Claudia Bieber

Hibernation is associated with increased survival and the evolution of slow life histories among mammals

Survival probability is predicted to underlie the evolution of life histories along a slow–fast continuum. Hibernation allows a diverse range of small mammals to exhibit seasonal dormancy, which might increase survival and consequently be associated with relatively slow life histories. We used phylogenetically informed GLS models to test for an effect of hibernation on seasonal and annual survival, and on key attributes of life histories among mammals. Monthly survival was in most cases higher during hibernation compared with the active season, probably because inactivity minimizes predation. Hibernators also have approximately 15 per cent higher annual survival than similar sized non-hibernating species. As predicted, we found an effect of hibernation on the relationships between life history attributes and body mass: small hibernating mammals generally have longer maximum life spans (50% greater for a 50 g species), reproduce at slower rates, mature at older ages and have longer generation times compared with similar-sized non-hibernators. In accordance with evolutionary theories, however, hibernating species do not have longer life spans than non-hibernators with similar survival rates, nor do they have lower reproductive rates than non-hibernators with similar maximum life spans. Thus, our combined results suggest that (i) hibernation is associated with high rates of overwinter and annual survival, and (ii) an increase in survival in hibernating species is linked with the coevolution of traits indicative of relatively slow life histories.

Body mass dependent use of hibernation: why not prolong the active season, if they can?

Summary 1. Hibernation is the most effective means for energy conservation during winter in mammals. The drawbacks of deep and prolonged torpor include reduced immunocompetence, and consequently, hibernators should be selected to minimize torpor expression when climatic conditions or energy availability (e.g. food or fat stores) permit. Therefore, it seems surprising that some hibernators employ extraordinary long hibernation seasons, lasting well beyond periods with unfavourable conditions. 2. Because of their extended use of torpor, edible dormice (Glis glis) provide an ideal model for scrutinizing interactions between energy reserves (i.e. body fat stores) and thermoregulatory patterns. We used a multimodel inference approach to analyse body temperature data (i.e. use of torpor) from 42 entire hibernation seasons over 4 years in females in relation to body mass. 3. Body mass prior to hibernation did not affect the duration of the hibernation season, but animals hibernated for c. 8 months, that is, 2 months longer than required by environmental conditions. Fatter individuals aroused significantly more often, had a higher mean minimum body temperature during torpor and remained euthermic for longer periods than leaner animals. 4. Surplus energy was therefore not used to shorten the hibernation season, but to rewarm more frequently, and to allow shallower torpor bouts. These adjustments apparently serve to avoid negative effects of torpor and, perhaps equally importantly, to minimize the time active above-ground. We argue that maintaining a short active season, despite surplus energy reserves, may be explained by known beneficial effects of hibernation on survival rates (via predator avoidance). 5. Our data provide quantitative evidence that hibernation is a flexible tool within life-history strategies. We conclude that, apart from energetic necessities due to harsh environmental conditions, predator avoidance may be an important factor influencing patterns of hibernation and torpor in mammals. Thus, our study indicates that climatic conditions alone are not a good predictor of hibernation patterns or survival in hibernating species during global climate change.

Survival rates in a small hibernator, the edible dormouse: a comparison across Europe

Understanding how local environmental factors lead to temporal variability of vital rates and to plasticity of life history tactics is one of the central questions in population ecology. We used long-term capture-recapture data from five populations of a small hibernating rodent, the edible dormouse Glis glis, collected over a large geographical range across Europe, to determine and analyze both seasonal patterns of local survival and their relation to reproductive activity. In all populations studied, survival was lowest in early summer, higher in late summer and highest during hibernation in winter. In reproductive years survival was always lower than in non-reproductive years, and females had higher survival rates than males. Very high survival rates during winter indicate that edible dormice rarely die from starvation due to insufficient energy reserves during the hibernation period. Increased mortality in early summer was most likely caused by high predation risk and unmet energy demands. Those effects have probably an even stronger impact in reproductive years, in which dormice were more active. Although these patterns could be found in all areas, there were also considerable differences in average survival rates, with resulting differences in mean lifetime reproductive success between populations. Our results suggest that edible dormice have adapted their life history strategies to maximize lifetime reproductive success depending on the area specific frequency of seeding events of trees producing energy-rich seeds.

Energy or information? The role of seed availability for reproductive decisions in edible dormice.

The edible dormouse is a specialized seed predator which is highly adapted to the fluctuations of food availability caused by mast seeding of beech and oak trees. Dormice produce young just in time with maximum food availability, and can completely skip reproduction in years with a lack of seeding. Because their decision to reproduce or not in any particular year is made long before the ripe seeds are available, it seems that dormice can anticipate the upcoming mast situation. We tested the hypothesis that the presence of high caloric food in spring affects their reproductive decision. Therefore, we supplementary fed dormice in a field experiment from spring to early summer with sunflower seeds, which also contain a high amount of energy. Supplemental feeding caused significant increases in the proportion of reproducing females and reproductively active males. These results suggest that edible dormice may use the occurrence of an energy rich food resource to predict the autumnal mast situation. Further, our data indicate that the decision to reproduce was not the result of an increased body mass due to the consumption of surplus food, but that sufficient seed abundance acts as an environmental signal to which dormice adjust their reproduction.

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.

What Is a Mild Winter? Regional Differences in Within-Species Responses to Climate Change.

Climate change is known to affect ecosystems globally, but our knowledge of its impact on large and widespread mammals, and possibly population-specific responses is still sparse. We investigated large-scale and long-term effects of climate change on local population dynamics using the wild boar (Sus scrofa L.) as a model species. Our results show that population increases across Europe are strongly associated with increasingly mild winters, yet with region-specific threshold temperatures for the onset of exponential growth. Additionally, we found that abundant availability of critical food resources, e.g. beech nuts, can outweigh the negative effects of cold winters on population growth of wild boar. Availability of beech nuts is highly variable and highest in years of beech mast which increased in frequency since 1980, according to our data. We conclude that climate change drives population growth of wild boar directly by relaxing the negative effect of cold winters on survival and reproduction, and indirectly by increasing food availability. However, region-specific responses need to be considered in order to fully understand a species’ demographic response to climate change.

Seasonal variation in telomere length of a hibernating rodent

Small hibernating rodents have greater maximum lifespans and hence appear to age more slowly than similar-sized non-hibernators. We tested for a direct effect of hibernation on somatic maintenance and ageing by measuring seasonal changes in relative telomere length (RTL) in the edible dormouse Glis glis. Average RTL in our population did not change significantly over the hibernation season, and a regression model explaining individual variation in post-hibernation RTL suggested a significant negative effect of the reduction in body mass over the inactive hibernation period (an index of time spent euthermic), supporting the idea that torpor slows ageing. Over the active season, RTL on average decreased in sub-adults but increased in adults, supporting previous findings of greater telomere shortening at younger ages. Telomere length increase might also have been associated with reproduction, which occurred only in adults. Our study reveals how seasonal changes in physiological state influence the progress of life-history traits, such as somatic maintenance and ageing, in a small hibernating rodent.

Local environmental factors affect reproductive investment in female edible dormice

Abstract Edible dormice (Glis glis) are exposed temporally and spatially to a tremendous variation in food resources. This variation strongly influences reproduction; in edible dormice reproduction is tightly linked to the availability of energy-rich seeds. Although most dormice reproduce in full mast years of beech or oak, entire populations skip reproduction in years without seed production; however, nearly 50% of all years are intermediate mast years, during which only part of the dormouse population reproduces. We investigated how the beech mast pattern, local habitat characteristics, and individual traits (body mass and age class) influence whether individual female edible dormice invest in reproduction in intermediate mast years. Our field study, conducted during 2006–2009 in the Vienna Woods, revealed that in intermediate mast years the probability of females reproducing increased with the age of trees but not with the proportion of beech trees within their home ranges. Mean litter size was larger in years with higher seed availability and also increased with the mean age of trees within the home range of the dormice. More adult than yearling females reproduced, but this effect was modulated by yearly and local variation in food availability. Whether a female edible dormouse reproduces in an intermediate mast year depends mainly on the local food availability and age of the individual.

Survival, Aging, and Life-History Tactics in Mammalian Hibernators

Hibernation is commonly viewed as an adaptation that simply allows animals to survive periods of food shortage and climatically harsh conditions. Here, we review accumulating evidence suggesting that hibernation is part of a specific “slow-paced” mammalian life-history tactic that is associated with increased survival, retarded physiological aging, increased maximum longevity, low rates of fecundity, and long generation times. We argue that these traits can be explained if the primary function of hibernation—at least in many species—is the reduction of extrinsic mortality risks, namely predation, under environmental conditions that are not life-threatening, but do not favor reproduction. According to this view, hibernation is but one element of a life-history strategy that maximizes fitness by bet-hedging, i.e., reducing the risk of losing offspring by spreading lifetime reproductive effort over a number of temporally separated bouts. Further, increased survival and spreading of reproductive bouts should allow hibernators to produce young at times when climate and food resources are optimal for the rearing of offspring.

Shy is sometimes better: personality and juvenile body mass affect adult reproductive success in wild boars, Sus scrofa

There is increasing evidence that animal personalities are linked to different life history strategies. However, studies examining whether these effects differ under varying environmental conditions are rare. Here, we investigated how animal personality affects reproductive success in a pulsed resource consumer, the wild boar. We determined the exploratory behaviour of 57 female wild boars in nine novel object tests and additionally assessed their aggressiveness. Exploration behaviour (i.e. approach latency and investigation duration) and aggressiveness were repeatable within individuals and both mapped on a single principal component yielding an individual personality score. Afterwards the females were kept together with 28 males under seminatural conditions in two large breeding enclosures from 2011 to 2014. Over winter 2013/2014 we applied high versus medium feeding regimes to the two enclosures. Our results show that adult body mass and reproductive success were affected by juvenile body mass and thus already determined early in life, which may point to a silver spoon effect in the wild boar. Whether a female reproduced or not, as well as the litter size shortly after birth, was only affected by female body mass. The postweaning litter size (i.e. at the time of independence at the age of about 6 months), however, was additionally affected by the personality score in interaction with food availability. Under high food availability less aggressive and explorative individuals raised more juveniles to independence. We conclude that lower aggressiveness and reduced exploratory tendency of the mother lead to lower juvenile mortality and hence have a positive impact on postweaning litter size. Under slightly decreased food availability, however, this effect vanished. As the impact of personality on reproductive success differed between changing environmental conditions, our results support the hypothesis that different personality phenotypes are evolutionarily maintained by varying selection pressures in heterogeneous environments.