Spermophilus Beldingi Research Articles

Ground Squirrel Shooting and Potential Lead Exposure in Breeding Avian Scavengers.

Recreational ground squirrel shooting is a popular activity throughout the western United States and serves as a tool for managing ground squirrel populations in agricultural regions. Belding’s ground squirrels (Spermophilus beldingi) are routinely shot in California, Nevada, and Oregon across habitats that overlap with breeding avian scavengers. Ground squirrels shot with lead (Pb)-based bullets may pose a risk to avian scavengers if they consume carcasses containing Pb fragments. To assess the potential risk to breeding avian scavengers we developed a model to estimate the number, mass, and distribution of Pb fragments in shot ground squirrels using radiographic images. Eighty percent of shot carcasses contained detectible Pb fragments with an average of 38.6 mg of Pb fragments. Seven percent of all carcasses contained Pb fragment masses exceeding a lethal dose for a model raptor nestling (e.g. American kestrel Falco sparverius). Bullet type did not influence the number of fragments in shot ground squirrels, but did influence the mass of fragments retained. Belding’s ground squirrels shot with .17 Super Mag and unknown ammunition types contained over 28 and 17 times more mass of Pb fragments than those shot with .22 solid and .22 hollow point bullets, respectively. Ground squirrel body mass was positively correlated with both the number and mass of Pb fragments in carcasses, increasing on average by 76% and 56% respectively across the range of carcass masses. Although the mass of Pb retained in ground squirrel carcasses was small relative to the original bullet mass, avian scavenger nestlings that frequently consume shot ground squirrels may be at risk for Pb-induced effects (e.g., physiology, growth, or survival). Using modeling efforts we found that if nestling golden eagles (Aquila chrysaetos), red-tailed hawks (Buteo jamaicensis), and Swainson’s hawks (B. swainsoni) consumed shot ground squirrels proportionately to the nestling’s mass, energy needs, and diet, 100% of the nestling period would exceed a 50% reduction in delta-aminolevulinic acid dehydratase production threshold, the last 13–27% of the nestling stage would exceed a reduced growth rate threshold, but no nestlings would be expected to exceed a level of Pb ingestion that would be lethal.

Cryptosporidium rubeyi n. sp. (Apicomplexa: Cryptosporidiidae) in multiple Spermophilus ground squirrel species.

Previously we reported the unique Cryptosporidium sp. “c” genotype (e.g., Sbey03c, Sbey05c, Sbld05c, Sltl05c) from three species of Spermophilus ground squirrel (Spermophilus beecheyi, Spermophilus beldingi, Spermophilus lateralis) located throughout California, USA. This follow-up work characterizes the morphology and animal infectivity of this novel genotype as the final step in proposing it as a new species of Cryptosporidium. Analysis of sequences of 18S rRNA, actin, and HSP70 genes of additional Cryptosporidium isolates from recently sampled California ground squirrels (S. beecheyi) confirms the presence of the unique Sbey-c genotype in S. beecheyi. Phylogenetic and BLAST analysis indicates that the c-genotype in Spermophilus ground squirrels is distinct from Cryptosporidium species/genotypes from other host species currently available in GenBank. We propose to name this c-genotype found in Spermophilus ground squirrels as Cryptosporidium rubeyi n. sp. The mean size of C. rubeyi n. sp. oocysts is 4.67 (4.4–5.0) μm × 4.34 (4.0–5.0) μm, with a length/width index of 1.08 (n = 220). Oocysts of C. rubeyi n. sp. are not infectious to neonatal BALB/c mice and Holstein calves. GenBank accession numbers for C. rubeyi n. sp. are DQ295012, AY462233, and KM010224 for the 18S rRNA gene, KM010227 for the actin gene, and KM010229 for the HSP70 gene.

Effects of Prey Abundance on Breeding Season Diet of Northern Goshawks (Accipiter gentilis) Within an Unusual Prey Landscape

A critical element of diet analysis is species adaptability to alternative prey sources. The breeding-season diet of Northern Goshawks (Accipiter gentilis) includes both mammalian and avian species, varies geographically, and is often dependent upon tree squirrels of the genera Sciurus and Tamiasciurus. We studied alternative prey sources of Northern Goshawks in the South Hills of south-central Idaho, an area where tree squirrels are naturally absent and other prey frequently important in the diet of goshawks, such as smaller corvids, are uncommon. We quantified the diet of goshawks using nest cameras and surveyed abundance of prey using line transects. We found that goshawks consumed roughly 18.5% birds and 78.7% mammals by biomass, with diet dominated by the Belding's ground squirrel (Urocitellus beldingi, also known as Spermophilus beldingi; 74.8% of total biomass consumed); however, the percentages of mammals and birds in the diet varied between years. The diet was low in diversity, with high overlap among nests, indicating a strong local dependence on the dominant food item. Lastly, the proportion of mammalian prey in the diet was greater in larger broods than in smaller broods. This study provides new insight into the adaptability of the goshawk, particularly in areas with unique prey assemblages.Un elemento crítico del análisis de la dieta es la adaptabilidad de las especies a fuentes de presa alternativas. La dieta de la estación reproductiva de Accipiter gentilis varía geográficamente e incluye especies de mamíferos y aves, y depende a menudo de ardillas arborícolas de los géneros Sciurus y Tamiasciurus. Estudiamos fuentes de presa alternativas de A. gentilis en las South Hills del centro sur de Idaho, un área donde las ardillas arborícolas están naturalmente ausentes y donde son poco comunes otras presas frecuentemente importantes en la dieta de A. gentilis, como córvidos más pequeños. Cuantificamos la dieta de A. gentilis colocando cámaras en los nidos y medimos la abundancia de presas usando transectas lineales. Encontramos que los individuos de A. gentilis consumieron aproximadamente 18.5% de aves y 78.7% de mamíferos en términos de biomasa, con una dieta dominada por la ardilla Urocitellus beldingi, también conocida como Spermophilus beldingi (74.8% de la biomasa total consumida). Sin embargo, los porcentajes de mamíferos y aves en la dieta variaron entre años. La dieta fue poco diversa, con un elevado solapamiento entre nidos, indicando una fuerte dependencia local en la presa dominante. Por último, la proporción de presas de mamíferos en la dieta fue mayor en las nidadas más grandes que en las pequeñas. Este estudio brinda una nueva perspectiva sobre la adaptabilidad de A. gentilis, particularmente en áreas con un ensamble de presa único.

Network structure and prevalence of Cryptosporidium in Belding’s ground squirrels

Althoughpathogen transmissiondynamics are pro- foundly affected by population social and spatial structure, few studies have empirically demonstrated the population- level implications of such structure in wildlife. In particular, epidemiological models predict that the extent to which con- tact patterns are clustered decreases a pathogen's ability to spread throughout an entire population, but this effect has yet to be demonstrated in a natural population. Here, we use network analysis to examine patterns of transmission of an environmentally transmitted parasite, Cryptosporidium spp., in Belding' sg round squirrels (Spermophilus beldingi). We found that the prevalence of Cryptosporidium was negatively correlated with transitivity, a measure of network clustering, and positively correlated with the percentage of juvenile males. Additionally, network transitivity decreased when there were higher percentages of juvenile males; the explor- atory behavior demonstrated by juvenile males may have altered the structure of the network by reducing clustering, and low clustering was associated with high prevalence. We suggest that juvenile males are critical in mediating the ability of Cryptosporidium to spread through colonies, and thus may function as "super-spreaders." Our results demonstrate the utility of a network approach in quantifying mechanistically how differences in contact patterns may lead to system-level differences in infection patterns.

Arthropod Vectors and Vector-Borne Bacterial Pathogens in Yosemite National Park

Ticks, fleas, and vector-borne pathogens were surveyed in diverse small mammals in Yosemite National Park, California, from 2005 to 2007. A total of 450 unique captures of small mammals was collected during a 3-yr period and yielded 16 species of fleas and 10 species of ticks, including known vectors of Anaplasma phagocytophilum and Borrelia burgdorferi and plague. Serology was performed for A. phagocytophilum, spotted fever group Rickettsia spp., B. burgdorferi, and Yersinia pestis. A. phagocytophilum exposure was identified in 12.1% of all wild small mammals tested, with seropositive animals in 10 species, notably Belding's ground squirrels (Spermophilus beldingi), jumping mice (Zapus princeps), and voles (Microtus sp.). Spotted fever group Rickettsia spp. exposure was detected in 13.9% of all small mammals tested, with seropositive animals in eight species. Additionally, 37.0% of rodents in five species tested were seropositive for B. burgdorferi. No individuals were seropositive for Y. pestis. No animals were polymerase chain reaction positive for any pathogen tested. These results provide baseline data for future research and prediction of emerging vector-borne disease in Yosemite National Park, as well as adding to the known ranges and host species for tick and fleas in California.

The causal role of odours in the development of recognition templates and social preferences

Despite decades of theoretical interest in the role of kin recognition in mate choice and nepotism, data on both the mechanisms and functions of recognition are available for only a few species. Even less common are demonstrations of direct causal links between the production and perceptual components of recognition and subsequent social preferences. Belding's ground squirrels, Spermophilus beldingi, produce odours that vary with kinship and can be used to discriminate classes of kin. However, the links between odours, recognition templates and differential treatment of conspecifics have not been shown empirically. Here I examined whether the manipulation of odour recognition templates influences juvenile behaviours. I induced recognition errors by exposing young to odours from a foreign mother before natal emergence. According to phenotype-matching mechanisms, developing young should incorporate all encountered odours into their kin template and later treat individuals matching the template as kin. As in previous studies, the most preferred play partners were littermates, but young also interacted preferentially with juveniles from the foreign family, whose odours were similar to the foreign mother and therefore matched their templates, compared with unfamiliar, unrelated juveniles. This preference for juveniles of the foreign family could not be due to relatedness or direct familiarity prior to emergence. Patterns of nasal investigations mirrored those of play bouts. This is a novel demonstration of a causal link between recognition cues, recognition templates and ‘kin’-differentiated behaviours, and highlights the potency of social odours during development on later social dynamics.

Inverted-U shape relationship between cortisol and learning in ground squirrels

Adrenal hormones regulate glucose levels, responses to unpredictable stressors and modulate cognition. Glucocorticoids can have an inverted-U shape relationship with cognition, as very low or high levels impair, whereas moderate elevations facilitate, acquisition and retention of memories. To date these relationships have been tested with humans and rodents in laboratory settings rather than with wild animals in biologically relevant contexts. This study examined whether the elevated cortisol observed in juvenile Belding’s ground squirrels ( Spermophilus beldingi) at natal emergence might promote both acquisition of adaptive responses to this species’ two alarm calls warning of predators and memory of the spatial configuration of mothers’ territories. Both experimentally increased and decreased basal cortisol levels interfere with acquisition and retention of an association between a warning call and the appropriate response compared with naturally occurring moderately elevated cortisol. Further, decreased cortisol impairs learning of a novel, complex spatial maze. Thus in the field the brief elevation of cortisol at emergence might facilitate acquisition of spatial memory of a three-dimensional environment and responses to alarm calls during a sensitive period of learning. This novel demonstration of the inverted-U shape function in a wild animal suggests that natural selection has favored a hormonal profile facilitating rapid acquisition of important survival behaviors.

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

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

Development of individually distinct recognition cues

Despite extensive research on the functions of kin recognition, little is known about ontogenetic changes in the cues mediating such recognition. In Belding's ground squirrels, Spermophilus beldingi, secretions from oral glands are both individually distinct and kin distinct, and function in social recognition across many contexts. Behavioral studies of recognition and kin preferences suggest that these cues may change across development, particularly around the time of weaning and emergence from natal burrows (around 25 days of age). I used an habituation-discrimination task with captive S. beldingi, presenting subjects with odors collected from a pair of pups at several ages across early development. I found that at 21 days of age, but not at 7 or 14, young produce detectable odors. Odors are not individually distinct, however, until 28 days of age, after young have emerged from their burrows and begun foraging. In addition, an individual's odor continues to develop after emergence: odors produced by an individual at 20 and 40 days of age are perceived as dissimilar, yet odors produced at 28 and 40 days are treated as similar. Developmental changes in odors provide a proximate explanation for why S. beldingi littermate preferences are not consolidated until after natal emergence, and demonstrate that conspecifics must update their recognition templates as young develop.

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.

Plasma glucocorticoid concentrations and body mass in ground squirrels: Seasonal variation and circannual organization

We examined variation in plasma glucocorticoid concentrations of free-living Belding’s ground squirrels ( Spermophilus beldingi) and captive golden-mantled ground squirrels ( Spermophilus lateralis) housed in constant environmental conditions. Plasma corticosterone concentrations were not significantly correlated with time held captive in traps prior to collection of blood samples in males or non-breeding females, but these variables were significantly correlated in breeding females during the pre-mating, lactation, and post-lactation periods. Among male S. beldingi, plasma corticosterone concentrations increased over the course of the active season, and were significantly higher in non-breeding than breeding individuals. Corticosterone concentrations also increased in non-breeding females throughout the active period. In breeding females, baseline (non-stress) corticosterone concentrations, determined from blood samples collected within 3 min of capture, increased during gestation and declined during lactation, whereas stress values of corticosterone, determined from blood samples collected within 4–11 min of capture, increased during gestation and then again during the period after young emerged from the natal burrow. Changes in plasma corticosterone concentrations of S. beldingi paralleled changes in body mass. Among S. lateralis, plasma concentrations of cortisol were elevated when males and females were in reproductive condition and lower in reproductively quiescent squirrels. The annual peak in plasma cortisol concentrations occurred just prior to increases in body mass associated with pre-hibernation fattening. Collectively, these results suggest that concentrations of circulating glucocorticoids fluctuate with circannual rhythmicity in conjunction with annual cycles of change in body mass and activity; within these circannual cycles glucocorticoid concentrations are influenced by stress and breeding status.

The nature and representation of individual recognition odours in Belding's ground squirrels

In many taxonomic groups, odours provide cues to species identity, reproductive status, genetic relatedness and individual identity. These odour cues are often used to mark territories or other resources and to recognize individuals through direct or indirect olfactory investigation. Belding's ground squirrels, Spermophilus beldingi , frequently scent-mark their environment and they also investigate the scent glands of conspecifics, which suggests that odours play a modulating role in their social relationships. I conducted studies to determine what information is conveyed by various S. beldingi odours and whether this information is used by conspecifics for social recognition. Spermophilus beldingi produce a number of cues that are individually distinct, including odours from oral, dorsal, pedal and anal glands and from ears, but apparently not from urine, although it is unclear whether all of these odours are used for social recognition. This discrimination among odours of individuals does not require prior familiarity with the odour bearers. The volatile components of some odours are sufficient to permit individual discrimination, which may explain how animals appear to ‘recognize’ each other from a short distance. Finally, S. beldingi incorporate multiple odours into their memories of conspecifics as perception of one odour of an individual generalizes to a second odour from it, suggesting a mental representation of familiar individuals. The production of multiple unique odours may facilitate accurate discrimination of conspecifics along several social dimensions, and some of these odours also vary with relatedness. Together, these results indicate a rich olfactory milieu mediating the social lives of S. beldingi .

Functions and consequences of play behaviour in juvenile Belding's ground squirrels

We evaluated hypotheses suggesting that play behaviour in free-living juvenile Belding's ground squirrels, Spermophilus beldingi, helps to regulate energy balance and promotes development of motor skills. We also examined the possibility that play behaviour and motor development influence important early life events in S. beldingi. We regularly measured body fat of juveniles using nondestructive methods, observed their behaviour, conducted motor skills tests, monitored dispersal status of males, and evaluated weaning success of females during their first effort to reproduce as yearlings. Rates of feeding were greater among juveniles who engaged in both social and nonsocial play behaviour at low compared to high rates, suggesting that play does not help young animals expend excess energy that they consume. By contrast, body fat was greater among juveniles who engaged in social play at high compared to low rates, supporting the idea that energetic variables such as body fat limit the expression of play behaviour. Motor skills of juvenile S. beldingi improved throughout the period in which juveniles engaged in play behaviour. Improvement in motor skills was greater in juveniles who engaged in social play at high compared to low rates, suggesting a link between social play and motor development. Motor skill levels at the end of the play period were greater among males who dispersed by the end of the juvenile summer than among males still residing in their natal areas. Rates of social play and improvement in motor skills over the course of the play period were greater in females who successfully weaned a litter as yearling than in females who did not. These last two results raise the possibility that play behaviour and motor development during the play period influence important events in the early lives of S. beldingi, which may ultimately influence long-term reproductive success.

Play behavior and motor development in juvenile Belding?s ground squirrels ( Spermophilus beldingi )

We evaluated the relationship between play behavior and motor development in juvenile Belding’s ground squirrels (Spermophilus beldingi). We observed the social play behavior of juvenile S. beldingi during their primary play period and conducted motor skills tests at the beginning and end of the play period. We also placed different-sized boxes in juveniles’ natal areas during the play period and observed box climbing behavior to assess the difficulty of non-social play tasks undertaken by juveniles. Rates of social play were greater in heavy compared to light individuals, supporting the idea that juveniles must selectively allocate available energy among competing demands such as growth and play behavior. Juveniles played almost exclusively with littermates; however, they did not play at equal rates with all partners. Rather, they tended to have one preferred partner and to devote significantly less time to playing with each additional partner, indicating that stability and familiarity are important in social play interactions. Motor skill levels at the end of the play period were greater among juveniles who played with many compared to few partners, suggesting that exposure to a variety of play interactions helps facilitate motor development. Improvement in motor skills was greater among juveniles who played at high compared to low rates, had several compared to few male play partners, and engaged in several compared to few play bouts with male partners, suggesting that elements of play with male partners prominently influence motor development. The partner with whom males played at the highest rate tended to be male, and rates of social play were highest in male biased litters, raising the possibility that improvement in motor proficiency arising from play with males may be especially important for young males. The size of experimental boxes that juveniles climbed increased during the play period, supporting the idea that individuals choose play tasks that pose the greatest challenge.

KIN RECOGNITION IN GROUND SQUIRRELS AND OTHER RODENTS

Significant advances have been made in understanding kin recognition as it pertains to nepotism (preferential treatment of kin) and mate choice (optimization of inbreeding and outbreeding). Yet complementary knowledge about how animals discriminate conspecifics on the basis of genetic relatedness remains unclear for most species. Because of the diversity of their scent sources and highly developed olfactory systems, rodents present a unique opportunity for examining chemical communication and kin recognition as a function of sociality. I review general processes of kin recognition and summarize mechanisms of recognition used by rodents. As a case study, I also examine recognition systems of ground squirrels, relating odor production and perception to differences in patterns of nepotism. Belding’s ground squirrels ( Spermophilus beldingi) produce $2 odors (from oral and dorsal glands) that correlate with relatedness (kin labels), and they are able to use these odors to make precise discriminations among their unfamiliar relatives. Thus, S. beldingi can recognize their distant female kin and male kin, even though these kin are not treated nepotistically (e.g., through cooperative territory defense or alarm call production). Furthermore, S. beldingi use these kin labels and recognition abilities to interact differentially with conspecifics as a function of relatedness. In ground squirrels and in other rodents, components of the kin recognition process (production of recognition cues, discrimination of these cues, and differential treatment of conspecifics) have evolved differentially among even closely related species. Kin recognition abilities in the absence of nepotism might reflect selection for inbreeding avoidance mechanisms, in addition to sex-biased natal dispersal. Together, data and the review demonstrate that recognition abilities cannot be predicted on the basis of sociality alone and suggest that comparative analyses, by multiple assays of discrimination, might be necessary to understand variation in the function of kin recognition within and across species.

Individual acoustic variation in Belding's ground squirrel alarm chirps in the High Sierra Nevada.

The acoustic structure of calls within call types can vary as function of individual identity, sex, and social group membership and is important in kin and social group recognition. Belding’s ground squirrels (Spermophilus beldingi) produce alarm chirps that function in predator avoidance but little is known about the acoustic variability of these alarm chirps. The purpose of this preliminary study was to analyze the acoustic structure of alarm chirps with respect to individual differences (e.g., signature information) from eight Belding’s ground squirrels from four different lakes in the High Sierra Nevada. Results demonstrate that alarm chirps are individually distinctive, and that acoustic similarity among individuals may correspond to genetic similarity and thus dispersal patterns in this species. These data suggest, on a preliminary basis, that the acoustic structure of calls might be used as a bioacoustic tool for tracking individuals, dispersal, and other population dynamics in Belding’s ground squirrels, and perhaps other vocal species.

Seasonal effects of food provisioning on body fat, insulin, and corticosterone in free-living juvenile Belding's ground squirrels (Spermophilus beldingi)

We evaluated the relationship between body fat and the metabolic hormones insulin and corticosterone in free-living juvenile Belding's ground squirrels (Spermophilus beldingi). Some free-living juveniles were provisioned with extra food high in fat and calories, and unprovisioned juveniles were used as controls. Body fat (as a percentage of body mass) of squirrels was regularly evaluated using non-invasive methods. Blood samples were also regularly collected from juveniles and assayed for plasma concentrations of insulin and corticosterone. Provisioned juveniles were fatter than unprovisioned juveniles during most of the active season, but differences in body fat disappeared near the end of summer as juveniles began fattening for hibernation. Thus, our data indicate that although body fat may fluctuate with energy availability early in the active season, it is regulated at precise levels as squirrels prepare for winter. Plasma corticosterone concentrations did not differ between provisioned and unprovisioned juveniles. However, plasma insulin concentrations were greater in provisioned than in unprovisioned juveniles early in the summer. Differences in insulin concentrations disappeared later in the active season, just prior to the disappearance of differences in body fat. Moreover, plasma insulin concentrations were significantly correlated with subsequent changes in body fat. Thus, our data suggest a link between insulin and seasonal regulation of body fat in juvenile S. beldingi.

Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas.

Little is known about to what extent the sensitivity of the hypothalamic-pituitary-adrenal (HPA) axis may be state dependent and vary in the same species between environments. Here we tested whether the faecal corticosteroid concentrations of matrilineal adult female spotted hyenas are influenced by social and reproductive status in adjacent ecosystems and whether they vary between periods with and without social stress. Females in the Serengeti National Park frequently become socially subordinate intruders in other hyena territories by undertaking long-distance foraging trips to migratory herds, whereas in the Ngorongoro Crater they usually forage inside their own small territories on resident prey. The faecal corticosteroid concentrations in Serengeti females were significantly higher than in Ngorongoro females. Energy expenditure by lactation is exceptionally high in spotted hyenas and this may be reflected in their corticosteroid levels. The faecal corticosteroid levels in both populations were higher in lactating than in non-lactating females. During periods of social stability, faecal corticosteroid concentrations increased in non-lactating females but not in lactating females as social status declined. Lactating Serengeti females had significantly higher faecal corticosteroid concentrations during periods with acute severe social stress than during periods without, indicating that the HPA axis is sensitive to social stimuli even in lactating females. So far few studies have used non-invasive monitoring methods for assessing social stress in freeranging animals. This study demonstrates for the first time, to the authors' knowledge, that corticosteroid concentrations may differ between periods with and without social stress for a free-ranging female mammal and that the modulating effect of social status may depend on reproductive status.

Food availability affects behavior but not circulating gonadal hormones in maternal Belding's ground squirrels

We tested predictions of hypotheses suggesting that the steroid hormones, testosterone (T), progesterone (P), and estradiol (E 2), contribute to the energetic regulation of behaviors associated with rearing young in free-living female Belding's ground squirrels ( Spermophilus beldingi). We provisioned some female S. beldingi with food rich in fat and calories, and used unprovisioned females as controls. We observed the behavior of females throughout the reproductive cycle, and regularly collected blood samples to measure plasma hormone concentrations. Circulating concentrations of T, P, and E 2 were similar in provisioned and unprovisioned females, as were temporal patterns of variation in these hormones. Peaks in rates of nest maintenance and aggressive behavior occurred during gestation and were associated with elevated concentrations of circulating T, P, and E 2, raising the possibility that one or more of these hormones mediates behaviors that help females establish maternal nest sites and territories after mating. Temporal patterns of variation in behavior were similar among provisioned and unprovisioned females; however, rates of resting, vigilance, and aggression were higher among provisioned females, whereas unprovisioned females devoted significantly more time to feeding and locomotion. Thus, our data suggest that in maternal S. beldingi, gonadal steroids play a role in mediating behavior associated with raising offspring, but do not facilitate changes in rates of behavior associated with increased energy availability.

Retention of social recognition after hibernation in Belding's ground squirrels

The retention of social memory during long periods of separation, such as hibernation or migration, has not been well documented, despite evidence for long-term social relationships in migrating species or in long-lived sedentary species. We investigated the ability of captive Belding's ground squirrels, Spermophilus beldingi, to remember previously familiar individuals as well as littermates after 9 months of isolation. Before hibernation, young ground squirrels discriminated between odours of familiar and unfamiliar individuals, as shown by greater investigation of a novel individual's odour. The following spring, these yearlings did not respond differentially to odours of previously familiar and unfamiliar individuals, suggesting that memory for familiar conspecifics was lost during hibernation. In contrast, both female and male yearlings continued to discriminate between odours of littermates and previously familiar nonlittermates. Thus, recognition of close kin was maintained during prolonged social isolation, but recognition of familiar, unrelated individuals was not. If re-establishment of familiarity is not costly or if adults rarely interact with the same individuals in successive years, then selection may not favour retention of individual memories of particular conspecifics over the winter. Even though males rarely encounter kin after dispersal, yearling males did recognize their siblings, suggesting that the relative costs of maintaining kin-recognition abilities year-round may be low. Possible mechanisms underlying the formation and maintenance of individual and kin recognition are discussed.