Ilse E. Hoffmann

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.

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.

Anthropogenic effects on the population ecology of European ground squirrels (Spermophilus citellus) at the periphery of their geographic range

Summary European ground squirrels typically inhabit dry grasslands throughout central and south-eastern Europe. Over the past decades, the species increasingly utilises anthropogenically shaped areas. During a 7-year field study on a population in a semi-urban habitat near Vienna, Austria, we monitored a 5.9-fold decrease in ground-squirrel abundance, with high densities having been maintained by immigration. The decline occurred parallel to an escalating urbanisation of the surroundings. A survey concerning the former dispersion of squirrels indicated an increase in population size during the late 1970s, after the region had been drained. Our findings suggest that improved river control of the Danube had ameliorated a sub-optimal habitat, which enhanced the formation of a dispersal sink. After several years of high population levels, abundance decreased, most likely due to anthropogenically promoted landscape fragmentation and habitat degradation. The results of our study support the assumption that artificially induced environmental changes may be crucial for the persistence of small-mammal populations at the edge of their geographic range.

Follicular development in European ground squirrels (Spermophilus citellus) in different phases of the annual cycle

In seasonally breeding mammals, in particular hibernators, reproduction underlies severe energetic and temporal constraints to enable the allocation of sufficient body fat reserves before winter. Thus, the timing of conception in spring can be crucial in terms of reproductive success. This study investigates follicular development in European ground squirrels (Spermophilus citellus) in three phases of the annual cycle: at vernal emergence, after weaning the offspring and shortly before hibernation. The animals were kept in outdoor enclosures within the natural habitat of the species. They were captured in weekly intervals, weighed and reproductive status was determined. Unilateral ovariectomy was scheduled such that the three periods were sampled. Numbers and diameters of tertiary follicles (TF) and corpora lutea (CL) in each ovary were determined, and plasma oestradiol and progesterone levels were analysed. The highest numbers of TF, including Graafian follicles, were found in ovaries at vernal emergence. During post-lactation, the number of TF was lower and active CL appeared in the investigated ovaries. Shortly before hibernation, active CL were present, but luteolysis had started in some individuals. Both oestradiol and progesterone secretion peaked after the termination of lactation and decreased before hibernation. The results demonstrate a second oestrus cycle in European ground squirrels after weaning, including an active luteal phase. This non-reproductive oestrus cycle with its endocrine output is an intriguing phenomenon. It may positively affect both prehibernatory fattening and reproduction in the subsequent season.

Vaginal oestrus during the reproductive and non-reproductive period in European ground squirrels

Most hibernating animals are thought to be monoestrous because reproductive activity is subject to strong time constraints. In previous studies, female European ground squirrels (Spermophilus citellus) turned out to have elevated oestradiol levels during late lactation and after weaning, indicating ovarian activity during summer. Therefore, we monitored vaginal cytology, endocrine changes, and vulval development in semi-free-living female European ground squirrels throughout one active season. Vaginal oestrus, defined by the predominance of cornified cells in smear samples, was found during the mating period shortly after vernal emergence. This phase was followed by metoestrus, characterised by the appearance of leukocytes, and a subsequent anoestrous phase. During weaning or postlactation, a second vaginal oestrus was documented in all experimental females, again followed by a metoestrous and an anoestrous phase lasting until hibernation. In line with the second vaginal oestrus, plasma oestradiol concentrations peaked during postlactation. Progesterone levels were elevated from gestation to postlactation, and titres were marginally higher during vaginal oestrus in summer than in spring. Vulval swelling was more pronounced during the first than the second vaginal oestrus. The second oestrous cycle was non-reproductive, as males were sexually inactive with regressed testes during summer. We assume that the second oestrous cycle and the accompanying endocrine changes have beneficial effects on prehibernatory fattening and reproductive performance in the subsequent season. This might allow females to become oestrous immediately after emergence from hibernation in spring.

Spermophilus citellus (Rodentia: Sciuridae)

Abstract:  Spermophilus citellus (Linnaeus, 1766) is a medium-sized sciurid commonly called the European ground squirrel. The species inhabits grasslands in central and southeastern Europe on a range from short-grass steppes to meadow orchards, and from sea level to an elevation of 2,500 m. These squirrels live in colonies and construct burrows used for hibernation, reproduction, refuge, and resting. Due to serious declines in many portions of its range, the species is listed as “Vulnerable” by the International Union for Conservation of Nature and Natural Resources. It is also protected by the Bern Convention (Appendix II), and the European Union Habitats and Species Directive (Annexes II and IV).

Testis development and testosterone secretion in captive European ground squirrels before, during, and after hibernation

In some hibernating species, an extended euthermic period before spring emergence has been reported during which testicular maturation occurred. In this study, we investigated whether male European ground squirrels Spermophilus citellus (Linnaeus, 1766) develop scrotal testes before or after the termination of hibernation. The course of testis development and testosterone concentrations were examined in young-of-year male ground squirrels (n = 4) before, during, and after their first hibernation. In the environmental chamber, all animals showed regular hibernation patterns with decreasing torpor bout lengths prior to the end of hibernation. Four weeks before hibernation ended, testosterone levels were elevated during spontaneous arousals. Testosterone concentrations peaked during the first 2 months post heterothermy and decreased thereafter. In 2 experimental males, testes descended from the inguinal region into the scrotum shortly before the end of heterothermy. The state of testis development and testosterone secretion corresponded to that found in semi-free-living males at spring emergence. Testis size increased in active animals to maximum widths during weeks 3 and 4 post heterothermy. Scrotal skin pigmentation was absent until heterothermy ended and developed during the first month thereafter. The data suggest that male S. citellus do not need a pre-emergence euthermic period for reproductive development.