Torpor is not the only option: seasonal variations of the thermoneutral zone in a small primate

The reddish-gray mouse lemur (Microcebus griseorufus) is one of only a few small mammals inhabiting the spiny forest of southwestern Madagascar. In this study we investigated the physiological adjustments which allow these small primates to persist under the challenging climatic conditions of their habitat. To this end we measured energy expenditure (metabolic rate) and body temperature of 24 naturally acclimatized mouse lemurs, kept in outdoor enclosures, during different seasons (summer, winter, and the transition period between the two seasons). Mouse lemurs displayed two main physiological strategies to compensate seasonal and diurnal fluctuations of ambient temperature. On the one hand, individuals entered hypometabolism with decreasing ambient temperature (T _a) during the transition period and winter, enabling them to save up to 21 % energy per day (92 % per hour) compared with the normal resting metabolic rate at comparable T _a. On the other hand, euthermic mouse lemurs also showed physiological adjustments to seasonality when resting: the lower critical temperature of the thermoneutral zone decreased from summer to winter by 7.5 °C, which allowed mouse lemurs to keep energy demands constant despite colder T _as during winter. In addition, the basal metabolic rate was substantially lowered prior to the winter period, which facilitated accumulation of fat reserves. The combination of physiological modifications during euthermia in addition to hypometabolism, which can be individually adjusted according to external parameters and respective body condition, is important as it allows M. griseorufus to cope with the environmental variability of an energetically challenging habitat.     

Fundamental avian energetics: 2. The ability of birds to change heat loss and explanation of the mass exponent for basal metabolism in homeothermic animals

The maximum ability of birds to generate heat due to increasing metabolism, as a result of both activity and heat stress, was determined in relation to the evaporative and nonevaporative heat losses at various temperatures in passerines and nonpasserines at the beginning and at the end of thermoneutral zones. The minimum (h _min) and maximum (h _max) nonevaporative thermal conductances in both species change similarly depending on the body mass, and the slopes of regression lines in h _min and h _max are identical. At the same time, h _max is approximately four times higher than h _min. Experimental data obtained both in this study and by other authors show that the ratio h _max/h _min = 4 is constant for all homeothermic animals and appears to be a sensible compromise found by the evolution between an increase in activity and the minimum effectiveness profitable for life of the transfer of metabolic power into mechanical power (?? = 1/4) during its fulfillment. An increase in the ratio h _max/h _min, although it allows an animal to augment its daily activity, leads to a reduction in the effectiveness and is, therefore, not used by homeothermic animals. The abilities of birds and mammals to change their heat loss are determined by the ratio h _max/h _min = 4, which is an integrated indicator of the level of development of blood circulation and respiration systems and the degree of development of external covers, as well as the ability of both to change heat loss. In homeothermic animals, this ratio is associated with the body mass exponent in allometric dependences for basal metabolism and determines the efficiency of transfer of metabolic power into mechanical work.     

Seasonal effects on thermoregulatory responses of the Rock Kestrel, Falco rupicolis

Thermoregulatory responses are known to differ seasonally in endotherms and this is often dependent on the environment and region they are resident. Holarctic animals are exposed to severe winters and substantial seasonal variation in ambient temperature. In contrast, those in the Afrotropics have less severe winters, but greater variation in temperature, rainfall and net primary production. These environmental factors place different selection pressures on physiological responses in endotherms. In this study, metabolic rate (VO₂) and body temperature (T_b) were measured in captive bred Rock Kestrels (Falco rupicolus) from the Afrotropics after a period of summer and winter acclimatisation. Resting metabolic rate was significantly lower after the winter acclimatisation period than after the summer acclimatisation period, and there was a shift in the thermoneutral zone from 20–33 °C in summer to 15–30 °C in winter. However, no significant difference in basal metabolic rate between summer and winter was found. The results show that Rock Kestrels reduce energy expenditure at low ambient temperatures in winter as expected in an Afrotropical species.     

An experimental test of the thermoregulatory hypothesis for the evolution of endothermy

The thermoregulatory hypothesis proposes that endothermy in mammals and birds evolved as a thermoregulatory mechanism per se and that natural selection operated directly to increase body temperature and thermal stability through increments in resting metabolic rate. We experimentally tested this hypothesis by measuring the thermoregulatory consequences of increased metabolic rate in resting lizards (Varanus exanthematicus). A large metabolic increment was induced by feeding the animals and consequent changes in metabolic rate and body temperature were monitored. Although metabolic rate tripled at 32 degrees C and quadrupled at 35 degrees C, body temperature rose only about 0.5 degrees C. The rate of decline of body temperature in a colder environment did not decrease as metabolic rate increased. Thus, increasing the visceral metabolic rate of this ectothermic lizard established neither consequential endothermy nor homeothermy. These results are inconsistent with a thermoregulatory explanation for the evolution of endothermy.     

The effect of He−O2 exposure on metabolic rate,thermoregulation and thermal conductance during normothermia and daily torpor

Recently it was proposed that the low metabolic rate during torpor may be better explained by the reduction of thermal conductance than the drop of body temperature or metabolic inhibition. We tested this hypothesis by simultaneously measuring body temperature and metabolic rate as a function of ambient temperature in both torpid and normothermic stripe-faced dunnarts, Sminthopsis macroura (Marsupialia; approx. 25 g body mass), exposed to either air or He–O₂ (21% oxygen in helium) atmospheres. He–O₂ exposure increases the thermal conductance of homeothermic mammals by about twofold in comparison to an air atmosphere without apparent side-effects. Normothermic S. macroura exposed to He–O₂ increased resting metabolic rate by about twofold in comparison to that in air because of the twofold increase in apparent thermal conductance. Torpid S. macroura exposed to He–O₂ at ambient temperatures above the set-point for body temperature showed a completely different metabolic response. In contrast to normothermic individuals, torpid individuals significantly decreased or maintained a similar metabolic rate as those in air although the apparent thermal conductance in He–O₂ was slightly raised. Moreover, the metabolic rate during torpor was only a fraction of that of normothermic individuals although the apparent thermal conductance differed only marginally between normothermia and torpor. Our study shows that a low thermal conductance is not the reason for the low metabolic rates during torpor. It suggests that interrelations between metabolic rate and body temperature of torpid endotherms above the set-point for body temperature differ fundamentally from those of normothermic and homeothermic endotherms.Abbreviations T _a ambient temperature - T _b body temperature - BMR basal metabolic rate - C apparent thermal conductance - He–O ₂ 21% oxygen in helium - MR metabolic rate - MSe mean square-error - RMR festing metabolic rate - TMR metabolic rate during torpor - T difference T _b-T _a - TNZ thermoneutral zone - T _set set-point for body temperature - O ₂ rate of oxygen consumption     

Reduction of metabolic rate and thermoregulation during daily torpor

Physiological mechanisms causing reduction of metabolic rate during torpor in heterothermic endotherms are controversial. The original view that metabolic rate is reduced below the basal metabolic rate because the lowered body temperature reduces tissue metabolism has been challenged by a recent hypothesis which claims that metabolic rate during torpor is actively downregulated and is a function of the differential between body temperature and ambient temperature, rather than body temperature per se. In the present study, both the steady-state metabolic rate and body temperature of torpid stripe-faced dunnarts, Sminthopsis macroura (Dasyuridae: Marsupialia), showed two clearly different phases in response to change of air temperature. At air temperatures between 14 and 30°C, metabolic rate and body temperature decreased with air temperature, and metabolic rate showed an exponential relationship with body temperature (r ²=0.74). The Q ₁₀ for metabolic rate was between 2 and 3 over the body temperature range of 16 to 32°C. The difference between body temperature and air temperature over this temperature range did not change significantly, and the metabolic rate was not related to the difference between body temperature and air temperature (P=0.35). However, the apparent conductance decreased with air temperature. At air temperatures below 14°C, metabolic rate increased linearly with the decrease of air temperature (r ²=0.58) and body temperature was maintained above 16°C, largely independent of air temperature. Over this air temperature range, metabolic rate was positively correlated with the difference between body temperature and air temperature (r ²=0.61). Nevertheless, the Q ₁₀ for metabolic rate between normothermic and torpid thermoregulating animals at the same air temperature was also in the range of 2–3. These results suggest that over the air temperature range in which body temperature of S. macroura was not metabolically defended, metabolic rate during daily torpor was largely a function of body temperature. At air temperatures below 14°C, at which the torpid animals showed an increase of metabolic rate to regulate body temperature, the negative relationship between metabolic rate and air temperature was a function of the differential between body temperature and air temperature as during normothermia. However, even in thermoregulating animals, the reduction of metabolic rate from normothermia to torpor at a given air temperature can also be explained by temperature effects.Abbreviations BM body mass - BMR basal metabolic rate - C apparent conductance - MR metabolic rate - RMR resting metabolic rate - RQ respiratory quotient - T _a air temperature - T _b body temperature - T _lc lower critical temperature - T _tc critical air temperature during torpor - TMR metabolic rate during torpor - TNZ thermoneutral zone - T difference between body temperature and air temperature - VO₂ rate of oxygen consumption     

Testing the fitness consequences of the thermoregulatory and parental care models for the origin of endothermy

The origin of endothermy is a puzzling phenomenon in the evolution of vertebrates. To address this issue several explicative models have been proposed. The main models proposed for the origin of endothermy are the aerobic capacity, the thermoregulatory and the parental care models. Our main proposal is that to compare the alternative models, a critical aspect is to determine how strongly natural selection was influenced by body temperature, and basal and maximum metabolic rates during the evolution of endothermy. We evaluate these relationships in the context of three main hypotheses aimed at explaining the evolution of endothermy, namely the parental care hypothesis and two hypotheses related to the thermoregulatory model (thermogenic capacity and higher body temperature models). We used data on basal and maximum metabolic rates and body temperature from 17 rodent populations, and used intrinsic population growth rate (R(max)) as a global proxy of fitness. We found greater support for the thermogenic capacity model of the thermoregulatory model. In other words, greater thermogenic capacity is associated with increased fitness in rodent populations. To our knowledge, this is the first test of the fitness consequences of the thermoregulatory and parental care models for the origin of endothermy.     

The origin of homoiothermy--unsolved problem

The analysis of allometric dependence of energy expenditure on body mass among reptiles, birds and mammals has shown that standard metabolic rate of reptiles when they are warmed up to the temperature of homoiothermic animals is an order of magnitude lower than that of birds and mammals. Basal metabolism is originated as special feature historically related to the metabolism during active behavior, rather than thermal regulation. Facultative endothermy was not advantageous for large animals because of long time needed to warm up the body. The ancestors of birds and animals escaped negative consequences of van't-Hoff equation by choosing constant body temperature. Heat conductivity of reptile's covers is so great, that it cannot keep endogenous warm of resting animal at any temperature of the body. Reptile "dressed" in covers of bird or mammal would be able to keep warm under conditions of maximal aerobic muscular activity and body temperature similar to that of homoiothermic animals. The base of chemical thermoregulation in birds and mammals is a thermoregulatory muscle tonus which remains unknown. One can suppose that during evolution of birds and mammals the saltation-liked origin of endothermy "fixed" the level of metabolism typical for running reptile and transformed in into the basal metabolism. This event took place at the cell and tissue level. The absence of palaeontological evidences and intermediate forms among recent species does not allow easy understanding of homoiothermy origin.     

Biomechanics of Running Indicates Endothermy in Bipedal Dinosaurs

Background

One of the great unresolved controversies in paleobiology is whether extinct dinosaurs were endothermic, ectothermic, or some combination thereof, and when endothermy first evolved in the lineage leading to birds. Although it is well established that high, sustained growth rates and, presumably, high activity levels are ancestral for dinosaurs and pterosaurs (clade Ornithodira), other independent lines of evidence for high metabolic rates, locomotor costs, or endothermy are needed. For example, some studies have suggested that, because large dinosaurs may have been homeothermic due to their size alone and could have had heat loss problems, ectothermy would be a more plausible metabolic strategy for such animals.

Methodology/Principal Findings

Here we describe two new biomechanical approaches for reconstructing the metabolic rate of 14 extinct bipedal dinosauriforms during walking and running. These methods, well validated for extant animals, indicate that during walking and slow running the metabolic rate of at least the larger extinct dinosaurs exceeded the maximum aerobic capabilities of modern ectotherms, falling instead within the range of modern birds and mammals. Estimated metabolic rates for smaller dinosaurs are more ambiguous, but generally approach or exceed the ectotherm boundary.

Conclusions/Significance

Our results support the hypothesis that endothermy was widespread in at least larger non-avian dinosaurs. It was plausibly ancestral for all dinosauriforms (perhaps Ornithodira), but this is perhaps more strongly indicated by high growth rates than by locomotor costs. The polarity of the evolution of endothermy indicates that rapid growth, insulation, erect postures, and perhaps aerobic power predated advanced “avian” lung structure and high locomotor costs.     

Do season and distribution affect thermal energetics of a hibernating bat endemic to the tropics and subtropics?

Although many tropical and subtropical areas experience pronounced seasonal changes in weather and food availability, few studies have examined and none have compared the thermal physiology and energetics of a hibernating mammal that is restricted to these regions. We quantified thermal energetics of northern long-eared bats (Nyctophilus bifax; body mass ～10 g) during summer, winter, and spring from a subtropical habitat, and also during winter from a tropical habitat, to determine how N. bifax cope with climate and seasonal changes in weather. We captured bats in the wild and measured metabolic rates via open-flow respirometry. The basal metabolic rate of subtropical bats at an ambient temperature (T(a)) of 32.6 ± 0.7°C was 1.28 ± 0.06 ml O(2)·g(-1)·h(-1) during both summer and winter, similar to other species of Nyctophilus. Resting metabolic rates below the thermoneutral zone increased similarly with decreasing T(a) during all seasons and in both regions. All individuals showed a high proclivity to enter torpor at T(a) values below the thermoneutral zone. Metabolic rates in torpid thermoconforming bats fell with T(a) and body temperature, and mean minimum metabolic rates during torpor were similar during all seasons and in both regions and as predicted from body mass in temperate zone hibernators. At very low T(a), torpid N. bifax thermoregulated, and this threshold T(a) differed significantly between subtropical (T(a) = 3.5 ± 0.3°C) and tropical (T(a) = 6.7 ± 0.7°C) individuals, but not between seasons. Our data show that thermal energetics of N. bifax do not vary seasonally and in many aspects are similar in tropical and subtropical bats; however, torpid individuals from the subtropics allow body temperature to fall to significantly lower values than those from the tropics.     

Shivering and non-shivering thermogenesis in a marsupial,the eastern barred bandicoot (Perameles gunnii)

We investigated the metabolic rate of the Tasmanian marsupial, the eastern barred bandicoot, Perameles gunnii, before and after acclimation to cold temperature (5 °C) for a 2-week period. Although body temperature did not change significantly, we observed a significant increase in the metabolic rate (MR) when measured at 5 °C before and after cold acclimation. Nor-epinephrine had a significant effect on the metabolic rate when measured in the thermoneutral zone and when measured at 5 °C after cold acclimation; however, there was no significant increase when measured at 5 °C before cold acclimation. Nor-epinephrine also resulted in a small but significant decrease in body temperature. Electromyography (EMG) measurements were obtained before and after cold acclimation during shivering. Shivering decreased after two weeks of cold exposure indicating that the bandicoot had acclimated to that temperature. Nor-epinephrine (NE) significantly reduced shivering before but not after cold acclimation. The metabolic rate and shivering decreased in the adult eastern barred bandicoot after acclimation at 5 °C and nor-epinephrine had similar effects to cold acclimation. Our findings of minor changes in thermal conductance suggest that insulation differences were unlikely explanations for our results. These experiments indicate that this marsupial is able to increase its heat production by non-shivering thermogenesis.     

The importance of microhabitat in thermoregulation and thermal conductance in two namib rodents—a crevice dweller, Aethomys namaquensis, and a burrow dweller, Gerbillurus paeba

1. 1.|Thermoregulatory measurements of two Nambi rodents; Gerbillurus paeba, a burrow dweller, and Aethomys namaquensis, a crevice dweller were compared. Both were similar to other small arid-adapted rodents in that basal metabolic rates were reduced, thermoneutral zones narrow and evaporative water losses low. Rates of conductance and thermal lability, however, at ambient temperatures (T_a) below thermoneutral zone, were significantly different (P 0.01).

2. 2.|The rock rat A. namaquensis, living in a microclimate characterized by a large diel range and low humidities, compensates for a reduced basal metabolic rate by having a low rate of conductance. In this way it maintains precise thermoregulatory control. G. paeba, on the other hand, living in a thermally-stable milieu, does not control body temperature precisely. This animal instead utilizes a high rate of conductance to remove metabolic heat produced within the body. This would be advantageous to an animal living in a plugged burrow where the high humidities encountered impede the rate of evaporative cooling.

3. 3.|The energetic responses of both species, above the thermoneutral zone, appear to reflect very closely the environmental conditions which occur in the microhabitat that they rest in during the day. G. paeba shows less tolerance to temperature fluctuations than A. namaquensis, but shows more marked increases in short-term cooling mechanisms at high T_as.

4. 4.|Despite the increased use of evaporative cooling through salivation and panting in addition to pulmocutaneous evaporation, exposure to T_as above 38°C is rapidly lethal to G. paeba.

The evolution of endothermy and its diversity in mammals and birds

Many elements of mammalian and avian thermoregulatory mechanisms are present in reptiles, and the changes involved in the transition to endothermy are more quantitative than qualitative. Drawing on our experience with reptiles and echidnas, we comment on that transition and on current theories about how it occurred. The theories divide into two categories, depending on whether selection pressures operated directly or indirectly on mechanisms producing heat. Both categories of theories focus on explaining the evolution of homeothermic endothermy but ignore heterothermy. However, noting that hibernation and torpor are almost certainly plesiomorphic (=ancestral, primitive), and that heterothermy is very common among endotherms, we propose that homeothermic endothermy evolved via heterothermy, with the earliest protoendotherms being facultatively endothermic and retaining their ectothermic capacity for "constitutional eurythermy." Thus, unlike current models for the evolution of endothermy that assume that hibernation and torpor are specialisations arising from homeothermic ancestry, and therefore irrelevant, we consider that they are central. We note the sophistication of thermoregulatory behavior and control in reptiles, including precise control over conductance, and argue that brooding endothermy seen in some otherwise ectothermic Boidae suggests an incipient capacity for facultative endothermy in reptiles. We suggest that the earliest insulation in protoendotherms may have been internal, arising from redistribution of the fat bodies that are typical of reptiles. We note that short-beaked echidnas provide a useful living model of what an (advanced) protoendotherm may have been like. Echidnas have the advantages of endothermy, including the capacity for homeothermic endothermy during incubation, but are very relaxed in their thermoregulatory precision and minimise energetic costs by using ectothermy facultatively when entering short- or long-term torpor. They also have a substantial layer of internal dorsal insulation. We favor theories about the evolution of endothermy that invoke direct selection for the benefits conferred by warmth, such as expanding daily activity into the night, higher capacities for sustained activity, higher digestion rates, climatic range expansion, and, not unrelated, control over incubation temperature and the benefits for parental care. We present an indicative, stepwise schema in which observed patterns of body temperature are a consequence of selection pressures, the underlying mechanisms, and energy optimization, and in which homeothermy results when it is energetically desirable rather than as the logical endpoint.     

Reproductive energetics and thermoregulatory status of nestlings in pampas mice Akodon azarae (rodentia: sigmodontinae)

We evaluated metabolic rates during reproduction and the thermoregulatory status of preweaning pups of Akodon azarae (Fisher 1829). Metabolic rates during late pregnancy and lactation were 159% and 200%, respectively, of the basal metabolic rate. Metabolic rates of 10-d-old pups were 447% of the adult's metabolic rates. No difference in metabolic rates of pups was detected among different ambient temperatures. Differences were detected in body temperatures between pups without mothers before and after exposure to different ambient temperatures below the thermoneutral zone. Differences were not detected in body temperatures among solitary or grouped pups.     

Substrate-specific changes in mitochondrial respiration in skeletal and cardiac muscle of hibernating thirteen-lined ground squirrels

During torpor, the metabolic rate (MR) of thirteen-lined ground squirrels (Ictidomys tridecemlineatus) is considerably lower relative to euthermia, resulting in part from temperature-independent mitochondrial metabolic suppression in liver and skeletal muscle, which together account for ~40 % of basal MR. Although heart accounts for very little (<0.5 %) of basal MR, in the present study, we showed that respiration rates were decreased up to 60 % during torpor in both subsarcolemmal (SS) and intermyofibrillar (IM) mitochondria from cardiac muscle. We further demonstrated pronounced seasonal (summer vs. winter [i.e., interbout] euthermia) changes in respiration rates in both mitochondrial subpopulations in this tissue, consistent with a shift in fuel use away from carbohydrates and proteins and towards fatty acids and ketones. By contrast, these seasonal changes in respiration rates were not observed in either SS or IM mitochondria isolated from hind limb skeletal muscle. Both populations of skeletal muscle mitochondria, however, did exhibit metabolic suppression during torpor, and this suppression was 2- to 3-fold greater in IM mitochondria, which provide ATP for Ca²⁺- and myosin ATPases, the activities of which are likely quite low in skeletal muscle during torpor because animals are immobile. Finally, these changes in mitochondrial respiration rates were still evident when standardized to citrate synthase activity rather than to total mitochondrial protein.     

The roles of energetics,water economy,foraging behavior,and geothermal refugia in the distribution of the bat,Macrotus californicus

Summary Energy metabolism, thermoregulation, and water flux ofMacrotus californicus, the most northerly representative of the Phyllostomidae, were studied in the laboratory using standard methods, and energy metabolism and water fluxes were studied in the field using the doubly labelled water method together with a time budget. Daily energy expenditures of free-living bats averaged 22.8 kJ during the winter study period. Approximately 60% of this was allocated to resting metabolism costs while in the primary roosts (22 h/day).Macrotus californicus is unable to use torpor. The thermoneutral zone (TNZ) in this species is narrow (33 to 40 °C) and metabolic rate increased rapidly as ambient temperature decreased below the TNZ. Basal metabolic rate was 1.25 ml O₂/g·h, or 24 J/g·h. Total thermal conductance below the TNZ. was 1.8 mW/g·°C, similar to values measured for other bats. Evaporative water loss showed a hyperbolic increase with increasing ambient temperature, and was approximately 1% of total body mass/h in the TNZ. The success of these bats as year-round residents in deserts in the southwestern United States is probably not due to special physiological adaptations, but to roosting and foraging behavior. They use geothermally-heated winter roost sites (stable year-round temperatures of approximately 29 °C) which minimize energy expenditures, and they have an energetically frugal pattern of foraging that relies on visual prey location. These seem to be the two major factors which have allowedM. californicus to invade the temperate zone.Abbreviations BMR basal metabolic rate - FMR field metabolic rate - T _a ambient temperature - T _b body temperature - T _lc,T _uc lower and upper critical temperature, respectively - TBW total body water - TNZ thermoneutral zone     

Allometries of the durations of torpid and euthermic intervals during mammalian hibernation: A test of the theory of metabolic control of the timing of changes in body temperature

Summary The durations of the intervals of torpor and euthermia during mammalian hibernation were found to be dependent on body mass. These relationships support the concept that the timing of body temperature changes is controlled by some metabolic process. Data were obtained from species spanning nearly three orders of magnitude in size, that were able to hibernate for over six months without food at 5°C. The timing of body temperature changes was determined from the records of copper-constantan thermocouples placed directly underneath each animal. Because all species underwent seasonal changes in their patterns of hibernation, animals were compared in midwinter when the duration of euthermic intervals was short and relatively constant and when the duration of torpid intervals was at its longest. Large hibernators remained euthermic longer than small hibernators (Fig. 2). This was true among and within species. The duration of euthermic intervals increased with mass at the same rate (mass^0.38) that mass-specific rates of euthermic metabolism decrease, suggesting that hibernators remain at high body temperatures until a fixed amount of metabolism has been completed. These data are consistent with the theory that each interval of euthermia is necessary to restore some metabolic imbalance that developed during the previous bout of torpor. In addition, small species remained torpid for longer intervals, than large species (Fig. 3). The absolute differences between different-sized species were large, but, on a proportional basis, they were comparatively slight. Mass-specific rates of metabolism during torpor also appear to be much less dependent on body mass than those during euthermia, but the precision of these metabolic measurements is insufficient for them to provide a conclusive test of the metabolic theory. Finally, small species with high mass-specific rates of euthermic metabolism are under tighter energetic constraints during dormancy than large species. The data presented here show that, in midwinter, small species compensate both by spending less time at high body temperatures following each arousal episode and by arousing less frequently, although the former is far more important energetically than the latter.     

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

Herbivores 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.     

Shivering,muscle tone,and uncoupling proteins in a developing marsupial,the Tasmanian bettong (Bettongia gaimardi)

This study examined the development of several physiological parameters that enable the development of endothermy during pouch life of the Tasmanian bettong (Bettongia gaimardi). By using several key age groups, we investigated the electromyography response of pouch young under different thermal conditions (35 or 20 °C), with and without injection of the β-agonist norepinephrine. We also used molecular techniques to examine the possible expression of uncoupling proteins 1, 2, and 3 (UCP1, 2, and 3), and if they were expressed, any association these may have with the timing of endothermic development. AT 6 weeks of age, pouch young were unable to thermoregulate via shivering or non-shivering mean, maintain a constant metabolic rate, or show any response to the β-agonist injection. When the animals were exposed to a cold stress (20 °C), 8-week-old pouch young initially shivered for 2–3 min before tapering off completely, causing body temperature to sharply decline. During the 10th week, cold-exposed pouch young began shivering, with the bout lasting approximately 10 min before ceasing and body temperature beginning to decline. It was also at this age that the expression of UCP2 was initially expressed. By the 12th week, cold exposed pouch young initially employed classical shivering; however, after approximately 12 min, this was replaced with an increase in muscular tone. This increase in muscular tone was also recorded in response to β-agonist injection at thermoneutral this age and was associated with an increase in metabolic rate. Also by this age, total body fat increased by approximately 300% from the levels expressed at 6 weeks of age and UCP2 was significantly upregulated. Although pouch young B. gaimardi did not show UCP1 expression at any time, UCP3 was expressed at every age investigated from 6 weeks of age. This study proposes that pouch young B. gaimardi use a mechanism of increased muscle tone as a source of heat production, and shows that UCP2 has an association with the onset of thermogenesis.     

Temperature regulation in a burrow-nesting tropical seabird,the Wedge-tailed Shearwater (Puffinus pacificus)

Summary At low air temperatures (2.3–13.9°C), Wedge-tailed Shearwaters (Puffinus pacificus) shivered and their oxygen consumption increased to as much as 283% of the mean value (0.77 ml O₂/g·h) within the thermoneutral zone of air temperature (23–34°C). The minimal thermal conductance of the tissues and plumage was similar to the value predicted from the body mass (320.5 g). The oxygen consumption of the birds within their thermoneutral zone was lower than predictions based on body mass. At elevated air temperatures, the shearwaters panted at respiratory frequencies as high as 260 respirations/min; maximal respiratory frequencies were not invoked until the birds had become hyperthermic. During exposure to a hot environment, the oxygen consumption of the birds increased and in most instances the shearwaters were not able to lose heat equivalent to their concurrent metabolic heat production.Symbols and abbreviations BMR basal metabolic rate - C _total total thermal conductance - f respiratory frequency - TEWL total evaporative water loss - T _st stomach temperature - T _re rectal temperature