Social Play in Free-ranging Columbian Ground Squirrels,Spermophilus columbianus

Play in the Columbian ground squirrel (Spermophilus columbianus) was examined using marked individuals in a population in southwestern Alberta, Canada. The components of play varied with the age, sex and relatedness of the interactors. Only in intra-sexual play were differences apparent in littermate and non-littermate play. Male-male non-littermate play had fewer contact behaviours than littermate play, whereas female-female non-littermate play had escalations in aggressive-related behaviours. Yearling play was longer and had more aggressive-related behaviours than juvenile play. Reversals were more common in yearling bouts. The significance of those differences in social play that were related to sex, age and relatedness are discussed in light of the social organization of the Columbian ground squirrel.     

Juvenile Richardson's Ground Squirrels (Spermophilus richardsonii) Manifest Both Littermate and Neighbour/Stranger Discrimination

Newborn ground squirrels (Spermophilus spp.) are reared in isolation of individuals belonging to other litters. At or near weaning, they broaden their social interactions to encompass conspecifics other than littermates. In laboratory studies, juvenile ground squirrels commonly discriminate littermates from non-littermates, but few studies have examined whether behavioural discrimination at that level persists under natural circumstances. Previous studies have also all but ignored the possibility of alternative levels of social discrimination augmenting or replacing the discrimination of littermates from non-littermates. To examine those possibilities, I staged interactions in a neutral arena between littermate, neighbour and non-neighbour (stranger) pairs of otherwise free-living juvenile Richardson's ground squirrels (Spermophilus richardsonii). Littermates interacted more frequently than other pair types and showed the highest proportion of cohesive behaviour and the least agonism. Strangers interacted less frequently than all other pair types, showed the fewest recognitive contacts, and were the least cohesive and most agonistic. Neighbours interacted less than littermates, but more than strangers, and showed intermediate levels of cohesion and agonism. Neighbours also engaged in more recognitive contacts than strangers, but did not have fewer recognitive contacts than littermates. Defecation rates also differed among interactant types: littermates left the fewest scats in the arena, neighbours deposited an intermediate number and strangers defecated the most. My results substantiate those of earlier laboratory studies suggesting that the discrimination of littermates from neighbouring juveniles persists in the natural context. These data also extend those earlier findings by demonstrating that juveniles come to discriminate neighbours from strangers. Comparisons of the behaviour of related vs. unrelated neighbours reveal that neighbour/stranger discrimination is contingent upon differential familiarity. Simultaneous social discrimination at the levels documented could promote kin-biased behaviour and cooperation among both related and unrelated neighbours.     

Alarm Calls of California Ground Squirrels (Spermophilus beecheyi)

California ground squirrel alarm vocalizations were recorded in field and laboratory, and sonagraphically analysed. The contexts of both naturally occurring and experimentally elicited calls were noted in the field. The components of this graded system are chatters, chats and whistles. Chatters and chats are often elicited by terrestrial predators, whistles commonly by low flying raptors. Whistles are more commonly associated with cryptic behavior and flight than chatter-chats, but both call types usually elicit bipedal alert postures. These calls grade along a number of dimensions which may signal redundantly the level of excitation of the caller. We propose that the chatter-chat calls of highly aroused squirrels are composed of more and longer notes, occur at a higher rate, are less noisy and contain more frequency modulation. Whistles, however, are single-note calls that contain no frequency modulation, even though they are emitted by highly aroused squirrels and are long and noise free. Preliminary data suggest that: 1) chats are easier for a human ♀ to localize than whistles; 2) elevation of the head, by adopting bipedal postures and mounting promontories, enhances the audibility of alarms.     

Environmental Influences on Infanticide in Columbian Ground Squirrels

Infanticide of preweaned and weanling juvenile Columbian ground squirrels (Spermophilus columbianus) has been previously reported, but its prevalence in most populations is poorly known. I examined evidence of infanticide in a six-year study of four populations in southwestern Alberta, two of which received an experimental supplementation of food for two years. Evidence of infanticide of weanling ground squirrels was uncommon, except for one population and year (previously supplemented population at 1580 m elevation in 1984) in which 9 dead young were found, suggesting an increased rate of infanticide. The rate of total loss of pre-weaned litters also increased at 1580 m in 1984. At higher elevation sites (2100 m), however, no evidence of infanticide was found under experimental or unmanipulated conditions. One factor that might have influenced the rate of infanticide of weanlings was their degree of development when they first emerged from natal burrows. A review of studies of 11 populations of Columbian ground squirrels suggested that under natural conditions, infanticide may have differed among environments. Differences in density among populations appeared to have little influence on the rate of infanticide, but elevation was significantly negatively associated with infanticide.     

Why are Male Columbian Ground Squirrels Territorial?

Male territorial defence is a component of many vertebrate mating systems and is often regarded as a tactic for acquiring mates. Traditionally considered within the context of overt site‐specific defence, territoriality actually may have several components which encompass a variety of behavioural tactics (e.g. post‐copulatory mate‐guarding, defence of resources that females need, defence of area around females) that underlie a mating system. The purpose of our study was to evaluate such influences on the territorial behaviour of male Columbian ground squirrels in southwestern Alberta, Canada. Males were dominant and territorial if they defended a minimum convex polygon activity range by chasing other males more within the activity range than they were chased. Subordinate males had no territory and were chased throughout their ranges, but they competed for mates by increasing chases in their activity range when nearby females were oestrous. Dominant males exhibited conditional breeding tactics, tending to chase other dominant males from their territory when nearby females were oestrous, but travelling outside their activity ranges to chase subordinate males when females were not oestrous. Although females mated first with a dominant male on whose territory they resided (and in order from oldest to youngest if several territories overlapped), mating pairs were not exclusive, as females usually mated with additional males. Males also guarded females after copulation and defended females directly just before oestrus, rather than defending territory per se during those times. Thus, males possess a repertoire of behaviours that complement site‐specific territoriality, and territory ownership serves to facilitate a first mating with females that live on the territory.     

Adenocarcinoma of the Dorsal Glands in 2 European Ground Squirrels (Spermophilus citellus)

Olfactory communication is an important aspect of the biology of ground squirrels; accordingly, some of their integumentary glands are associated with scent-marking behavior. Although reports of neoplasms in ground squirrels are limited, the literature on tumors in this family of rodents is extensive, with hepatocellular carcinomas in woodchucks and fibromas in squirrels being the 2 most common neoplasms. Apocrine gland tumors occur frequently in domestic animals such as cats and dogs but to our knowledge have not previously been reported in squirrels. Here we describe 2 cases of adenocarcinoma of the dorsal glands in privately owned European ground squirrels (Spermophilus citellus). The skin nodules were characterized histologically by proliferation of epithelial cells, which were arranged in a tubuloacinar pattern with neoplastic emboli within the blood vessels. Adenocarcinoma of the dorsal glands was diagnosed in light of the anatomic localization, immunohistochemistry results, and histochemistry findings.Olfactory communication is an important aspect of the biology of most ground squirrels;^10,12 accordingly, some of their integumentary glands are associated with scent-marking behavior.^5,10 Squirrels have 3 glandular anatomic areas: the oral–cheek area, dorsal area, and the anal area.¹⁰ The dorsal gland field in the skin extends from the scapular region caudally and from the scapular region anterioventrally to the ear.^9,10Approximately 60 individual oval-shaped sudoriparous glands comprise the dorsal gland field. Individual dorsal glands are composed of a tightly coiled and branched fundus, a large sinus, and a singular duct, which opens on the free surface of the skin.^9,10 The strong- smelling oil secreted by the glands probably is released on vegetation and serves as a source of information to other members of the species.⁹ These glands seem to be more active during spring and summer than during winter. They are stimulated by excitement, present in both sexes, and larger in adult male squirrels.¹⁰ Here we describe 2 cases of neoplasia of the dorsal glands in 2 privately owned European ground squirrels (Spermophilus citellus; Sciuridae).     

Parasite removal and its impact on litter size and body condition in Columbian ground squirrels (Spermophilus columbianus)

The current interest in studies of parasite-host relationships is focusing on the impact of parasites on mate choice, sexual selection and individual fitness. While most studies have been done on birds and fishes, little is known about the interactions between parasites and reproductive success in mammals. In this study, I experimentally removed ectoparasites (mainly fleas) from some female Columbian ground squirrels using a commercially available powder, whereas other squirrels were left untreated as controls. The anti-parasite treatment led to an increase in female body condition during lactation and at weaning and an increase in litter size. The increase of body mass in treated females between birth of the young and weaning is also different from observations done over 8 years in the same population, where untreated females usually lost mass. In close to 400 litters from untreated females in the same area, only 2% had litter sizes as big as the treated females. I conclude that ectoparasites can have a profound impact not only on individuals but probably on the dynamics of the whole population.     

Plasticity of Alarm-call Response Development in Belding's Ground Squirrels (Spermophilus beldingi, Sciuridae)

Plasticity in the alarm-call responses of Belding's ground squirrels ( Spermophilus beldingi ) may function to prepare young to respond appropriately to calls according to the predator environment and habitat in which the young develop. To examine the extent to which antipredator responses are sensitive to early rearing environments, we studied the development of behavioural responses to playbacks of alarm calls and non-alarm calls in free-living juveniles and captive juveniles housed in large outdoor enclosures. Compared with same-aged, free-living juveniles, captive juveniles were more likely to show an observable response to playbacks, exhibited more exaggerated initial responses (e.g. enter a burrow vs. freeze), and remained alert longer following playbacks. The influence of rearing history on antipredator responses was limited to responses to auditory stimuli, as the two groups of juveniles reacted similarly to fast-moving visual stimuli. The responses of free-living juveniles appeared to be more discriminating than responses of captive juveniles, particularly following playbacks of calls associated with less immediate threats.
The responses of captive and free-living mothers were similar, indicating a developmental component to the juvenile response differences observed here. Free-living juveniles developed a discrimination among alarm and non-alarm calls sooner than captive young. Response differences were evident within 1 wk of first emergence from natal burrows and persisted at least 4 wk, at around the age of natal dispersal. This suggests that early rearing history has an enduring effect on response repertoires, which may be adaptive if animals continue to inhabit the predator environment in which they developed.     

The Antipredator Vigilance of Adult and Juvenile Thirteen-lined Ground Squirrels (Sciuridae: Spermophilus tridecemlineatus): Visual Obstruction and Simulated Hawk Attacks

Visual antipredator vigilance was predicted to increase in the presence of visual obstructions that do not otherwise provide cover. This hypothesis was tested using 13-lined ground squirrels as they fed in four Plexiglas boxes that varied in the extent and location of visual obstruction. Adults and juveniles of both sexes were studied. Adults reacted to long-range lateral visual occlusion and total occlusion by withdrawing more often and assuming both more pronounced and lengthy alert postures relative to short-range lateral occlusion and no occlusion. Juveniles were less vigilant than adults and did not behave differently in the four treatment conditions. There were no sex differences. Simulated hawk attacks on squirrels feeding in the boxes indicate that the greater vigilance of adults led to significantly reduced reaction times compared with juveniles.     

How Rearing History Affects Alarm-call Responses of Belding's Ground Squirrels (Spermophilus beldingi, Sciuridae)

Juvenile, but not adult, Belding’s ground squirrels (Spermophilus beldingi) exhibit markedly different responses to alarm calls as a function of their environment. Compared with same-aged, free-living juveniles, captive juveniles (housed in large outdoor enclosures) are more likely to respond to playbacks, to exhibit more exaggerated initial responses (e.g. enter a burrow vs. freeze) and to remain alert longer following playbacks of alarm and non-alarm calls. Two studies were conducted to identify the factors contributing to these response differences. Postemergent rearing environments (such as the opaque enclosure walls that limited visual and auditory stimulation in captivity, or the increased number of conspecifics and natural alarm calls that free-living juveniles experienced) could not account for the majority of response differences between captive and free-living juveniles (Study 1). To determine if the attenuated responses of free-living juveniles were due to foraging pressures, we compared the behaviours of food-provisioned captive juveniles with those of non-provisioned captive juveniles. Although sample sizes were small, no differences were evident in the development or expression of responses as a function of foraging pressure. Next, the development of captive juveniles was compared with that of juveniles reared in the field but housed in captivity after emergence (Study 2). Differences in the response patterns of field-reared and captive-reared animals matched the differences reported previously, as the responses of field-reared animals observed in captivity mirrored those of free-living juveniles that remained in the field. Thus, the differences in alarm-call responses originally observed between captive and free-living juveniles are attributed to their pre-emergent, but not post-emergent, rearing histories. Captive pups experienced levels of auditory, visual, tactile, and olfactory stimulation that were greater than those typically experienced by free-living pups. The increased exposure to conspecific alarm calls may have primed captive pups to respond more often and more intensely to the auditory stimuli they heard as juveniles. Sensitivity to early rearing environments may be adaptive for young ground squirrels if it facilitates the development of antipredator behaviour patterns that are appropriate for the local predator environment (e.g. openness of habitat, frequency of predators, availability of refuges).     

Quantitative Shedding of Two Genotypes of Cryptosporidium parvum in California Ground Squirrels (Spermophilus beecheyi)

Sixteen percent of California ground squirrels (Spermophilus beecheyi) were found to be shedding an average of 53,875 Cryptosporidium parvum oocysts/g of feces. Male squirrels had a higher prevalence and higher intensity of shedding than did female squirrels. The majority of C. parvum isolates matched a bovine-murine genotype, with a few isolates resembling a porcine genotype. Higher intensities of shedding by males may enhance dissemination and genotypic mixing of this protozoa given males' proclivity to disperse to nonnatal colonies.     

Pathology of Ground Squirrels in a Research Colony

This paper presents a retrospective review of the postmortem findings in a colony of wild-caught ground squirrels used in medical research. The species included in this study were Richardson''s ground squirrel Urocitellus richardsonii, Columbian ground squirrel Urocitellus columbianus and golden-mantled ground squirrel Callospermophilus lateralis. The pathologic findings in 160 ground squirrels from this colony demonstrated a wide variety of conditions, with chronic nephritis and hepatic adenomas being the most frequent overall. All animals with gross lesions of chronic interstitial nephritis had both glomerular and tubulointerstitial disease upon microscopic examination. As the first review of pathology in a research colony of ground squirrels. this study provides data for use in comparative studies about rodent diseases and important information for those who maintain such animals for research.

Ground squirrels are commonly but incorrectly referred to as gophers and are terrestrial members of the Order Rodentia, family Sciuridae. True gophers are members of the family Geomyidae. In the Canadian province of Alberta, the 3 most common species of ground squirrels are Richardson ground squirrel (Urocitellus richardsonii),^4,13 the Columbian ground squirrel (Urocitellus columbianus),⁵ and the golden-mantled ground squirrel (Callospermophilus lateralis).⁷ Thirteen lined (Ictidomys tridecemlineatus) and Franklin (Poliocitellus franklinii)⁶ ground squirrels are also present but less numerous in Alberta.The 3 species in this study vary in lifespan, litter size, population density,⁵ annual mortality rate and timing of reproduction,¹³ but have several common attributes. An overview of these ground squirrels in the wild is as follows. In a natural habitat, which includes open sagebrush, grasslands,⁴ and mountain meadows, ground squirrels live in complex burrows on stable,⁴ sandy, well-drained soils^4,5 at elevations from 1828 to over 3658 meters in the western 2-thirds of North America.¹ Litters are born in late April to early May and consist of 6 to 8 pups. Ground squirrels are social animals, with densities ranging from 5 to 60 per hectare. In the wild, mortality among male Richardson ground squirrels is as much as 80% per year, partly due to heavy predation.¹⁴ Females have a slightly lower annual mortality rate and are considered to have reached old age at 3 to 4 y of age.¹⁴ One study in southern Alberta found 5 and 6 y old females were present but only a single male that had survived to 4 y.¹³ Ground squirrel burrows can damage to agricultural land because their holes are a hazard to livestock, their mounds can damage equipment, and burrowing can damage crops.¹¹ For these reasons, they are often considered a pest species. On the other hand, ground squirrels till the soil and can serve as a food source for predators.¹¹ As such, they are an integral part of the prairie and mountain ecosystem and food chain.Ground squirrels are most often used to study hibernation and metabolism, as their basal metabolic rate varies according to environmental conditions. They have large amounts of brown fat and are deep seasonal hibernators.³ Unlike most rodents, they are strictly diurnal with peak activities in the morning and late afternoon. Hibernation in ground squirrels consists of periods of torpor interspersed with brief thermogenic arousals that last less than 24 h. Torpor bouts increase in length with decreasing soil temperature. During periods of inactivity, body temperature drops to near ambient soil temperature, falling as low as 2 to 3 °C in late winter.¹² Despite the metabolic costs of thermogenesis and euthermy during intertorpor arousals, hibernating ground squirrels can achieve an overall energy saving over the hibernating season of 88% compared with euthermic animals.¹⁹ Complex regulation of body temperature makes ground squirrels ideal subjects for studies of basal metabolism,⁹ body composition during euthermic and hibernating states, and gene expression during hibernation.⁸ Other research applications for which ground squirrels are useful include the study of liver neoplasia,^10,15,18 cholesterol gallstones,¹⁷ obesity, and diabetes mellitus.¹⁵Ground squirrels seldom produce fertile matings in captivity, and research colonies must be maintained by capture from the wild, posing biosecurity challenges for such colonies. Despite the need to capture of wild ground squirrels for research, these animals habituate easily and adapt well to captivityKnowledge of the pathology of captive ground squirrels is important to investigators and veterinarians who maintain colonies for research purposes. Although wild ground squirrels are used as a laboratory animal in some research institutions, little information is available in the scientific literature about the naturally occurring diseases and pathology of ground squirrels, with the exception of hepatic tumors.¹⁸ The purpose of the current study was to describe conditions that may occur in a research colony of wild-caught ground squirrels, potentially resulting in death or the need for humane euthanasia. The species included in this study were primarily U. richardsonii and U. columbianus, with 6 C. lateralis.     

Age Differences in the Response of California Ground Squirrels (Spermophilus beecheyi) to Conspecific Alarm Calls

Juvenile California ground squirrel responses to adult alarm calls and juvenile alarm calling may be modified during development to achieve adult form. Adult conspecific chatter and whistle alarm calls were played back to juvenile and adult ground squirrels at an agricultural field site. In response to chatter playbacks, adults spent more time visually orienting to the environment and less time out of view and in covered habitats than juveniles; the converse was true in response to whistle playbacks. To test the evocativeness of juvenile calling, a subset of adult subjects received juvenile chatter and whistle playbacks. Adults spent less time out of view to juvenile call types than to adult calls, and showed more similar responses to juvenile chatters and whistles than to adult chatters and whistles. Age differences in the ground squirrel's alarm call system may reflect adjustments to changing risks during development.     

Adult Richardson's Ground Squirrels (Spermophilus richardsonii) Ignore Rate Changes in Juvenile Alarm Calls: Age‐Differential Response Urgency Perception?

Juvenile Richardson's ground squirrels (RGS; Spermophilus richardsonii) communicate response urgency by modulating the rate of syllable production in repetitive alarm calls, although longer call bouts do not promote more pronounced or longer‐lasting (tonic) vigilance in juvenile call recipients. We exposed free‐living adult RGS to playbacks of alarm calls differing in rate and length to determine whether adult receivers respond to the same alarm parameters as juveniles. Adult squirrels did not respond differentially to differences in call rate or length, suggesting that adult RGS do not attend to call rate as do juveniles. This difference in response may be attributable to a developmental change in the perceptual mechanisms by which individuals extract information regarding response urgency, but could also be a product of adult receivers devaluing information encoded in alarm calls emitted by relatively inexperienced juvenile signalers.     

Antipredator Responses to a Previously Neutral Sound by Free-living Adult Golden-mantled Ground Squirrels, Spermophilus lateralis (Sciuridae)

I investigated whether free-living adult golden-mantled ground squirrels ( Spermophilus lateralis ) could learn to associate a novel sound with the appearance of a predator. Using a classical conditioning protocol, I presented adult squirrels with a novel tone followed by the appearance of a model hawk. After repeated trials, I again measured the squirrels' behavioral responses to the tone and compared them with their pretraining responses. Individuals that experienced the tone paired with the hawk responded with antipredator behavior of longer duration after pairing than before and these responses were indistinguishable from responses to natural, conspecific alarm calls. By examining the process, rather than simply the pattern, of call recognition ontogeny, this study provides new evidence for a mechanism by which animals can develop the ability to respond to both conspecific and heterospecific calls.     

A Comparative Study of Social Behaviour of Two Sympatric Ground Squirrels (Spermophilus spilosoma,S. mexicanus)

During the reproductive period, intraspecific dyadic encounters were staged within and between S. spilosoma and S. mexicanus individuals under controlled conditions. Video recordings were used to describe and quantify behaviour of males and females of these two sympatric ground squirrels. To compare dyads within and between species two indices (an Agonistic index and a Tolerance index) were designed from measures of behavioural frequencies. During intrasexual encounters, S. mexicanns males and females appear to be more aggressive than male and female S. spilosoma. In both species, encounters between males were more aggressive than between females, which were very tolerant to each other in S. spilosoma. In most cases encounters between male and female conspecifics exhibit an intermediate level of agonistic behaviour and tolerance. The null hypothesis of similarity of the social behaviour of S. spilosoma and S. mexicanus is falsified. Some alternative hypotheses are proposed. First, the tolerance of S. spilosoma is an adaptation to the difficult environmental conditions. Thus differences between the two species reflect differences in behavioural evolution in allopatric populations. Second, S. spilosoma tolerance is a behavioural response to S. mexicanus' recent arrival.