Eva Millesi

Hibernation effects on memory in European ground squirrels (Spermophilus citellus).

Effects of hibernation on memory were tested in European ground squirrels (Spermophilus citellus). The animals were trained in summer to successfully accomplish two tasks: a spatial memory task in a maze and an operant task on a feeding machine. One group hibernated normally, and the other was prevented from hibernation by maintaining ambient temperature at 22 °C. In spring, the same tasks were repeated for both groups and their individual performances compared to the initial training phase. The experimental groups differed significantly in both tasks. The nonhibernating animals had higher levels of retention and needed significantly fewer trials to relearn the tasks than the group that had hibernated. In addition to testing the retention of conditioned tasks, social memory was also studied. The ground squirrels were given a social recognition test in spring with one familiar and one unfamiliar conspecific. In contrast to the conditioned tasks, social memory did not seem to be affected by hibernation. The results indicate negative effects of hibernation on the retention of conditioned tasks, which could produce important constraints on animals. A potential explanation for this memory loss might be changes in neuronal activity, which occur during hibernation.

Sex and age differences in mass, morphology, and annual cycle in European ground squirrels, Spermophilus citellus

We collected 6 years of data (1990-1995) on survival, hibernation, body-mass changes, and morphological parameters for a suburban population of European ground squirrels (Spermophilus citellus) using censusing and capture-recapture techniques. We attempted to determine differences in sex and age in these parameters. In the focal population, sex ratios of adults and yearlings were female-biased, but the sex ratio of juveniles was balanced. Overwinter mortality was low, but losses during the active season were high in all sex and age groups. Male and female juveniles disappeared from their natal area in roughly equal proportions. Among older individuals, more males disappeared than females. Hibernation patterns were similar to other Spermophilus species, except that females began hibernation before males. Therefore, females had significantly longer hibernation periods and higher proportional overwinter losses of mass than males. All adult (greater than or equal to 2 years) but only a few yearling males were reproductively active. Yearling males emerged from hibernation with a lower mass than adults but were indistinguishable from them before subsequent immergence. Adult and yearling females reproduced and lost mass during late lactation, a pattern more pronounced in older than yearling females. Juvenile males were heavier than juvenile females before hibernation, although no difference was found at weaning. Skull size increased in the first two active seasons but did not change thereafter. Differences in sex and age resembled those of most hibernating,ground squirrels in many aspects but also showed some unusual patterns that probably have evolved due to specific environmental constraints in this species.

Reproductive effort and costs of reproduction in female European ground squirrels

Abstract Reproductive effort, factors affecting reproductive output and costs of reproduction were studied in primiparous yearling compared to multiparous older female European ground squirrels (Spermophilus citellus). Yearling females weaned smaller litters than older ones. Litter size increased with posthibernation body mass at the expense of slightly lighter young for yearling but not for older mothers. In older females, on the other hand, emergence body mass influenced offspring mass, whereas litter size was affected by oestrus date. High reproductive effort entailed reproductive costs in terms of reduced subsequent fecundity but not subsequent survival for both yearling and older females. The production of large litters and long duration of lactation delayed subsequent oestrus, which, in turn, correlated negatively with litter size. During the second half of lactation, oestradiol levels were significantly elevated, indicating the initiation of follicular maturation processes. Oestradiol levels during that time correlated negatively with current, but positively with subsequent litter size. We therefore assume that inhibitory effects of lactation on gonadal development may mediate the negative relationship between reproductive effort and subsequent reproductive timing in adults. This effect is absent in yearlings because they are reproducing for the first time. Reproductive output in yearlings was influenced by interactions between structural growth and puberty.

Living in a Seasonal World

Some mammal lineages survived the global fires that occurred in the hours following the asteroid impact at Chicxulub, Yucatan, at the Cretaceous/Tertiary Boundary (K/T Boundary) 65 mya. Several studies have proposed that it was the capacity for torpor and refuge underground, in tree holes, caves, and underwater, that ensured the shortand long-term survival of the post-impact conditions. Here I test the hypothesis that heterothermy was a pleisiomorphic condition in ancestral mammals which allowed certain mammal lineages to survive the K/T Boundary. I employed a maximum likelihood approach to reconstruct the likely heterothermic status of the last mammalian ancestor. With our current knowledge, the probability of heterothermy (58%) slightly exceeds that of no heterothermy. However, if some mammals that have yet to be studied, but which have been identified as highly likely heterotherms, are scored as heterotherms, the proportional likelihood of heterothermy in ancestral mammals exceeds the 96% probability. At the least, these data confirm that there was single origin of heterothermy in mammals, but further research is required to determine how extensive heterothermy was in Mesozoic mammals.

POPULATION DYNAMICS OF EUROPEAN GROUND SQUIRRELS (SPERMOPHILUS CITELLUS ) IN A SUBURBAN AREA

Abstract We monitored European ground squirrels (Spermophilus citellus) in a recreation area near Vienna, Austria, over a 7-year period to follow their population dynamics. Data were obtained by mark–recapture and daily checklists in an attempt to track the fates of individuals present in a defined area. Abundance of nonjuveniles present in spring decreased from 56.0 individuals/ha in 1992 to 6.3 individuals/ha in 1998. Litter size and yearling-male reproduction were inversely related to density, whereas immigration, juvenile survival, and proportions of nonjuvenile males exhibited a positive relationship. We conclude that the study population had been a dispersal sink and that ceasing immigration combined with poor local survival caused the population to crash. The temporal coincidence of these 2 effects indicates an extrinsic factor acting both on residents and potential immigrants.

Seasonal variation in daily activity patterns of free-ranging European ground squirrels (Spermophilus citellus)

Daily aboveground activity of European ground squirrels (Spermophilus citellus) in their natural habitat was recorded with a visual scanning procedure during the active seasons of 1992 and 1993. Activity patterns were analyzed with respect to time of year and to the animals reproductive state. Aboveground activity started on average 3.9 h (SD 0.6 h, n = 37 days) after civil twilight at dawn and ended on average 3.2 h (SD 0.9 h, n = 37 days) before civil twilight at dusk. Between onset and offset of activity, 54% was spent aboveground, of which 73% was spent foraging. Activity patterns were influenced by photoperiod, rainfall, and by reproductive state. During mating, reproductively active males started activity earlier than females and reproductively inactive males. For females, time spent foraging was high during lactation. The midpoint of daily activity was at 12:16 h (SD 0.37 h, n = 37 days). Activity patterns of European ground squirrels thus appear robustly positioned in the middle of the photoperiod.

Vernal changes in the behavioral and endocrine responses to GnRH application in male European ground squirrels.

This field study was aimed at examining hypothalamic involvement in the behavioral changes of male European ground squirrels (Spermophilus citellus) before, during, and after the mating season. The effects of exogenous gonadotropin-releasing hormone (GnRH) application on androgen secretion and behavioral patterns were investigated. Animals were captured, bled, and injected intramuscularly with 40 ng/100 g of GnRH. A second plasma sample was collected 40 min after the treatment to document changes in testosterone secretion. Behavioral parameters such as intra-sexual aggression, scent marking, and home range size were compared on the days before and after the stimulation. In the first two phases, before female emergence and during mating, GnRH-injection caused increases in plasma testosterone. In the post-mating phase, initial plasma testosterone levels had decreased and no elevation could be induced. Sham treatment of controls had no effect in any phase. Conditional parameters like emergence body mass and testicular size covaried with androgen increases only in the pre-mating period. Behavioral changes after GnRH administration occurred during the pre-mating period. Intra-sexual aggression, scent marking, and home range size increased significantly in experimental individuals. Later, during mating and post-mating, we found no behavioral changes associated with the GnRH treatment or the testosterone increase. The results demonstrate changes in the endocrine and behavioral sensitivity to GnRH application, according to the phases of the active season. An exogenous pulse of GnRH can apparently release behavior in male European ground squirrels, which is normally context dependent with the emergence of females.

Sexually mature and immature yearling male European ground squirrels: A comparison of behavioral and physiological parameters

Early puberty may increase lifetime reproductive success, but may also entail diverse costs. In male European ground squirrels (Spermophilus citellus), age at sexual maturity varies among individuals. We compared sexually active and inactive yearling males under standardized conditions in outdoor enclosures. Non-reproductive yearling males hibernated significantly longer than mature males and emerged when the mating period had already started. Testosterone concentrations peaked in the precocious males during premating and mating, and were depressed in the non-reproductive individuals throughout the study period. Emergence body mass was similar in both groups, although sexually immature males were significantly heavier at the end of the active season. Additionally, non-reproductive yearlings grew faster than precocious individuals. Male-male aggression peaked during mating and the following 4 weeks. Intense aggressive interactions like chases and fights were mostly initiated by reproductive males and were directed towards mature competitors. Aggressive behavior in immature males was mainly expressed as spatial displacements. Non-agonistic interactions with females were only observed in sexually active males. Concentrations of fecal cortisol metabolites did not differ between the two male groups and were elevated in the second half of the active season. Leucocyte numbers were reduced during mating in mature males, whereas in immature animals, cell numbers did not change significantly. Our results indicate that early puberty in European ground squirrels involves lower growth rates, high intrasexual aggression, lower prehibernatory body mass, and probably worse immunological condition during mating.

Spatial learning and memory differs between single and cohabitated guinea pigs.

In socially-living animals, social enrichment enhances spatial learning and memory while separation from conspecifics can severely impair these abilities. In the present work, guinea pigs were kept in isolation or cohabitated in heterosexual pairs and then subjected to a labyrinth task. Latency-time to bait, error-rate, amount of movement and pre- and post-experimental cortisol (CORT) were registered. During a 5d-acquisition phase, single animals (N=19) showed a more efficient encoding of spatial information, with significantly decreased latency-time and error-rate over the time course. In contrast, cohabitated animals (N=19) did not show a significant improvement. Three days after acquisition, memory was tested in a retention test, under the same conditions. With regard to behavioral performance, there was no significant difference between cohabitated and single animals. Pre-experimental CORT was significantly higher in cohabitated animals when compared to single ones. Post-experimentally, CORT increased significantly in singles but not in cohabitated animals when compared to pre-experimental values. Thus, both groups did not differ from each other at that point. Social condition seemed to be an important modulator, in that learning and memory were more impaired in paired animals than in single ones. The failure of cohabitated animals to encode spatial memory more quickly may have been caused by a more chronically up-regulated HPA-axis. The post-experimental CORT increase of singles may be due to more efficient handling of short-term stress exposure.

Follicular Development and Hibernation in European Ground Squirrels

Obligate hibernators such as European ground squirrels are severely limited by time constraints. Adult females mate shortly after emergence from hibernation, often within one or two days. Follicular maturation therefore has to occur either before or during winter. In this study oestrogen levels of females were monitored throughout the active season in the field. These data were supplemented with information on individuals in captivity during the active season and hibernation. Adult females had high oestrogen levels shortly after the termination of hibernation whereas yearling oestradiol levels were lower and increased later. In adult individuals oestrogens peaked post-lactation and decreased rapidly with the onset of prehibernatory fattening. During hibernation oestrogens remained baseline in all individuals. Ovaries of juvenile and adult females were collected and analysed shortly before and after hibernation. In juveniles, follicles remained primordial through hibernation without reaching an antral stage. In older females differing numbers of intact tertiary follicles were detected. These data suggest that in European ground squirrels follicular maturation is initiated after lactation and terminated at pre-hibernatory fattening. During hibernation gonadal activity is suppressed and follicles are arrested. Females which complete follicular development in summer become oestrous earlier in spring. This is part of an adaptive scheme which can affect reproductive effort and success.