Sources and significance of variation in basal,summit and maximal metabolic rates in birds

The rates at which birds use energy may have profound effects on fitness, thereby influencing physiology, behavior, ecology and evolution. Comparisons of standardized metabolic rates （e.g., lower and upper limits of metabolic power output） present a method for elucidating the effects of ecological and evolutionary factors on the interface between physiology and life history in birds. In this paper we review variation in avian metabolic rates [basal metabolic rate （BMR; minimum normothermic metabolic rate）, summit metabolic rate （Msum; maximal thermoregulatory metabolic rate）, and maximal metabolic rate （MMR; maximal exercise metabolic rate）], the factors associated with this variation, the evidence for functional links between these metabolic traits, and the ecological and evolutionary significance of avian metabolic diversity. Both lower and upper limits to metabolic power production are phenotypically flexible traits, and vary in association with numerous ecological and evolutionary factors. For both inter- and intraspecific comparisons, lower and upper limits to metabolic power production are generally upregulated in response to energetically demanding conditions and downregulated when energetic demands are relaxed, or under conditions of energetic scarcity. Positive correlations have been documented between BMR, Msum and MMR in some, but not all studies on birds, providing partial support for the idea of a functional link between lower and upper limits to metabolic power production, but more intraspecific studies are needed to determine the robustness of this conclusion. Correlations between BMR and field metabolic rate （or daily energy expenditure） in birds are variable, suggesting that the linkage between these traits is subject to behavioral adjustment, and studies of the relationship between field and maximal metabolic rates are lacking. Our understanding of avian metabolic diversity would benefit from future studies of： （1） the functional and mechanistic links between lower and upper limits of metabolic power output; （2） the environmental and ecological cues driving phenotypically flexible metabolic responses, and how responses to such cues might impact population responses to climate change; （3） the shapes of metabolic reaction norms and their association with environmental variability; and （4） the relationship of metabolic variation to fitness, including studies of repeatability and heritability of minimum and maximum metabolic power output [Current Zoology 56 （6）： 741-758, 2010].

Seasonal acclimatization and temperature acclimation in small passerine birds is achieved via metabolic adjustments

Temperature and other environmental factors play an integral role in the metabolic adjustments of animals and drive a series of morphological,physiological,and behavioral adaptions essential to survival.However,it is not clear how the capacity of an organism for temperature acclimation translates into seasonal acclimatization to maintain survival.Basal metabolic rate(BMR),evaporative water loss(EWL),and energy budget were measured in the Chinese Hwamei(Garrulax canorus)following winter and summer acclimatization,and in those acclimatized to 15℃(cold)and 35℃(warm)under laboratory conditions for 28 days.In addition to the above indicators,internal organ masses,as well as state 4 respiration and cytochrome c oxidase(COX)activity were also measured for the liver,skeletal muscle,heart,and kidney.Both winter-acclimatized and cold-acclimated birds exhibited significantly higher BMR,EWL,and energy budget,as well as organ masses,state 4 respiration,and COX activity compared with the summer-acclimatized and warm-acclimated birds.This indicated that the Chinese Hwamei could adapt to seasonal or just temperature changes through some physiological and biochemical thermogenic adjustments,which would be beneficial to cope with natural environmental changes.A general linear model showed that body mass,BMR,GEI,state 4 respiration in the liver and kidney,and COX activity in the skeletal muscle,liver,and kidney were significantly affected by temperature and acclimation.A positive correlation was observed between BMR and each of the other parameters(body mass,EWL,energy budget,heart dry mass,kidney dry mass,state 4 respiration)in the muscle,heart,and kidney and also between BMR and COX activity in the muscle and kidney.The results suggested that similar to seasonal acclimatization,Chinese Hwameis subjected to temperature acclimation also exhibited significant differences in metabolism-related physiological and biochemical parameters,depending on the temperature.The data also supported the prediction that metabolic adjustment might be the primary means by which small birds meet the energetic challenges triggered by cold conditions.

Seasonal phenotypic flexibility in body mass,basal thermogenesis,and tissue oxidative capacity in the male Silky Starling(Sturnus sericeus)

Background: Acclimatization to winter conditions is an essential prerequisite for the survival of small birds in the northern temperate zone.Changes in photoperiod,ambient temperature and food availability trigger seasonal physiological and behavioral acclimatization in many passerines.Seasonal trends in metabolic parameters are well known in avian populations from temperate environments;however,the physiological and biochemical mechanisms underlying these trends are incompletely understood.In this study,we used an integrative approach to measure variation in the thermogenic properties of the male Silky Starling(Sturnus sericeus) at different levels or organization,from the whole organism to the biochemical.We measured body mass(Mb),basal metabolic rate(BMR),energy budget,the mass of selected internal organs,state 4 respiration and cytochrome c oxidase(COX) activity in the heart,liver and muscle.Methods: Oxygen consumption was measured using an open-circuit respirometry system.The energy intake of the birds were then determined using an oxygen bomb calorimeter.Mitochondrial state 4 respiration and COX activity in heart,liver and pectoral muscle were measured with a Clark electrode.Results: The results suggest that acclimatization to winter conditions caused significant change in each of the measured variables,specifically,increases in Mb,organ mass,BMR,energy intake and cellular enzyme activity.Furthermore,BMR was positively correlated with body mass,energy intake,the mass of selected internal organs,state 4 respiration in the heart,liver and muscle,and COX activity in the heart and muscle.Conclusions: These results suggest that the male Silky Starling's enhanced basal thermogenesis under winter conditions is achieved by making a suite of adjustments from the whole organism to the biochemical level,and provide further evidence to support the notion that small birds have high phenotypic plasticity with respect to seasonal changes.

The role of temperature as a driver of metabolic flexibility in the Red-billed Leiothrix(Leiothrix lutea)

Background:The thermoregulatory ability of animals is strongly influenced by the temperature of their environment.Acclimation to cold requires a range of physiological and morphological adjustments.In this study,we tested the hypothesis that a small passerine,the Red-billed Leiothrix(Leiothrix lutea),can maintain homeothermy in cold conditions by adjusting the physiology and biochemistry of its tissue and organs and return to its former physiological and biochemical state when moved to a warm temperature.Methods:Phenotypic variation in thermogenic activity of the Red-billed Leiothrixs(Leiothrix lutea)was investigated under warm(35℃),normal(25℃)or cold(15℃)ambient temperature conditions.Oxygen consumption was measured using an open-circuit respirometry system.Mitochondrial state-4 respiration and cytochrome-c oxidase(COX)activity in liver,kidney heart and pectoral muscle were measured with a Clark electrode.Results:Birds acclimated to an ambient temperature of 15℃ for 4 weeks significantly increased their basal metabolic rate(BMR)compared to a control group kept at 25℃.Birds acclimated to 35℃ decreased their BMR,gross energy intake(GEI)and digestible energy intake(DEI).Furthermore,birds acclimated to 15℃ increased state-4 respiration in their pectoral muscles and cytochrome-c oxidase(COX)activity in their liver and pectoral muscle,compared to the 25℃ control group.Birds acclimated to 35℃ also displayed lower state-4 respiration and COX activity in the liver,heart and pectoral muscles,compared to those kept at 25℃.There was a positive correlation between BMR and state-4 respiration,and between BMR and COX activity,in all of the above organs except the liver and heart.Conclusions:Our study illustrates that the morphological,physiological,and enzymatic changes are associated with temperature acclimation in the Red-billed Leiothrix,and supports the notion that the primary means by which small birds meet the energetic challenges of cold conditions is through metabolic adjustments.

Short photoperiod increases energy intake, metabolic thermogenesis and organ mass in silky starlings Sturnus sericeus

Environmental cues play important roles in the regulation of an animal＇s physiology and behavior. One such cue, photoperiod, plays an important role in the seasonal acclimatization of birds. It has been demonstrated that an animal＇s body mass, basal metabolic rate （BMR）, and energy intake, are all affected by photoperiod. The present study was designed to examine photoperiod induced changes in the body mass, metabolism and metabolic organs of the silky starling, Stumus sericeus. Captive silky starlings increased their body mass and BMR during four weeks of acclimation to a short photoperiod. Birds acclimated to a short photopedod also increased the mass of certain organs （liver, gizzard and small intestine）, and both gross energy intake （GEl） and digestible energy intake （DEI）, relative to those acclimated to a long photoperiod. Furthermore, BMR was positively correlated with body mass, liver mass, GEl and DEI. These results suggest that silky starlings increase metabolic thermogenesis when exposed to a short photoperiod by increasing their body and metabolic organ mass, and their GEl and DEI. These findings support the hypothesis that bird species from temperate climates typically display high phenotypic flexibility in thermogenic capacity.

On the intraspecific variability in basal metabolism and the food habits hypothesis in birds

The food habits hypothesis （FHH） stands as one of the most striking and often-cited interspecific patterns to emerge from comparative studies of endothermic energetics. The FHH identifies three components of diet that potentially produce variability in mass-independent BMR, i.e. food quality, food availability, and food predictability or environmental productivity. The hypothesis predicts that species with diets of low energy content and/or low digestibility should evolve low mass-independent BMRs. The effects of food habits on BMR have been widely investigated at the interspecific level, but the variation between individuals and populations has been largely ignored. Our focus is to compare predictions derived from interspecific studies with data collected from within-species studies to explore the mechanisms and functional significance of adaptive responses predicted by the food-habits hypothesis among birds. We conclude that if BMR is correlated with daily energy expenditure, then organisms that can lower BMR will reduce daily energy expenditure and hence, food requirements. Birds that lower BMR in stressful environments may increase survival. Nevertheless, the mechanism （s） by which birds eating a low quality diet reduce BMR and whether lower BMR affects fitness remain to be determined [Current Zoology 56 （6）： 759-766, 2010].

Metabolic rate and evaporative water loss in the silky starling （Sturnus sericeus）

To better understand the physiological characteristics of the silky starling（Sturnus sericeus）, its body temperature（Tb）, basal metabolic rate（BMR）, evaporative water loss（EWL） and thermal conductance（C） elicited by different ambient temperatures（Ta）（5-30 ℃） were determined in the present study. Our results showed that they have a high Tb（41.6±0.1 ℃）, a wide thermal neutral zone（TNZ）（20-27.5 ℃） and a relatively low BMR within the TNZ（3.37±0.17 mL O2/g·h）. The EWL was nearly stable below the TNZ（0.91±0.07 mg H2O/g·h） but increased remarkably within and above the TNZ. The C was constant below the TNZ, with a minimum value of 0.14±0.01 mL O2/g·h·℃. These findings indicate that the BMR, Tb and EWL of the silky starling were all affected by Ta, especially when Ta was below 20℃ and the EWL plays an important role in thermal regulation.

New Mathematical Modelling on BMR and Weight Prediction for Ghanaians

Background: Basal Metabolic Rate (BMR) is the quantum of calories needed for optimum body function when at rest. This has long been an indicator of one’s health and the basis for determining the metabolic age of individuals. Many scholastic projects have led to the establishment of mathematical models and inventions that measure the BMR and other body composition parameters. However, existing computations have limitations as they do not offer accurate results for Ghanaians. Aim: The purpose of the study was to model BMR metrics that are most suitable for Ghanaians and to investigate the effect of caloric difference on weight, Lean Body Mass (LBM) and % fat composition that can be implemented with Information Technology. Research Methods and Procedures: This was an experimental study that adopted a quantitative approach. BMR and body composition were measured in a sample of 242 Ghanaian adults (141 males and 101 females) from 19 to 30 years of age. Body composition was measured using bioelectrical impendence analysis (BIA) in all participants. Each participant was under study for 7 days. A simple linear regression model was used to examine associations between BMR/calorie intake and total body weight and LBM. Results: There was a significant statistical relation between BMR and LBM and between BMR and weight of both men and women. Equations for BMR and weight were established for males and females. Furthermore, caloric intake differences affected changes in total weight as well as differences in % fat composition. Caloric intake however did not affect the difference in LBM. Conclusion: Caloric difference had an impact on total body weight and Lean Body Mass. The model derived from the study predicts weight change and BMR of Ghanaians from 19 to 30 years of age. It is termed the Health and Age Monitoring System (HAMS).

Metabolism and thermoregulation between Mrs Hume's Pheasant(Syrmaticus humiae) and Elliot's Pheasant(S.ellioti)

To understand metabolic adaptations,the basal metabolic rate（BMR） of Mrs Hume＇s Pheasant（Syrmaticus humiae） and Elliot＇s Pheasant（Syrmaticus ellioti） were investigated.Metabolic rate（MR）,body temperature（Tb） and thermal conductance（C） were determined in both species at a temperatrue range of 5-35 ℃,respectively.Oxygen consumption was measured with a closed circuit respirometer.The thermal neutral zones（TNZ） were 24.5-31.6 ℃,and 23.0-29.2 ℃,respectively.With a temperature range of 5-35 ℃,Mrs Hume＇s Pheasant and Elliot＇s Pheasant could maintained stable Tb at a mean of（40.47±0.64） and（40.36±0.10） ℃,respectively.Mean BMRs within TNZs were（1.36±0.84） mLO2/（g.h） for Mrs Hume＇s Pheasant and（2.03±0.12） mLO2/（g.h） for Elliot＇s Pheasant,which were 77% and 86% of the expected value based on their body mass,respectively.Thermal conductance of Mrs Hume＇s Pheasant and Elliot＇s Pheasant were（0.12±0.01） and（0.17±0.01） mLO2/（g.h.℃）,below the lower critical temperature,respectively,which were 119% and 124% of the expected value based on their body mass,respectively.The ecophysiological characteristics of these species were low metabolic rate,high body temperature,and high thermal conductance,which allow both species to better adapt to the warmer climate environment in south China.

Interspecific variation of thermoregulation between small migratory and resident passerines in Wenzhou

Physiological adaptation arises from several fundamental sources of phenotypic variation. Most analyses of metabolic adaptation in birds have focused on the basal metabolic rate （BMR）, the lower limit of avian metabolic heat production. In this study, we investigated thermoregulation in three passerine species; the yellow-billed grosbeak Eophona migratoria, white-rumped munia Lonchura striata and black-throated bushtit Aegithalos concinnus, in Wenzhou, China. Metabolic rate was measured using the closed-circuit respirometer containing 3.5 L animal chambers. Body temperature （Tb） was measured during metabolic measurements using a lubricated thermocouple. The minimum thermal conductance of these species was calculated by measuring their Tb and metabolic rates. The yellow-billed grosbeak remained largely normothermic, and the white-rumped munia and black-throated bushtit exhibited variable Tb at ambient temperatures （Ta）. Mean metabolic rates within thermal neutral zone were 2.48±0.09 02 （mL）/g/h for yellow-billed grosbeaks, 3.44±0.16 02 （mL）/g/h for white-rumped munias, and 3.55±0.20 O2 （mL）/g/h for black-throated bushtits, respectively. Minimum thermal conductance of yellow-billed grosbeak, white-rumped munia and black-throated bushtit were 0.13±0.00, 0.36±0.01, and 0.37±0.01 02 （mL）/g/h/℃, respectively. The ecophysiological characteristics of these species were： （1） the yellowbilled grosbeak had relatively high Tb and BMR, a low lower critical temperature and thermal conductance, and a metabolic rate that was relatively insensitive to variation in Ta; all of which are typical of cold adapted species and explain its broader geographic distribution; （2） the white-rumped munia and black- throated bushtit had high thermal conductance, lower critical temperature, and relatively low BMR, all which are adapted to warm environments where there is little selection pressure for metabolic thermogenesis. Taken together, these data illustrate small migratory and resident passerines that exhibit the different characteristics of thermoregulation.

Thermogenic responses in Eurasian Tree Sparrow(Passer montanus)to seasonal acclimatization and temperature-photoperiod acclimation

Background:Small birds in temperate habitats must either migrate,or adjust aspects of their morphology,physiology and behavior to cope with seasonal change in temperature and photoperiod.It is,however,difficult to accurately measure how seasonal changes in temperature and photoperiod affect physiological processes such as basal metabolic rate(BMR)and metabolic activity.To address this problem,we collected data in each month of the year on body mass(Mb)and BMR,and conducted a series of experiments to determine the effect of temperature and photoperiod on Mb,BMR and physiological markers of metabolic activity,in the Eurasian Tree Sparrow(Passer montanus).Methods:In one experiment,we measured monthly change in Mb and BMR in a captive group of birds over a year.In another experiment,we examined the effects of acclimating birds to two different temperatures,10 and 30℃,and a long and a short photoperiod(16 h light:8 h dark and 8 h light:16 h dark,respectively)for 4 weeks.Results:We found that these treatments induced sparrows to adjust their Mb and metabolic rate processes.Acclimation to 30℃for 4 weeks significantly decreased sparrows’Mb,BMR,and energy intake,including both gross energy intake and digestible energy intake,compared to birds acclimated to 10℃.The dry mass of the liver,kidneys and digestive tract of birds acclimated to 30℃also significantly decreased,although their heart and skeletal muscle mass did not change significantly relative to those acclimated to 10℃.Birds acclimated to 30℃also had lower mitochondrial state-4 respiration(S4R)and cytochrome c oxidase(COX)activity in their liver and skeletal muscle,compared to those acclimated to 10℃.Birds acclimated to the long photoperiod also had lower mitochondrial S4R and COX activity in their liver,compared to those acclimated to the short photoperiod.Conclusions:These results illustrate the changes in morphology,physiology,and enzyme activity induced by seasonal change in temperature and photoperiod in a small temperate passerine.Both temperature and photoperiod probably have a strong effect on seasonal variation in metabolic heat production in small birds in temperate regions.The effect of temperature is,however,stronger than that of photoperiod.

Increased BMR in Overweight and Obese Patients with Type 2 Diabetes may Result from an Increased Fat-free Mass

The study aimed to determine the relationships between the basal metabolic rate（BMR） and body composition of overweight and obese Chinese adults with type 2 diabetes mellitus（DM）. This cross-sectional clinical study enrolled 193 Chinese adults with type 2 DM who were overweight（24 kg/m2≤BMI〈28 kg/m2, n=99）, or obese（BMI ≥28 kg/m2, n=94）. Ninety-seven adults with normal BMIs, including 50 DM patients and 47 healthy adults, were recruited as a control group. BMR was measured by indirect calorimetry; predicted BMR was calculated according to the Schofield equation; and the relationships between BMR, body composition, and biochemical results were determined by the Pearson correlation. The results showed that obese DM patients had significantly higher BMRs than both overweight patients（P〈0.05） and patients with normal BMI did（P〈0.05）. The measured BMR was significantly lower than the predicted BMR（P〈0.05） in all groups. Obese and overweight DM patients had significantly greater weight, waist circumference, hip circumference, BMI, body surface area, body fat percentage, fat mass, and fat-free mass than patients with normal BMI. Except for waist circumference, these body composition measurements were significantly increased in obese DM patients when compared with those in overweight DM patients（P〈0.05）. Fat-free mass was closely correlated with BMR in both DM patients（r=0.874, P〈0.01） and in healthy controls（r=0.902, P〈0.01）. It was concluded that overweight and obese Chinese adults with type 2 DM had increased BMRs compared with normal-weight controls, which may result from the difference in fat-free mass.

Beyond Biological Aging: Table Analysis

Keeping in mind the relationship between the basal metabolic rate and the change in weight in the aging process, we propose to verify the holographic description of the same. For this we set ourselves the following objectives: Verify the correlation between total energy dissipation and energy dissipation per unit body mass, and verify the correlation between the total energy dissipation and the body mass. As a result of the data analysis, we obtained a coherent representation of our proposal. A high degree of correlation between the total energy dissipation in an organism and the basal metabolic rate/dry kg was found. Such a condition implies that the stated biological system satisfies the Holographic Principle.

Metabolic enzymes in seasonally acclimatized and cold acclimated rufous-collared sparrow inhabiting a Chilean Mediterranean environment

Due to the higher energy requirements of birds during winter, it is predicted that the activities of metabolic enzymes （e.g., citrate synthase, CS and cytochrome C oxidase, COX） should increase in tandem with increases in rates of energy expendi ture （e.g., basal metabolic rate, BMR）. However, there is mixed support for the hypothesis of enzymatic acclimatization. Fur thermore, there is little information about the effect of ambient temperature on energetics and tissue enzyme activity levels in passerines inhabiting seasonal Mediterranean environments. In this study we evaluated the interplay between BMR and enzyme activities of freshly caught individuals of the passerine Zonotrichia capensis in winter and summer in a Mediterranean environment from central Chile, and also in warm （30℃） and cold （15℃） labacclimated birds. The results revealed a lack of seasonal variation in BMR, thermal conductance and in the activity of CS and COX. However, we found higher BMR and lower thermal conductance in coldacclimated than in warmacclimated birds. Also, total CS activity was higher in the flight muscles of coldacclimated than in warmacclimated birds. We found also a significant correlation between BMR and total CS activity in pectoral muscle. Although some authors have suggested that BMR mainly depends on the metabolic intensity and mass of internal organs, our results revealed that skeletal muscles such as the flight muscles may also affect BMR. Finally, differences in the accli mation and acclimatization responses in Rufouscollared sparrows suggest that largescale oscillations in the physical environment might maintain the capacity for flexibility in thermogenic traits through generations .

Implication of metabolomic profiles to wide thermoneutral zone in Mongolian gerbils (Meriones unguiculatus)

Mongolian gerbils(Meriones unguiculatus)have evolved a wide thermoneutral zone(26.5-38.9°C)and high upper critical temperature,and appear to have a high tolerance for heat exposure.Here,we use a metabolom­ic approach to measure global metabolite profiles for gerbils between lower(27°C)and upper critical tempera­tures(38°C)to investigate the role of metabolomic characterization in maintaining basal metabolic rates within a wide thermoneutral zone.We found that in serum and liver,14 and 19 metabolites were significantly altered,respectively.In the aerobic respiration-related tricarboxylic cycle(TCA),5 intermediates(isocitric acid,cis-ac­onitic acid,α-ketoglutaric acid,fumaric acid and malic acid)were increased in serum in 38°C animals;how­ever,no such increase was found in the liver.A stable level of hepatic TCA cycle intermediates may be relat­ed to the steady state of aerobic respiration at 38°C.Metabolomic results also revealed that acute heat exposure caused increased oxidative stress and low molecular weight antioxidants in Mongolian gerbils.Increased me­thionine and 2-hydroxybutyrate suggest an accelerated synthesis of glutathione.Increased urate and its precur­sors,inosine and hypoxanthine,were detected at 38°C.Glucuronate,threonate and oxalate involved in ascor­bate synthesis and degradation were increased in serum at 38°C.In conclusion,although dramatic metabolomic variation was found,a stable hepatic TCA cycle may contribute to maintaining a constant basal metabolic rate within a wide thermoneutral zone in Mongolian gerbils.