Spatiotemporal variation in reproductive parameters of yellow-bellied marmots

Spatiotemporal variation in reproductive rates is a common phenomenon in many wildlife populations, but the population dynamic consequences of spatial and temporal variability in different components of reproduction remain poorly understood. We used 43 years (1962–2004) of data from 17 locations and a capture–mark–recapture (CMR) modeling framework to investigate the spatiotemporal variation in reproductive parameters of yellow-bellied marmots (Marmota flaviventris), and its influence on the realized population growth rate. Specifically, we estimated and modeled breeding probabilities of two-year-old females (earliest age of first reproduction), >2-year-old females that have not reproduced before (subadults), and >2-year-old females that have reproduced before (adults), as well as the litter sizes of two-year old and >2-year-old females. Most reproductive parameters exhibited spatial and/or temporal variation. However, reproductive parameters differed with respect to their relative influence on the realized population growth rate (λ). Litter size had a stronger influence than did breeding probabilities on both spatial and temporal variations in λ. Our analysis indicated that λ was proportionately more sensitive to survival than recruitment. However, the annual fluctuation in litter size, abetted by the breeding probabilities, accounted for most of the temporal variation in λ. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

Factors affecting corticosteroid concentrations in yellow-bellied marmots.

1. Bound and total corticosteroid concentrations of yellow-bellied marmots (Marmota flaviventris) were lowest in May after emergence from hibernation and peaked in August prior to immergence. 2. Total corticosteroids were affected by age but not by sex or reproductive status. 3. There was no consistent relationship between measures of population density and concentrations of corticosteroids; when a significant relationship occurred, only 22-34% of the variation was explained. 4. Social status and social behavior were the major factors affecting corticosteroid concentrations.     

Masculinized female yellow-bellied marmots initiate more social interactions

The presence of male siblings in utero influences female morphology and life-history traits because testosterone transferred among foetuses may masculinize females. Similarly, litter sex composition might alter the display of sexually dimorphic behaviour, such as play and allogrooming, since they are modulated by androgens. We explored whether masculinization alters the frequency of play and sociopositive behaviour in female yellow-bellied marmots (Marmota flaviventris). We found that masculinized juvenile females were more likely to initiate play and allogrooming, but yearling females exhibited higher levels of oestrogen-modulated sociopositive behaviours. Additionally, the more they interacted, the greater number of different partners they interacted with. Our results suggest that masculinization increases the rate of age-dependent social behaviour. This probably works by increasing exploration that predisposes individuals to higher encounter rates. Further support comes from previous findings showing that masculinized females were more likely to disperse. Our study stresses the importance of considering litter sex composition as a fitness modulator.     

Litter sex composition affects life-history traits in yellow-bellied marmots

1. The presence of siblings might have long-lasting fitness consequences because they influence the early environment in which an animal develops. Several studies under laboratory conditions have shown long-lasting consequences from the presence of male siblings in utero on morphology and life-history traits. However, in wild animals, such effects of litter sex composition are unexplored. 2. We capitalized on a long-term study of individually marked yellow-bellied marmots (Marmota flaviventris) and documented the effects of weaned litter sex composition and anogenital distance on several life-history and fitness traits. 3. First, we demonstrated that the number of males in a litter influenced anogenital distance. Then, we found that masculinized females, those with larger anogenital distances, were less likely to survive their first hibernation, were more likely to disperse and were less likely to become pregnant and wean young. Males from male-biased litters had lower growth rates, but we failed to detect longer-term consequences. 4. Taken together, our results show profound sex-dependent effects of litter sex composition, probably due to differential prenatal exposure to androgens, in free-living animals. We conclude that masculinization might constitute an alternative mechanism explaining variation in different demographic traits. This finding highlights the importance of studying these maternal effects, and they enhance our concern over the widespread use of endocrine disrupting compounds.     

Nutritional ecology of yellow-bellied marmots in the White Mountains of California

This study examined the basis of diet preference in a mammalian hibernator, the yellow-bellied marmot Marmota flaviventris , in the White Mountains of California. Preference indices calculated from dietary data and food plant availability in the habitat indicated that forb species were preferred over graminoids, particularly in the spring and early summer. Chemical analysis of food plant species suggested that marmots preferred forbs over graminoids because of their lower fiber (cellulose) content and higher concentrations of phosphorus, sodium and possibly protein. Inclusion of graminoids in the diets was probably due to their greater availability in the habitat coupled with the need to maximize the rate of nutrient intake during the short (4–5 month) active season. Seasonal changes in diet composition were noted which may reflect, in part, temporal changes in nutrient demands.     

Dispersal of yearling yellow-bellied marmots (Marmota flaviventris)

Field studies of the social organization of yellow-bellied marmots (Marmota flaviventris) in the vicinity of Gothic, Colorado, were initiated in 1962. Data collected during the subsequent 14 years are sufficient to analyse the behaviours that correlate with the time yearling male and yearling female marmots leave their natal home sites. Dispersal of yearling male yellow-bellied marmots was delayed when there were many yearling males in a harem, when yearling males were underweight, and when the rates of amicable interactions between yearling males and adults were high. Dispersal of yearling females was delayed when adults behaved amicably toward them and when the rates of adult aggression were low. Dispersal of yearling females was independent of the number of females in a harem. These observations are in accord with a model of dispersal that relates sexual differences in dispersal to maternal reproductive tactics, and to responses of yearlings that would maximize their own fitness.     

Sociality, individual fitness and population dynamics of yellow-bellied marmots

Social behaviour was proposed as a density-dependent intrinsic mechanism that could regulate an animal population by affecting reproduction and dispersal. Populations of the polygynous yellow-bellied marmot (Marmota flaviventris) fluctuate widely from year to year primarily driven by the number of weaned young. The temporal variation in projected population growth rate was driven mainly by changes in the age of first reproduction and fertility, which are affected by reproductive suppression. Dispersal is unrelated to population density, or the presence of the father; hence, neither of these limits population growth or acts as an intrinsic mechanism of population regulation; overall, intrinsic regulation seems unlikely. Sociality affects the likelihood of reproduction in that the annual probability of reproducing and the lifetime number of offspring are decreased by the number of older females and by the number of same-aged females present, but are increased by the number of younger adult females present. Recruitment of a yearling female is most likely when her mother is present; recruitment of philopatric females is much more important than immigration for increasing the number of adult female residents. Predation and overwinter mortality are the major factors limiting the number of resident adults. Social behaviour is not directed towards population regulation, but is best interpreted as functioning to maximize direct fitness.     

Faecal glucocorticoid metabolites and alarm calling in free-living yellow-bellied marmots

When individuals of a variety of species encounter a potential predator, some, but not all, emit alarm calls. To explain the proximate basis of this variation, we compared faecal glucocorticoid metabolite concentrations in live-trapped yellow-bellied marmots (Marmota flaviventris) between occasions when they did and did not emit alarm calls. We found that marmots had significantly higher glucocorticoid levels when they called than when they did not call, suggesting that stress or arousal may play an important role in potentiating alarm calls. Marmots are sensitive to variation in the reliability of callers. The present finding provides one possible mechanism underlying caller variation: physiological arousal influences the propensity to emit alarm calls.     

Group hibernation does not reduce energetic costs of young yellow-bellied marmots

We investigated mechanisms of energy conservation during hibernation. The amount of time torpid was significantly less for groups of three young marmots than for marmots hibernating singly. Mean daily mass loss (DML; as mg d(-1) g(-1) immergence mass) averaged 1.33 for single marmots and 1.46 for grouped young. Animals were active 17.3% of the time, which used 82.4% of the energy, and were torpid 82.7% of the time, which used 17.6% of the energy expenditure. During longer torpor bouts, more time was spent in deep torpor, which decreased the hourly cost of a complete bout. Bout oxygen consumption V dot o2, percent time in deep torpor, and body temperature (T(B)) during deep torpor changed seasonally and were curvilinearly related to when in the hibernation period the measurements were made and probably represent a stage in the circannual metabolic cycle. The decrease of environmental temperature (T(E)) to 2 degrees C significantly increased metabolism. Potential costs of low T(E) were reduced by allowing T(B) to decrease, thereby reducing the T(B) to T(E) gradient. Average monthly metabolic rate was high early and late in the hibernation period when time spent euthermic was greater and when VO2 was higher. Over the hibernation period, energy saved averaged 77.1% and 88.0% of the costs for winter and summer euthermic metabolism, respectively. Hibernation costs were reduced by the seasonal changes, the high percentage of time in torpor, the rapid decline in V dot o2 following arousal, and allowing T(B) to decline at lower T(E). Asynchrony in the torpor cycles increased energy expenditures in group hibernators, which negated possible beneficial effects of group hibernation.     

Age-class differences in the pattern of hibernation in yellow-bellied marmots,Marmota flaviventris

Summary Age-related differences in the patterns of body temperature regulation during hibernation were found in yellow-bellied marmots. The timing of all entrances into and arousals from torpor was determined from continuous records of thermocouples mounted in each animal's nest box. Older marmots spent more time at high body temperatures following periodic arousals from torpor than did juveniles undergoing their first season of hibernation. In addition, older marmots spontaneously terminated their hibernation seasons in the spring, whereas most juveniles continued to hibernate until either they were emaciated from starvation or they were fed. These two patterns of hibernation reflect age- and size-related differences in the degree to which the animals are constrained energetically and the probability that they can successfully reproduce in spring. The patterns also are consistent with age-related differences in the timing of dormancy in nature.     

The effect of maternal glucocorticoid levels on juvenile docility in yellow-bellied marmots

Maternal effects can have significant and long-term consequences on offspring behavior and survival, while consistent individual differences (i.e., personality) can have profound impacts on individual fitness. Thus, both can influence population dynamics. However, the underlying mechanisms that determine variation in personality traits are poorly understood. Maternal effects are one potential mechanism that may explain personality variation. We capitalized on a long-term study of yellow-bellied marmots (Marmota flaviventris) to identify maternal effects on juvenile docility. To do so, we partitioned the variance in juvenile docility using a quantitative genetic modeling approach to isolate potential maternal effects. We also directly tested whether maternal stress, measured through fecal glucocorticoid metabolite levels during lactation of 82 mothers, was associated with offspring docility. Docility scores were estimated for 645 juveniles trapped between 2002 and 2012. We found an interaction between maternal glucocorticoid levels and dam age on juvenile docility. We also found significant maternal, litter, permanent environment, and year effects. These results suggest that a mother's life history stage interacts with stress to influence offspring personality. This early life influence can have long lasting effects on an individual's docility throughout life.