Energy metabolism, thermogenesis and body mass regulation in Brandt's voles (Lasiopodomys brandtii) during cold acclimation and rewarming

Environmental cues play important roles in the regulation of an animal's physiology and behavior. The purpose of the present study was to test the hypothesis that ambient temperature was a cue to induce adjustments in body mass, energy intake and thermogenic capacity, associated with changes in serum leptin levels in Brandt's voles (Lasiopodomys brandtii). We found that Brandt's voles increased resting metabolic rate (RMR) and energy intake and kept body mass stable when exposed to the cold while showed a significant increase in body mass after rewarming. The increase in body mass after rewarming was associated with the higher energy intake compared with control. Uncoupling protein 1 (UCP1) content in brown adipose tissue (BAT) increased in the cold and reversed after rewarming. Serum leptin levels decreased in the cold while increased after rewarming, associated with the opposite changes in energy intake. Further, serum leptin levels were positively correlated with body mass and body fat mass. Together, these data supported our hypothesis that ambient temperature was a cue to induce changes in body mass and metabolism. Serum leptin, as a starvation signal in the cold and satiety signal in rewarming, was involved in the processes of thermogenesis and body mass regulation in Brandt's voles.     

Variations in thermal physiology and energetics of the tree shrew (<Emphasis Type="Italic">Tupaia belangeri</Emphasis>) in response to cold acclimation

Variations in environmental factors instigate significant changes in the physiology and behavior of animals, necessary for their survival. The present study investigated the hypothesis that ambient temperature is a cue capable of inducing changes in body mass, energy intake, and thermogenic capacity. Moreover, the current study determined the potential role of leptin in regulating adaptive thermogenesis in tree shrews (Tupaia belangeri). The tree shrew was chosen as the experimental animal as they inhabit a wide area of Asia and must acclimatize to the cold. Animals were subjected to either 5°C over 28 days to simulate cold acclimation, or maintained under the original climate of room temperature. At 28 days cold-acclimatized shrews had increased body mass by 9.41 g compared to controls. The increase in body mass was found primarily to be due to growth of the digestive organs, combined with significantly increased food intake. Under cold acclimation, uncoupling protein 1 (UCP1) expression in brown adipose tissue (BAT) was significantly elevated, while serum leptin concentration was significantly depressed below control levels. Serum leptin concentration was negatively correlated with body mass, energy intake, and thermogenic capacity during cold acclimation. In summary, these findings indicate that tree shrews adjust energy intake, thermogenic capacity, and body reserves in response to the cold, and further suggest that circulating leptin may act as a key signaling protein to regulate these adaptations.     

大绒鼠冷驯化和脱冷驯化能量代谢特征的变化

通过测定冷驯化(5℃)到脱冷驯化(30℃)条件下,大绒鼠(Eothenomys miletus)的体重、摄入能、静止代谢率(RMR)、非颤抖性产热(NST)和血清瘦素含量等参数,探讨了血清瘦素浓度与能量收支的关系。结果表明,冷驯化可致大绒鼠体重下降,RMR、NST、摄入能升高,血清瘦素浓度降低;脱冷驯化后大绒鼠体重增加,RMR、NST、摄入能降低,血清瘦素浓度增加。血清瘦素含量与体重呈正相关,与RMR、NST、摄入能呈负相关。表明大绒鼠的体重、摄入能和产热能力具有较强的可塑性,且瘦素可能参与了大绒鼠适应冷驯化及恢复过程中的能量平衡和体重的调节。     

Thermogenesis, energy intake and serum leptin in Apodemus chevrieri in Hengduan Mountains region during cold acclimation

Environmental factors play an important role in the seasonal adaptation of body mass and thermogenesis in small, wild mammals. The purpose of the present study was to test the hypothesis that ambient temperature was a cue to trigger the adjustments in body mass, energy intake, and serum leptin level in Apodemus chevrieri during 42 days of cold exposure. Our data demonstrated that cold acclimation induced a decrease in body mass and a significant increase in energy intake in A. chevrieri. Serum leptin levels were positively correlated with body mass and fat mass. These data suggest that A. chevrieri reduced the body mass and increased energy intake and thermogenic capacity under cold acclimation. Further, serum leptin appears to be involved in the energy intake regulation and thermoregulation.     

Adaptive character of metabolism in Eothenomys miletus in Hengduan Mountains region during cold acclimation

Environmental factors play an important role in the seasonal adaptation of body mass and thermogenesis in small, wild mammals. The purpose of the present study was to test the hypothesis that ambient temperature was a cue to trigger the seasonal adjustments in body mass, energy intake, uncoupling protein 1 (UCP1) in brown adipose tissue (BAT), and other biochemical characteristics of Eothenomys miletus during 49 days of cold exposure. Our data demonstrated that cold acclimation induced a remarkable decrease in body mass, a significant increase in energy intake and metabolic rate, and high expression of UCP1 in BAT of E. miletus. Biochemical characteristics of BAT and liver respiration were also increased following cold acclimation. These data suggest that E. miletus reduced the body mass and increased energy intake and expenditure under cold acclimation. Increased expression of UCP1 was potentially involved in the regulation of energy metabolism and thermogenic capacity following cold acclimation.     

冷驯化及复温对中缅树鼩白色脂肪组织中Ucp1和Cd137表达的影响

为探讨中缅树鼩(Tupaia belangeri) 白色脂肪组织（white adipose tissue, WAT）应对环境温度变化的适应机制,以荧光标记的Ucp1和Cd137抗体分别对中缅树鼩WAT进行标记,利用流式细胞术分选分析出对照组、冷驯化28d组、复温28d组阳性的白色脂肪细胞。结果发现：WAT中表达Ucp1、Cd137阳性的白色脂肪细胞百分数,在冷驯化组均显著高于对照组,而复温组均显著低于冷驯化组,恢复至对照组水平。表明：冷驯化诱导中缅树鼩WAT中表达Ucp1、Cd137的阳性细胞群增加,显示冷驯化能诱导中缅树鼩的WAT发生褐变;复温后表达Ucp1、Cd137阳性的白色脂肪细胞百分数恢复到对照水平,反映出WAT的可塑性。因此,WAT的可塑性调节也是中缅树鼩适应环境温度变化的重要产热机制。     

冷驯化对中缅树鼩产热能力的影响

在 ( 5± 1)℃条件下对中缅树 (Tupaiabelangeri)进行低温胁迫处理 ( 0～ 2 8d) ,测定其冷驯化过程中的静止代谢率 (RMR)、非颤抖性产热 (NSTmax)、冷诱导最大产热 (CIRMR)、体重、体温等生理指标 ,探讨低温对中缅树产热能力的影响。结果表明 :①冷驯化期间中缅树体重增加 ,体温降低 ,产热能力显著增强 ;②在冷驯化过程中 ,增加RMR和CIRMR是中缅树抵抗低温胁迫的主要产热模式。     

The effect of cold-acclimation on energy strategies of Apodemus draco in Hengduan Mountain region

Environmental factors play an important role in the seasonal adaptation of body mass and thermogenesis in small mammals. The purpose of the present study was to test the hypothesis that ambient temperature triggers adjustments in body mass, body temperature, energy intake, digestible energy intake, metabolic energy intake, and the length and weight of the digestive tract, in Apodemus draco during 42 days of cold exposure. Body mass and body temperature of the cold-acclimated group decreased during the first 28 days and then stabilized at the lower levels. After 14 days of cold acclimation, the body mass of the cold-exposed group was significantly lower and the energy intake, digestible energy intake, and metabolic energy intake were significantly elevated relative to control animals. The differences were maximal after 21 days. The length and weight of the digestive tract (both wet and dry mass of the stomach, small intestine, large intestine, and cecum) changed significantly in response to decreasing temperature. During cold exposure, A. draco was able to maintain physiological functions and reduce its absolute energy demands by reducing the body mass, increasing energy intake, and adjusting the length of the digestive tract.     

高山姬鼠冷驯化过程中的能量收支

为探讨栖息于横断山地区高山姬鼠的能量代谢特征,采用食物平衡法,在冷驯化条件下,对其能量收支进行了测定。分别测定了冷驯化(5 ± 1℃ ,42 d)过程中,高山姬鼠体重、体温、每日摄入能、消化能、消化率、粪便能及可代谢能、可代谢率的变化。结果表明:随着冷驯化时间的延长,高山姬鼠的体重和体温降低,28 d 时达到最低值后保持稳定,其中体重在冷驯化14 d 时即与对照组有显著差异,28 d 时平均比对照组降低了15.5% ,体温在14 d 后和对照组有显著差异。每日摄入能、消化能、可代谢能升高,三者均在冷驯化14 d 后与对照组有极显著差异,21 d 时达到最高后保持稳定。粪便能、消化率和可代谢率在冷驯化过程中没有显著变化。高山姬鼠在冷暴露过程中,通过降低体重减少绝对能量需求;通过降低体温减少用于维持体温恒定所消耗的能量;通过增加能量摄入维持正常的生理机能。高山姬鼠在冷驯化过程中表现出的变化模式,与其低纬度、高海拔、年平均温度较低的生存环境有关,这在一定程度上反映了横断山区小型哺乳动物在低温胁迫下的生存机制和适应对策。     

Effects of cold acclimation on body mass,serum leptin level,energy metabolism and thermognesis in Eothenomys miletus in Hengduan Mountains region

Eothenomys miletus is an important species inhabiting Hengduan mountains region. In order to study adaptive strategy and the role of serum leptin level in response to a 49 d cold exposure, body mass, energy intake, basal metabolic rate (BMR), nonshivering thermogenesis (NST) in E. miletus were measured. During cold exposure (5±1 ^oC), body mass decreased; serum leptin levels decreased significantly and were positively correlated with body mass and fat mass; energy intake, BMR and NST were higher at 5 °C than that of controls. These results suggest that E. miletus enhanced thermogenic capacity and increased maintenance cost during cold acclimation, resulting in increased energy intake. Serum leptin participated in the regulation of energy balance and body mass in E. miletus.     

Seasonal changes in body mass and thermogenesis in tree shrews (Tupaia belangeri): The roles of photoperiod and cold

Environmental factors play an important role in the seasonal adaptation of body mass and thermogenesis in small, wild mammals. To determine the contributions of photoperiod and cold on seasonal changes in energy metabolism and body mass, the resting metabolic rates (RMR), nonshivering thermogenesis (NST), energy intake and gut morphology of the tree shrews were determined in winter and summer and in laboratory acclimated animals. Body mass, RMR and NST increased in winter, and these changes were mimicked by exposing animals to short-day photoperiod or cold in the animal house. Energy intake and digested energy also increased significantly in winter, and also during exposure of housed animals to both short-day photoperiod and cold. The lengths and weights of small intestine increased in winter. These results indicated that Tupaia belangeri overcomes winter thermoregulatory challenges by increasing energy intake and thermogenesis, and adjusted gut morphology to balance the total energy requirements. Short-day photoperiod and cold can serve as environmental cues during seasonal acclimatization.     

Photoperiodic regulation in energy intake, thermogenesis and body mass in root voles (Microtus oeconomus)

The present study was designed to examine whether photoperiod alone was effective to induce seasonal regulations in physiology in root voles (Microtus oeconomus) from the Qinghai-Tibetan plateau noted for its extreme cold environment. Root voles were randomly assigned into either long photoperiod (LD; 16L:8D) or short photoperiod (SD; 8L:16D) for 4 weeks at constant temperature (20 degrees C). At the end of acclimation, SD voles showed lower body mass and body fat coupled with higher energy intake than LD voles. SD greatly enhanced thermogenic capacities in root voles, as indicated by elevated basal metabolic rate (BMR), nonshivering thermogenesis (NST), mitochondrial protein content and uncoupling protein-1 (UCP1) content in brown adipose tissue (BAT). Although no variations in serum leptin levels were found between SD and LD voles, serum leptin levels were positively correlated with body mass and body fat mass, and negatively correlated with energy intake and UCP1 content in BAT, respectively. To summarize, SD alone is effective in inducing higher thermogenic capacities and energy intake coupled with lower body mass and body fat mass in root voles. Leptin is potentially involved in the photoperiod induced body mass regulation and thermogenesis in root voles.     

光周期和高脂食物对雌性高山姬鼠能量代谢和产热的影响

为了研究光周期和高脂食物对小型哺乳动物能量代谢和产热的影响,将成年雌性高山姬鼠分别驯化于长光照低脂、高脂食物和短光照低脂、高脂食物条件下,7周后测定动物的体重、能量摄入、产热、身体组成、血清瘦素浓度以及体脂含量等参数。结果发现:1)短光照抑制体重增长,降低血清瘦素浓度,增加非颤抖性产热;2)高脂食物使摄入能减少,消化率和体脂含量提高,但未显著影响体重、基础代谢率、非颤抖性产热和血清瘦素浓度;3)血清瘦素浓度与摄入能不相关,但与体脂重量正相关。结果暗示:短光照下瘦素作用敏感性增加和产热能力增强,可能介导了抵抗高脂食物诱导的肥胖。在野外条件下,高山姬鼠能通过能量代谢和产热的适应性调节避免体重的过度增长,有利于降低捕食风险,增强生存能力。     

Radiant heat affects thermoregulation and energy expenditure during rewarming from torpor

The high expenditure of energy required for endogenous rewarming is one of the widely perceived disadvantages of torpor. However, recent evidence demonstrates that passive rewarming either by the increase of ambient temperature or by basking in the sun appears to be common in heterothermic birds and mammals. As it is presently unknown how radiant heat affects energy expenditure during rewarming from torpor and little is known about how it affects normothermic thermoregulation, we quantified the effects of radiant heat on body temperature and metabolic rate of the small (body mass 25 g) marsupial Sminthopsis macroura in the laboratory. Normothermic resting individuals exposed to radiant heat were able to maintain metabolic rates near basal levels (at 0.91 ml O(2) g(-1) h(-1)) and a constant body temperature down to an ambient temperature of 12 degrees C. In contrast, metabolic rates of individuals without access to radiant heat were 4.5-times higher at an ambient temperature of 12 degrees C and body temperature fell with ambient temperature. During radiant heat-assisted passive rewarming from torpor, animals did not employ shivering but appeared to maximise uptake of radiant heat. Their metabolic rate increased only 3.2-times with a 15- degrees C rise of body temperature (Q(10)=2.2), as predicted by Q(10) effects. In contrast, during active rewarming shivering was intensive and metabolic rates showed an 11.6-times increase. Although body temperature showed a similar absolute change between the beginning and the end of the rewarming process, the overall energetic cost during active rewarming was 6.3-times greater than that during passive, radiant heat-assisted rewarming. Our study demonstrates that energetic models assuming active rewarming from torpor at low ambient temperatures can substantially over-estimate energetic costs. The low energy expenditure during passive arousal provides an alternative explanation as to why daily torpor is common in sunny regions and suggests that the prevalence of torpor in low latitudes may have been under-estimated in the past.     

冷驯化对中缅树鼩能量代谢的影响

在5 ±1 ℃条件下对中缅树鼠句进行冷驯化处理, 测定其能量代谢。冷驯化28 d 后, 体重比对照组显著增加7.33 %; 整体能值达到30.47 ±0.46 kJ / g (N = 8) , 比对照组增加4.98 %; 摄入能比对照组增加36.17 %; 同化能比对照组增加66.2 %; 生长能达到6.98 ±0.53 kJ / 100 g (N = 7) 体重·天, 是对照组的4.85 倍; 维持能比对照组增加64.0 % , 达到352.96 ±28.34 kJ / 100 g 体重·天(N = 7) 。以上结果表明中缅树鼠句在冷胁迫影响下, 以增加能量摄入、能量储存和维持能和降低排泄能量的生理机制来维持能量代谢平衡, 以此对策来提高低温环境适应能力。
     

Seasonal changes in body mass, energy intake and thermogenesis in Maximowiczi’s voles (Microtus maximowiczii) from the Inner Mongolian grassland

Small mammals inhabiting temperate and arctic regions exhibit annual adaptive adjustments in physiology, anatomy, and behavior. No data on the physiology of Maximowicz’s voles (Microtus maximowiczii) are available at present. Here we examined the seasonal changes in body mass, food intake, thermogenic capacity, serum leptin and thyroid hormone levels in wild-captured individuals from Inner Mongolian grassland, China. We further examined the effects of photoperiod on these parameters. Energy intake, resting metabolic rate, nonshivering thermogenesis (NST), and serum tri-iodothyronine (T3) levels increased while serum leptin and body mass decreased in the cold seasons. Serum T3 levels were positively correlated with NST and uncoupling protein 1 (UCP1) contents in brown adipose tissue, and leptin levels were negatively correlated with energy intake and resting metabolic rate. Furthermore, laboratory data showed these changes could be induced by short photoperiod alone. Taken together, our results indicate that Maximowicz’s voles can increase thermogenic capacity and energy intake to cope with cold stress. Serum leptin seems to be involved in the regulation of energy intake and changes in T3 level may be important for the variations in NST and/or UCP1. Short photoperiod can serve as a seasonal cue for the winter acclimatization of energy balance in free-living Maximowicz’s voles.     

长期强迫运动对大绒鼠体重、能量代谢和血清瘦素的影响

动物稳定体重的维持需要能量摄入和消耗之间的平衡。运动是影响动物能量平衡的重要因素之一。为了解运动对大绒鼠(Eothenomys miletus)的生理学效应,在室内条件下,测定了强迫运动训练(运用小鼠封闭跑台)8周后大绒鼠的体重、代谢率、摄入能、血清瘦素和身体组成的变化。结果显示,强迫运动训练8周对大绒鼠的体重无显著影响;大绒鼠的代谢率和摄入能均显著增加,训练8周后静止代谢率较对照组增加了29.9%,运动最大代谢率较对照组增加了10.7%;强迫运动训练8周组的身体脂肪重量比对照组降低了28.9%,血清瘦素水平比对照组下降了27.4%,对照组的瘦素与体脂含量具有明显的相关性,但运动组则不具有相关性;运动组的肝重量和消化道重量较对照组均显著增加;而体水重量则显著降低。这些结果表明,在强迫运动训练期间大绒鼠主要通过动员储存的脂肪、增加代谢率和食物摄入的方式来维持自身的体重及能量平衡。瘦素在长期强迫运动过程中对身体脂肪含量的变化具有调节作用。     

Cold exposure does not decrease serum leptin concentration,but increases energy intake and thermogenic capacity in pregnant Brandt's voles (Lasiopodomys brandtii)

In most mammals, maternal body mass and fat mass increase during pregnancy due to hyperphagia. These physiological changes provide the fetus with energy and nutrients and prepare the mother for the high energetic demands of lactation. In the present study, metabolic changes in response to cold and pregnancy were examined in female Brandt's voles (Lasiopodomys brandtii). At 23±1 °C, the voles increased body mass and deposited body fat during pregnancy. However, at 5±1 °C pregnant voles did not deposit body fat even though energy intake increased above the level in the warm. Serum leptin concentration increased during pregnancy and was not influenced by cold exposure. Thermogenic capacity, as indicated by uncoupling protein 1 (UCP1) content in brown adipose tissue (BAT), increased in cold-exposed pregnant voles. The number and mass of fetuses were not affected by cold exposure. Our data may indicate the importance of an increased serum leptin concentration for a successful outcome of the pregnancy and also the independence of leptin secretion from body fat in pregnant voles. It also implies the need to develop central leptin resistance with respect to control of energy balance for pregnant voles.     

Effects of photoperiod on energy intake, thermogenesis and body mass in Eothenomys miletus in Hengduan Mountain region

The present study was designed to examine whether photoperiod alone was effective to induce seasonal changes in physiology in voles (Eothenomys.) from the Hengduan Mountain region. Eothenomys miletus were randomly assigned into either long photoperiod (LD; 16L: 8D) or short photoperiod (SD; 8L: 16D) for 4 weeks at constant temperature (25 °C). At the end of acclimation, SD voles showed lower body mass and body fat coupled with higher energy intake than LD voles. SD greatly enhanced the thermogenic capacity of E. miletus, as indicated by an elevated nonshivering thermogenesis (NST), mitochondrial protein in brown adipose tissue (BAT); basal metabolic rate (BMR) was also raised. Although no variations in serum leptin levels were found between SD and LD voles, serum leptin levels were positively correlated with body mass and body fat mass, and negatively correlated with energy intake and UCP1 content in BAT, respectively. To summarize, SD alone is effective in inducing higher thermogenic capacities and energy intake coupled with lower body mass and body fat mass in root voles. Leptin is potentially involved in the photoperiod induced body mass regulation and thermogenesis in E. miletus. Our study shows that SD alone is effective.     

渐变的光周期和温度对布氏田鼠能量代谢和身体成分的影响

为探讨在同时逐渐缩短光照时间和降低温度的过程中,动物能量代谢水平和身体成分的适应性变化, 我们以成年雄性布氏田鼠为对象, 测定了温度为20℃ 和光周期为12L:12D (对照组),以及从温度为20℃ 和长光照条件(16L:8D)逐渐转换到温度为4℃ 和短光照条件(8L:16D)的过程中(实验组), 其体重、静止代谢率和能量摄入的变化, 以及经过8 周驯化后身体器官和组织重量的变化。结果发现:实验组动物的体重增长率低于对照组。在驯化期间, 静止代谢率无组内和组间差异。实验组动物的干物质摄入、能量摄入和消化能等组内差异不明显, 但对照组动物在驯化的第8 周显著降低。实验组动物的能量摄入水平在驯化后显著升高;小肠和胃的干重, 以及小肠和心脏等器官的湿重也都显著高于对照组。结果表明,布氏田鼠能够采取降低体重、增加能量摄入和调整体内某些器官和组织重量的方式来适应变化的环境条件。