Heat for nothing or activity for free? Evidence and implications of activity-thermoregulatory heat substitution

If heat generated through activity can substitute for heat required for thermoregulation, then activity in cold environments may be energetically free for endotherms. Although the possibility of activity-thermoregulatory heat substitution has been long recognized, its empirical generality and ecological implications remain unclear. We combine a review of the literature and a model of heat exchange to explore the generality of activity-thermoregulatory heat substitution, to assess the extent to which substitution is likely to vary with body size and ambient temperature, and to examine some potential macroecological implications. A majority of the 51 studies we located showed evidence of activity-thermoregulatory heat substitution (35 of 51 studies), with 28 of 32 species examined characterized by substitution in one or more study. Among studies that did detect substitution, the average magnitude of substitution was 57%, but its occurrence and extent varied taxonomically, allometrically, and with ambient temperature. Modeling of heat production and dissipation suggests that large birds and mammals, engaged in intense activity and exposed to relatively warm conditions, have more scope for substitution than do smaller endotherms engaged in less intense activity and experiencing cooler conditions. However, ambient temperature has to be less than the lower critical temperature (the lower bound of the thermal neutral zone) for activity-thermoregulatory heat substitution to occur and this threshold is lower in large endotherms than in small endotherms. Thus, in nature, substitution is most likely to be observed in intermediate-sized birds and mammals experiencing intermediate ambient temperatures. Activity-thermoregulatory heat substitution may be an important determinant of the activity patterns and metabolic ecology of endotherms. For example, a pattern of widely varying field metabolic rates (FMR) at low latitudes that converges to higher and less variable FMR at high latitudes has been interpreted as suggesting that warm environments at low latitudes allow a greater variety of feasible metabolic niches than do cool, high-latitude environments. However, activity-thermoregulatory heat substitution will generate this pattern of latitudinal FMR variation even if endotherms from cold and warm climates are metabolically and behaviorally identical, because the metabolic rates of resting and active animals are more similar in cold than in warm environments. Activity-thermoregulatory heat substitution is an understudied aspect of endotherm thermal biology that is apt to be a major influence on the physiological, behavioral and ecological responses of free-ranging endotherms to variation in temperature.     

Heritability of flight and resting metabolic rates in the Glanville fritillary butterfly

Dispersal capacity is a key life‐history trait especially in species inhabiting fragmented landscapes. Evolutionary models predict that, given sufficient heritable variation, dispersal rate responds to natural selection imposed by habitat loss and fragmentation. Here, we estimate phenotypic variance components and heritability of flight and resting metabolic rates (RMRs) in an ecological model species, the Glanville fritillary butterfly, in which flight metabolic rate (FMR) is known to correlate strongly with dispersal rate. We modelled a two‐generation pedigree with the animal model to distinguish additive genetic variance from maternal and common environmental effects. The results show that FMR is significantly heritable, with additive genetic variance accounting for about 40% of total phenotypic variance; thus, FMR has the potential to respond to selection on dispersal capacity. Maternal influences on flight metabolism were negligible. Heritability of flight metabolism was context dependent, as in stressful thermal conditions, environmentally induced variation dominated over additive genetic effects. There was no heritability in RMR, which was instead strongly influenced by maternal effects. This study contributes to a mechanistic understanding of the evolution of dispersal‐related traits, a pressing question in view of the challenges posed to many species by changing climate and fragmentation of natural habitats.     

A global assessment of Bergmann's rule in mammals and birds

Bergmann's rule states that endotherms have a large body size in high latitudes and cold climates. However, previous empirical studies have reported mixed evidence on the relationships between body size and latitude, raising the question of why some clades of endotherms follow Bergmann's rule, whereas others do not. Here, we synthesized the interspecific relationships between body size and latitude among 16,187 endothermic species (5422 mammals and 10,765 birds) using Bayesian phylogenetic generalized linear mixed models to examine the strength and magnitude of Bergmann's rule. We further assessed the effect of biological and ecological factors (i.e., body mass categories, dietary guild, winter activity, habitat openness, and climate zone) on the variations in the body mass–latitude relationships by adding an interaction term in the models. Our results revealed a generally weak but significant adherence to Bergmann's rule among all endotherms at the global scale. Despite taxonomic variation in the strength of Bergmann's rule, the body mass of species within most animal orders showed an increasing trend toward high latitudes. Generally, large-bodied, temperate species, non-hibernating mammals, and migratory and open-habitat birds tend to conform to Bergmann's rule more than their relatives do. Our results suggest that whether Bergmann's rule applies to a particular taxon is mediated by not only geographic and biological features, but also potential alternate strategies that species might have for thermoregulation. Future studies could explore the potential of integrating comprehensive trait data into phylogenetic comparative analysis to re-assess the classic ecogeographic rules on a global scale.     

Disentangling environmental drivers of metabolic flexibility in birds: the importance of temperature extremes versus temperature variability

Examining physiological traits across large spatial scales can shed light on the environmental factors driving physiological variation. For endotherms, flexibility in aerobic metabolism is especially important for coping with thermally challenging environments and recent research has shown that aerobic metabolic scope [the difference between maximum thermogenic capacity (M_sum) and basal metabolic rate (BMR)] increases with latitude in mammals. One explanation for this pattern is the climatic variability hypothesis, which predicts that flexibility in aerobic metabolism should increase as a function of local temperature variability. An alternative explanation is the cold adaptation hypothesis, which predicts that cold temperature extremes may also be an important driver of variation in metabolic scope. To determine the thermal drivers of aerobic metabolic flexibility in birds, we combined data on metabolic scope from 40 bird species sampled across a range of environments with several indices of local ambient temperature. Using phylogenetically‐informed analyses, we found that minimum winter temperature was the best predictor of variation in avian metabolic scope, outperforming all other thermal variables. Additionally, M_sum was a better predictor of latitudinal patterns of metabolic scope than BMR, with species inhabiting colder environments exhibiting increased M_sum over their counterparts in warmer environments. Taken together, these results suggest that cold temperature extremes drive latitudinal patterns of metabolic scope via selection for enhanced thermogenic performance in cold environments, supporting the cold adaptation hypothesis. Temperature extremes may therefore be an important selective pressure driving macrophysiological trends of aerobic performance in endotherms.     

Relative longevity and field metabolic rate in birds

Metabolism is a defining feature of all living organisms, with the metabolic process resulting in the production of free radicals that can cause permanent damage to DNA and other molecules. Surprisingly, birds, bats and other organisms with high metabolic rates have some of the slowest rates of senescence begging the question whether species with high metabolic rates also have evolved mechanisms to cope with damage induced by metabolism. To test whether species with the highest metabolic rates also lived the longest I determined the relationship between relative longevity (maximum lifespan), after adjusting for annual adult survival rate, body mass and sampling effort, and mass-specific field metabolic rate (FMR) in 35 species of birds. There was a strongly positive relationship between relative longevity and FMR, consistent with the hypothesis. This conclusion was robust to statistical control for effects of potentially confounding variables such as age at first reproduction, latitude and migration distance, and similarity in phenotype among species because of common phylogenetic descent. Therefore, species of birds with high metabolic rates senesce more slowly than species with low metabolic rates.     

Climatic adaptation and the evolution of basal and maximum rates of metabolism in rodents

Metabolic rate is a key aspect of organismal biology and the identification of selective factors that have led to species differences is a major goal of evolutionary physiology. We tested whether environmental characteristics and/or diet were significant predictors of interspecific variation in rodent metabolic rates. Mass-specific basal metabolic rates (BMR) and maximum metabolic rates (MMR, measured during cold exposure in a He-O2 atmosphere) were compiled from the literature. Maximum (Tmax) and minimum (Tmin) annual mean temperatures, latitude, altitude, and precipitation were obtained from field stations close to the capture sites reported for each population (N = 57). Diet and all continuous-valued traits showed statistically significant phylogenetic signal, with the exception of mass-corrected MMR and altitude. Therefore, results of phylogenetic analyses are emphasized. Body mass was not correlated with absolute latitude, but was positively correlated with precipitation in analyses with phylogenetically independent contrasts. Conventional multiple regressions that included body mass indicated that Tmax (best), Tmin, latitude, and diet were significant additional predictors of BMR. However, phylogenetic analyses indicated that latitude was the only significant predictor of mass-adjusted BMR (positive partial regression coefficient, one-tailed P = 0.0465). Conventional analyses indicated that Tmax, Tmin (best), and altitude explained significant amounts of the variation in mass-adjusted MMR. With body mass and Tmin in the model, no additional variables were significant predictors. Phylogenetic contrasts yielded similar results. Both conventional and phylogenetic analyses indicated a highly significant positive correlation between residual BMR and MMR (as has also been reported for birds), which is consistent with a key assumption of the aerobic capacity model for the evolution of vertebrate energetics (assuming that MMR and exercise-induced maximal oxygen consumption are positively functionally related). Our results support the hypothesis that variation in environmental factors leads to variation in the selective regime for metabolic rates of rodents. However, the causes of a positive association between BMR and latitude remain obscure. Moreover, an important area for future research will be experiments in all taxa are raised under common conditions to allow definitive tests of climatic adaptation in endotherm metabolic rates and to elucidate the extent of adaptive phenotypic plasticity.     

Broad‐scale ecological implications of ectothermy and endothermy in changing environments

Aim Physiology is emerging as a basis for understanding the distribution and diversity of organisms, and ultimately for predicting their responses to climate change. Here we review how the difference in physiology of terrestrial vertebrate ectotherms (amphibians and reptiles) and endotherms (birds and mammals) is expected to influence broad‐scale ecological patterns. Location Global terrestrial ecosystems. Methods We use data from the literature and modelling to analyse geographic gradients in energy use and thermal limits. We then compare broad‐scale ecological patterns for both groups with expectations stemming from these geographic gradients. Results The differences in thermal physiology between ectotherms and endotherms result in geographically disparate macrophysiological constraints. Field metabolic rate (FMR) is stable or decreases slightly with temperature for endotherms, while it generally increases for ectotherms, leading to opposing latitudinal gradients of expected FMR. Potential activity time is a greater constraint on the distributions of ectotherms than endotherms, particularly at high latitudes. Differences in the primary correlates of abundance and species richness for two representative taxonomic groups are consistent with the consequences of these basic physiological differences. Ectotherm richness is better predicted by temperature, whereas endotherm richness is more strongly associated with primary productivity. Finally, in contrast to endotherms, ectotherm richness is not strongly related to abundance. Main conclusions Differences in thermal physiology affect how organisms interact with and are constrained by their environment, and may ultimately explain differences in the geographic pattern of biodiversity for endotherms and ectotherms. Linking the fields of physiological and broad‐scale ecology should yield a more mechanistic understanding of how biodiversity will respond to environmental change.     

Explaining differences in the lifespan and replicative capacity of cells: a general model and comparative analysis of vertebrates

A better understanding of the factors that govern individual cell lifespan and the replicative capacity of cells (i.e. Hayflick's limit) is important for addressing disease progression and ageing. Estimates of cell lifespan in vivo and the replicative capacity of cell lines in culture vary substantially both within and across species, but the underlying reasons for this variability remain unclear. Here, we address this issue by presenting a quantitative model of cell lifespan and cell replicative capacity. The model is based on the relationship between cell mortality and metabolic rate, which is supported with data for different cell types from ectotherms and endotherms. These data indicate that much of the observed variation in cell lifespan and cell replicative capacity is explained by differences in cellular metabolic rate, and thus by the three primary factors that control metabolic rate: organism size, organism temperature and cell size. Individual cell lifespan increases as a power law with both body mass and cell mass, and decreases exponentially with increasing temperature. The replicative capacity of cells also increases with body mass, but is independent of temperature. These results provide a point of departure for future comparative studies of cell lifespan and replicative capacity in the laboratory and in the field.     

Individual variation in field metabolic rate of kittiwakes (Rissa tridactyla) during the chick-rearing period

Field metabolic rate (FMR), using the doubly labelled water (DLW) method, was measured in free-ranging adult kittiwakes (Rissa tridactyla) early and late in the chick-rearing period at Svalbard, Norway. Individual variation in FMR was analysed by comparing FMR with body mass, sex, nest attendance, chick age, brood size, and basal metabolic rate (BMR). Mean FMR of kittiwakes during the chick-rearing period was 27.0+/-0.9 (SE) W kg(-1), while the individual variation (calculated as coefficient of variation [CV]) in FMR was 24%. Sex, time spent away from the nest, age of the chicks, and brood size contributed significantly to FMR and explained 65% of the variation in FMR. The FMR increased by 32% from early until late in the chick-rearing period. This occurred simultaneously with an increase in the time spent away from the nest. In 15 of 20 pairs, one of the mates had 15% or higher (mean of the 15 pairs, 22%+/-8%) FMR (W kg(-1)) than their partner, even though the mates spent equal amounts of time away from the nest. This indicates an intrapair conflict in FMR. The variation in total FMR of pairs was 40% less than the individual variation, and total FMR of pairs increased with age of the chicks. This indicates that the mates adjust their energy expenditure within a relatively constant FMR determined by the energy needs of the chicks. Individual variation in FMR could not be explained by variation in body mass or BMR. BMR measured late in the chick-rearing period was 26% lower than previous measurements of BMR from the prebreeding and incubation periods. The increase in FMR and simultaneous decrease in BMR caused a 40% increase in metabolic intensity (FMR/BMR) of kittiwakes during the chick-rearing period. It is suggested that the metabolic intensity is not a proper measure of the metabolic load in seabirds.     

Seasonal effects on thermoregulatory responses of the Rock Kestrel, Falco rupicolis

Thermoregulatory responses are known to differ seasonally in endotherms and this is often dependent on the environment and region they are resident. Holarctic animals are exposed to severe winters and substantial seasonal variation in ambient temperature. In contrast, those in the Afrotropics have less severe winters, but greater variation in temperature, rainfall and net primary production. These environmental factors place different selection pressures on physiological responses in endotherms. In this study, metabolic rate (VO₂) and body temperature (T_b) were measured in captive bred Rock Kestrels (Falco rupicolus) from the Afrotropics after a period of summer and winter acclimatisation. Resting metabolic rate was significantly lower after the winter acclimatisation period than after the summer acclimatisation period, and there was a shift in the thermoneutral zone from 20–33 °C in summer to 15–30 °C in winter. However, no significant difference in basal metabolic rate between summer and winter was found. The results show that Rock Kestrels reduce energy expenditure at low ambient temperatures in winter as expected in an Afrotropical species.     

Expenditure freeze: the metabolic response of small mammals to cold environments

There is renewed focus on the ecological determinants of animal metabolism and recent comparative analyses support the physiological expectation that the field metabolic rate (FMR) of homeotherms should increase with declining ambient temperature. However, sustained elevation of FMR during prolonged, seasonal cold could be prevented by intrinsic limits constraining FMR to some multiple of basal metabolic rate (BMR) or extrinsic limits on resource abundance. We analysed previous measures of mammalian FMR and BMR to establish the effect of ambient temperature on both traits and found no support for intrinsic limitation. We also measured the FMR of a northern population of red squirrels (Tamiasciurus hudsonicus) exposed to ambient temperatures much colder than all but one previous study of mammal FMR. These measurements revealed levels of energy expenditure that are, unexpectedly, among the lowest ever recorded in homeotherms and that actually decrease as it gets colder. Collectively, these results suggest the metabolic niche space of cold climate endotherms may be much larger than previously recognized.     

Field metabolic rates and water uptake in the blossom-bat Syconycteris australis (Megachiroptera)

Blossom-bats, Syconycteris australis (18 g) are known to be highly active throughout the night. Since this species frequently enters torpor, we postulated that their use of heterothermy may be related to a high energy expenditure in the field. To test this hypothesis we measured field metabolic rates (FMR) of S. australis at a subtropical site using the doubly labelled water (DLW) method. We also measured DLW turnover in captive animals held at constant ambient temperature (T _a) with ad libitum food to estimate whether T _a and food availability affect energy expenditure under natural conditions. The FMR of S. australis was 8.55 ml CO₂ g⁻¹h⁻¹ or 76.87 kJ day⁻¹ which is 7.04 times the basal metabolic rate (BMR) and one of the highest values reported for endotherms to date. Mass-specific energy expenditure by bats in the laboratory was about two-thirds of that of bats in the field, but some of this difference was explained by the greater body mass in captive bats. This suggests that foraging times in the field and laboratory were similar, and daily energy expenditure was not strongly affected by T _a or ad libitum food. Water uptake in the field was significantly higher than in the laboratory, most likely because nectar contained more water than the laboratory diet. Our study shows that S. australis has a FMR that is about double that predicted for its size although its BMR is lower than predicted. This supports the view that caution must be used in making assumptions from measurements of BMR in the laboratory about energy and other biological requirements in free-ranging animals. Accepted: 4 January 1999     

Untargeted metabolic profiling reveals geography as the strongest predictor of metabolic phenotypes of a cosmopolitan weed

Plants produce a multitude of metabolites that contribute to their fitness and survival and play a role in local adaptation to environmental conditions. The effects of environmental variation are particularly well studied within the genus Plantago; however, previous studies have largely focused on targeting specific metabolites. Studies exploring metabolome‐wide changes are lacking, and the effects of natural environmental variation and herbivory on the metabolomes of plants growing in situ remain unknown. An untargeted metabolomic approach using ultra‐high‐performance liquid chromatography–mass spectrometry, coupled with variation partitioning, general linear mixed modeling, and network analysis was used to detect differences in metabolic phenotypes of Plantago major in fifteen natural populations across Denmark. Geographic region, distance, habitat type, phenological stage, soil parameters, light levels, and leaf area were investigated for their relative contributions to explaining differences in foliar metabolomes. Herbivory effects were further investigated by comparing metabolomes from damaged and undamaged leaves from each plant. Geographic region explained the greatest number of significant metabolic differences. Soil pH had the second largest effect, followed by habitat and leaf area, while phenological stage had no effect. No evidence of the induction of metabolic features was found between leaves damaged by herbivores compared to undamaged leaves on the same plant. Differences in metabolic phenotypes explained by geographic factors are attributed to genotypic variation and/or unmeasured environmental factors that differ at the regional level in Denmark. A small number of specialized features in the metabolome may be involved in facilitating the success of a widespread species such as Plantago major into such wide range of environmental conditions, although overall resilience in the metabolome was found in response to environmental parameters tested. Untargeted metabolomic approaches have great potential to improve our understanding of how specialized plant metabolites respond to environmental change and assist in adaptation to local conditions.     

Temperature dependence of evolutionary diversification: differences between two contrasting model taxa support the metabolic theory of ecology

Biodiversity patterns are largely determined by variation of diversification rates across clades and geographic regions. Although there are multiple reasons for this variation, it has been hypothesized that metabolic rate is the crucial driver of diversification of evolutionary lineages. According to the metabolic theory of ecology (MTE), metabolic rate – and consequently speciation – is driven mainly by body size and environmental temperature. As environmental temperature affects metabolic rate in ecto‐ and endotherms differently, its impact on diversification rate should also differ between the two types of organisms. Employing two independent approaches, we analysed correlates of speciation rates and, ultimately, net diversification rates for two contrasting taxa: plethodontid salamanders and carnivoran mammals. Whereas in the ectothermic plethodontids speciation rates positively correlated with environmental temperature, in the endothermic carnivorans a reverse, negative correlation was detected. These findings comply with predictions of the MTE and suggest that similar geographic patterns of biodiversity across taxa (e.g. ecto‐ and endotherms) might have been generated by different ecological and evolutionary processes.     

Quantifying energetic and fitness consequences of seasonal heterothermy in an Arctic ungulate

Animals have adapted behavioral and physiological strategies to conserve energy during periods of adverse conditions. Heterothermy is one such adaptation used by endotherms. While heterothermy—fluctuations in body temperature and metabolic rate—has been shown in large vertebrates, little is known of the costs and benefits of this strategy, both in terms of energy and in terms of fitness. Hence, our objective was to model the energetics of seasonal heterothermy in the largest Arctic ungulate, the muskox (Ovibos moschatus), using an individual‐based energy budget model of metabolic physiology. We found that the empirically based drop in body temperature (winter max ~−0.8°C) overwinter in adult females resulted in substantial fitness benefits in terms of reduced daily energy expenditure and body mass loss. Body mass and energy reserves were 8.98% and 14.46% greater in modeled heterotherms compared to normotherms by end of winter. Based on environmental simulations, we show that seasonal heterothermy can, to some extent, buffer the negative consequences of poor prewinter body condition or reduced winter food accessibility, leading to greater winter survival (+20%–30%) and spring energy reserves (+10%–30%), and thus increased probability of future reproductive success. These results indicate substantial adaptive short‐term benefits of seasonal heterothermy at the individual level, with potential implications for long‐term population dynamics in highly seasonal environments.     

Climate change and community disassembly: impacts of warming on tropical and temperate montane community structure

Both tropical and temperate species are responding to global warming through range shifts, but our understanding of the consequences of these shifts for whole communities is limited. Here, we use current elevational range data for six taxonomic groups spanning 90° in latitude to examine the potential impacts of climate-driven range shifts on community change, or 'disassembly', across latitude. Elevational ranges are smaller at low latitudes for most groups and, as a consequence, tropical communities appear to be more sensitive to temperature increases compared with temperate communities. Under site-specific temperature projections, we generally found greater community disassembly in tropical compared with temperate communities, although this varied by dispersal assumptions. Mountain height can impact the amount of community disassembly, with greater change occurring on smaller mountains. Finally, projected community disassembly was higher for ectotherms than endotherms, although the variation among ectotherms was greater than the variation separating endotherms and ectotherms.     

The balance between predictions and evidence and the search for universal macroecological patterns: taking Bergmann’s rule back to its endothermic origin

Geographical variation in environmental temperatures is expected to impose clinal phenotypic selection that results in the expression of large-scale gradients of body mass variation within animal clades. Body size is predicted to increase with increasing latitude and elevation, and hence, with decreasing temperature, a pattern broadly known as Bergmann’s rule. However, empirical observations are highly conflicting. Whilst most studies support this prediction in endotherms (birds and mammals), analyses conducted on ectotherms often fail to report this pattern. Does it reduce the validity of this macroecological rule? Since the original formulation of Bergmann’s rule only involved endothermic organisms, I argue that the controversy is not a consequence of its predictive power, but a result of the later inclusion of ectotherms as part of the prediction. Here, I propose that the common conception of Bergmann’s rule maintained for half a century is changed back to its original definition restricted to endotherms. This temperature–size relationship might therefore consolidate as a well-established macroecological rule if its original formulation is respected. Finally, I develop these claims on my initial suggestion that Bergmann’s rule should be recognized as the evolutionary outcome of a general process with no phylogenetic scale distinction of species or populations, being equally applicable amongst and within species.     

The covariance between metabolic rate and behaviour varies across behaviours and thermal types: meta‐analytic insights

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.     

Field Metabolic Rate Is Dependent on Time-Activity Budget in Ring-Billed Gulls (Larus delawarensis) Breeding in an Anthropogenic Environment

Environmental and behavioral factors have long been assumed to affect variation in avian field metabolic rate (FMR). However, due to the difficulties in measuring continuous behavior of birds over prolonged periods of time, complete time-activity budgets have rarely been examined in relation to FMR. Our objective was to determine the effect of activity (measured by detailed time-activity budgets) and a series of extrinsic and intrinsic factors on FMR of the omnivorous ring-billed gull (Larus delawarensis). The experiment was conducted during the incubation period when both members of the pair alternate between attending the nest-site and leaving the colony to forage in aquatic and anthropogenic environments (city, agricultural). FMR was determined using the doubly labeled water method. Time-activity budgets were extrapolated from spatio-temporal data (2-5 days) obtained from bird-borne GPS data loggers. Gulls had low FMRs compared to those predicted by allometric equations based on recorded FMRs from several seabird species. Gulls proportioned their time mainly to nest-site attendance (71% of total tracking time), which reduced FMR/g body mass, and was the best variable explaining energy expenditure. The next best variable was the duration of foraging trips, which increased FMR/g; FMR/g was also elevated by the proportion of time spent foraging or flying (17% and 8% of tracking time respectively). Most environmental variables measured did not impact FMR/g, however, the percent of time birds were subjected to temperatures below their lower critical temperature increased FMR. Time-activity budgets varied between the sexes, and with temperature and capture date suggesting that these variables indirectly affected FMR/g. The gulls foraged preferentially in anthropogenic-related habitats, which may have contributed to their low FMR/g due to the high availability of protein- and lipid-rich foods. This study demonstrates that activities were the best predictors of FMR/g in ring-billed gulls, thus providing strong support for this long-standing theory in bioenergetics.     

Lower body mass and higher metabolic rate enhance winter survival in root voles,Microtus oeconomus

Although the biological significance of individual variation in physiological traits is widely recognized, studies of their association with fitness in wild populations are surprisingly scarce. We investigated the effect of individual phenotypic variation in body mass, resting (RMR) and peak metabolic rates (PMR) on mortality of the root vole Microtus oeconomus. Body mass and metabolic rates varied significantly among consecutive years and were also age dependent, as individuals born in late summer and autumn were characterized by significantly lower body mass and metabolic rates than animals born earlier. At the beginning of winter voles born in spring and early summer exhibited reduced body mass and metabolic rates, whereas animals born later maintained lower body mass and RMR, which may be interpreted as phenotypic plasticity enhancing the probability of survival. Body mass had no significant effect on vole survival during summer. In contrast, smaller individuals were characterized by lower mortality during early winter, whereas higher body mass was positively associated with survival later in the season. High body‐mass‐corrected RMR positively affected survival in both summer and winter. The effect of PMR was apparent only during winter, though its direction (and correlation with RMR) varied among years. Deep snow cover negatively affected the survival of voles in both early and late winter. Ambient temperature was positively associated with winter survival, except for late winter, when rising temperature caused flooding of vole habitat. We conclude that the lack of consistency in the directionality and strength of the effects of body mass and metabolic rates on winter survival does not undermine their importance, but rather demonstrates the ability of individuals to adjust metabolic rate to changing environmental conditions. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 297–309.