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.     

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 Molecular Genetic Study of Hybridization in Four Species of Ground Squirrels (Spermophilus: Rodentia,Sciuridae)

Four species of ground squirrel—yellow (Spermophilus fulvus), russet (S. major), small (S. pygmaeus), and spotted (S. suslicus)—occur in the Volga region. Between S. major and S. pigmaeus, S. major and S. fulvus, and S. major and S. suslicus, sporadic hybridization was reported. Using sequencing and restriction analysis, we have examined the mtDNA C region in 13 yellow, 60 russet, 61 small, 45 spotted ground squirrels, and 9 phenotypic hybrids between these species. It was shown that 43% of S. major individuals had alien mitotypes typical of S. fulvus and S. pygmaeus. Alien mitotypes occurred both within and outside sympatric zones. No alien mitotypes were found in 119 animals of the other three species, which suggests that only one parental species (S. major) predominantly participates in backcrosses. Phenotypic hybrids S. fulvus × S. major and S. major × S. pygmaeus) were reliably identified using RAPD–PCR of nuclear DNA. However, we could find no significant traces of hybridization in S. major with alien mitotypes. Analysis of p53 pseudogenes of S. major and S. fulvus that were for the first time described in the present study produced similar results: 59 out of 60 individuals of S. major (including S. major with S. fulvus mitotypes) had only the pseudogene variant specific for S. major. This situation is possible even at low hybridization frequencies (less than 1% according to field observations and 1.4 to 2.7% according to nuclear DNA analysis) if dispersal of S. major from the sympatric zones mainly involved animals that obtained alien mtDNA via backcrossing. The prevalence of animals with alien mitotypes in some S. major populations can be explained by the founder effect. Further studies based on large samples are required for clarifying the discrepancies between mitochondrial and nuclear DNA data.     

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.     

Developmental and geographic variation in stress hormones in wild Belding's ground squirrels (Spermophilus beldingi)

Extensive research has been conducted on the role of glucocorticoids in regulating growth, mobilizing energy, responding to stressors and modulating learning and memory. However, little is known about the production of corticoids during early development in free-living animals, particularly during sensitive periods of acquisition of important behaviors. In a four-year study of Belding's ground squirrels, Spermophilus beldingi, a non-invasive assay of glucocorticoids was used to quantify age and population differences among juveniles from three California locations. Fecal-cortisol metabolites are elevated during a short period when juveniles first emerge aboveground from their natal burrows at about 4 weeks of age. This period of cortisol elevation coincides with when young are learning survival behaviors such as anti-predator responses and foraging strategies. Population differences in juvenile cortisol levels, which may reflect local variation in habitat quality and predator environments, were not evident until 2 weeks after emergence. Elevated cortisol at the age of emergence was also observed in juveniles born and reared in captivity without exposure to typical stressors that occur around the age of emergence. These results indicate that corticoids are regulated during early development, and the possible functions of age-related corticoid levels are discussed, including mobilization of glucose for natal emergence and later facilitation of growth and energy storage during the short summer before hibernation. In some species, elevated corticoids can also facilitate learning and memory, and current work is exploring whether the higher cortisol observed in all three S. beldingi populations just after emergence function to promote rapid acquisition of survival behaviors.     

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.     

Colony Member Discrimination by Juvenile Columbian Ground Squirrels (Spermophilus columbianus)

Whether an individual strives to breed or restrains from reproducing directly but increases the fitness of another individual through its help, may be viewed as a result of a trade-off between fitness costs and benefits arising from this decision. A population of the large carpenter bee Xylocopa sulcatipes Maa was studied in southeast Israel over a two year period. Female reproductive success, in terms of genetic representation in the gene pool (genetic gain), was calculated using coefficients of relatedness and the number of offspring produced by solitary, reproductively dominant and helper bees of social nests. In one year helper females, that shared a nest with a related female accrued a higher genetic gain than did solitary females. In the subsequent year solitary females did better than the helper bees. In nests founded by unrelated females a helper bee accrued only little genetic gain. However, evidence is presented to show that subordinate behaviour can have an adaptive value and can ultimately be beneficial through nest inheritance by the subordinate bee.     

Historical Biogeography and Body Form Evolution of Ground Squirrels (Sciuridae: Xerinae)

Xerinae is the most species-rich subfamily of the Sciuridae (Rodentia). This group of animals has a long complex evolutionary history, which witnessed severe environmental changes. In this paper, a comprehensive approach integrating information from fossil records, morphological, molecular and geographical data of extant species, and events of paleoclimate and paleogeography, were used to explore the evolutionary processes in the Xerinae. Xerinae probably originated in Eurasia around the early Oligocene, and dispersed to Africa via the Africa-Eurasia Land Bridge on two occasions during the Miocene, and subsequently evolved into the Protoxerini and African Xerini. The tribe Marmotini derived from a Eurasian ancestor and thrived in North America. Tamias re-occupied Eurasia in the early Miocene, while the distributions of Marmota and ‘Spermophilus’ genus-groups were restricted to North America at least until the late Miocene. Global cooling and the emergence of grass-dominated ecosystems from 15 Ma are likely to be the main causes for the radiation of Marmotini. The body form of Xerinae displays an allometric mode of evolution, with ground-living taxa, such as Marmota, Cynomys and Xerus notably enlarged, while Tamias has remained slim in body form. To cope with the global environmental changes, particularly the global cooling induced forest degradation and grassland expansion in the late Miocene, most Marmotini developed into true ground squirrels with short tails. The slim body adaptation in Tamias may be related to competition from tree squirrels, or their hoarding behavior, the latter helping them to cope with cold winter.     

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.     

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).     

Features of Interspecific Contacts and Hybridization of Ground Squirrels (Marmotinae,Sciuridae, Rodentia) in Mongolia

Using molecular genetic methods, we investigated the secondary contact zones of two pairs of species of ground squirrels of Mongolia. In common colonies of marmots M. sibirica and M. baibacina, we revealed a high frequency of occurrence of hybrid individuals that were viable and fertile. A hybridization between S. alaschanicus and S. pallidicauda was sporadic in nature. The hypothesis about an extensive hybrid zone in these species of ground squirrels was not confirmed. An occupation of suboptimal biotopes by individuals of different species was the main factor contributing to hybridization in both case. The complex social behavior in marmots affected on the localization and diffusion of the hybridization process.     

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.     

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.     

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.     

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.     

Parameters of Mating Effort and Success in Male European Ground Squirrels,Spermophilus citellus

Behavioural and physiological changes during the reproductive period were documented in male European ground squirrels including: initiated conflict, scent marking, locomotion and range size, as well as testis size, scrotal pigmentation, testosterone levels and changes in body mass. Spring emergence dates in adult males varied but preceded those of females. Gonadal maturation was complete in adult males at emergence. Most yearlings did not mature and emerged with females. After a quiescent premating phase, male range, range overlap, conflict rates and locomotion increased at female emergence. The synchrony of females, their small ranges and short latencies to ovulation produced a highly male-biased operational sex ratio (OSR) and potential for scramble competition polygyny. In contrast to other ground squirrel species, each female apparently mated with only a single male. Scramble competition did appear to occur, in that males tried to contact as many females as often as possible before copulation. Females placed high temporal prerequisites on males. Costs of scrambling were documented by body mass loss during mating, which covaried with the number of ‘acquired’ females. Testicular regression occurred earlier, and fattening, moult and onset of next hibernation were delayed in successful males. The determinant factor in these costs was found to be mass loss intensity during the main mating period. Surprisingly, this factor was best related to feeding changes and not to locomotion or aggression. Time budget constraints perhaps imposed by the female, with compounding influences of exercise and stress effects of conflict, then negatively affected ensuing seasonal activities. The individual changes may adversely affect individual survivability and/or future reproductive success.     

Eimeria beldingii n. sp. and Other Coccidia (Apicomplexa) of the Ground Squirrel Spermophilus beldingi1

Fecal samples of 36 ground squirrels, Spermophilus beldingi, from Tioga Pass (elev. ca. 3315 m) in the Sierra Nevada, California, yielded oocysts of Eimeria beckeri in nine squirrels, E. citelli in four squirrels, E. beldingii n. sp. in two squirrels, and degenerated, unidentifiable oocysts in ten squirrels. Eimeria beldingii n. sp. oocysts are ellipsoidal, 30–34 × 24–30 (mean 32 × 26) μm with a two-layered, rough, striated wall, without a micropyle or residuum, with polar granules; they contain ellipsoidal or ovoid sporocysts 11–15 × 9–12 (mean 13 × 10) μm with a Stieda body and residuum.     

Phylogeny and Evolutionary History of the Ground Squirrels (Rodentia: Marmotinae)

Although ground squirrels (Spermophilus) and prairie dogs (Cynomys) are among the most intensively studied groups of mammals with respect to their ecology and behavior, a well-resolved phylogeny has not been available to provide a framework for comparative and historical analyses. We used complete mitochondrial cytochrome b sequences to construct a phylogeny that includes all 43 currently recognized species in the two genera, as well as representatives of two closely related genera (Marmota and Ammospermophilus). In addition, divergence times for ground squirrel lineages were estimated using Bayesian techniques that do not assume a molecular clock. All methods of phylogenetic analysis recovered the same major clades, and showed the genus Spermophilus to be paraphyletic with respect to both Marmota and Cynomys. Not only is the phylogeny at odds with previous hypotheses of ground squirrel relationships, but it suggests that convergence in morphology has been a common theme in ground squirrel evolution. A well-supported basal clade, including Ammospermophilus and two species in the subgenus Otospermophilus, diverged from all other ground squirrels an estimated 17.5 million years ago. Between 10 and 14 million years ago, a relatively rapid diversification gave rise to lineages leading to marmots and to several distinct groups of ground squirrels. The Eurasian ground squirrels diverged from their North American relatives during this period, far earlier than previously hypothesized. This period of diversification corresponded to warming climate and spread of grasslands in western North America and Eurasia. Close geographic proximity of related forms suggests that most species evolved in or near their current ranges.     

Comparative Ontogeny of Behaviour in Four Species of Squirrels (Sciuridae)

The development of behaviour in four species of Sciurid rodents, having terrestrial, arboreal and gliding way of life, is quantified and compared. The studied species are: Spermophilus columbianus, Spermophilus lateralis, Tamiasciurus hudsonicus and Glaucomys sabrinus. For each behaviour pattern, the earliest and latest age of emergence is given along with a mean calculated for a series of young of each species. The development of locomotion, feeding, comfort, alertness, exploration, nest building and social behaviour and the principal events of physical development are analysed. The discussion shows that the specific differences in ontogenetic rate are controlled by a series of factors including predation pressure, hibernation and the specific complexity of locomotion.     

Thirteen-lined Ground Squirrel (Sciuridae: Spermophilus tridecemlineatus) Antipredator Vigilance: Monitoring the Sky for Aerial Predators

Despite the success of antipredator vigilance research, the specific focus of this vigilance has been difficult to determine. We have previously shown that thirteen-lined ground squirrels ( Spermophilus tridecemlineatus ) increase their vigilance when their lateral field of view is obstructed. In this paper, we describe an experiment in which we attempt to determine the predator class for which this vigilance is directed. Using six differentially occluded Plexiglas foraging boxes with hinged 'eaves', we were able to obstruct the squirrels' view of the sky while not obstructing their view of terrestrial threats. In general, across the box types, when their sky view was obstructed, ground squirrels increased their vigilance by increasing the percentage of time spent withdrawn from the boxes. This result suggests that a significant portion of ground squirrel antipredator vigilance is directed at the sky and is surveillance for aerial predators.