Temperature alone is insufficient to understand hibernation energetics

Energy conservation has long been a focal point in hibernation research. A long-standing assumption is that ambient temperature (Ta) largely defines the rate of energy expenditure because of well-known relationships between Ta, metabolic rate, and frequency of arousal from torpor. Body condition and humidity also affect energy expenditure but are usually considered secondary factors. We held bats in captivity under multiple environmental conditions to directly compare the importance of Ta, fat mass, and humidity for energy expenditure of hibernating tricolored bats (Perimyotis subflavus). Fat mass was the best predictor of female mass loss, followed by Ta and humidity. However, males had less fat and adopted a more energetically conservative hibernation strategy. Our results demonstrate that understanding the evolution of behavior, physiology, and ecology of hibernation requires disentangling the relative contributions of multiple drivers of hibernation energetics, and that Ta is not always the most important factor driving energy expenditure.

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Starvation-induced changes in metabolic rate, blood flow, and regional energy expenditure in rats

Canadian Journal of Physiology and Pharmacology ◽

10.1139/y86-211 ◽

1986 ◽

Vol 64 (9) ◽

pp. 1252-1258 ◽

Cited By ~ 59

Author(s):

Stephanie W. Y. Ma ◽

David O. Foster

Keyword(s):

Blood Flow ◽

Cardiac Output ◽

Energy Expenditure ◽

Energy Conservation ◽

Metabolic Rate ◽

Whole Body ◽

Tissue Blood Flow ◽

Energy Conserving ◽

Overnight Fasting ◽

Quantitative Changes

Starvation results in an energy-conserving reduction in metabolic rate that has features of an adaptive response. Tissue and organ sites of this response were investigated by examining the effects of starvation for 5 d on tissue blood flow (microsphere method) and regional arteriovenous O2 differences [Formula: see text] in conscious rats resting quietly at 28 °C. Comparison was with fed and overnight-fasted animals. Whole body resting metabolic rates (MR), colonic temperatures (Tc), and tissue weights were also determined. Quantitative changes in energy expenditure (as O2 consumption) were obtained for two regions: the portal-drained viscera (PDV) and the hindquarters (HQ). Fasting overnight resulted in increased blood flow to white adipose tissue (WAT) and decreased flow to the brain, PDV, testes, and skin; however, MR, Tc, the two regional [Formula: see text], and the weights of most tissues were not significantly altered. In comparison with overnight fasting, starvation for 5 d resulted in a 13% reduction in body weight, weight loss in many tissues and organs, a 26% reduction in MR, a decline of 0.5 °C in Tc, decreased [Formula: see text] across both the PDV and HQ, reduced cardiac output, and decreased blood flow to the heart, PDV, skin, WAT, leg muscle, HQ, and the musculoskeletal body as a whole. Utilization of O2 by the PDV and HQ [Formula: see text] declined by amounts that accounted for 22 and 18%, respectively, of the reduction in MR. The reductions in cardiac output (18%) and heart blood flow (36%) indicate that the heart also made a contribution to energy conservation (roughly estimated as 5%). Overall, the data suggest that gut and muscle together accounted for two-thirds to three-quarters of the starvation-induced energy conservation.

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Metabolic Adaptations to Weight Loss: Relative Changes in Resting Metabolic Rate and Energy Expenditure for Physical Activity and Association With Weight Loss Maintenance

Current Developments in Nutrition ◽

10.1093/cdn/nzab041_041 ◽

2021 ◽

Vol 5 (Supplement_2) ◽

pp. 526-526

Author(s):

Rachel Silver ◽

Sai Das ◽

Michael Lowe ◽

Susan Roberts

Keyword(s):

Physical Activity ◽

Weight Loss ◽

Linear Regression ◽

Energy Expenditure ◽

Metabolic Rate ◽

Fat Mass ◽

Weight Regain ◽

Resting Metabolic Rate ◽

Fat Free Mass ◽

The Mean

Abstract Objectives There is persistent controversy over the extent to which different components of energy expenditure disproportionately decrease after weight loss and contribute to weight regain through decreased energy requirements. We conducted a secondary analysis of the CALERIE I study to test the hypothesis that decreased resting metabolic rate (RMR) and energy expenditure for physical activity (EEPA) after a 6-month calorie restriction intervention would predict weight regain at 12 months, with a greater decrease in RMR than EEPA. Methods Participants (n = 46) received all food and energy-containing beverages for 6 months. Outcome measures included total energy expenditure by doubly labeled water, RMR by indirect calorimetry, and body composition by BOD POD. Predictions for RMR and EEPA were derived from baseline linear regression models including age, sex, fat mass, and fat free mass. Baseline regression coefficients were used to calculate the predicted RMR and EEPA at 6 months. Residuals were calculated as the difference between measured and predicted values and were adjusted for body weight. The presence of metabolic adaptation was evaluated by a paired t-test comparing measured and predicted RMR at 6 months. Differences between 6-month RMR and EEPA residuals were evaluated by the same method. Linear regression was used to assess the association between 6-month residuals and weight loss maintenance (% weight change, 6 to 12 months). Results Mean weight loss was 6.9% at 6 months with 2.1% regain from 6 to 12 months. No adaptation in RMR was observed at 6 months (mean residual: 19 kcal; 95% confidence interval: −9, 48; P = 0.18). However, significant adaptation was observed in EEPA (mean residual: −199 kcal; −126, −272; P < 0.0001). In addition, the mean 6-month RMR residual was significantly greater than the mean 6-month EEPA residual (218 kcal; 133, 304; P < 0.0001). There was no significant association between 6-month RMR or EEPA residuals and weight regain at 12 months (P = 0.56, 0.34). Conclusions There was no measurable decrease in RMR with weight loss after adjusting for changes in fat free mass and fat mass, but there was a decrease in EEPA. Changes in RMR and EEPA with weight loss over 6 months did not predict weight regain at 12 months. Funding Sources Jean Mayer USDA Human Nutrition Research Center on Aging Doctoral Scholarship; USDA agreement #8050–51000-105–01S

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Standard metabolic rate does not associate with age-at-maturity genotype in juvenile Atlantic salmon

10.1101/2021.08.25.457673 ◽

2021 ◽

Cited By ~ 1

Author(s):

Eirik R Asheim ◽

Jenni M Prokkola ◽

Sergey Morozov ◽

Tutku Aykanat ◽

Craig R Primmer

Keyword(s):

Energy Expenditure ◽

Atlantic Salmon ◽

Metabolic Rate ◽

Body Condition ◽

Life Stage ◽

Standard Metabolic Rate ◽

Metabolic Phenotype ◽

Life History Strategies ◽

Maintenance Energy ◽

Significant Difference

Atlantic salmon (Salmo salar) is a species with diverse life-history strategies, to which the timing of maturation contributes considerably. Recently, the genome region including the gene vgll3 has gained attention as a locus with a large effect on salmon maturation timing, and recent studies on the vgll3 locus in salmon have indicated that its effect might be mediated through body condition and accumulation of adipose tissue. However, the cellular and physiological pathways leading from vgll3 genotype to phenotype are still unknown. Standard metabolic rate is a potentially important trait for resource acquisition and assimilation and we hypothesized that this trait, being a proxy for the maintenance energy expenditure of an individual, could be an important link in the pathway from vgll3 genotype to maturation-timing phenotype. As a first step to studying links between vgll3 and the metabolic phenotype of Atlantic salmon, we measured the standard metabolic rate of 150 first year Atlantic salmon juveniles of both sexes, originating from 14 different families with either late maturing or early maturing vgll3 genotypes. No significant difference in mass-adjusted standard metabolic rate was detected between individuals with different vgll3 genotypes, indicating that juvenile salmon of different vgll3 genotypes have similar maintenance energy requirements in the experimental conditions used and that the effects of vgll3 on body condition and maturation are not strongly related to maintenance energy expenditure in either sex at this life stage.

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Heart rate and energy expenditure in resting and running Svalbard and Norwegian reindeer

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1984.246.6.r963 ◽

1984 ◽

Vol 246 (6) ◽

pp. R963-R967 ◽

Cited By ~ 6

Author(s):

K. J. Nilssen ◽

H. K. Johnsen ◽

A. Rognmo ◽

A. S. Blix

Keyword(s):

Heart Rate ◽

Energy Expenditure ◽

Metabolic Rate ◽

Ambient Temperature ◽

High Arctic ◽

O2 Consumption ◽

Ambient Temperatures ◽

Svalbard Reindeer ◽

The Relationship ◽

Cost Of Transportation

The purpose of this study was to determine whether a convenient relationship could be found between heart rate (HR) and energy expenditure at rest and during running in the high arctic Svalbard reindeer (SR) and the subarctic Norwegian reindeer (NR). Measurements of HR and energy expenditure (O2 consumption) were made at different ambient temperatures, at rest, and during running at different speeds during both summer and winter. Cost of transportation (Science 177: 222-228, 1972) was 3.56 and 2.67 J X g-1 X km-1 in SR and NR, respectively. The y-intercept value obtained for NR was close to the predicted value (J. Exp. Biol. 97: 1-22, 1982), whereas that of SR was much lower. In NR the relationship between HR and energy expenditure at running speeds from 0 to 9.2 km X h-1 is, regardless of ambient temperature (in the -30 to +10 degrees C range), described by the following equations: y = 8.04x + 48.70, r = 0.92, n = 27 (summer); and y = 7.48x + 31.20, r = 0.95, n = 52 (winter). In SR, the corresponding equations were y = 7.60x + 49.20, r = 0.94, n = 29 (summer); and y = 8.90x + 32.10, r = 0.96, n = 44 (winter), where y is HR (beats X min-1) and x is metabolic rate (W X kg-1).

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Abstract P293: Resting Metabolic Rate, Cardiorespiratory Fitness, and Racial Differences in Adiposity among Adult Women

Circulation ◽

10.1161/circ.127.suppl_12.ap293 ◽

2013 ◽

Vol 127 (suppl_12) ◽

Author(s):

Robin P Shook ◽

Gregory A Hand ◽

Amanda E Paluch ◽

James R Hebert ◽

Xuewen Wang ◽

...

Keyword(s):

Body Weight ◽

Energy Expenditure ◽

Metabolic Rate ◽

Cardiorespiratory Fitness ◽

Body Fat ◽

Fat Mass ◽

Resting Metabolic Rate ◽

Overweight And Obesity ◽

Vigorous Activity

Background: African American (AA) adult females have a higher prevalence of overweight and obesity compared to their Caucasian (Cauc) peers. Lower resting metabolic rate (RMR) values, a hypothesized contributor to higher levels of adiposity, have been observed among AA women. However, it is unknown whether cardiorespiratory fitness (CRF) is associated with RMR in this population. Methods: Sixty-two overweight/obese (body mass index [BMI] ≥25.0) yet healthy women (42 Cauc, 20 AA) between the ages of 21-35 years were recruited for the present study. RMR was measured using a ventilated hood system. Participants arrived fasted for at least 12 hrs and having refrained from alcohol/exercise for at least 24 hrs. Participants rested in a supine position for 30-minutes, followed by a 30-minute RMR gas collection period. Body weight (BW) and height were measured and body fat (BF) was calculated as the percentage of total weight identified as fat tissue by dual x-ray absorptiometry. CRF was measured via a metabolic cart during a modified Bruce treadmill protocol. Total energy expenditure (TEE) was assessed using an arm-based physical activity monitor worn at all times for 10 consecutive days. Energy intake (EI) was assessed over a 14-day period via interviewer-administered dietary recall. Results: Cauc and AA participants were similar in terms of age (27.6±4.2 years), weight (79.9±9.9 kg), BMI (29.4±2.9 kg/m2), body fat percentage (41.0±5.1 percent), and EI (1760±397 kcal/day). Compared to Cauc, AA women were slightly shorter (162.4±7.0 vs. 165.8±5.1 cm, p=0.0371), lower CRF (27.4±3.8 vs. 31.4±5.2 ml/kg/min, p=0.0032), lower TEE (2438±264 vs. 2598±303 kcal/day, p=0.0102) and lower RMR (1436±222 vs. 1569±181 kcal/day, p=0.0154). Energy expenditure resulting from moderate/vigorous activity was higher in Cauc females (552±386 vs. 355±197 kcal/day, p=0.0102). RMR was correlated with fat mass, CRF and race. After adjustment for age, race, body weight, fat-free mass, fat mass, and CRF, the least squares means for RMR remained lower in AA compared to Cauc (1444 vs. 1565 kcal/day, p=0.0034) and was only significantly related race (p=0.0034). Conclusion: The results of this study confirm previous research reporting lower RMR values among AA females compared to their Cauc counterparts, though these differences did not result in variations of adiposity. The current analyses suggest CRF plays an important role in the determination of RMR. The differences among racial groups in energy expenditure resulting from moderate/vigorous activity may play a key role in the determination of CRF and ultimately RMR.

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The Role of Exercise in the Interplay between Myokines, Hepatokines, Osteokines, Adipokines, and Modulation of Inflammation for Energy Substrate Redistribution and Fat Mass Loss: A Review

Nutrients ◽

10.3390/nu12061899 ◽

2020 ◽

Vol 12 (6) ◽

pp. 1899 ◽

Cited By ~ 6

Author(s):

Adrian M. Gonzalez-Gil ◽

Leticia Elizondo-Montemayor

Keyword(s):

Energy Expenditure ◽

Mass Loss ◽

Fat Mass ◽

Significant Loss ◽

Healthy Weight ◽

Loss Of Weight ◽

Cardiometabolic Disorders ◽

Response To Exercise ◽

Fat Mass Loss

Exercise is an effective strategy for preventing and treating obesity and its related cardiometabolic disorders, resulting in significant loss of body fat mass, white adipose tissue browning, redistribution of energy substrates, optimization of global energy expenditure, enhancement of hypothalamic circuits that control appetite-satiety and energy expenditure, and decreased systemic inflammation and insulin resistance. Novel exercise-inducible soluble factors, including myokines, hepatokines, and osteokines, and immune cytokines and adipokines are hypothesized to play an important role in the body’s response to exercise. To our knowledge, no review has provided a comprehensive integrative overview of these novel molecular players and the mechanisms involved in the redistribution of metabolic fuel during and after exercise, the loss of weight and fat mass, and reduced inflammation. In this review, we explain the potential role of these exercise-inducible factors, namely myokines, such as irisin, IL-6, IL-15, METRNL, BAIBA, and myostatin, and hepatokines, in particular selenoprotein P, fetuin A, FGF21, ANGPTL4, and follistatin. We also describe the function of osteokines, specifically osteocalcin, and of adipokines such as leptin, adiponectin, and resistin. We also emphasize an integrative overview of the pleiotropic mechanisms, the metabolic pathways, and the inter-organ crosstalk involved in energy expenditure, fat mass loss, reduced inflammation, and healthy weight induced by exercise.

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Abnormal Sympathoadrenal Activity, but Normal Energy Expenditure in Hypopituitarism

The Journal of Clinical Endocrinology & Metabolism ◽

10.1210/jc.2003-030870 ◽

2003 ◽

Vol 88 (12) ◽

pp. 5689-5695 ◽

Cited By ~ 5

Author(s):

Henriette Mersebach ◽

Ole Lander Svendsen ◽

Arne Astrup ◽

Ulla Feldt-Rasmussen

Keyword(s):

Energy Expenditure ◽

Metabolic Rate ◽

Lean Body Mass ◽

Body Mass ◽

Fat Mass ◽

Basal Metabolic Rate ◽

Healthy Controls ◽

Urinary Catecholamines ◽

Sympathoadrenal Activity

Abstract In this study of 23 hypopituitary patients and 26 healthy controls, we have addressed whether the obese state of substituted hypopituitary patients is facilitated by abnormal sympathoadrenal activity or energy expenditure (EE). All patients received adequate substitution therapy including GH therapy. The investigation program included assessment of sympathoadrenal activity (urinary catecholamines), body composition (dual-energy x-ray absorptiometry), appetite sensations (visual analog scale), and EE (indirect calorimetry in respiration chamber). Twenty-four-hour urinary epinephrine adjusted for lean body mass and fat mass was significantly lower in patients compared with controls. GH and hydrocortisone were single negative predictors of urinary epinephrine. The major determinants of EE in patients were lean body mass and fat mass, explaining 96, 95, and 80% of the variance in 24-h EE, sleeping EE, and basal metabolic rate, respectively. Addition of urinary catecholamines explained another 1–4% of the variance in 24-h EE and basal metabolic rate, respectively. Lean patients exhibited significantly more hunger than obese patients and lean controls. In conclusion, hypopituitary patients have lower sympathoadrenal activity but normal EE, compared with healthy controls. This may reflect a central defect in hypopituitarism, however the possible impact of long-term GH and hydrocortisone treatment requires further attention.

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Behavioural microclimate selection and physiological responses to environmental conditions in a hibernating bat

Canadian Journal of Zoology ◽

10.1139/cjz-2021-0193 ◽

2022 ◽

Author(s):

Justin Boyles ◽

Emily Johnson ◽

Nathan W. Fuller ◽

Kirk Silas ◽

Lily Hou ◽

...

Keyword(s):

Relative Humidity ◽

Energy Conservation ◽

Metabolic Rate ◽

Environmental Conditions ◽

Physiological Responses ◽

Selective Pressures ◽

Laboratory Conditions ◽

Energy Stores ◽

Different Temperatures ◽

Maximal Expression

Hibernators adjust the expression of torpor behaviourally and physiologically to balance the benefits of energy conservation in hibernation against the physiological and ecological costs. Small fat-storing species, like many cave-hibernating bats, have long been thought to be highly constrained in their expression of hibernation because they must survive winter relying only on endogenous energy stores. We evaluated behavioural microclimate selection in tri-colored bats (Perimyotis subflavus (Cuvier, 1832)) across a three-month hibernation experiment under laboratory conditions. We also opportunistically tested for evidence of acclimatization in torpid metabolic rate (TMR). When given access to gradients in microclimate, bats tended to choose the warmest temperature available (11°C) while almost completely avoiding the driest condition available (85% relative humidity at 8°C). Further, bats held at different temperatures over the course of the hibernation showed no differences in TMR when measured under common conditions at the end of hibernation. Taken together, our results suggest selective pressures to conserve energy during hibernation are not overwhelmingly strong and further support the proposition that optimal expression of hibernation is something less than the maximal expression of hibernation unless the animal is nearing starvation.

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Thermoneutral housing does not influence fat mass or glucose homeostasis in C57BL/6 mice

Journal of Endocrinology ◽

10.1530/joe-18-0279 ◽

2018 ◽

Vol 239 (3) ◽

pp. 313-324 ◽

Cited By ~ 9

Author(s):

Lewin Small ◽

Henry Gong ◽

Christian Yassmin ◽

Gregory J Cooney ◽

Amanda E Brandon

Keyword(s):

Glucose Metabolism ◽

Ambient Temperature ◽

Fat Mass ◽

Glucose Homeostasis ◽

Dietary Intervention ◽

Whole Body ◽

Housing Temperature ◽

Brown Adipose ◽

Normal Chow ◽

Obesogenic Diet

One major factor affecting physiology often overlooked when comparing data from animal models and humans is the effect of ambient temperature. The majority of rodent housing is maintained at ~22°C, the thermoneutral temperature for lightly clothed humans. However, mice have a much higher thermoneutral temperature of ~30°C, consequently data collected at 22°C in mice could be influenced by animals being exposed to a chronic cold stress. The aim of this study was to investigate the effect of housing temperature on glucose homeostasis and energy metabolism of mice fed normal chow or a high-fat, obesogenic diet (HFD). Male C57BL/6J(Arc) mice were housed at standard temperature (22°C) or at thermoneutrality (29°C) and fed either chow or a 60% HFD for 13 weeks. The HFD increased fat mass and produced glucose intolerance as expected but this was not exacerbated in mice housed at thermoneutrality. Changing the ambient temperature, however, did alter energy expenditure, food intake, lipid content and glucose metabolism in skeletal muscle, liver and brown adipose tissue. Collectively, these findings demonstrate that mice regulate energy balance at different housing temperatures to maintain whole-body glucose tolerance and adiposity irrespective of the diet. Despite this, metabolic differences in individual tissues were apparent. In conclusion, dietary intervention in mice has a greater impact on adiposity and glucose metabolism than housing temperature although temperature is still a significant factor in regulating metabolic parameters in individual tissues.

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Metabolic traits in brown trout (Salmo trutta) vary in response to food restriction and intrinsic factors

Conservation Physiology ◽

10.1093/conphys/coaa096 ◽

2020 ◽

Vol 8 (1) ◽

Author(s):

Louise C Archer ◽

Stephen A Hutton ◽

Luke Harman ◽

W Russell Poole ◽

Patrick Gargan ◽

...

Keyword(s):

Life History ◽

Metabolic Rate ◽

Intraspecific Variation ◽

Brown Trout ◽

Environmental Conditions ◽

Food Restriction ◽

Metabolic Rates ◽

Intrinsic Factors ◽

Metabolic Traits ◽

Food Conditions

Abstract Metabolic rates vary hugely within and between populations, yet we know relatively little about factors causing intraspecific variation. Since metabolic rate determines the energetic cost of life, uncovering these sources of variation is important to understand and forecast responses to environmental change. Moreover, few studies have examined factors causing intraspecific variation in metabolic flexibility. We explore how extrinsic environmental conditions and intrinsic factors contribute to variation in metabolic traits in brown trout, an iconic and polymorphic species that is threatened across much of its native range. We measured metabolic traits in offspring from two wild populations that naturally show life-history variation in migratory tactics (one anadromous, i.e. sea-migratory, one non-anadromous) that we reared under either optimal food or experimental conditions of long-term food restriction (lasting between 7 and 17 months). Both populations showed decreased standard metabolic rates (SMR—baseline energy requirements) under low food conditions. The anadromous population had higher maximum metabolic rate (MMR) than the non-anadromous population, and marginally higher SMR. The MMR difference was greater than SMR and consequently aerobic scope (AS) was higher in the anadromous population. MMR and AS were both higher in males than females. The anadromous population also had higher AS under low food compared to optimal food conditions, consistent with population-specific effects of food restriction on AS. Our results suggest different components of metabolic rate can vary in their response to environmental conditions, and according to intrinsic (population-background/sex) effects. Populations might further differ in their flexibility of metabolic traits, potentially due to intrinsic factors related to life history (e.g. migratory tactics). More comparisons of populations/individuals with divergent life histories will help to reveal this. Overall, our study suggests that incorporating an understanding of metabolic trait variation and flexibility and linking this to life history and demography will improve our ability to conserve populations experiencing global change.

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