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.     

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.     

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.     

Seasonal shedding of multiple Cryptosporidium genotypes in California ground squirrels (Spermophilus beecheyi)

Twelve percent of 853 California ground squirrels (Spermophilus beecheyi) from six different geographic locations in Kern County, Calif., were found to be shedding on average 44,482 oocysts g of feces(-1). The mean annual environmental loading rate of Cryptosporidium oocysts was 57,882 oocysts squirrel(-1) day(-1), with seasonal patterns of fecal shedding ranging from <10,000 oocysts squirrel(-1) day(-1) in fall, winter, and spring to levels of 2 x 10(5) oocysts squirrel(-1) day(-1) in summer. Juveniles were about twice as likely as adult squirrels to be infected and shed higher concentrations of oocysts than adults did, with particularly high levels of infection and shedding being found among juvenile male squirrels. Based on DNA sequencing of a portion of the 18S small-subunit rRNA gene, there existed three genotypes of Cryptosporidium species in these populations of squirrels (Sbey03a, Sbey03b, and Sbey03c; accession numbers AY462231 to AY462233, respectively). These unique DNA sequences were most closely related (96 to 97% homology) to porcine C. parvum (AF115377) and C. wrairi (AF115378). Inoculating BALB/c neonatal mice with up to 10,000 Sbey03b or Sbey03c fresh oocysts from different infected hosts did not produce detectable levels of infection, suggesting that this common genotype shed by California ground squirrels is not infectious for mice and may constitute a new species of Cryptosporidium.     

Patterns of progesterone secretion in free-living California ground squirrels (Spermophilus beecheyi)

During a long-term field study of a free-living population of California ground squirrels (Spermophilus beecheyi), blood samples were drawn at regular intervals from marked females via femoral venipuncture, and plasma progesterone (P) and prolactin (PRL) were measured by radioimmunoassay. Marked fluctuations with season and reproductive condition occurred in circulating levels of both hormones, with peak levels occurring during the spring breeding season. Two peaks in P concentrations were observed each spring, the first occurring during pregnancy, and the second during lactation. Peak PRL levels in females were also reached during the lactation interval, midway between the two P peaks. Analysis of repeated measures from individual females showed a marked decline in circulating P around the time of parturition. Juveniles had lower mean P levels than adults, and yearlings had lower peak levels during their initial reproductive episodes than older females did. The observed pattern of P secretion in S. beecheyi differs from that known for most mammals, but resembles those reported for other ground-dwelling sciurid rodents.     

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.     

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).     

Purification and partial characterization of prolactin from the California ground squirrel (Spermophilus beecheyi)

Prolactin (Prl) secreted by cultured ground squirrel (Spermophilus beecheyi) pituitaries (SbPrl) was purified by gel filtration on Sephadex G-100 and ion-exchange chromatography on Polybuffer Exchanger 94. Purification from culture medium from 190 pituitaries yielded 1.1 mg of purified SbPrl. The SbPrl has an apparent molecular weight of 27,000 by polyacrylamide gel electrophoresis in the presence of sodium dodecyl sulfate, an isoelectric point of 6.3, and does not contain any asparagine-linked carbohydrate. Purified SbPrl displaces 125I-labeled ovine Prl from binding sites on lactating rabbit mammary gland membranes and stimulates secretion of alpha-lactalbumin by cultured mouse mammary gland epithelial cells.     

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.     

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.     

Multiple unique Cryptosporidium isolates from three species of ground squirrels (Spermophilus beecheyi, S. beldingi, and S. lateralis) in California

Phylogenetic analyses of the 18S small-subunit (SSU) rRNA and Cryptosporidium oocyst wall protein (COWP) genes indicate that multiple unique Cryptosporidium isolates are shed by separate species of Spermophilus ground squirrels (S. beecheyi, S. beldingi, and S. lateralis) throughout California, despite some squirrel populations' being geographically isolated. The data support our assertion that Spermophilus squirrels shed novel Cryptosporidium species.     

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.     

Development of an homologous radioimmunoassay for secreted prolactin from the California ground squirrel (Spermophilus beecheyi)

A sensitive homologous radioimmunoassay was developed for secreted prolactin from the California ground squirrel (Spermophilus beecheyi). S. beecheyi plasma and pituitary extracts displaced 125I-labeled S. beecheyi prolactin in a parallel manner with S. beecheyi prolactin (sbPRL). Mean minimum sensitivity of the assay was 0.21 ng/ml, and mean intra- and interassay coefficients of variation were 4.1% and 14.5%, respectively. The assay was used to measure basal prolactin concentrations in male and female ground squirrels at various stages of their annual reproductive cycles. Mean concentrations in nonpregnant, nonlactating young females, pregnant females, and lactating females were 1.63, 11.35, and 10.86 ng/ml, respectively. Mean concentrations in nonreproductive and breeding males were 1.50 and 9.81 ng/ml, respectively. Finally, the assay was used to evaluate cross-reactivity between sbPRL and prolactins and growth hormones from other rodent species. Of the tested hormones, only hamster prolactin showed any cross-reactivity with sbPRL (about 0.03%).     

Failure of temperature to entrain a circannual rhythm of mass in California ground squirrels (Spermophilus beecheyi)

Abstract

To determine what environmental factor is the Zeitgeber for the annual change in mass, California ground squirrels (Spermophilus beecheyi) were exposed to several regimes of temperature and length of day. The squirrels were captured when age 4–5 months, kept individually in cages with excess food and nesting material. The temperature was varied with a 6‐month phase shift (SH). The length of day was the same as Santa Barbara (SB) or 6‐month phase shift (SH). The light was provided by cool white bulbs at 10–600 lux.

The first experiment consisted of keeping squirrels at either SB or SH length of day and at constant temperature (20°) for three years and then changing to SH temperature for 3 years. None entrained although at age 6, 2 might be entrained. The second experiment repeated the first except that the SH temperature started at age zero. None has entrained by age 5. None of a third group, placed at SH temperature and SB length of day, has entrained by age 3. The conclusion is that these regimes of temperature and length of day, which resemble natural conditions, do not entrain the annual change of mass.     

Environmental influences on spatial and temporal patterns of body-size variation in California ground squirrels (Spermophilus beecheyi)

Aim  In order to understand how ground squirrels ( Spermophilus beecheyi ) may respond to future environmental change, we investigated five biotic and environmental factors potentially responsible for explaining body-size variation in this species across California. We examined the concordance of spatial patterns with temporal body-size change since the last glacial maximum (LGM).
Location  California, western North America.
Methods  We quantified body size of modern populations of ground squirrels ( n  = 81) and used a model-selection approach to determine the best variables (sex, vegetation, number of congeners, temperature and/or precipitation) explaining geographical variation in body size among modern populations. We also quantified body size of one fossil population in northern California ( n  = 39) and compared temporal body-size change in S. beecheyi at this location since the LGM with model predictions.
Results  Body size of modern populations conformed to Bergmann's rule, with larger individuals in northern (wetter and cooler) portions of California. However, the models suggest that precipitation, rather than temperature or other variables, may best explain variation in body size across modern spatial gradients. Our conclusion is supported by the temporal data, demonstrating that the body size of S. beecheyi has increased in northern California since the LGM, concordant with precipitation but not temperature change in the region.
Main conclusions  Precipitation, rather than temperature, vegetation or number of congeneric species, was the main factor explaining both spatial and temporal patterns of body-size variation in S. beecheyi . The integration of space and time provides a powerful mechanism for predicting how local populations may respond to current and future climatic changes.     

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.     

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).     

Seasonal fluctuations in hormones and behavior of free-living male California ground squirrels (Spermophilus beecheyi).

Plasma testosterone (T), prolactin (PRL), and behavior were monitored concurrently in free-living male California ground squirrels (Spermophilus beecheyi). Male plasma T peaked in January, 2-3 months after males emerged from their annual period of estivation. PRL peaked 6 to 10 weeks after T. Temporal patterns of space use by males were directly correlated with plasma T levels, but seasonal maxima in rates of most monitored male behaviors occurred 4 weeks after the T peak. No monitored behavior rates were correlated with plasma PRL values. Yearling and adult males did not differ with respect to circulating levels of either T or PRL. Both groups of males mated in our study population, and did not differ significantly with respect to rates of most monitored behaviors. However, yearlings pursued fewer females, mated less frequently, and required more mounts to complete each copulation than did adults. We suggest that T serves an important priming function for various seasonally fluctuating behaviors, but also that mating experience might influence the efficiency of copulatory behavior in this species.