Social thermoregulation during hibernation in alpine marmots (Marmota marmota)

Summary Body temperature (T _b) of socially hibernating alpine marmots, a pair and two family groups, was monitored continuously from October to March with implanted temperature-sensitive radiotransmitters. At the same time, the animals' behaviour was observed. The recurrent entrances into and arousals from hibernation were highly synchronised within groups. Group members always lay huddled together when euthermic and also when torpid with a few exceptions at higher ambient temperatures (T _a). Body contact with euthermic nestmates warmed torpid marmots passively. TheT _b of animals reentering hibernation did not fall to values close toT _a as long as euthermic group members were present. Although animals presumably save energy through social thermoregulation, especially when euthermic, these benefits are not necessarily mutual among group members. Differences in thermoregulatory behaviour of individuals described in this study could be responsible for differential weight losses during winter as found in the natural habitat (Arnold 1986).     

Isolation and characterization of microsatellites in European alpine marmots (Marmota marmota)

For future investigations of the mating system of a highly social mammal (Marmota marmota), we identified 16 new microsatellites using an enrichment protocol. Five loci were revealed to be polymorphic. The polymorphism was rather low (two to six alleles among 24 individuals). However, these markers, added to the other six published microsatellites for M. marmota and Spermophilus citellus, will help to assess dispersal patterns and test for genetic monogamy in alpine marmots from the European Alps.     

Postweaning mass gain in juvenile alpine marmots Marmota marmota

The effects of several environmental factors on the postweaning growth of wild Alpine marmots were investigated. Factors considered were year of birth, sun exposure in the home range, litter size, and sex of young. Components of growth were juvenile mass at emergence from the natal burrow (as a result of preweaning growth) and postweaning growth rate. We also considered the length of the active season during which growth occurs. Mass at emergence and postweaning growth rate varied according to year of birth, were higher in south-facing than in north-facing home ranges, and were higher in small litters. Mass at emergence was higher for males than for females. We suggest that environmental factors affected the juvenile growth pattern through influences on maternal body condition. Our results support Trombulak's hypothesis that mothers maintain as many young as physiologically possible. We suggest that mothers in poor condition sacrificed the mass of their offspring rather than their number. A body mass sexual dimorphism of juveniles occurred at emergence, suggesting that mothers may provide more care for their male than their female offspring. Received: 9 June 1997 / Accepted: 22 September 1997     

Regulation of body temperature and energy requirements of hibernating alpine marmots (Marmota marmota)

Body temperature and metabolic rate were recorded continuously in two groups of marmots either exposed to seasonally decreasing ambient temperature (15 to 0 degrees C) over the entire hibernation season or to short-duration temperature changes during midwinter. Hibernation bouts were characterized by an initial 95% reduction of metabolic rate facilitating the drop in body temperature and by rhythmic fluctuations during continued hibernation. During midwinter, we observed a constant minimal metabolic rate of 13.6 ml O(2) x kg(-1) x h(-1) between 5 and 15 degrees C ambient temperature, although body temperature increased from 7.8 to 17.6 degrees C, and a proportional increase of metabolic rate below 5 degrees C ambient temperature. This apparent lack of a Q(10) effect shows that energy expenditure is actively downregulated and controlled at a minimum level despite changes in body temperature. However, thermal conductance stayed minimal (7.65 +/- 1.95 ml O(2) x kg(-1) x h(-1) x degrees C(-1)) at all temperatures, thus slowing down cooling velocity when entering hibernation. Basal metabolic rate of summer-active marmots was double that of winter-fasting marmots (370 vs. 190 ml O(2) x kg(-1) x h(-1)). In summary, we provide strong evidence that hibernation is not only a voluntary but a well-regulated strategy to counter food shortage and increased energy demands during winter.     

Thermoregulation as a limit to habitat use in alpine marmots (Marmota marmota)

Summary The body temperature (T _b) of free-living alpine marmots rose with activity; the higher the effective environmental temperature (T _e), the higher the rise. Maximum T _bof 40° C was reached at the time of greatest activity in late afternoon or evening. The activity pattern was strongly influenced by the microclimate. Up to an T _eof 25° C the animals spent more time above ground and were more active the higher T _ewas, but above 25° C this trend was reversed, and the animals withdrew increasingly into their burrows. On warm days the activity pattern was therefore bimodal and above ground presence was reduced, in contrast to cool days. Hence behavioural thermoregulation limits the available time for above ground activity on days with high T _ein this strictly diurnal species. We suggest that the alpine marmots' preference for south oriented slopes is due to the better conditions for hibernation there, the microclimate during summer is more favourable on northerly slopes. Thermoregulatory constraints could also keep alpine marmots away from lower elevations.     

Genetic diversity-fitness correlation revealed by microsatellite analyses in European alpine marmots (Marmota marmota)

The relationship between individual genetic diversity and fitness-related traits are poorly understood in the wild. The availability of highly polymorphic molecular markers, such as microsatellites, has made research on this subject more feasible. We used three microsatellite-based measures of genetic diversity, individual heterozygosity H, mean d ² and mean d ² _outbreeding to test for a relationship between individual genetic diversity and important fitness trait, juvenile survival, in a population of alpine marmots (Marmota marmota), after controlling for the effects of ecological, social and physiological parameters that potentially influence juvenile survival in marmots. Analyses were conducted on 158 juveniles, and revealed a positive association between juvenile survival and genetic diversity measured by mean H. No association was found with mean d ² and with mean d ² _outbreeding. This suggests a fitness disadvantage to less heterozygous juveniles. The genetic diversity-fitness correlation (GDFC) was somewhat stronger during years with poor environmental conditions (i.e. wet summers). The stressful environmental conditions of this high mountain population might enhance inbreeding depression and make this association between genetic diversity and fitness detectable. Moreover the mating system, allowing extra pair copulation by occasional immigrants, as well as close inbreeding, favours a wide range of individual genetic diversity (mean H ranges from 0.125 to 1), which also may have facilitated the detection of the GDFC. The results further suggest that the observed GDFC is likely to be explained by the “local effect” hypothesis rather than by the “general effect” hypothesis.     

Male-caused failure of female reproduction and its adaptive value in alpine marmots (Marmota marmota)

We studied reproductive performance of free-living alpine marmots (Marmotamarmota) for 14 years in the National Park of Berchtesgaden, Germany.Female reproduction was influenced by body condition and social factors.Reproduction depleted fat reserves, and only females emergingfrom hibernation with sufficient body mass were able to reproducesuccessfully. Marmots lived in social groups in territoriesdefended by a dominant male and female. Subordinate femalesnever reproduced, regardless of body mass. Territory takeoversby males impaired reproduction of dominant females, but onlyif the takeover occurred after the mating period. Reproductivefailures occurred despite clear signs of pregnancy such enlargednipples or late molt. Decreasing progesterone levels after themating period and the lack of evidence for direct infanticideby new territorial males suggest a block of pregnancy as a likelyexplanation for reproductive failures in groups with male takeoversduring gestation. Rendering female reproduction impossible increasedfuture reproductive success of new territory owners. Nonparous femalessaved the energetic cost of maternal investment and thus emergedwith higher body mass in the following spring. In line withthis, females failing to wean young had higher reproductivesuccess in the subsequent year.     

Evaluation of three combinations of anesthetics for use in free-ranging alpine marmots (Marmota marmota)

From April 1998 to September 2000, 241 free-ranging alpine marmots (Marmota marmota) were anesthetized in the course of a field project using either xylazine plus ketamine (XK), medetomidine plus ketamine (MK), or xylazine plus a 1:1 mixture of zolazepam and tiletamine (XZT). For each of the combinations, the respective doses for short term and long-term surgery were established and seasonal variations in the amount of drugs needed were assessed. No fatalities occurred, and doses for efficient and safe anesthesia in spring were as follows (XK, MK, and XZT, respectively, in mg/kg body mass): short term surgery 3 + 40, 0.25 + 35, and 3 + 15; long term surgery 20 + 80, 0.5 + 70, and 10 + 20. In late summer/autumn, higher doses (20 + 60, 0.2 + 60, and 10 + 15 for short term surgery) had to be administered, probably due to increase of marmots' body fat content. Heart rate, respiratory rate, rectal temperature, palpebral reflex, muscle relaxation, and analgesia were monitored to evaluate the animals' responses to each of the drug combinations. Hypothermia was induced by all combinations and heart rate significantly decreased during anesthesia, especially in marmots receiving MK. Respiratory rate was highly variable and no significant differences between the drugs were found. Muscle relaxation was rather poor in marmots anesthetized with XK. The XZT combination tended to have a longer induction period but was found to subsequently depress the palpebral reflex and induce muscle relaxation and analgesia very efficiently. We conclude that, regardless of the anesthetics used, doses should always be adjusted to the planned manipulations, the marmots' nutritional state, and to the time of year. Furthermore, close monitoring of physiologic parameters, especially body temperature, should be guaranteed. On the basis of physiologic and behavioral responses, XZT is the most effective drug combination for anesthetizing alpine marmots, especially for long term, potentially painful procedures.     

Age-specific effect of heterozygosity on survival in alpine marmots, Marmota marmota

The fitness consequences of heterozygosity and the mechanisms underpinning them are still highly controversial. Using capture–mark–recapture models, we investigated the effects of individual heterozygosity, measured at 16 microsatellite markers, on age-dependent survival and access to dominance in a socially monogamous mammalian species, the alpine marmot. We found a positive correlation between standardized multilocus heterozygosity and juvenile survival. However, there was no correlation between standardized multilocus heterozygosity and either survival of older individuals or access to dominance. The disappearance of a significant heterozygosity fitness correlation when individuals older than juveniles are considered is consistent with the prediction that differences in survival among individuals are maximal early in life. The lack of a correlation between heterozygosity and access to dominance may be a consequence of few homozygous individuals attaining the age at which they might reach dominance. Two hypotheses have been proposed to explain heterozygosity-fitness correlations: genome-wide effects reflected by all markers or local effects of specific markers linked to genes that determine fitness. In accordance with genome-wide effects of heterozygosity, we found significant correlations between heterozygosities calculated across single locus or across two sets of eight loci. Thus, the genome-wide heterozygosity effect seems to explain the observed heterozygosity-fitness correlation in the alpine marmot.     

Ectoparasite loads decrease the fitness of alpine marmots (Marmota marmota) but are not a cost of sociality

Parasites arc often considered an unavoidable cost of livingin groups. We examined this hypothesis by investigating theectoparasite fauna of a free-living alpine marmot population,a highly social sciurid species. Only a single important ectoparasitewas found, the mite Echinonyssus blanchardi. Heavy infestationwith this mite correlated with reproductive success of marmotsin two ways. Infant winter mortality increased with ectoparasiteload, probably because ectoparasites reduced the ability ofparents and alloparents to warm infants during hibernation.Litters produced by females exposed to a high number of mitesduring the preceding winter were weaned later. Late weanershad a lower chance of surviving hibernation. However, we foundno relationship between ectoparasite load and group size ormarmot density. Instead, the number of E. blanchardi per animalwas lower in areas where marmot groups were clumped, i.e., infavorable habitats. Although ectoparasites most likely decreasethe fitess of alpine marmots to some extent, they should notbe considered a cost of social life in this species.     

Seasonal changes in serum metabolites in free-ranging alpine marmots (<Emphasis Type="Italic">Marmota marmota</Emphasis>)

Circannual changes in serum parameters and body mass were studied in free-ranging Marmota marmota that had been shot in Switzerland (Grisons) for management reasons in May, July, and September of 1995, 1996, and 1997; and in April 1996. Markers of lipid (triglycerides, cholesterol), protein (total protein, urea-nitrogen) and mineral (calcium, inorganic phosphate) metabolism were evaluated in 111 haemolysis-free serum samples; the effects of sex, age, reproductive status, season and year were tested. Mean body mass was higher in adult males than in adult females in July and September, and serum cholesterol concentrations were lower in adult males in May. Pregnant females had lower concentrations of total protein than non-pregnant females, and triglyceride concentrations were negatively correlated with the number of uterine ampullae. Inorganic phosphate decreased and total protein increased with age. In adults, triglycerides, cholesterol and urea-nitrogen increased mainly from May to July and decreased between September and May. Total protein, calcium and phosphate did not change throughout the year. This suggests that, during the active season, ingested lipids and amino acids were utilised for metabolic needs or lipid storage, while in winter, lipids were catabolised and protein was spared. Quantitative differences between years, observed for triglycerides and total protein during the active season, were probably due to different climatic conditions in each year.     

Sex ratio variation in the cooperatively breeding alpine marmot Marmota marmota

In cooperatively breeding vertebrate species, a clear theoreticalprediction about the direction of sex ratio adjustment can bemade: mothers should bias the sex ratio of their offspring towardsthe helping sex when helpers are absent. A consistent trendin the direction predicted by theory exists in cooperative birds,but theory is still poorly tested in cooperative mammals. Here,multivariate analyses are applied to a long-term data set totest this prediction in two ways in the alpine marmot: (1) acrossfemales in a population and (2) in individual females acrossmultiple years. It was shown that in the alpine marmot offspringsex ratio was biased towards the helping sex (males) when helperswere absent, whereas helped mothers produced unbiased sex ratio.Unhelped mothers did not adjust the litter size but producedmore sons and fewer daughters than helped mothers. These resultssupport the theoretical prediction and explain well the malebias observed among juvenile alpine marmots at the populationlevel. The occurrence of possible sex ratio manipulations incooperatively breeding vertebrates is also discussed.     

Seasonal glucose uptake in marmots (Marmota flaviventris): the role of pancreatic hormones.

1. Glucose uptake was measured throughout the year in marmots (Marmota flaviventris) by the hyperglycemic clamp technique. During each 2 hr experiment, the plasma glucose level was maintained at 215 mg/dl while blood samples were collected and analysed for glucose, insulin, glucagon, cortisol and catecholamines. 2. Glucose uptake was calculated from the glucose infusion rate, changes in the glucose pool (using a correction factor), and urinary glucose excretion. 3. In autumn, animals peaked in body weight (greater than 4.0 kg) and ceased to feed. Basal plasma insulin levels in autumn were significantly elevated over all other seasons (P less than 0.01) and glucose uptake in autumn was 9.7 +/- 2.4 mg/min which was significantly lower (P less than 0.05) than summer (21.7 +/- 2.4 mg/min) during the steady state phase of the glucose clamp (90-120 min). 4. Plasma glucagon levels declined during the clamp in all seasons but there was no significant difference between seasons. Plasma cortisol and catecholamine (norepinephrine and epinephrine) levels remained unchanged under basal and experimental conditions throughout the seasons. 5. During glucose infusion, beta-hydroxybutyrate levels were suppressed suggesting that lipolysis was reduced during the experiment. 6. These results suggest that the marmot exhibits seasonal changes in glucose uptake; the lowest rate of glucose uptake occurring in the autumn after the animals peak in body weight and cease to feed.     

Cheek-rubbing in golden marmots (Marmota caudata aurea)

We studied the function of cheek-rubbing in golden marmots ( Marmota caudata aurea ) by combining observations of the external morphology of the orbital gland, observational studies of marmots cheek-rubbing, and experimental studies of marmots'responses to olfactory secretions from the orbital gland. Adult males had larger eyepatches–areas without hair above the orbital gland–than adult females. Both sexes produced sufficient glandular exudate to pool on the surface of the skin or fur above the orbital gland. Adult males cheek-rubbed more than adult females throughout the summer active season, but both males and females generally cheek-rubbed within 10m of a main burrow. Adult males responded more vigorously to the smells of non-group members of both sexes than to group members of either sex. Adult females responded more vigorously to the smell of non-group females than to non-group males or group members of either sex. Our results are consistent with the hypothesis that marmot cheek-rubbing functions to mark defended areas, possibly to minimize costs of aggressive interactions.     

Habitat preferences in gray marmots (Marmota baibacina)

We examined habitat preferences of the Southern Altai subspecies of gray marmots (Marmota baibacina baibacina) both at the small and large scale. Considerable differences in habitat use among the gray marmot (sub)species complex have been described; Marmota kastschenkoi possibly represents the only forest-dwelling Palearctic marmot. Our results show that habitat use in Southern Altai marmots is determined mainly by vegetation type. The Altai marmots preferred grasslands and shrublands and their distribution was limited to the alpine zone above timberline. Marmots clearly avoided woodlands, even the forest edges and forest-steppe areas with a tree cover greater than 10 %. Gray marmots occur rarely in habitats occupied by alpine pikas, whereas presence of ground squirrels had no effect on marmot distribution. Altai marmots preferred mesic habitats with permeable subsoil layers. Livestock grazing and human disturbance did not affect marmot occurrence. Habitat requirements of examined Altai subspecies M. baibacina baibacina differ from the forest-steppe M. kastschenkoi; nevertheless, the ecological factors to which the forest-dwelling species responds remain to be analyzed. A recent speciation process in gray marmot complex was followed by the evolution of ecological requirements resulting in adaptation to forest dwelling.     

Energetics of hibernating yellow-bellied marmots (Marmota flaviventris)

Yellow-bellied marmots (Rodentia: Sciuridae) typically hibernate for eight months. This study explored energetic costs of hibernation in young and adults at 10 and 6 degrees C. Age significantly affected the percent time torpid, total and mass-specific VO(2), use of energy during torpor, and daily mass loss at 6 degrees C. Thus young had a higher mass-specific VO(2) during a torpor bout, which was attributed to higher metabolism during deep torpor. Total VO(2) during a bout was higher in young and there were significant temperature/age interactions; young had a higher VO(2) during torpor and deep torpor at 6 degrees C than at 10 degrees C. VO(2) increased at T(E)s below 6 degrees C. Young had a higher daily mass loss than adults at 6 degrees C. Euthermy increased energetic costs 19.3 times over those of torpor and 23.5 times over those of deep torpor. Energy costs are minimized by spending 88.6% of the hibernation period in torpor, by the rapid decline of VO(2) from euthermy to torpor and by allowing T(B) to decline at low T(E). Torpidity results in average energy savings during winter of 83.3% of the costs of maintaining euthermy. Energy savings are greater than those reported for Marmota marmota and M. monax.     

Modelling the role of social behavior in the persistence of the alpine marmot Marmota marmota

A general rule of thumb for biological conservation obtained from simple models of hypothetical species is that for populations with strong environmental noise moderate increases in habitat size or quality do not substantially reduce extinction risk. However, whether this rule also holds for real species with complex behavior, such as social species with breeding units and reproductive suppression, is uncertain. Here we present a population viability analysis of the alpine marmot Marmota marmota, which displays marked social behavior, i.e. it lives in social groups of up to twenty individuals. Our analysis is based on a long‐term field study carried out in the Bavarian Alps since 1982. During the first fifteen years of this study, 687 marmots were individually marked and the movements and fate of 98 dispersing marmots were recorded with radio‐telemetry. Thus, in contrast to most other viability analyses of spatially structured populations, good data about dispersal exist. A model was constructed which is individual‐based, spatially explicit at the scale of clusters of neighbouring territories, and spatially implicit at larger scales. The decisive aspect of marmot life history, winter mortality, is described by logistic regression where mortality is increased by age and the severity of winter, and decreased by the number of subdominant individuals present in a group. Model predictions of group size distribution are in good agreement with the results of the field study. The model shows that the effect of sociality on winter mortality is very effective in buffering environmental harshness and fluctuations. This underpins theoretical results stating that the appropriate measure of the strength of environmental noise is the ratio between the variance of population growth rate and the intrinsic rate of increase. The lessons from our study for biological conservation are that simple, unstructured models may not be sufficient to assess the viability of species with complex behavioral traits, and that even moderate increases in habitat capacity may substantially reduce extinction risk even if environmental fluctuations seem high.