Nocturnal hypometabolism as an overwintering strategy of red deer (Cervus elaphus)

Abstract

. 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...

Physiological and life history strategies of a fossil large mammal in a resource-limited environment

“…The occasional presence of LAGs in these large endothermic (nonhibernating and nonestivating) mammals led some (26) to conclude that such growth lines reflect phylogenetic legacy rather than a physiological response to environmental cycles or stresses. Nevertheless, evidence is accumulating that certain ungulates significantly reduce endogenous heat production to cope with energetically challenging situations (food shortage, harsh climatic conditions) (32). Thus, seasonal fluctuations in metabolic rate and in body temperature (heterothermy) have been described for ungulates with a winter nadir in northern species (32)(33)(34) and with a summer nadir in desert species (35,36).…”

“…Nevertheless, evidence is accumulating that certain ungulates significantly reduce endogenous heat production to cope with energetically challenging situations (food shortage, harsh climatic conditions) (32). Thus, seasonal fluctuations in metabolic rate and in body temperature (heterothermy) have been described for ungulates with a winter nadir in northern species (32)(33)(34) and with a summer nadir in desert species (35,36). Taking into account these recent advances in ungulate physiology, the zonal bone of Myotragus quite likely reflects seasonal fluctuations in metabolic rate and/or body temperature over an extended juvenile period in response to fluctuating resource conditions on the island.…”

Evolutionary adaptations of ruminants and their potential relevance for modern production systems

“…Seasonality Like other animals, ruminants are subjected to seasonal rhythms of body mass gain or loss, food intake (Barry et al, 1991;Rhind et al, 2002), energy expenditure and metabolism (Mauget et al, 1997;Arnold et al, 2004) and reproduction (Asher et al, 1999;Santiago-Moreno et al, 2006). Two major mechanisms for this seasonality are recognised: the availability of resources (resource-induced seasonality) Figure 2 (a) Differences in relative dry matter intake (rDMI, per unit metabolic body weight; means, ranges and 25% to 75% percentile) between hindgut fermenters (n 5 49 species), nonruminant foregut fermenters (n 5 19) and ruminants (n 5 25) (data from Clauss et al, 2007b).…”

Foraging Strategy of Mouflon During the Hunting Season as Related to Food Supply

“…Low-quality food in the growing season or a reduced availability of high-quality food could have the same influence on survival of herbivores as extreme winters do. Arnold et al (2004) found that red deer, similar to many other northern ungulates, show large seasonal fluctuations of the metabolic rate, as indicated by the heart rate, with a 60% reduction at the winter nadir compared with the summer peak. A mechanism of energy conservation associated with peripheral cooling extensively lowers energy expenditure during winter.…”