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.     

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.     

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).     

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.     

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.     

Molecular genetic relationships among east Palearctic ground squirrels of the genus Spermophilus (Sciuridae, Rodentia)

Genetic diversity in the four east Palearctic ground squirrel species of the genus Spermophilus--S. undulatus, S. parryi (subgenus Urocitellus), S. dauricus, and S. relictus (subgenus Citellus)--- was investigated using RAPD PCR with ten random primers. Siberian chipmunk, Tamias sibiricus, was used as an outgroup. Molecular markers for different taxonomic ranks were identified, including those for the genera Spermophilus and Tamias, subgenera Urocitellus and Citellus, as well as for each of the four species, S. undulatus, S. parryi, S. dauricus, and S. relictus. For the ground squirrel species and subgenera, genetic differentiation indices (H(t), H(s), D(st), G(st), Nm, and D) were calculated. In addition, for these groups the NJ phylogenetic reconstructions and UPGMA dendrograms of genetic similarity of the individuals and combined populations were constructed. Comparative molecular genetic analysis revealed a high genetic differentiation between S. undulates, S. dauricus, S. relicts, and S. parryi (G(st) = 0.58 to 0.82; D = 0.53 to 1.06), along with a low level of genetic differentiation of the subgenera Citellus and Urocitellus (G(st) = 0.33; D = 0.27), distinguished in accordance with the existing taxonomic systems of the genus Spermophilus.     

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.     

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.     

Natural Diversity and Phylogeny of Asian Red-Cheeked Squirrels (Rodentia,Sciuridae, Dremomys) in Eastern Indochina

Biology Bulletin - Based on new molecular data for mitochondrial (Cyt b) and nuclear (IRBP, RAG1) genes, as well as an extensive analysis of morphological material, we accessed actual species...     

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.     

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.     

Serum thyroxine and seasonal fattening of free-living Piute ground squirrels, Spermophilus mollis (Rodentia: Sciuridae)

Serum thyroxine and body composition of free-living Piute ground squirrels were examined during the season of above-ground activity. Serum thyroxine titers were 2-10 times higher than those reported in laboratory studies on other species. Among juveniles, both body size and lipid content were negatively correlated with thyroxine, whereas these variables were not significantly correlated among adults. Significant sex differences in serum thyroxine were observed for both age groups. Results suggest that the seasonal cycle of body weight is driven by an underlying metabolic cycle but that individual fattening schedules are determined by environmental conditions.     

Biology and Conservation Status of Flying Squirrels (Pteromyini,Sciuridae, Rodentia) in India: An Update and Review

Flying squirrels are capable of gliding and one of the least known mammals of the world. Work on these animals is less and sporadic due to their crepuscular and cryptic habits. At the present scenario, a complete pilot study is in an urgent need to formulate conservation strategies and policies to conserve them in India. Therefore, a thorough review on biology and conservation status of flying squirrels in India is provided here. A total of 13 species of flying squirrels present in India i.e., Belomys pearsonii, Biswamoyopterus biswasi, Eupetaurus cinereus, Eoglaucomys fimbriatus, Hylopetes alboniger, Petaurista elegans, P. mishmiensis, P. magnificus, P. mechukaensis, P. nobilis, P. petaurista, P. philippensis and Petinomys fuscocapillus, wherein three are endemic to the country. P. philippensis has broader distribution and is found to be more studied than others. Eastern part of the country contains the highest species number (n = 10) follows three in northern part, two in southern part and one in western part subsequently. All species are facing threat to their population due to native habitat loss, degradation and hunting. Harmonization, alliances and partnership between various stakeholders along with better application of standard techniques would be strengthen to develop conservation strategies and implementing their coordinated actions could preserve flying squirrels’ future in the country landscape.     

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.     

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.     

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).