Thermoregulation in the wild boar (Sus scrofa).

The wild boar (Sus scrofa) originates from warm islands but now inhabits large areas of the world, with Antarctica as the only continent not inhabited by this species. One might be tempted to think that its wide distribution results from increasing environmental temperatures. However, any effect of temperature is only indirect: Abundant availability of critical food resources can fully compensate the negative effects of cold winters on population growth. Here, we asked if temperature as a habitat factor is unimportant compared with other habitat indices, simply because wild boars are excellent thermoregulators. We found that the thermoneutral zone in summer was approximately 6-24 °C. In winter, the thermoneutral zone was lowered to 0-7 °C. The estimated increase in the heart rate and energy expenditure in the cold was less than 30% per 10 °C temperature decline. This relatively small increase of energy expenditure during cold exposure places the wild boar in the realm of arctic animals, such as the polar bear, whereas tropical mammals raise their energy expenditure several fold. The response of wild boars to high Ta was weak across all seasons. In the heat, wild boars avoid close contact to conspecifics and particularly use wallowing in mud or other wet substrates to cool and prevent hyperthermia. Wild boars also rely on daily cycles, especially of rhythms in subcutaneous temperature that enables them to cheaply build large core-shell gradients, which serve to lower heat loss. We argue it is predominantly this ability which allowed wild boars to inhabit most climatically diverse areas in the world.

Why hibernate? Predator avoidance in the edible dormouse.

We address the question of ultimate selective advantages of hibernation. Biologists generally seem to accept the notion that multiday torpor is primarily a response to adverse environmental conditions, namely cold climate and low food abundance. We closely examine hibernation, and its summer equivalent estivation, in the edible dormouse, Glis glis. We conclude that in this species, hibernation is not primarily driven by poor conditions. Dormice enter torpor with fat reserves in years that are unfavourable for reproduction but provide ample food supply for animals to sustain themselves and even gain body energy reserves. While staying in hibernacula below ground, hibernators have much higher chances of survival than during the active season. We think that dormice enter prolonged torpor predominantly to avoid predation, mainly nocturnal owls. Because estivation in summer is immediately followed by hibernation, this strategy requires a good body condition in terms of fat reserves. As dormice age, they encounter fewer occasions to reproduce when calorie-rich seeds are available late in the year, and phase advance the hibernation season. By early emergence from hibernation, the best territories can be occupied and the number of mates maximised. However, this advantage comes at the cost of increased predation pressure that is maximal in spring. We argue the predator avoidance is generally one of the primary reasons for hibernation, as increased perceived predation pressure leads to an enhanced torpor use. The edible dormouse may be just an example where this behaviour becomes most obvious, on the population level and across large areas.

Atypical for northern ungulates, energy metabolism is lowest during summer in female wild boars (Sus scrofa).

Typically, large ungulates show a single seasonal peak of heart rate, a proxy of energy expenditure, in early summer. Different to other large ungulates, wild boar females had peak heart rates early in the year (at ~ April, 1), which likely indicates high costs of reproduction. This peak was followed by a trough over summer and a secondary summit in autumn/early winter, which coincided with the mast seeding of oak trees and the mating season. Wild boars counteracted the effects of cold temperatures by decreasing subcutaneous body temperature by peripheral vasoconstriction. They also passively gained solar radiation energy by basking in the sun. However, the shape of the seasonal rhythm in HR indicates that it was apparently not primarily caused by thermoregulatory costs but by the costs of reproduction. Wild boar farrow early in the year, visible in high HRs and sudden changes in intraperitoneal body temperature of females. Arguably, a prerequisite for this early reproduction as well as for high energy metabolism over winter is the broad variety of food consumed by this species, i.e., the omnivorous lifestyle. Extremely warm and dry summers, as experienced during the study years (2017, 2018), may increasingly become a bottleneck for food intake of wild boar.

Insights in the regulation of trimetylamine N-oxide production using a comparative biomimetic approach suggest a metabolic switch in hibernating bears.

Experimental studies suggest involvement of trimethylamine N-oxide (TMAO) in the aetiology of cardiometabolic diseases and chronic kidney disease (CKD), in part via metabolism of ingested food. Using a comparative biomimetic approach, we have investigated circulating levels of the gut metabolites betaine, choline, and TMAO in human CKD, across animal species as well as during hibernation in two animal species. Betaine, choline, and TMAO levels were associated with renal function in humans and differed significantly across animal species. Free-ranging brown bears showed a distinct regulation pattern with an increase in betaine (422%) and choline (18%) levels during hibernation, but exhibited undetectable levels of TMAO. Free-ranging brown bears had higher betaine, lower choline, and undetectable TMAO levels compared to captive brown bears. Endogenously produced betaine may protect bears and garden dormice during the vulnerable hibernating period. Carnivorous eating habits are linked to TMAO levels in the animal kingdom. Captivity may alter the microbiota and cause a subsequent increase of TMAO production. Since free-ranging bears seems to turn on a metabolic switch that shunts choline to generate betaine instead of TMAO, characterisation and understanding of such an adaptive switch could hold clues for novel treatment options in burden of lifestyle diseases, such as CKD.

Physiological, Behavioral, and Life-History Adaptations to Environmental Fluctuations in the Edible Dormouse.

The edible dormouse (Glis glis, formerly Myoxus glis) is a small arboreal mammal inhabiting deciduous forests in Europe. This rodent shows behavioral and physiological adaptations to three types of environmental fluctuations: (i) predictable seasonal variation in climate and food resources (ii) unpredictable year-to-year fluctuation in seed-production by trees and (iii) day-to-day variation in ambient temperature and precipitation. They cope with seasonally fluctuating conditions by seasonal fattening and hibernation. Dormice have adjusted to tree-mast fluctuations, i.e., pulsed resources, by sensing future seed availability in spring, and restricting reproduction to years with at least some seed production by beech and oak trees, which are a crucial food-resource for fast-growing juveniles in fall. Finally, dormice respond to short-term drops in ambient temperature by increased use of daily torpor as well as by huddling in groups of up to 24 conspecifics. These responses to environmental fluctuations strongly interact with each other: Dormice are much more prone to using daily torpor and huddling in non-reproductive years, because active gonads can counteract torpor and energy requirements for reproduction may prevent the sharing of food resources associated with huddling. Accordingly, foraging activity in fall is much more intense in reproductive mast years. Also, depending on their energy reserves, dormice may retreat to underground burrows in the summers of non-reproductive years, causing an extension of the hibernation season to up to 11.4 months. In addition to these interactions, responses to environmental fluctuations are modulated by the progression of life-history stages. With increasing age and diminishing chances of future reproduction, females reproduce with increasing frequency even under suboptimal environmental conditions. Simultaneously, older dormice shorten the hibernation season and phase-advance the emergence from hibernation in spring, apparently to occupy good breeding territories early, despite increased predation risk above ground. All of the above adaptions, i.e., huddling, torpor, hibernation, and reproduction skipping do not merely optimize energy-budgets but also help to balance individual predation risk against reproductive success, which adds another layer of complexity to the ability to make flexible adjustments in this species.

How climate change and wildlife management affect population structure in wild boars.

Global climate change affects many species and contributes to the exceptional population growth of wild boar populations and thus to increasing human-wildlife conflicts. To investigate the impact of climate change on wild boar populations we extended existing models on population dynamics. We included for the first time different juvenile conditions to account for long-lasting effects of juvenile body mass on adult body mass and reproductive success. Our analysis shows that incorporating phenotypes, like body mass differences within age classes, has strong effects on projected population growth rates, population structures and the relative importance of certain vital rates. Our models indicated that an increase in winter temperatures and food availability will cause a decrease in mean body mass and litter size within Central European wild boar populations. We further analysed different hunting regimes to identify their effects on the population structure as well as their efficiency in limiting population growth. While targeting juveniles had the lowest effect on population structure, such strategies are, however, rather ineffective. In contrast, culling predominantly yearlings seems very effective. Despite being equally effective, only focusing on adults will not result in a reduction of population size due to their low proportion within populations.

Use of social thermoregulation fluctuates with mast seeding and reproduction in a pulsed resource consumer.

Edible dormice (Glis glis) can remain entirely solitary but frequently share sleeping sites with conspecifics in groups of up to 16 adults and yearlings. Here, we analysed grouping behaviour of 4564 marked individuals, captured in a 13-year study in nest boxes in a deciduous forest. We aimed to clarify (i) whether social thermoregulation is the primary cause for group formation and (ii) which factors affect group size and composition. Dormice temporarily formed both mixed and single-sex groups in response to acute cold ambient temperatures, especially those individuals with small body mass. Thus, thermoregulatory huddling appears to be the driving force for group formation in this species. Huddling was avoided-except for conditions of severe cold load-in years of full mast seeding, which is associated with reproduction and high foraging activity. Almost all females remained solitary during reproduction and lactation. Hence, entire populations of dormice switched between predominantly solitary lives in reproductive years to social behaviour in non-reproductive years. Non-social behaviour pointed to costs of huddling in terms of competition for local food resources even when food is generally abundant. The impact of competition was mitigated by a sex ratio that was biased towards males, which avoids sharing of food resources with related females that have extremely high energy demands during lactation. Importantly, dormice preferentially huddled in male-biased groups with litter mates from previous years. The fraction of related individuals increased with group size. Hence, group composition partly offsets the costs of shared food resources via indirect fitness benefits.

Author Correction: Effects of aging on timing of hibernation and reproduction.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Muscle nonshivering thermogenesis in a feral mammal.

Muscle nonshivering thermogenesis (NST) was recently suggested to play an important role in thermoregulation of species lacking brown adipose tissue (BAT). The mechanism, which is independent of muscle contractions, produces heat based on the activity of an ATPase pump in the sarcoplasmic reticulum (SERCA1a) and is controlled by the protein sarcolipin. To evaluate whether muscle NST could indeed play an important role in thermoregulation in species lacking BAT, we investigated the thermogenic capacities of newborn wild boar piglets. During cold exposure over the first 5 days of life, total heat production was improved while shivering intensity decreased, indicating an increasing contribution of NST. Sampling skeletal muscle tissue for analyses of SERCA activity as well as gene expression of SERCA1a and sarcolipin, we found an age-related increase in all three variables as well as in body temperature. Hence, the improved thermogenesis during the development of wild boars is not due to shivering but explained by the observed increase in SERCA activity. Our results suggest that muscle NST may be the primary mechanism of heat production during cold stress in large mammals lacking BAT, strengthening the hypothesis that muscle NST has likely played an important role in the evolution of endothermy.

Effects of aging on timing of hibernation and reproduction.

Small hibernators are long-lived for their size because seasonal dormancy greatly reduces predation risk. Thus, within a year, hibernators switch between states of contrasting mortality risk (active season versus hibernation), making them interesting species for testing the predictions of life-history theory. Accordingly, we hypothesized that, with advancing age and hence diminishing reproductive potential, hibernators should increasingly accept the higher predation risk associated with activity to increase the likelihood of current reproductive success. For edible dormice (Glis glis) we show that age strongly affects hibernation/activity patterns, and that this occurs via two pathways: (i) with increasing age, dormice are more likely to reproduce, which delays the onset of hibernation, and (ii) age directly advances emergence from hibernation in spring. We conclude that hibernation has to be viewed not merely as an energy saving strategy under harsh climatic conditions, but as an age-affected life-history trait that is flexibly used to maximize fitness.

The insensitive dormouse: reproduction skipping is not caused by chronic stress in Glis glis.

Entire populations of edible dormice (Glis glis) can skip reproduction in years without mast seeding of deciduous trees (particularly beech or oak seed), because juveniles require high-calorie seeds for growth and fattening prior to hibernation. We hypothesized that, in mast failure years, female dormice may be forced to spend larger amounts of time foraging for low-quality food, which would increase their exposure to predators, mainly owls. This may lead to chronic stress, i.e. long-term increased secretion of glucocorticoids (GC), which can have inhibitory effects on reproductive function in both female and male mammals. We monitored reproduction in free-living female dormice over 3 years with varying levels of food availability, and performed a supplemental feeding experiment. To measure stress hormone levels, we determined fecal GC metabolite (GCM) concentrations collected during the day, which reflect hormone secretion rates in the previous nocturnal activity phase. We found that year-to-year differences in beech mast significantly affected fecal GCM levels and reproduction. However, contrary to our hypothesis, GCM levels were lowest in a non-mast year without reproduction, and significantly elevated in full-mast and intermediate years, as well as under supplemental feeding. Variation in owl density in our study area had no influence on GCM levels. Consequently, we conclude that down-regulation of gonads and reproduction skipping in mast failure years in this species is not caused by chronic stress. Thus, in edible dormice, delayed reproduction apparently is profitable in response to the absence of energy-rich food in non-mast years, but not in response to chronic stress.

Edible dormice (Glis glis) avoid areas with a high density of their preferred food plant - the European beech.

BACKGROUND: Numerous species, especially among rodents, are strongly affected by the availability of pulsed resources. The intermittent production of large seed crops in northern hemisphere tree species (e.g., beech Fagus spec.,oak Quercus spec., pine trees Pinus spec.) are prime examples of these resource pulses. Adult edible dormice are highly dependent on high energy seeds to maximize their reproductive output. For juvenile dormice the energy rich food is important to grow and fatten in a very short time period prior to hibernation. While these erratic, often large-scale synchronized mast events provide overabundant seed availability, a total lack of seed production can be observed in so-called mast failure years. We hypothesized that dormice either switch territories between mast and non-mast years, to maximize energy availability or select habitats in which alternative food sources are also available (e.g., fleshy fruits, cones). To analyze the habitat preferences of edible dormice we performed environmental niche factor analyses (ENFA) for 9 years of capture-recapture data. RESULTS: As expected, the animals mainly used areas with high canopy closure and vertical stratification, probably to avoid predation. Surprisingly, we found that dormice avoided areas with high beech tree density, but in contrast preferred areas with a relatively high proportion of coniferous trees. Conifer cones and leaves can be an alternative food source for edible dormice and are less variable in availability. CONCLUSION: Therefore, we conclude that edible dormice try to avoid areas with large fluctuations in food availability to be able to survive years without mast in their territory.

The costs of locomotor activity? Maximum body temperatures and the use of torpor during the active season in edible dormice.

Measuring T b during the active season can provide information about the timing of reproduction and the use of short bouts of torpor and may be used as a proxy for the locomotor activity of animals (i.e., maximum T b). This kind of information is especially important to understand life-history strategies and energetic costs and demands in hibernating mammals. We investigated T b throughout the active season in edible dormice (Glis glis), since they (i) have an expensive arboreal life-style, (ii) are known to show short bouts of torpor, and (iii) are adapted to pulsed resources (mast of beech trees). We show here for the first time that maximum T b's in free-living active dormice (during the night) increase regularly and for up to 8 h above 40 °C, which corresponds to slight hyperthermia, probably due to locomotor activity. The highest weekly mean maximum T b was recorded 1 week prior to hibernation (40.45 ± 0.07 °C). At the beginning of the active season and immediately prior to hibernation, the mean maximum T b's were lower. The time dormice spent at T b above 40 °C varied between sexes, depending on mast conditions. The date of parturition could be determined by a sudden increase in mean T b (plus 0.49 ± 0.04 °C). The occurrence of short torpor bouts (<24 h) was strongly affected by the mast situation with much higher torpor frequencies in mast-failure years. Our data suggest that locomotor activity is strongly affected by environmental conditions, and that sexes respond differently to these changes.

Differences in growth rates and pre-hibernation body mass gain between early and late-born juvenile garden dormice.

Juvenile hibernators have to allocate energy to both growth and fattening, to survive winter, and to avoid possible disadvantages during their first reproductive season. Being born late in the active season may have important effects on growth and fattening. This study aimed at determining potential differences in rates and maximal level of growth, and in pre-hibernation body fat mass between early and late-born juvenile garden dormice (Eliomys quercinus), and kept in outdoor enclosures with ad libitum food and water. We first assessed mean pup mass in early and late-born litters (n = 31) from birth to their early weaning phase, at which time body composition was determined. Then, growth and body mass of early and late-born individuals (six males and six females, for each group) were measured weekly until hibernation onset (n = 24). We also assessed fat content in a group of juveniles during pre-hibernation fattening (n = 16) and after their first winter hibernation (n = 18). During the pre-weaning phase, young from early and late litters mainly grew structurally and gained mass at similar rates. After weaning, late-born juveniles grew and gained mass twice as fast as early born individuals. Body mass was positively associated with fat content during pre-hibernation fattening. Late-born females reached similar structural sizes, but had lower pre-hibernation fat reserves than early born females. Conversely, late-born males showed lower maximal size and pre-hibernation body fat content, compared with early born males. Thus, individuals born late in the season cannot fully compensate the lack of available time before the winter onset.

Telomeres are elongated in older individuals in a hibernating rodent, the edible dormouse (Glis glis).

Telomere shortening is thought to be an important biomarker for life history traits such as lifespan and aging, and can be indicative of genome integrity, survival probability and the risk of cancer development. In humans and other animals, telomeres almost always shorten with age, with more rapid telomere attrition in short-lived species. Here, we show that in the edible dormouse (Glis glis) telomere length significantly increases from an age of 6 to an age of 9 years. While this finding could be due to higher survival of individuals with longer telomeres, we also found, using longitudinal measurements, a positive effect of age on the rate of telomere elongation within older individuals. To our knowledge, no previous study has reported such an effect of age on telomere lengthening. We attribute this exceptional pattern to the peculiar life-history of this species, which skips reproduction in years with low food availability. Further, we show that this "sit tight" strategy in the timing of reproduction is associated with an increasing likelihood for an individual to reproduce as it ages. As reproduction could facilitate telomere attrition, this life-history strategy may have led to the evolution of increased somatic maintenance and telomere elongation with increasing age.

Basking hamsters reduce resting metabolism, body temperature and energy costs during rewarming from torpor.

Basking can substantially reduce thermoregulatory energy expenditure of mammals. We tested the hypothesis that the largely white winter fur of hamsters (Phodopus sungorus), originating from Asian steppes, may be related to camouflage to permit sun basking on or near snow. Winter-acclimated hamsters in our study were largely white and had a high proclivity to bask when resting and torpid. Resting hamsters reduced metabolic rate (MR) significantly (>30%) when basking at ambient temperatures (Ta) of ∼15 and 0°C. Interestingly, body temperature (Tb) also was significantly reduced from 34.7±0.6°C (Ta 15°C, not basking) to 30.4±2.0°C (Ta 0°C, basking), which resulted in an extremely low (<50% of predicted) apparent thermal conductance. Induced torpor (food withheld) during respirometry at Ta 15°C occurred on 83.3±36.0% of days and the minimum torpor MR was 36% of basal MR at an average Tb of 22.0±2.6°C; movement to the basking lamp occurred at Tb<20.0°C. Energy expenditure for rewarming was significantly reduced (by >50%) during radiant heat-assisted rewarming; however, radiant heat per se without an endogenous contribution by animals did not strongly affect metabolism and Tb during torpor. Our data show that basking substantially modifies thermal energetics in hamsters, with a drop of resting Tb and MR not previously observed and a reduction of rewarming costs. The energy savings afforded by basking in hamsters suggest that this behaviour is of energetic significance not only for mammals living in deserts, where basking is common, but also for P. sungorus and probably other cold-climate mammals.

How to spend the summer? Free-living dormice (Glis glis) can hibernate for 11 months in non-reproductive years.

Edible dormice are arboreal rodents adapted to yearly fluctuations in seed production of European beech, a major food source for this species. In years of low beech seed abundance, dormice skip reproduction and non-reproductive dormice fed ad libitum in captivity can display summer dormancy in addition to winter hibernation. To test whether summer dormancy, that is, a very early onset of hibernation, actually occurs in free-living dormice, we monitored core body temperature (Tb) over ~12 months in 17 animals during a year of beech seeding failure in the Vienna Woods. We found that 8 out of 17 dormice indeed re-entered hibernation as early as in June/July, with five of them having extreme hibernation durations of 11 months or more (total range: 7.8-11.4 months). Thus, we show for the first time that a free-living mammal relying on natural food resources can continuously hibernate for >11 months. Early onset of hibernation was associated with high body mass in the spring, but the distribution of hibernation onset was bimodal with prolonged hibernation starting either early (prior to July 28) or late (after August 30). This could not be explained by differences in body mass alone. Animals with a late hibernation onset continued to maintain high nocturnal Tb's throughout summer but used short, shallow torpor bouts (mean duration 7.44 ± 0.9 h), as well as occasional multiday torpor for up to 161 h.

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.

High survival during hibernation affects onset and timing of reproduction.

The timing of reproduction is one of the most crucial life history traits, with enormous consequences for the fitness of an individual. We investigated the effects of season and timing of birth on local survival probability in a small mammalian hibernator, the common dormouse (Muscardinus avellanarius). Local monthly survival probability was lowest in the early active season (May-August, ϕ(adult) = 0.75-0.88, ϕ(juvenile) = 0.61-0.68), increased during the late active season (August-October), and highest during hibernation (October-May, ϕ(adult) = 0.96-0.98, ϕ(juvenile) = 0.81-0.94). Consequently, dormice had an extremely high winter survival probability. We observed two peaks in the timing of reproduction (June and August/September, respectively), with the majority of juveniles born late in the active season. Although early investment in reproduction seems the better life history tactic [survival probability until onset of reproduction: ϕ(born early) = 0.46, 95% confidence interval (CI) 0.28-0.64; ϕ(born late) = 0.19, 95% CI = 0.09-0.28], only females with a good body condition (significantly higher body mass) invest in reproduction early in the year. We suggest the high over-winter survival in dormice allows for a unique life history pattern (i.e., combining slow and fast life history tactics), which leads to a bimodal seasonal birth pattern: (1) give birth as early as possible to allow even the young to breed before hibernating, and/or (2) give birth as late as possible (leaving just enough time for these young to fatten) and enter directly into a period associated with the highest survival rates (hibernation) until maturity.