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.     

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.     

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.     

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.     

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.     

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.     

Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots (Marmota marmota)

The gastrointestinal tracts of 76 free-living alpine marmots ( Marmota marmota) shot during a population control program in Switzerland were collected and analysed for patterns of change in morphology and function over the period from emergence from hibernation in April to just before re-entry into hibernation in September. Between first emergence and mid-summer (July) the fresh tissue mass of the stomach increased by 105%, the small intestine by 259% (among the largest recorded for a mammal), caecum by 185%, proximal colon by 138%, and distal colon by 144%. Mitotic activity was greatest in the small intestine; the mitotic index was high (40%) compared with indexes in the stomach and hindgut (approximately 4%) even at emergence, and increased to approximately 60% by mid-summer. Microbial activity in the caecum was also significant at emergence. The stomach (length) and caecum (length and fresh mass) increased in response to ingested food earlier than did the small intestine. Between mid-summer and September there were decreases in small intestinal tissue mass and mitotic activity. It is concluded that the gastrointestinal tract of alpine marmots probably continues to function throughout hibernation at a low level, with a mid-winter trough as part of an endogenous circannual rhythm. However, after emergence in spring, increases in size and activity of the tract appear to be a response to ingested food rather than to an endogenous signal. The early signs of down-regulation of the small intestine before re-entry into hibernation, together with its delayed up-regulation in response to food in spring, are consistent with the high costs of maintaining this section of the digestive system.     

Low genetic variability in a natural alpine marmot population (Marmota marmota, Sciuridae) revealed by DNA fingerprinting

Genetic heterogeneity is usually considered an important factor for the viability of a population, yet there are cases in which populations sustain themselves despite virtual homozygosity. A prior step to studying the effects of such low levels of genetic variability can be the analysis of its causes. We analysed a population of the highly social alpine marmot ( Marmota marmota , Sciuridae) by multilocus DNA fingerprinting. The fingerprint patterns revealed a very low degree of polymorphism in our main study population. We show that this lack of hypervariability is caused by a low effective population size, rather than by an unusual low mutation rate of the fingerprint loci studied. However, the current number of breeding pairs was found to be about an order of magnitude larger than the one that would be expected to lead to such a low degree of heterozygosity. We conclude that there must have been bottlenecks in the history of the Berchtesgaden marmot population that have severely affected its genetic heterozygosity.     

Hotspots of (sub)alpine plants in the Irano-Anatolian global biodiversity hotspot are insufficiently protected

Aim

The mountainous regions in SW Asia harbour a high number of endemic species, many of which are restricted to the high-elevation zone. The (sub)alpine habitats of the region are under particular threat due to global change, but their biodiversity hotspots and conservation status have not been investigated so far.

Location

Subalpine-alpine habitats of SW Asia.

Methods

Distribution data of all (sub)alpine vascular plant species of the region were compiled, resulting in 19,680 localities from 1672 (sub)alpine species, the majority of them being restricted to the region (76%). Six quantitative indices of species diversity were used on the basis of 0.5° × 0.5° grid cells to identify (sub)alpine hotspots. Hotspots whose surface area in the (sub)alpine zone was covered by nature reserves maximally by 10% were defined as conservation gaps.

Results

A high proportion (80%) of the endemic species of the study area is range-restricted and narrowly distributed. The results of all six indices were highly correlated. Using the top 5%, 10% and 20% richest cells supported by any index, 32, 53 and 98 cells, respectively, were identified as Hotspots. Almost 60% of these Hotspots at all three levels were identified as unprotected (i.e. constituted Conservation Gaps). Generally, only 22%, 18% and 16%, respectively, of the alpine surface area of the identified Hotspots were covered by nature reserves for the top 5%, 10% and 20% richest cells, respectively.

Main conclusions

Although the rate of protection in (sub)alpine Hotspots exceeds that of the entire region it is still insufficient, because these Hotspots are much richer in endemic and in range-restricted species, but at the same time are under high pressure of global change. Therefore, the establishment of new nature reserves with high conservation efficiency in (sub)alpine habitats with a particular focus on the identified Hotspots is strongly recommended.     

Phylogenetic and environmental components of morphological variation: skull, mandible, and molar shape in marmots (Marmota, Rodentia)

The phenotype is a product of its phylogenetic history and its recent adaptation to local environments, but the relative importance of the two factors is controversial. We assessed the effects of diet, habitat, elevation, temperature, precipitation, body size, and mtDNA genetic divergence on shape variation in skulls, mandibles, and molars, structures that differ in their genetic and functional control. We asked whether these structures have adapted to environment to the same extent and whether they retain the same amount of phylogenetic signal. We studied these traits in intra- and interspecific populations of Eurasian marmots whose last common ancestor lived 2-5 million years ago. Path Analysis revealed that body size explained 10% of variation in skulls, 7% in mandibles, and 15% in molars. Local vegetation explained 7% of variation in skulls, 11% in mandibles, and 12% in molars. Dietary category explained 25% of variation in skulls, 11% in mandibles, and 9% in molars. Cyt b mtDNA divergence (phylogeny) explained 15% of variation in skulls, 7% in mandibles, and 5% in molars. Despite the percentages of phylogenetic variance, maximum-likelihood trees based on molar and skull shape recovered most phylogenetic groupings correctly, but mandible shape did not. The good performance of molars and skulls was probably due to different factors. Skulls are genetically and functionally more complicated than teeth, and they had more mathematically independent components of variation (5-6-in skulls compared to 3-in molars). The high proportion of diet-related variance was not enough to mask the phylogenetic signal. Molars had fewer independent components, but they also have less ecophenotypic variation and evolve more slowly, giving each component a proportionally stronger phylogenetic signal. Molars require larger samples for each operational taxonomic unit than the other structures because the proportion of within-taxon to between-taxon variation was higher. Good phylogenetic signal in quantitative skeletal morphology is likely to be found only when the taxa have a common ancestry no older than hundreds of thousands or millions of years (1% to 10% mtDNA divergence)--under these conditions skulls and molars provide stronger signal than mandibles.     

Microsatellite variation in autochthonous and introduced populations of the Alpine marmot (Marmota marmota) along a European west–east transect

Microsatellite variation was studied in 11 populations of the Alpine marmot along a west–east transect through the present distribution range. The samples represent five autochthonous and six introduced populations. Eleven loci were analysed in nine populations and six loci in the two populations from France. In the populations from the Western Alps, there is no indication for reduced variability as has been assumed in previous studies. However, a decrease of variation in the autochthonous populations was observed from the west to the east. The introduced populations showed a heterogeneous pattern reflecting the geographic origin of the released individuals. The population from the Spanish Pyrenees harbours a high level of variation and is genetically closest to the French populations. In Austria, three of the introduced populations have low variation and are closely related to the autochthonous populations from the western part of Austria. In contrast, two introduced populations from the central part of Austria are highly variable and resemble the populations from France. At least for one of these populations an early introduction of founder individuals from the Western Alps has been documented.     

Heritability and genetic correlations of personality traits in a wild population of yellow‐bellied marmots (Marmota flaviventris)

Describing and quantifying animal personality is now an integral part of behavioural studies because individually distinctive behaviours have ecological and evolutionary consequences. Yet, to fully understand how personality traits may respond to selection, one must understand the underlying heritability and genetic correlations between traits. Previous studies have reported a moderate degree of heritability of personality traits, but few of these studies have either been conducted in the wild or estimated the genetic correlations between personality traits. Estimating the additive genetic variance and covariance in the wild is crucial to understand the evolutionary potential of behavioural traits. Enhanced environmental variation could reduce heritability and genetic correlations, thus leading to different evolutionary predictions. We estimated the additive genetic variance and covariance of docility in the trap, sociability (mirror image stimulation), and exploration and activity in two different contexts (open‐field and mirror image simulation experiments) in a wild population of yellow‐bellied marmots (Marmota flaviventris). We estimated both heritability of behaviours and of personality traits and found nonzero additive genetic variance in these traits. We also found nonzero maternal, permanent environment and year effects. Finally, we found four phenotypic correlations between traits, and one positive genetic correlation between activity in the open‐field test and sociability. We also found permanent environment correlations between activity in both tests and docility and exploration in the MIS test. This is one of a handful of studies to adopt a quantitative genetic approach to explain variation in personality traits in the wild and, thus, provides important insights into the potential variance available for selection.     

High nest failure but better nestling quality for early breeders in an alpine population of Northern Wheatear (Oenanthe oenanthe)

Climate change is leading to the advancement of spring conditions, resulting in an earlier snowmelt and green-up, with highest rates of change in highly seasonal environments, including alpine habitats. Migratory birds breeding at high elevations need to time their arrival and lay dates accurately with this advancement, but also with the annually variable spring conditions at their breeding sites, to maximize nest survival probabilities and reproductive output. Nest survival probability and mean nestling mass were analysed in relation to lay date and habitat conditions in an alpine population of the migratory Northern Wheatear Oenanthe oenanthe collected over six consecutive breeding seasons in the Western Italian Alps. This open grassland species showed the lowest nest survival probability in years with an early onset of spring conditions. Within-season, nest survival was highest when breeding late, at lower elevations, and when grass cover and grass height were higher. Both across- and within-season, severe weather conditions may indirectly lead to higher early season nest failure rates by increasing predation risk. By contrast, mean nestling mass, and thus the quality of the fledglings, was lower when breeding late. This might be driven by a mismatch with the peak in food abundance. Breeding early is thus generally advantageous in terms of chick quality in our high-elevation population, but reproductive success is limited by the risk of nest failure that is higher in early springs and early in the season. This trade-off between breeding early and late may thus allow Northern Wheatears to maximize fitness under highly variable spring conditions. However, climate change may cause disruption to this trade-off, and shifts in phenology could become a threat for migratory alpine birds that might not be able to keep track of advancing spring conditions.     

Contrasting patterns of selection acting on MHC class I and class II DRB genes in the Alpine marmot (Marmota marmota)

The major histocompatibility complex (MHC) genes code for proteins that play a critical role in the immune system response. The MHC genes are among the most polymorphic genes in vertebrates, presumably due to balancing selection. The two MHC classes appear to differ in the rate of evolution, but the reasons for this variation are not well understood. Here, we investigate the level of polymorphism and the evolution of sequences that code for the peptide-binding regions of MHC class I and class II DRB genes in the Alpine marmot (Marmota marmota). We found evidence for four expressed MHC class I loci and two expressed MHC class II loci. MHC genes in marmots were characterized by low polymorphism, as one to eight alleles per putative locus were detected in 38 individuals from three French Alps populations. The generally limited degree of polymorphism, which was more pronounced in class I genes, is likely due to bottleneck the populations undergone. Additionally, gene duplication within each class might have compensated for the loss of polymorphism at particular loci. The two gene classes showed different patterns of evolution. The most polymorphic of the putative loci, Mama-DRB1, showed clear evidence of historical positive selection for amino acid replacements. However, no signal of positive selection was evident in the MHC class I genes. These contrasting patterns of sequence evolution may reflect differences in selection pressures acting on class I and class II genes.     

Patterns of resource allocation in the dioecious alpine herb Aciphylla simplicifolia (Apiaceae)

Abstract Patterns of reproductive and vegetative biomass allocation were compared in male and female plants of the alpine herb Aciphylla simplicifolia. Male and female plants had similar vegetative biomass but differed in the pattern of resource allocation. Inflorescences of males and females were similar in weight at the time of flowering, but differed in biomass allocation to some structures within the inflorescences, particularly those associated with ovule production and pollinator attraction (number and size of flowers). At the time of fruit production, female inflorescences were 2.6 times heavier than at flowering with developing fruit six times heavier than flowers. In addition to the increase in biomass allocated to structures associated with the provisioning and dissemination of seed, support structures (main and side stalks) were also heavier. As a result of this additional investment of resources at the time of fruit production, the reproductive effort (RE) of female plants was much higher than that of males: 37% of above ground biomass compared with 21% for males. Differences in RE did not change with plant size; however, allocation to reproduction appeared to be a constant proportion of biomass over nearly all plant sizes sampled. These results show that sex‐specific resource allocation can be a complex of temporal and morphological patterns.     

Alpine marmot (Marmota marmota) distribution evolution under climate change: The use of species distribution models at a local scale in the western Pyrenees massif (France)

The Alpine marmot (Marmota marmota) is a social mammal living in mountainous grassland areas and has the particularity to hibernate in winter. Recent studies on a population in the French Alps found that climate change is affecting Alpine marmot population dynamics and might impact their overall distribution in the future. Using Species Distribution Models (SDMs), the effect of climate change on Alpine marmot's future distribution was investigated at a local scale, in the western part of the Pyrenean massif (New-Aquitaine region, France). This scale was chosen as an appropriate action scale for the conservation strategy for the species. Three climatic scenarios were used (RCP 2.6, RCP 4.5, and RCP 8.5) over three future 30-year periods (2021–2050, 2040–2070, 2071–2100) to predict the short- to long-term potential distribution of the target species. The results are consistent with naturalistic knowledge of the species´ ecological needs in terms of variable importance and response type. Mean maximum temperature in winter, standard-deviation of daily temperature in winter, along with the median rainfall amount in summer were the three most important climatic variables. Predictions under the two most pessimistic climate scenarios showed potential large habitat loss. In the long term, for RCP 4.5, an estimated habitat loss of 18% was predicted. In the case of RCP 8.5, a higher impact was predicted, with a 54% habitat loss. Our results show that high impact due to climate change can be expected at a long term. In addition, if winter climatic conditions are important for marmot survival through hibernation, drought in summer might be one of the drivers of future population dynamic and distribution. Our findings can be applied for other species living in grassland mountainous environments and for which access to food resources in summer is essential, facilitating the conservation of target areas.     

Analysis of developmental preformation in the alpine herb Caltha leptosepala (Ranunculaceae)

Developmental preformation is ubiquitous among alpine and arctic tundra plant species and may cause a delay in plant morphological responses to environmental variation. The duration of preformation and seasonal pattern of development were examined in Caltha leptosepala to identify characteristics of architecture and development that may influence the timing of plant responses to environmental cues, both within a single growing season and between years. All structures in C. leptosepala are preformed: leaves are initiated one or two growing seasons before they mature and flowers are initiated one growing season before maturation. Features of development and architecture in C. leptosepala, however, appear to differ from the determinate growth patterns of other exclusively preforming species, and may allow within-season variability in the seasonal development and maturation of structures. Cohorts of leaves initiated are asynchronous with maturation cohorts, and each year the number of leaf primordia per plant at snowmelt exceeds the number to mature aboveground. Therefore, some flexibility in whether leaves complete a 2-yr or 3-yr developmental trajectory might occur. Plasticity in reproductive phenotype might also occur via the process of floral abortion. Despite developmental characteristics that might facilitate the expression of phenotypic plasticity, only slight variability was observed in the duration of preformation or in the seasonal pattern of initiation and emergence of structures. Growth patterns of C. leptosepala thus appear to be fundamentally constrained, and limitations to annual growth may assure that sufficient preformed primordia remain belowground at the end of each growing season for maturation of a full cohort during the subsequent season.     

Isolation and characterization of microsatellite loci in a polyploid alpine herb,Callianthemum miyabeanum (Ranunculaceae)

• Premise of the study: Nuclear microsatellite primers were developed to analyze the clonal diversity and population genetic structure of the endemic polyploid herb Callianthemum miyabeanum. • Methods and Results: Using a protocol for constructing microsatellite-enriched libraries, 15 primer sets were developed for use in C. miyabeanum. The number of alleles found ranged from five to 22. The estimated range of expected heterozygosities was 0.574 to 0.907, and the Shannon–Weiner diversity index ranged from 1.061 to 2.733. Cross-amplification of all loci was also successful in the closely related endemic species C. kirigishiense and C. hondoense. • Conclusions: The development of these microsatellite loci will facilitate a deeper understanding of the genetic diversity, mode of reproduction, and population structure of not only C. miyabeanum, but also the other Callianthemum species endemic to Japan.     

Encentrum (Parencentrum) walterkostei n. sp., a new dicranophorid rotifer (Rotatoria: Monogononta) from the high alpine zone of the Central Alps (Austria)

A new dicranophorid rotifer, Encentrum (Parencentrum) walterkostei n.sp., is described from an oligotrophic alpine lake. The species was abundant in the psammolittoral of the Unterer Schwarzhornsee, 2543 m above sea level. The main distinguishing taxonomic features of the new species are long, swordshaped toes and only four vitellary nuclei. Its known occurrence in the sandy substrate of only one lake suggests a stenobiontic nature of this apparently oligothermic new species. Taxonomic problems associated with the Encentrum/Dicranophorus group are briefly discussed.