Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (<Emphasis Type="Italic">Meriones unguiculatus</Emphasis>): the roles of short photoperiod and cold

Seasonal adjustments in body mass and thermogenesis are important for the survival of small mammals during acclimatization in the temperate zone. To determine the contributions of short photoperiod and cold temperatures to seasonal changes in thermogenesis and body mass in Mongolian gerbils (Meriones unguiculatus), body mass, basal metabolic rate (BMR), nonshivering thermogenesis (NST), energy intake and energy digestibility were determined in seasonally acclimatized and laboratory acclimated animals. Body mass showed significant seasonal changes and decreased to a minimum in winter. Both BMR and NST increased in winter, and these changes were mimicked by exposing animals to short photoperiod or cold temperatures in the animal house. Digestible energy intake also increased significantly in winter, and also during exposure of housed animals to both short photoperiod and cold. These results suggest that Mongolian gerbils overcome winter thermoregulatory challenges by increasing energy intake and thermogenesis, and decreasing body mass to reduce total energy requirements. Short photoperiod and cold can serve as effective environmental cues during seasonal acclimatization.     

光周期对布氏田鼠和长爪沙鼠体重和能量代谢的影响

本文测定了光周期对雄性布氏田鼠和长爪沙鼠的体重、基础代谢率和能量代谢的影响。动物从长光照(16L∶8D , LD) 转入短光照(8L∶16D , SD) 条件下驯化6 周(田鼠) 和7 周(沙鼠) 。结果显示: (1) 无论在LD还是SD 条件下, 两种动物的体重都趋于增加, 但反应程度不同也具有种间差异性。两种动物的体重对光周期的反应有时段性, 约14 d 前两种动物的体重增加迅速, 而后增加缓慢, 3 周左右趋于稳定。短光照条件下布氏田鼠和长爪沙鼠的体重分别增长了37 %和11 % , 均低于长光照组(分别为47 %和25 %) , 说明短光照条件下布氏田鼠和长爪沙鼠的体重增长较长光照缓慢; (2) 光照对两种动物的摄入能、消化能和可代谢能均没有显著影响,摄入能与体重的增长无关; (3) 光照对两种动物的基础代谢率无显著影响。这些结果表明: 布氏田鼠和长爪沙鼠在自然环境中, 可能以光周期作为一种信号, 当环境温度降低、食物质量变劣时, 采取降低体重以减少绝对能量需求的策略而适应环境。     

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.     

Regulation of body weight and thermogenesis in seasonally acclimatized Brandt's voles (Microtus brandti)

Seasonal changes in an animal's morphology, physiology, and behavior are considered to be an adaptive strategy for survival and reproductive success. In the present study, we examined body weight and several behavioral, physiological, hormonal, and biochemical markers in seasonally acclimatized Brandt's voles (Microtus brandti) to test our hypothesis that Brandt's voles can decrease energy intake associated with decrease in body weight, body fat content, serum leptin level, and increasing thermogenesis in winter conditions. We found that the body weight of Brandt's voles was lowest in winter (December to February) and highest in spring and early summer (May to June). This seasonal variation in body weight was associated with changes in other markers examined. For example, the winter decrease in body weight was accompanied by increased energy intake and enhanced nonshivering thermogenesis (NST) as well as by decreased body fat mass and reduced levels of circulating leptin. Further, circulating levels of leptin were positively correlated with body weight and body fat mass, and negatively correlated with energy intake and uncoupling protein 1 contents. Together, these data do not support our hypothesis and suggest that leptin may be involved in this process and serve as a starvation signal in Brandt's voles.     

Short photoperiod influences energy intake and serum leptin level in Brandt's voles (Microtus brandtii)

Photoperiod cues play important roles in the regulation of seasonal variations in body mass (BM) and energy balance for many small mammals. The present study was designed to examine the effects of photoperiod acclimation on BM, energy intake, and serum leptin levels in Brandt's voles (Microtus (Lasiopodomys) brandtii). After 4 weeks of acclimation to either long (LD; light:dark, 16:8) or short (SD; 8:16) photoperiod, SD voles had lower BM, body fat mass, and dry mass of liver and kidneys, but higher digestible energy intake in comparison to LD voles. SD voles also showed a lower level of serum leptin than did LD voles. Furthermore, the level of serum leptin was correlated positively with body fat mass and negatively with gross energy intake. Together, these data suggest that Brandt's voles employ a strategy of minimizing body growth, increasing energy intake, and mobilizing fat deposition in response to cues associated with short photoperiod. Furthermore, leptin seems to be involved in the regulation of BM and energy balance mediated by photoperiod.     

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.     

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.     

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.     

单宁酸对布氏田鼠能量代谢的影响

为了解单宁酸对成年布氏田鼠(Lasiopodomys bandtii**)能量代谢和产热的影响,本文采用含0、3.3%和6.6%单宁酸浓度的食物饲喂布氏田鼠21 d,对其体重、基础代谢率、非颤抖性产热和能量收支等进行了测定。代谢率采用封闭式流体压力呼吸计测定;非颤抖性产热用皮下注射去甲肾上腺素诱导;能量摄人采用食物平衡法测定。结果发现:(1) 单宁酸食物对布氏田鼠的体重没有明显影响;(2)取食含6.6%单宁酸食物的动物的基础代谢率于第10 d高于对照组。20 d时,3组动物的基础代谢率没有显著差异;(3) 单宁酸食物对非颤抖性产热没有显著影响;(4) 食用含单宁酸食物的动物的摄人能和消化能于第10 d显著低于对照组,但第20 d时则差异不显著。这些结果表明:布氏田鼠的基础代谢率和能量摄入对单宁酸的反应具有时段性,短期内能量消耗增加,随着动物对食物的适应,生理功能恢复到正常水平。     

Effects of diet quality on energy budgets and thermogenesis in Brandt's voles

Food quality and availability play an important role in an animal's life history. The aim of this study was to examine the effect of diet quality [high-fiber diet (HF) or low-fiber diet (LF)] on energy budgets and thermogenesis in Brandt's voles (Lasiopodomys (Microtus) brandtii). Dry matter intake and gross energy intake increased and digestibility decreased in HF voles compared with LF voles, while the digestible energy intake was similar for both HF and LF voles. Nonshivering thermogenesis (NST) decreased in HF voles, while LF voles kept stable; no significant differences were detected in basal metabolic rate (BMR), BAT uncoupling protein 1 (UCP1) content and the levels of serum thyroid hormones (T3 and T4) between HF and LF voles. Although there were no differences in body fat content and serum leptin concentrations between HF and LF voles, serum leptin concentrations in HF voles were reduced to nearly half as those seen in LF voles after 4-weeks acclimation. These results support the hypothesis that Brandt's voles can compensate the poor quality diet physiologically by the means of increasing food intake and decreasing thermogenesis.     

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.     

Seasonal changes in thermogenesis and body mass in wild Mongolian gerbils (Meriones unguiculatus)

Seasonal adjustments in body mass (BM), nonshivering thermogenesis (NST) and several physiological, hormonal, and biochemical markers were measured in wild-trapped Mongolian gerbils (Meriones unguiculatus) from Inner Mongolia, China. Sexual differences were detected in BM, NST, brown adipose tissue (BAT) mass, and mitochondrial protein content. BM and NST in males were higher in winter (January) and spring (May) than in summer (August), and BM of females was also the highest in winter, but NST remained relatively constant throughout the year. Cytochrome c oxidase activity and mitochondrial uncoupling protein 1 (UCP1) content in BAT were enhanced in winter in males or females, respectively. Serum leptin concentration was the lowest in winter and positively correlated with BM and body fat mass but was negatively correlated with BAT UCP1 content. These data suggest that wild Mongolian gerbils do not depend on a decrease in BM, but instead increase their thermogenic capacity to cope with cold stress. Leptin may be involved in the seasonal regulation in energy balance and thermogenesis in field Mongolian gerbils.     

自愿转轮运动对雄性长爪沙鼠体重和能量代谢的影响

运动是影响动物能量平衡和体重变化的重要因素之一。为研究自愿转轮运动对体重和能量代谢的影响,我们监测了8 周自愿转轮运动过程中,雄性长爪沙鼠的体重、能量摄入、消化率、静止代谢率(RMR) 和非颤抖性产热(NST)的变化,以及8 周后的体脂含量、血清甲状腺激素(T3、T4 )和瘦素(leptin)水平的变化等。结果发现,8 周自愿转轮运动增加了长爪沙鼠的体重和能量摄入以及血清瘦素水平(血清瘦素浓度比对照组高27% ),但对消化率、RMR 和褐色脂肪组织的线粒体蛋白浓度等没有明显影响。尽管体脂含量和血清T₃ 和T₄ 没有显著差异,但运动组体脂含量比对照组高33%,血清T₃ 和T₄ 水平分别比对照组低10% 和38%。血清瘦素浓度与体脂重量呈正相关。因此,自动转轮运动并没有降低动物的体重和体脂含量,但瘦素和甲状腺素在雄性长爪沙鼠能量代谢和能量平衡中的作用尚需进一步确定。     

Different physiological roles of serum leptin in the regulation of energy intake and thermogenesis between pregnancy and lactation in primiparous Brandt's voles (Lasiopodomys brandtii)

Reproduction, especially lactation, is associated with major metabolic adaptive changes. In this study, we investigated the metabolic changes and the roles of leptin during different periods of reproduction in primiparous Brandt's voles (Lasiopodomys brandtii). Energy intake, thermogenic capacity and serum leptin levels were examined in non-reproductive, mid pregnant, late pregnant, early lactating and peak lactating voles. Voles increased body mass by nearly 70% during late pregnancy compared to the non-breeding controls. The increase in body mass was mainly due to the increase in body fat mass which increased by 56%, and the growth of the reproductive tissues and digestive organs. Lactating voles decreased body fat by nearly 27% at peak lactation compared to the controls, and 53% compared to late pregnant voles. At the same time they increased food intake significantly. Uncoupling protein 1 (UCP1) content in brown adipose tissue (BAT) decreased significantly at peak lactation. Serum leptin increased significantly in the mid pregnancy, at a time when there was no increase in body fat, and remained at this high level in late pregnancy. Leptin levels decreased after parturition and reached a nadir at peak lactation. Serum leptin was negatively correlated with energy intake during lactation, but not during pregnancy. These data suggest that Brandt's voles adjust energy intake, thermogenic capacity and body reserves to match the high energy demands for reproduction. Hyperleptinemia, without decreased energy intake suggests a state of leptin resistance during pregnancy, and hypoleptinemia during lactation might act as a signal to stimulate energy intake.     

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。     

High body weight associated with impaired nonshivering thermogenesis but improved glucose tolerance in Mongolian gerbils (Meriones unguiculatus)

Overweight and obesity correspond with metabolic syndromes, such as glucose intolerance and type 2 diabetes. The objective of this study was to determine whether decreased thermogenesis mass and glucose intolerance are directly related to changes in body mass in Mongolian gerbils. High body weight gerbils displayed increase in total body fat mass especially epididymal fat pad, and decrease in nonshivering thermogenesis, as indicated by depressed mitochondrial protein content and uncoupling protein-1 content in brown adipose tissue. No variations of sirtuin 1 and subunit IV of cytochrome oxidase expression were found in brown adipose tissue and skeletal muscle between the two groups. High body weight gerbils showed increased serum leptin and insulin concentrations but surprisingly increased glucose tolerance, suggesting a difference from other obese species in the regulation of glucose metabolism. Serum leptin levels were negatively correlated with UCP1 content in BAT and positively correlated with energy intake and insulin concentration. Our data suggest that leptin may be involved in thermogenesis regulation, insulin secretion and glucose metabolism in HBW gerbils.     

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.     

Effects of temperature and photoperiod on thermogenesis in plateau pikas (Ochotona curzoniae) and root voles (Microtus oeconomus)

We examined the effects of temperature and photoperiod on metabolic thermogenesis and the thermogenic characteristics of brown adipose tissue in plateau pikas (Ochotona curzoniae) and root voles (Microtus oeconomus), the dominant species of small mammals in the alpine meadow ecosystems on the Qinghai-Tibetan Plateau. Pikas and voles were acclimated in the following groups: (1) Long day – warm temperature (16L:8D, 23 °C), (2) Long day – cold temperature (16L:8D, 5 °C), (3) short day – warm temperature (8L:16D, 23 °C), and (4) short day – cold temperature (8L:16D, 5 °C). Both temperature and photoperiod were important environmental cues for changes in thermogenesis for both species. Low temperature and short photoperiod induced increases in metabolic rate, nonshivering thermogenesis (NST), mitochondrial protein contents of brown adipose tissue, and cytochrome C oxidase activity of brown adipose tissue mitochondria in both species. Plateau pikas were more sensitive to cold (79% of the total NST response) than to short photoperiod (21%), while root voles were more sensitive to short photoperiod (60% of the total NST response) than to cold (40%), although cold clearly enhanced thermogenesis. Their thermogenic characteristics correlated with their preferred habitats: plateau pikas are found mainly in more exposed microhabitats in open sunny meadow, while root voles live in more sheltered microhabitats in relatively closed shrub. Our results also showed that temperature and photoperiod combined induce thermogenic adjustments in both species in seasonal acclimatization in their alpine meadow macrohabitat. Accepted: 10 November 1998     

Effects of photoperiod on energy budgets and thermogenesis in Mongolian gerbils (Meriones unguiculatus)

(1)

To investigate the role of photoperiod on the regulation of energy budgets and thermogenesis in Mongolian gerbils, body mass (BM), body fat mass (BFM), basal metabolic rate (BMR), nonshivering thermogenesis (NST), gross energy intake (GEI), mitochondrial cytochrome c oxidase (COX) activity and uncoupling protein1 (UCP1) content of brown adipose tissue (BAT), and serum tri-iodothyronine (T₃), thyroxine (T₄) and leptin levels were measured.     

Effects of photoperiod and food availability on growth, leptin, sexual maturation and maintenance in the Mongolian gerbils (Meriones unguiculatus)

Reproductive activity of Mongolian gerbils is regulated by photoperiod nevertheless body weight regulation is controlled without ambient photoperiod. Food intake is a major factor affecting rodent reproductive efficiency. Leptin is a hormone secreted by adipose tissue and modulates food intake, energy expenditure and body fat stores. In this study we studied the interaction of photoperiod and food availability on growth, sexual maturation and leptin concentration in the male and female gerbils. Gerbils were gestated and reared in either 14L:10D or 2L:22D. At weaning, gerbils were housed individually and divided into three groups: fed ad libitum, fed 80% of ad libitum or fed 60% of ad libitum. Body weights were recorded at weaning and every week thereafter. After twelve weeks of treatment, animals were sacrificed and testes and uterine weights were determined and blood was collected for leptin measurement. Food restriction reduced body weight and inhibited reproductive development. Absolute paired testis weights were similar in ad lib and 80% of ad lib groups but significantly different compared with the 60% of ad lib group in both photoperiods. Body weights were also directly dependent upon the level of food restriction. Uterine mass was only affected in the 60% of ad lib group in 14L but both food restriction levels significantly affected the uterine weights in 2L. Significant variations were found in leptin profiles. Leptin concentration was highest in ad lib and 80% of ad lib groups and lowest in 60% of ad lib groups. These results suggest that the reproductive activity of Mongolian gerbils is sensitive to food intake and multiple potential environmental cues (e.g., food availability, temperature) can be utilized.