. Nocturnal hypometabolism as an overwintering strategy of red deer (Cervus elaphus). Am J Physiol Regul Integr Comp Physiol 286: R174-R181, 2004. First published September 11, 2003 10.1152/ajpregu.00593.2002Herbivores of temperate and arctic zones are confronted during winter with harsh climatic conditions and nutritional shortness. It is still not fully understood how large ungulates cope with this twofold challenge. We found that red deer, similar to many other northern ungulates, show large seasonal fluctuations of metabolic rate, as indicated by heart rate, with a 60% reduction at the winter nadir compared with the summer peak. A previously unknown mechanism of energy conservation, i.e., nocturnal hypometabolism associated with peripheral cooling, contributed significantly to lower energy expenditure during winter. Predominantly during late winter night and early morning hours, subcutaneous temperature could decrease substantially. Importantly, during these episodes of peripheral cooling, heart rate was not maintained at a constant level, as to be expected from classical models of thermoregulation in the thermoneutral zone, but continuously decreased with subcutaneous temperature, both during locomotor activity and at rest. This indicates that the circadian minimum of basal metabolic rate and of the set-point of body temperature regulation varied and dropped to particularly low levels during late winter. Our results suggest, together with accumulating evidence from other species, that reducing endogenous heat production is not restricted to hibernators and daily heterotherms but is a common and well-regulated physiological response of endothermic organisms to energetically challenging situations. Whether the temperature of all tissues is affected, or the body shell only, may simply be a result of the duration and degree of hypometabolism and its interaction with body size-dependent heat loss. hypometabolism; hypothermia; winter adaptation; body temperature regulation MANY UNGULATES ARE CAPABLE of withstanding long and cold winters with low food availability. Large body size, excellent fur insulation, and countercurrent heat exchange mechanisms contribute to minimize energy requirements under cold load. However, reduced heat loss alone can hardly explain the substantially lowered metabolic rate (MR) of northern ungulates and the apparently ubiquitous decrease of voluntary food intake during winter (4,13,18,28,35,37,42,44,59,63,72). The search for mechanism to explain reduced energy expenditure during winter has so far produced equivocal results. Studies on white-tailed deer [Odocoileus virginianus (66)], moose [Alces alces (56, 57)], roe deer [Capreolus capreolus (69)], and wapiti [Cervus elaphus nelsoni (49)] reported that animals had reduced MRs during winter. However, other studies failed to find any differences between summer and winter basal metabolic rate (BMR) and concluded that seasonal variations in MR were merely consequences of different activity levels and failures to measure animals within thei...
Polyunsaturated fatty acids (PUFAs) can have strong effects on hibernation and daily torpor in mammals. High dietary PUFA contents were found to increase proneness for torpor, decrease body temperatures, prolong torpor bout duration, and attenuate hibernation mass loss. The mechanism by which PUFAs enhance torpor and hibernation is unknown, however. On the basis of a review of the literature, and on reexamining our own data on alpine marmots, we propose that effects on hibernation are not due to PUFAs in general, but to shifts in the ratio of n-6 PUFAs to n-3 PUFAs in membrane phospholipids. Specifically, high ratios of n-6 to n-3 PUFAs increase the activity of the Ca2+-Mg2+ pump in the sarcoplasmic reticulum of the heart (SERCA) and counteract Q10 effects on SERCA activity at low tissue temperatures. Therefore, high n-6 to n-3 PUFA ratios in cardiac myocyte membranes appear to protect the hibernating heart from arrhythmia, which in hypothermic nonhibernators is caused by massive increases in cytosolic Ca2+. The resulting reduced risk of cardiac arrest during hypothermia may explain why increased dietary uptake of n-6 PUFAs, but not of n-3 PUFAs, can strongly enhance the propensity for hibernation, and allows heterotherms to reach lower body temperatures, with associated increased energy savings. Therefore, at least for herbivorous hibernators, such as marmots, linoleic acid (C18:2 n-6)--the dietary source of all n-6 PUFAs--appears to represent a crucial and limited resource in natural environments.
Summary 1.The extent to which free-ranging large north-temperate mammals seasonally adjust thermoregulation and their energy expenditure under fully natural conditions are unknown. 2. Therefore, using telemetry we measured the heart rate (as a proxy for metabolic rate), rumen temperature (T r ) and locomotor activity (LA) over 2 years for 20 free-ranging Alpine ibex (Capra ibex ibex) living at high altitudes in the Alps. 3. Ibex showed strong seasonal changes in mean daily heart rate with a winter nadir of about 60% below the summer peak. Only 40% of this variation could be attributed to the changes in daily mean T r , LA, wind chill, body size and snowfall. The unexplained residual variation in heart rate still showed a strong seasonal pattern. 4. The amplitude of daily rhythms in T r was twice as high during the winter when compared with summer. This was predominantly due to lower daily minimum T r . Thus, the substantial down-regulation of endogenous heat production during winter -as indicated by heart rate -had surprisingly small effects on T r , indicating decreased thermal conductance. 5. Rewarming from the daily T r minimum during the morning hours was independent of heart rate throughout the year, and occurred phase-delayed to the increase in black bulb temperature (BBT). The effects of BBT and LA on the rate of rewarming were maximized within a small range of BBT around 0°C. This suggests that the ibex moved at sunrise to the closest sunny spot to facilitate extensive basking. 6. The energetic benefits of basking can explain the strong residual seasonality of heart rate in Alpine ibex. This partially ectothermic strategy -together with metabolic depression -apparently enables a thrifty use of body fat reserves, the major metabolic fuel during winter, and thus survival of extremely harsh winter conditions despite the virtual absence of food. Therefore, hypometabolism and passive rewarming by basking may be of general importance as a strategy for non-hibernating mammals to survive winter in strongly seasonal habitats.
The rhythm of life on earth is shaped by seasonal changes in the environment. Plants and animals show profound annual cycles in physiology, health, morphology, behaviour and demography in response to environmental cues. Seasonal biology impacts ecosystems and agriculture, with consequences for humans and biodiversity. Human populations show robust annual rhythms in health and well-being, and the birth month can have lasting effects that persist throughout life. This review emphasizes the need for a better understanding of seasonal biology against the backdrop of its rapidly progressing disruption through climate change, human lifestyles and other anthropogenic impact. Climate change is modifying annual rhythms to which numerous organisms have adapted, with potential consequences for industries relating to health, ecosystems and food security. Disconcertingly, human lifestyles under artificial conditions of eternal summer provide the most extreme example for disconnect from natural seasons, making humans vulnerable to increased morbidity and mortality. In this review, we introduce scenarios of seasonal disruption, highlight key aspects of seasonal biology and summarize from biomedical, anthropological, veterinary, agricultural and environmental perspectives the recent evidence for seasonal desynchronization between environmental factors and internal rhythms. Because annual rhythms are pervasive across biological systems, they provide a common framework for trans-disciplinary research.
Summary1. During the past 15 years, models have been used increasingly in predictive population ecology. Matrix models used for predicting the fates of populations are often extremely basic, ignoring density dependence, spatial scale and behaviour, and often based on one sex only. We tested the importance of some of these omissions for model realism, by comparing the performance of a variety of population models of varying levels of complexity. 2. Detailed data from more than 13 years of behavioural and demographic research on a population of alpine marmots Marmota marmota in Berchtesgaden National Park, southern Germany, were used to parameterize four different population models. The models ranged from a simple population-based matrix model, to a spatially explicit behaviour-based model. 3. The performance of the models was judged by their ability to predict basic population dynamics under equilibrium conditions. Only a spatially explicit individual-based model ignoring optimal behaviour predicted dynamics significantly different to those observed in the field, highlighting the importance of considering realistic patterns of behaviour in spatially explicit models. 4. Using realistic levels of environmental and demographic stochasticity, variance in population growth rates predicted by all models was high, even within the range of population densities experienced in the field. This emphasizes the difficulty of using population-level field data to determine overall patterns of density dependence for use in population models. 5. All models were also used to predict potential density-dependent effects on alpine marmot population growth. In this regard, the models differed greatly. It was concluded that the simplest matrix model was adequate for making predictions regarding population sizes or densities under equilibrium conditions, but that for predictions requiring an understanding of transient dynamics only the behavioural model would be adequate.6. An emergent feature of this study of alpine marmot population dynamics was the prediction of a demographic Allee effect with a profound influence on population dynamics across a very broad range of population sizes. Three mechanisms were identified as underlying this Allee effect: stochastic skews in sex ratio and demographic composition at low population sizes; less efficient social thermoregulation during hibernation in small groups; and difficulties with mate finding during dispersal, even at relatively high population sizes.
SUMMARY Many large mammals show pronounced seasonal fluctuations of metabolic rate(MR). It has been argued, based on studies in ruminants, that this variation merely results from different levels of locomotor activity (LA), and heat increment of feeding (HI). However, a recent study in red deer (Cervus elaphus) identified a previously unknown mechanism in ungulates -nocturnal hypometabolism - that contributed significantly to reduced energy expenditure, mainly during late winter. The relative contribution of these different mechanisms to seasonal adjustments of MR is still unknown, however. Therefore, in the study presented here we quantified for the first time the independent contribution of thermoregulation, LA and HI to heart rate(fH) as a measure of MR in a free-roaming large ungulate,the Przewalski horse or Takhi (Equus ferus przewalskii Poljakow). f H varied periodically throughout the year with a twofold increase from a mean of 44 beats min-1 during December and January to a spring peak of 89 beats min-1 at the beginning of May. LA increased from 23% per day during December and January to a mean level of 53% per day during May, and declined again thereafter. Daily mean subcutaneous body temperature (Ts) declined continuously during winter and reached a nadir at the beginning of April (annual range was 5.8°C),well after the annual low of air temperature and LA. Lower Ts during winter contributed considerably to the reduction in fH. In addition to thermoregulation, fH was affected by reproduction, LA, HI and unexplained seasonal variation, presumably reflecting to some degree changes in organ mass. The observed phase relations of seasonal changes indicate that energy expenditure was not a consequence of energy uptake but is under endogenous control, preparing the organism well in advance of seasonal energetic demands.
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