What causes intraspecific variation in resting metabolic rate and what are its ecological consequences?

Individual differences in the energy cost of self-maintenance (resting metabolic rate, RMR) are substantial and the focus of an emerging research area. These differences may influence fitness because self-maintenance is considered as a life-history component along with growth and reproduction. In this review, we ask why do some individuals have two to three times the ‘maintenance costs’ of conspecifics, and what are the fitness consequences? Using evidence from a range of species, we demonstrate that diverse factors, such as genotypes, maternal effects, early developmental conditions and personality differences contribute to variation in individual RMR. We review evidence that RMR is linked with fitness, showing correlations with traits such as growth and survival. However, these relationships are modulated by environmental conditions (e.g. food supply), suggesting that the fitness consequences of a given RMR may be context-dependent. Then, using empirical examples, we discuss broad-scale reasons why variation in RMR might persist in natural populations, including the role of both spatial and temporal variation in selection pressures and trans-generational effects. To conclude, we discuss experimental approaches that will enable more rigorous examination of the causes and consequences of individual variation in this key physiological trait.     

鲫幼鱼(Carassius auratus)标准代谢个体差异与力竭后代谢特征及行为的关联

为考察鲫(Carassius auratus)幼鱼标准代谢的个体差异与运动力竭后代谢特征和行为的关系,在(25.0±0.5)℃条件下测定80尾鲫幼鱼标准代谢率(SMR),筛选出40尾实验鱼[体重(13.54±0.20)g,体长(8.05±0.07)cm],其中包括20尾高SMR个体和20尾低SMR个体,测定运动至力竭实验鱼的最大代谢率(MMR),并计算代谢空间(AS=MMR-SMR)、相对代谢空间(FAS)和过量耗氧(EPOC)总量,随后测定单尾鱼的快速启动行为[反应时间(RT)、最大线速度(Umax)、最大线加速度(Amax)和120ms移动距离(S120)]以及个性行为(勇敢性和活跃性)。结果显示鲫幼鱼的SMR与AS、FAS和EPOC总量均呈负相关,而与MMR不相关;MMR与AS、FAS和EPOC总量均呈正相关;协方差分析显示高SMR个体组的代谢恢复速率与低SMR个体组无显著差异。鲫幼鱼的SMR与快速启动行为的RT呈正相关,与Amax呈负相关,而与Umax和S120均不相关。在快速启动行为中,鲫幼鱼的RT与Umax、Amax和S120均呈负相关,而Umax与Amax和S120呈正相关。鲫幼鱼的SMR与其勇敢性指标如潜伏期(L)、曝露时间(ET)和探头频率(AF)以及活跃性指标如运动时间比(PTM)、撞墙频率(FHW)均不相关,但鲫幼鱼的PTM与FHW和ET呈正相关。研究表明在实验室条件下鲫幼鱼的能量代谢特征、快速启动和个性行为存在明显的个体差异现象,并且部分表型特征之间存在权衡,提示这些权衡可能是鲫幼鱼的生理、行为与栖息环境相互作用的综合结果。     

The metabolic rate of roach in relation to body size and temperature

Standard and routine metabolic rates of roach Rutilus rutilus for a wide size and temperature range (3–200 g, 5–23° C) were analysed by automated, computerized intermittent flow respirometry. The mass exponent b ranged from 0·68 to 0·82 for standard metabolism, and from 0·65 to 0·92 for routine metabolism depending on the experimental temperature. For routine metabolism b was lowest at 10° C. At both decreasing and increasing temperatures, b increased significantly. Roach were exponentially temperature-dependent for both metabolic levels. For roach <20 g, however, an asymptotic relationship was observed between temperature and routine metabolic rate. The 'flattening of the curve' in the latter case may be explained by reduced spontaneous activities at the lower threshold of the preferred temperature range.     

Gene or Size: Metabolic Rate and Body Temperature in Obese Growth Hormone‐Deficient Dwarf Mice

Objective: SMA1 mice carry a missense mutation in the growth hormone gene that leads to semidominant dwarfism and obesity. In this study, the basic thermal and metabolic properties of SMA1 mice were examined to detect metabolic alterations that can support the accretion of excess fat. Research Methods and Procedures: Basal and resting metabolic rates (RMRs) in wild‐type and SMA1 (sma1/+ and sma1/sma1) mice were determined by indirect calorimetry. Body temperature (T_b) was recorded using intraperitoneally implanted temperature‐sensitive transmitters, and body composition was determined by DXA. Results: SMA1 mice have proportionally lower basal and resting metabolic rates, higher body mass (BM)‐specific RMRs, and a higher lower critical temperature, and display a decrease in T_b by 0.4 °C in sma1/+ and 0.9 °C in sma1/sma1. Discussion: The analysis of gene effects on BM and energy expenditure in mouse mutants must consider the appropriate allometric relationship between BM and metabolic rate. With the exception of T_b, all metabolic alterations observed in SMA1 reflect reduced size.     

Improved Equations for Estimating the Resting Metabolic Rate

New models were developed for predicting the resting metabolic rate (RMR) with sufficient accuracy for use in epidemiologic studies and for weight control of individuals. For this purpose, the RMR of 213 women and 76 men was measured, and physical measurements were taken. The RMR was regressed on correlates of RMR, avoiding harmful degrees of collinearity by rejecting interregressor correlations exceeding r=0.5. For women, the best model (R₂=0.71) included the regressors age, race, weight, pulse rate, smoking, and body temperature. The best model for males (R2 = 0.81) included age, race, weight, blood pressure, smoking, time (of day the RMR was measured), and whether subjects had a meal prior to calorimetry. The models were cross validated internally and also validated using an external database. In both cases, the mean estimated RMR did not differ significantly from the measured RMR. The accuracy of the models was compared with four models reported in the literature, three of which overestimated the RMR by up to 17%. In conclusion, improved RMR prediction models have been developed, more accurate than existing models, rendering them suitable for application to epidemiological databases and for individual weight control programs.     

Winter feeding influences the cost of living in boreal passerines

The plastic regulation of internal energy reserves is acknowledged as the main adaptive response to winter conditions of resident small birds in northern latitudes, a strategy that may be altered whenever human‐supplemented food is available. We investigated the effects of supplementary feeding on the energy management strategy of two wild passerine species, the Willow Tit Poecile montanus and Blue Tit Cyanistes caeruleus, wintering in boreal conditions by measuring body mass and the energy cost of living, i.e. basal metabolic rate. Individuals of both species were heavier, larger and exhibited a higher energy cost of living when captured at the feeders than were individuals captured away from feeders. Fed Willow Tits expended more energy in maintenance, although this difference disappeared once mass was accounted for. Conversely, Blue Tits at feeders had higher mass‐adjusted energy cost of living, but only at low ambient temperatures. The results indicate that winter feeding has species‐specific effects on overall energy management strategy and modifies the response to environmental conditions of wintering passerines.     

A New Hand‐Held Indirect Calorimeter to Measure Postprandial Energy Expenditure

Objective: To verify the accuracy of a new hand‐held metabolic rate measuring device (MedGem) in quantifying postprandial energy expenditure (PP EE). MedGem measurements were compared to measurements obtained with a conventional indirect calorimeter (Delta‐Trac). Research Methods and Procedures: The resting metabolic rate of 15 healthy subjects was measured for 20 minutes using Delta‐Trac followed by a 10‐minute measurement period using MedGem. EE was again measured for 7 hours after consumption of a 2510‐kJ breakfast. Measurements were read from the Delta‐Trac for the initial 50 minutes of each hour followed by a single reading from the MedGem after 5 to 10 minutes of measurement. Measured EE was calculated as the average of the total measurement period for Delta‐Trac and for eight readings using MedGem; PP EE was calculated as the average of all measurements obtained after breakfast consumption. Results: There was no difference in resting metabolic rate between the two methods (6455.1 ± 417.6 vs. 6468.5 ± 337.2 kJ/d for Delta‐Trac and MedGem, respectively). Measured EE and PP EE values with Delta‐Trac (7019.1 ± 400.8 and 7099.8 ± 399.2 kJ/d, respectively) and MedGem (6775.6 ± 372.0 and 6819.5 ± 379.9 kJ/d, respectively) were not significantly different. There was no bias detected in any of the measurements made with MedGem compared with those of Delta‐Trac. Discussion: The new hand‐held EE measuring device can accurately track PP EE relative to a conventional indirect calorimetry system and, therefore, provides a new opportunity to assess PP EE in research settings and large‐scale trials.     

The measurement of resting metabolic rate in preschool children

Objective: This study examined the repeatability of measuring resting metabolic rate (RMR) in preschool children and the effect of different calculation protocols. Research Methods and Procedures: Eleven children (4 females and 7 males) participated in the project. They were recruited through advertisements in local schools and community centers. Resting metabolic rate was measured on 3 occasions over a 2‐week period, each after an overnight fast and each lasting ～20 to 25 minutes. Results were compared using repeated‐measures ANOVA to check for repeatability, and a number of methods of calculating RMR were assessed. Results: Repeatability of RMR measurements was good (coefficient of variation of replicates, 6.8%), with no significant difference between days of measurement. The lowest RMR measurement was obtained when the first 10 minutes were excluded and periods during which large activity was observed were excluded. This measurement was, on average, 4% lower than averaging the measurements after the first 5 minutes, including body movements. Discussion: This study suggests that RMR can be measured in preschool children and that the best method for calculating RMR in these subjects is to exclude periods when large body movements occur and the first 10 minutes of the measurement period. Only a single measurement of RMR is needed to obtain a reliable estimate.     

Developmental stress can uncouple relationships between physiology and behaviour

Phenotypic correlations (r_P) have frequently been observed between physiological and behavioural traits, and the nature of these associations has been shown to be modulated by a range of environmental stressors. Studies to date have examined the effects of acute stressors on physiology–behaviour interrelations, but the potential for permanent changes induced by exposure to stress during development remains unexplored. We exposed female zebra finches to dietary restriction during the nestling stage and tested how this affected r_P among a variety of physiological traits (haematocrit, stress-induced corticosterone level and basal metabolic rate (BMR)) and behavioural traits (activity and feeding rates in novel and familiar environments). Developmental stress completely uncoupled the relationship between activity in a novel environment and two physiological traits: haematocrit and BMR. This suggests that nutritionally based developmental stress has provoked changes in the energy budget that alleviate the trade-off between maintenance (BMR) and locomotor activities.     

Comparative brain transcriptomic analyses of scouting across distinct behavioural and ecological contexts in honeybees

Individual differences in behaviour are often consistent across time and contexts, but it is not clear whether such consistency is reflected at the molecular level. We explored this issue by studying scouting in honeybees in two different behavioural and ecological contexts: finding new sources of floral food resources and finding a new nest site. Brain gene expression profiles in food-source and nest-site scouts showed a significant overlap, despite large expression differences associated with the two different contexts. Class prediction and ‘leave-one-out’ cross-validation analyses revealed that a bee''s role as a scout in either context could be predicted with 92.5% success using 89 genes at minimum. We also found that genes related to four neurotransmitter systems were part of a shared brain molecular signature in both types of scouts, and the two types of scouts were more similar for genes related to glutamate and GABA than catecholamine or acetylcholine signalling. These results indicate that consistent behavioural tendencies across different ecological contexts involve a mixture of similarities and differences in brain gene expression.     

Contribution of Different Mechanisms to Compensation for Energy Restriction in the Mouse

Objective: Restriction of energy intake produces weight loss, but the rate of loss is seldom sustained. This is presumed to be a consequence of compensatory reductions in energy expenditure, although the exact contributions of different components to the energy budget remain uncertain. We examined the compensatory responses of mice to a 20% dietary restriction. Research Methods and Procedures: We measured body mass, body fatness, body temperature, and the components of daily energy expenditure for 50 MF1 mice. Forty mice were then placed on a restricted diet at 80% of their ad libitum intake for 50 days. The remaining 10 mice continued to feed ad libitum. Ten days before the end of the restriction period, the same measurements were taken. Results: There were no significant differences between the control and restricted groups in any parameters before restriction. During the restriction period, body mass increased in both the control and restricted groups, but at a slower rate in the restricted mice. The control group increased in both fat and fat free mass; however, although the restricted group increased fat to the same extent as the controls, fat free mass increased to a lesser extent. The contributions of the different components of the expended energy to compensate for the reduced energy intake were energy deposition, 2.2%; resting metabolic rate, 22.3%; and activity, 75.5%. Discussion: Mice were able to compensate almost completely for the restricted energy intake that was achieved by altering the amount of energy required for each component of the energy budget except digestive efficiency.     

Effect of fasting and repeat feeding on metabolic rate in Southern Catfish, Silurus meridionalis chen

Southern catfish juvenile (37.6-65.9 g) were fasted for two weeks and fed with cutlets of freshly killed loach species at 2% body mass per meal twice daily (06:00 and 18:00) for four days at 27.5°C. Metabolic rates were measured during the fasting and feeding periods and all metabolic rates were adjusted to a standard body mass of 1 kg using an exponent of 0.75. The aim of this study was to investigate the effect of fasting and repeat feeding on the resting metabolic rate and the feeding metabolic rate. The results demonstrated that the standardized value of the resting metabolic rate gradually decreased from 69.6 ± 2.7 (means ± S.E.) to 42.8 ± 2.3 mgO₂ h^-1 during the two weeks of fasting. The peak feeding metabolic rate and average metabolic rate of each feeding (12 h) gradually increased with repeat feeding before leveling off. The results of this study suggest that southern catfish can regulate digestive function and gradually alter the characteristics of metabolism according to the availability of a food resource.     

Effect of fasting and repeat feeding on metabolic rate in Southern Catfish,Silurus meridionalis chen

Southern catfish juvenile (37.6-65.9 g) were fasted for two weeks and fed with cutlets of freshly killed loach species at 2% body mass per meal twice daily (06:00 and 18:00) for four days at 27.5°C. Metabolic rates were measured during the fasting and feeding periods and all metabolic rates were adjusted to a standard body mass of 1 kg using an exponent of 0.75. The aim of this study was to investigate the effect of fasting and repeat feeding on the resting metabolic rate and the feeding metabolic rate. The results demonstrated that the standardized value of the resting metabolic rate gradually decreased from 69.6 ± 2.7 (means ± S.E.) to 42.8 ± 2.3 mgO2 h-1 during the two weeks of fasting. The peak feeding metabolic rate and average metabolic rate of each feeding (12 h) gradually increased with repeat feeding before leveling off. The results of this study suggest that southern catfish can regulate digestive function and gradually alter the characteristics of metabolism according to the availability of a food resource.     

Differences in basal energy expenditure and obesity

Objective: To assess the impact of differences in basal energy expenditure on adiposity. Research Methods and Procedures: Statistical analysis was performed on a published database giving anthropometric and energy expenditure measurements for 433 women and 335 men. Published equations derived by multiple regression analysis were used to predict basal metabolic rates in women and in men as a function of age, weight, and height. The differences between the observed and predicted rates (i.e., the residuals) were computed and expressed in terms of percentage deviation from the predicted rates of basal energy expenditure (BEE). In addition, individual body fat contents were computed using equations based on National Health and Nutrition Examination Study 3 data relating to body fat content determined by bioimpedance to BMI. Results: There is no correlation between percentage body fat content and deviations from predicted (which one would refer to as normal) BEE. Discussion: It can be concluded that relatively high or relatively low rates of BEE do not influence body weights and adiposity in a statistically identifiable manner. This contradicts and challenges the widely held view that low resting metabolic rates promote the development of obesity.     

Weekly changes in basal metabolic rate with eight weeks of overfeeding

Objective : The contribution of basal metabolic rate (BMR) to weight gain susceptibility has long been debated. We wanted to examine whether BMR changes in a linear fashion with overfeeding. Our hypothesis was that BMR does not increase linearly with 1000‐kcal/d overfeeding in lean healthy subjects over 8 weeks. The null hypothesis states that BMR increases linearly with 1000‐kcal/d overfeeding in lean healthy subjects. Research Methods and Procedures : Initially, 16 lean healthy sedentary subjects completed 2 weeks of weight maintenance feeding at the General Clinical Research Center. The subjects were then overfed by 1000 kcal/d over 8 weeks. BMR was measured under standard conditions each week using indirect calorimetry. Results : Baseline BMR was 1693 ± 154.5 kcal/d. BMR increased from 1711 ± 201.3 kcal/d at week 1 of overfeeding to 1781 ± 171.65 kcal/d at the second week of overfeeding (p = 0.05). BMR fell during the third week of overfeeding to 1729 ± 179.5 kcal/d (p = 0.05). After 5 weeks of overfeeding, BMR reached a plateau. Thereafter, there was no further change. Comparison of BMR with weeks of overfeeding was significantly different compared with the linear model (p < 0.05). Discussion : Increases in BMR in lean sedentary healthy subjects with 1000‐kcal/d overfeeding are not linear over 8 weeks. There seems to be a short‐term increase in BMR in the first 2 weeks of overfeeding that is not representative of longer‐term changes.     

Explorative behaviour is not associated with metabolism in the European Pied Flycatcher Ficedula hypoleuca

The pace‐of‐life syndrome hypothesis (POLS) represents an attractive theoretical framework suggesting that physiological and behavioural traits have evolved together with environmental conditions and life‐history strategies. POLS predicts that metabolic differences covary with behavioural variation such that high metabolic rate is associated with risk‐prone behaviour and a faster pace‐of‐life, whereas a low metabolic rate is associated with risk‐averse behaviour and a slower pace‐of‐life. We tested the POLS hypothesis in captive European Pied Flycatchers during their first year by examining the relationship between explorative behaviour and basal metabolic rate. Our results are inconsistent with POLS. The positive association of explorative behaviour with basal metabolic rate was not recovered for either sex, possibly due to foraging conditions in the aviaries where control and trial groups were fed twice a day, the birds' young age, developmental plasticity, or a non‐existent syndrome.