ABSTRACT
Energy metabolism has received much attention as a potential driver of repeatable among‐individual differences in behaviour (animal personality). Several factors have been hypothesized to ...mediate this relationship. We performed a systematic review with a meta‐analysis of >70 studies comprised of >8000 individuals reporting relationships between measures of maintenance metabolic rates (i.e. basal metabolic rate, resting metabolic rate, and standard metabolic rate) and behaviour. We evaluated support for three hypothesized mediators: (i) type of behaviour, (ii) opportunities for energy re‐allocation, and (iii) magnitude of energetic constraints. Relationships between measures of maintenance metabolic rate (MR) and behaviour are predicted to be strongest for behaviours with strong consequences for energy turnover (acquisition or expenditure). Consistent with this, we found that behaviours with known consequences for energy gain (e.g. foraging, dominance, boldness) or expenditure (e.g. maximum sprint speed, sustained running speed, maximum distance travelled, etc.) had strong positive correlations with MR, while behaviours with putatively weak and/or inconsistent associations with net energy gain or loss (e.g. exploration, activity, sociability) were not correlated with MR. Greater opportunities for energy reallocation are predicted to weaken relationships between MR and behaviour by creating alternative pathways to balance energy budgets. We tested this by contrasting relationships between MR and behaviour in ectotherms versus endotherms, as thermoregulation in endotherms creates additional opportunities for energy reallocation compared with ectotherms. As predicted, the relationship between behaviour and MR was stronger in ectotherms compared with endotherms. However, statistical analyses of heterogeneity among effect sizes from different species did not support energy re‐allocation as the main driver of these differences. Finally, we tested whether conditions where animals face greater constraints in meeting their energy budgets (e.g. field versus laboratory, breeding versus non‐breeding) increased the strength of the relationship between MR and behaviour. We found that the relationship between MR and behaviour was unaffected by either of these modifiers. This meta‐analysis provides two key insights. First, we observed positive relationships of similar magnitude between MR and behaviours that bring in net energy, and behaviours that cost net energy. This result is only consistent with a performance energy‐management model. Given that the studies included in our meta‐analysis represent a wide range of taxa, this suggests that the performance model may be the most common model in general. Second, we found that behaviours with putatively weak or inconsistent consequences for net energy gain or expenditure (exploration, activity, sociability) show no relationship with MR. The lack of relationship between MR and behavioural traits with weak and/or inconsistent consequences for energy turnover provides the first systematic demonstration of the central importance of the ecological function of traits in mediating relationships between MR and behaviour.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
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.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
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.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Summary
Variation in aerobic capacity has far reaching consequences for the physiology, ecology, and evolution of vertebrates. Whether at rest or active, animals are constrained to operate within the ...energetic bounds determined by their minimum (minMR) and sustained or maximum metabolic rates (upperMR). MinMR and upperMR can differ considerably among individuals and species but are often presumed to be mechanistically linked to one another. Specifically, minMR is thought to reflect the idling cost of the machinery needed to support upperMR. However, previous analyses based on limited datasets have come to conflicting conclusions regarding the generality and strength of their association.
Here we conduct the first comprehensive assessment of their relationship, based on a large number of published estimates of both the intra‐specific (n = 176) and inter‐specific (n = 41) phenotypic correlations between minMR and upperMR, estimated as either exercise‐induced maximum metabolic rate (VO2max), cold‐induced summit metabolic rate (Msum), or daily energy expenditure (DEE).
Our meta‐analysis shows that there is a general positive association between minMR and upperMR that is shared among vertebrate taxonomic classes. However, there was stronger evidence for intra‐specific correlations between minMR and Msum and between minMR and DEE than there was for a correlation between minMR and VO2max across different taxa. As expected, inter‐specific correlation estimates were consistently higher than intra‐specific estimates across all traits and vertebrate classes.
An interesting exception to this general trend was observed in mammals, which contrast with birds and exhibit no correlation between minMR and Msum. We speculate that this is due to the evolution and recruitment of brown fat as a thermogenic tissue, which illustrates how some species and lineages might circumvent this seemingly general association.
We conclude that, in spite of some variability across taxa and traits, the contention that minMR and upperMR are positively correlated generally holds true both within and across vertebrate species. Ecological and comparative studies should therefore take into consideration the possibility that variation in any one of these traits might partly reflect correlated responses to selection on other metabolic parameters.
A lay summary is available for this article.
Lay Summary
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
Acclimatization of certain ectothermic vertebrates to winter conditions is associated with reduced energy consumption (winter dormancy). Principally, this may be achieved by reducing movement ...activity, depression of basal cellular functions, or by switching from aerobic to anaerobic energy production to sustain low energy consumption during anoxia. Therefore, we determined standard (SMR), routine (RMR) and anoxic (AMR) metabolic rates in summer- (SumA; 20 °C) and winter-acclimatized (WinA; 2 °C) crucian carp (Carassius carassius), an anoxia-tolerant teleost fish. At 20 °C, RMR was 39% lower in WinA than SumA fish (p < 0.05), indicating reduced movements in winter. SMR, measured for the first time in crucian carp, was 45% lower in WinA than SumA fish at 10 °C (p < 0.05), indicating significant reduction of energy consumption in vital cellular processes. At 2 °C, AMR - measured from ethanol production- was 78% and 97% of the SMR and RMR levels at the same temperature, respectively. The current study revealed that the winter dormancy in anoxia-tolerant crucian carp is achieved in 3 different steps: (1) by active reduction of SMR, possibly in anticipation of seasonal anoxia, (2) acute Arrhenius Q10 effect that slows SMR as well as RMR, and (3) direct response to the absence of oxygen (AMR). Furthermore, the anoxic energy production was strongly dependent on body mass with scaling exponents of -0.335 and - 0.421 for WinA and SumA fish, respectively.
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GEOZS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Summary
Metabolic rates can vary as much as threefold among individuals of the same size and age in a population, but why such variation persists is unclear given that they determine the energetic ...cost of living. Relationships between standard metabolic rate (SMR), growth and survival can vary with environmental conditions, suggesting that the fitness consequences of a given metabolic phenotype may be context‐dependent. Less attention has focused on the link between absolute aerobic scope (AS, the difference between standard and maximum metabolic rate) and fitness under different environmental conditions, despite the importance of aerobic scope to an organism's total energetic capacity.
We examined the links between individual variation in both SMR and AS and somatic growth rates of brown trout (Salmo trutta) under different levels of food availability.
Standard metabolic rate and AS were uncorrelated across individuals. However, SMR and AS not only had interactive effects on growth, but these interactions depended on food level: at ad libitum food levels, AS had a positive effect on growth whose magnitude depended on SMR; at intermediate food levels, AS and SMR had interactive effects on growth, but at the low food level, there was no effect of either AS or SMR on growth. As a result, there was no metabolic phenotype that performed best or worst across all food levels.
These results demonstrate the importance of aerobic scope in explaining somatic growth rates and support the hypothesis that links between individual variation in metabolism and fitness are context‐dependent.
The larger metabolic phenotype and the environmental context in which performance is evaluated both need to be considered in order to better understand the link between metabolic rates and fitness and thereby the persistence of individual variation in metabolic rates.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
The origin and shape of metabolic scaling has been controversial since Kleiber found that basal metabolic rate of animals seemed to vary as a power law of their body mass with exponent 3/4, instead ...of 2/3, as a surface-to-volume argument predicts. The universality of exponent 3/4 -claimed in terms of the fractal properties of the nutrient network- has recently been challenged according to empirical evidence that observed a wealth of robust exponents deviating from 3/4. Here we present a conceptually simple thermodynamic framework, where the dependence of metabolic rate with body mass emerges from a trade-off between the energy dissipated as heat and the energy efficiently used by the organism to maintain its metabolism. This balance tunes the shape of an additive model from which different effective scalings can be recovered as particular cases, thereby reconciling previously inconsistent empirical evidence in mammals, birds, insects and even plants under a unified framework. This model is biologically motivated, fits remarkably well the data, and also explains additional features such as the relation between energy lost as heat and mass, the role and influence of different climatic environments or the difference found between endotherms and ectotherms.
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IZUM, KILJ, NUK, PILJ, PNG, SAZU, UL, UM, UPUK
Aim
The ‘rate‐of‐living’ theory predicts that life expectancy is a negative function of the rates at which organisms metabolize. According to this theory, factors that accelerate metabolic rates, ...such as high body temperature and active foraging, lead to organismic ‘wear‐out’. This process reduces life span through an accumulation of biochemical errors and the build‐up of toxic metabolic by‐products. Although the rate‐of‐living theory is a keystone underlying our understanding of life‐history trade‐offs, its validity has been recently questioned. The rate‐of‐living theory has never been tested on a global scale in a phylogenetic framework, or across both endotherms and ectotherms. Here, we test several of its fundamental predictions across the tetrapod tree of life.
Location
Global.
Time period
Present.
Major taxa studied
Land vertebrates.
Methods
Using a dataset spanning the life span data of 4,100 land vertebrate species (2,214 endotherms, 1,886 ectotherms), we performed the most comprehensive test to date of the fundamental predictions underlying the rate‐of‐living theory. We investigated how metabolic rates, and a range of factors generally perceived to be strongly associated with them, relate to longevity.
Results
Our findings did not support the predictions of the rate‐of‐living theory. Basal and field metabolic rates, seasonality, and activity times, as well as reptile body temperatures and foraging ecology, were found to be unrelated to longevity. In contrast, lower longevity across ectotherm species was associated with high environmental temperatures.
Main conclusions
We conclude that the rate‐of‐living theory does not hold true for terrestrial vertebrates, and suggest that life expectancy is driven by selection arising from extrinsic mortality factors. A simple link between metabolic rates, oxidative damage and life span is not supported. Importantly, our findings highlight the potential for rapid warming, resulting from the current increase in global temperatures, to drive accelerated rates of senescence in ectotherms.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Phylogeny and metabolic scaling in mammals Capellini, Isabella; Venditti, Chris; Barton, Robert A
Ecology (Durham),
September 2010, Volume:
91, Issue:
9
Journal Article
Peer reviewed
Open access
The scaling of metabolic rates to body size is widely considered to be of great biological and ecological importance, and much attention has been devoted to determining its theoretical and empirical ...value. Most debate centers on whether the underlying power law describing metabolic rates is 2/3 (as predicted by scaling of surface area/volume relationships) or 3/4 ("Kleiber's law"). Although recent evidence suggests that empirically derived exponents vary among clades with radically different metabolic strategies, such as ectotherms and endotherms, models, such as the metabolic theory of ecology, depend on the assumption that there is at least a predominant, if not universal, metabolic scaling exponent. Most analyses claimed to support the predictions of general models, however, failed to control for phylogeny. We used phylogenetic generalized least-squares models to estimate allometric slopes for both basal metabolic rate (BMR) and field metabolic rate (FMR) in mammals. Metabolic rate scaling conformed to no single theoretical prediction, but varied significantly among phylogenetic lineages. In some lineages we found a 3/4 exponent, in others a 2/3 exponent, and in yet others exponents differed significantly from both theoretical values. Analysis of the phylogenetic signal in the data indicated that the assumptions of neither species-level analysis nor independent contrasts were met. Analyses that assumed no phylogenetic signal in the data (species-level analysis) or a strong phylogenetic signal (independent contrasts), therefore, returned estimates of allometric slopes that were erroneous in 30% and 50% of cases, respectively. Hence, quantitative estimation of the phylogenetic signal is essential for determining scaling exponents. The lack of evidence for a predominant scaling exponent in these analyses suggests that general models of metabolic scaling, and macro-ecological theories that depend on them, have little explanatory power.
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BFBNIB, FZAB, GIS, IJS, INZLJ, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK, ZRSKP
Direct calorimetry is the gold standard means of measuring human metabolic rate and its use has been fundamental for understanding metabolism in health and disease. While metabolic rate is now more ...commonly estimated indirectly from measures of the oxygen consumed during respiration, direct calorimetry provides the user with the unique capacity to quantify the heat produced from aerobic and anaerobic metabolism by measuring heat exchange between the body and the environment. This review provides a brief historical overview of the fundamental concepts which underlie direct calorimetry, of pioneer scientists which developed these concepts into functional pieces of equipment and the subsequent use of direct calorimetry to advance our understanding of energy balance, nutrition, and the pathogenesis of metabolic diseases. Attention is directed to seminal studies that successfully employed direct calorimetry to verify that the law of energy conservation also applies to human beings and to establish the validity of indirect calorimetry. Finally, we discuss the more recent use of direct calorimetry for the measurement of whole-body heat exchange and body heat storage in the study of human thermoregulation.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OBVAL, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
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