investigated. Data were gathered on 664 ground squirrel-hawk interactions, most of which were induced by flying trained raptors over individually marked study animals of known sex and age. The sight of a flying hawk and the sound of whistles stimulated widespread calling and running to shelter by the ground squirrels (Fig. 1). Wild raptors were rarely successful at capturing the rodents once a whistle had been given, and fewer callers than noncallers were killed (Table 1). Individuals of both sexes and all ages whistled equally often (Fig. 4), and females' tendencies to whistle were not affected by the presence of relatives, including offspring (Fig. 5). The most frequent callers were animals in exposed positions: far from cover and close to the predatory bird (Table 2). Taken together the data suggest that unlike trills, which increase vulnerability to terrestrial predators (Table 1) and function to warn relatives, whistle directly benefit callers by increasing their chances of escaping from hawks.