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It is generally assumed that small birds improve their shivering heat production capacity by developing the size of their pectoralis muscles. However, some studies have reported an enhancement of thermogenic capacity in the absence of muscle mass variation between seasons or thermal treatments. We tested the hypothesis that an increase in muscle mass is not a prerequisite for improving avian thermogenic capacity. We measured basal (BMR) and summit (M sum ) metabolic rates of black capped chickadees (Poecile atricapillus) acclimated to thermoneutral (27 °C) and cold (-10 °C) temperatures and obtained body composition data from dissections. Cold acclimated birds consumed 44% more food, and had 5% and 20% higher BMR and M sum , respectively, compared to individuals kept at thermoneutrality. However, lean dry pectoralis and total muscle mass did not differ between treatments, confirming that the improvement of thermogenic capacity did not require an increase in skeletal muscle mass. Nevertheless, within temperature treatments, M sum was positively correlated with the mass of all measured muscles, including the pectoralis. Therefore, for a given acclimation temperature individuals with large muscles do benefit from muscle size in term of heat production but improving thermogenic capacity during cold acclimation likely requires an upregulation of cell functions.

Small resident bird species living at northern latitudes increase their metabolism in winter, and this is widely assumed to improve their chances of survival. However, the relationship between winter metabolic performance and survival has yet to be demonstrated. Using capture-mark-recapture, we followed a population of free-living black-capped chickadees (Poecile atricapillus) over 3 yr and evaluated their survival probability within and among winters. We also measured the size-independent body mass (M s ), hematocrit (Hct), basal metabolic rate (BMR), and maximal thermogenic capacity (Msum) and investigated how these parameters influenced survival within and among winters. Results showed that survival probability was high and constant both within (0.92) and among (0.96) winters. They also showed that while M s , Hct, and BMR had no significant influence, survival was positively related to Msum-following a sigmoid relationship-within but not among winter. Birds expressing an Msum below 1.26 W (i.e., similar to summer levels) had a <50% chance of survival, while birds with an Msum above 1.35 W had at least a 90% chance of surviving through the winter. Our data therefore suggest that black-capped chickadees that are either too slow or unable to adjust their phenotype from summer to winter have little chances of survival and thus that seasonal upregulation of metabolic performance is highly beneficial. This study is the first to document in an avian system the relationship between thermogenic capacity and winter survival, a proxy of fitness.

Resident passerines inhabiting high latitude environments are faced with strong seasonal changes in thermal conditions and energy availability. Summit metabolic rate (maximal metabolic rate elicited by shivering during cold exposure: M(sum)) and basal metabolic rate (BMR) vary in parallel among seasons and increase in winter due to cold acclimatization, and these adjustments are thought to be critical for survival. Wintering individuals expressing consistently higher M(sum) and BMR could therefore be seen as better performers with higher chances of winter survival than those exhibiting lower metabolic performance. In this study, we calculated repeatability to evaluate temporal consistency of body mass, BMR and M(sum) within and across three consecutives winters in black-capped chickadees (Poecile atricapillus). We found that body mass was significantly repeatable both within and across winters (R 0.51-0.90). BMR (R 0.29-0.47) was only repeatable within winter while M(sum) was repeatable both among (R 0.33-0.49) and within winters (R 0.33-0.49) with the magnitude and significance of repeatability in both variables depending on the year and whether they were corrected for body mass or body size. The patterns of repeatability observed among years also differed between the two variables. Our findings suggest that the relative ranking of individuals in winter metabolic performance is affected by local ecological conditions and can change within relatively short periods of time., (© 2015 Wiley Periodicals, Inc.)

In small resident bird species living at northern latitudes, winter cold acclimatization is associated with an increase in pectoral muscle size and haematocrit level, and this is thought to drive the seasonal increase in summit metabolic rate (Msum, a measure of maximal shivering thermogenic capacity). However, evidence suggesting that pectoral muscle size influences Msum is correlational and the link between haematrocrit level and Msum remains to be demonstrated. We experimentally tested the relationship between pectoral muscle size and Msum by manipulating muscle size using a feather clipping protocol in free-living wintering black-capped chickadees (Poecile atricapillus). This also allowed us to investigate the link between haematocrit and thermogenic capacity. After a first series of measures on all birds, we cut half of the flight feathers of experimental individuals (N=14) and compared their fat and pectoral muscle scores, Msum and haematocrit level at recapture with their previous measures and with those of control birds (N=17) that were captured and recaptured at comparable times. Results showed that: (1) experimental birds developed larger pectoral muscles than control individuals and (2) mass-independent Msum was up to 16% higher in birds expressing large pectoral muscles. Msum was also positively correlated with haematocrit, which was not affected by the experimental manipulation. These findings demonstrate that, for a given body mass, large pectoral muscles are associated with a higher Msum in black-capped chickadees and that oxygen carrying capacity likely supports thermogenesis in this species.

Stochastic winter weather events are predicted to increase in occurrence and amplitude at northern latitudes and organisms are expected to cope through phenotypic flexibility. Small avian species wintering in these environments show acclimatization where basal metabolic rate (BMR) and maximal thermogenic capacity (MSUM) are typically elevated. However, little is known on intra-seasonal variation in metabolic performance and on how population trends truly reflect individual flexibility. Here we report intra-seasonal variation in metabolic parameters measured at the population and individual levels in black-capped chickadees (Poecileatricapillus). Results confirmed that population patterns indeed reflect flexibility at the individual level. They showed the expected increase in BMR (6%) and MSUM (34%) in winter relative to summer but also, and most importantly, that these parameters changed differently through time. BMR began its seasonal increase in November, while MSUM had already achieved more than 20% of its inter-seasonal increase by October, and declined to its starting level by March, while MSUM remained high. Although both parameters co-vary on a yearly scale, this mismatch in the timing of variation in winter BMR and MSUM likely reflects different constraints acting on different physiological components and therefore suggests a lack of functional link between these parameters.

Winter requires physiological adjustments in northern resident passerines. Cold acclimatization is generally associated with an increase in physiological maintenance costs, measured as basal metabolic rate (BMR), and cold endurance, reflected by summit metabolic rate (M(sum)). However, several northern species also form social groups in winter and a bird's hierarchical position may influence the size of its metabolically active organs as well as its BMR. Winter metabolic performance in these species may therefore reflect a complex set of adjustments to both seasonal climatic variations and social environment. We studied the effect of social status on parameters of cold acclimatization (body mass, size of fat reserves and pectoral muscles, BMR and M(sum)) in free-living black-capped chickadees (Poecile atricapillus). Birds that were structurally large and heavy for their body size, mostly dominant individuals, carried more fat reserves and had larger pectoral muscles. However, social status had little effect on metabolic performance in the cold. Indeed, M(sum) was independent of social rank while mass-corrected BMR was slightly lower in dominant individuals, likely due to a statistical dilution effect caused by large metabolically inactive fat reserves. BMR and M(sum), whether considered in terms of whole-animal values, corrected for body mass or body size were nevertheless correlated, suggesting a functional link between these metabolic components. Our results therefore indicate that the energy cost of social dominance is not a generalized phenomenon in small wintering birds.

Recent studies have shown that the metabolic cost of avian egg production involves a 16-27% increase in metabolic rate (MR) above non-reproductive basal or resting values (BMR and RMR, respectively). To determine how the metabolic cost of egg production interacted with the costs of other essential processes (such as cold acclimation and active heat production), we measured the MR of non-breeding and egg-producing zebra finches (Taeniopygia guttata) while (a) warm-acclimated (to 19-21 degrees C) and measured within their thermoneutral zone (at 35 degrees C), (b) cold-acclimated (to 7 degrees C) and measured at thermoneutrality (at 35 degrees C, i.e. not actively producing heat), and (c) cold-acclimated and measured below thermoneutrality (at 7 degrees C) (i.e. during active heat production). The metabolic cost of egg production was small (24% above BMR) compared with the additive costs of cold acclimation and active heat production (224% above BMR). Exposure to low ambient temperatures was accompanied by an increase in seed consumption (by 72%) and a decrease in locomotor activity (by 72%) compared with warm-acclimated, non-breeding values. By contrast, egg production in heat-producing females was associated with an 11% decrease in MR and a 22% decrease in seed consumption compared with non-breeding thermoregulating values. Our data suggest that while the increase in MR associated with egg production is small in relation to the birds' capacity to increase MR in response to other energetically demanding processes, the addition of egg production to these metabolically costly activities may be enough to necessitate the use of energy-saving strategies, such as internal energy reallocation, to cope with the additional energetic demands.

Basal metabolic rate (BMR) in animals is interpreted as reflecting the size and metabolic intensity of energy-consuming tissues. However, studies investigating relationships between the mass of specific organs and interindividual variation in BMR have produced inconsistent patterns with regard to which organs have the largest impact on BMR variation. Because of the known flexibility in organ mass and metabolic intensity within individual organs, relationships between BMR and body-composition variables are bound to be context specific. Altricial nestlings are excellent models to illustrate this phenomenon because of the extreme variation in body composition occurring during growth. Using European starlings at three age classes, we studied changes in body composition together with its effect on variation in resting metabolic rate (RMR) in order to highlight the context-specific nature of these relationships. Our data suggest a transition in metabolic costs during growth in starling nestlings. During the linear phase of growth, energy is mainly consumed by tissue-synthesis processes, with fast-growing organs having a large influence on RMR. In the plateau phase of growth, the energy expenditure is transferred to functional costs, with high-intensity organs having a predominant effect on RMR variation. Our data illustrates the context-specific nature of organ mass-metabolic rate correlations, which complicates inter- and intraspecific comparisons of BMR. In the future, such comparisons must be done while taking the physiological state of the study animal into account.

It is axiomatic that whole-animal metabolism, measured for example as daily energy expenditure (DEE), plays a central role in determining reproductive success and survival (fitness) in all organisms. Nevertheless, strong evidence for consistent systematic relationships between DEE and either individual traits (age, sex, body size), environmental factors (e.g. food availability, temperature) or 'fitness' traits (e.g. number of offspring, survival) remains far from compelling in birds and mammals. Recently, we suggested that female birds might utilise complex, individually variable energy management strategies to meet the metabolic demands of reproduction, generating a wide spectrum of effects on reproductive DEE, from overcompensation (net decrease in DEE) to additive effects (net increase in DEE). Here we show that this individually variable adjustment or 'plasticity' in energy expenditure associated with egg production is repeatable among individuals between successive breeding attempts in female zebra finches (Taeniopygia guttata). Our study highlights the importance (a) of measuring 'plasticity' or change associated with transitions of physiological state (e.g. non-breeding to breeding) based on multiple measurements of the same individual, and (b) of extending consideration of how selection might drive the evolution of phenotypic plasticity per se to include physiological and metabolic traits.

Even though molt involves both endocrine and energetic changes in bird bodies, this study is among the first to combine assessments of energy costs together with thyroid hormone variations in molting birds. Individual shorebirds (red knots Calidris canutus islandica) were measured while in full summer and winter plumage as well as during peak of molt. Molt was associated with a 9.8% increase in average mass-independent basal metabolic rate (BMR) above nonmolting levels. Individual plasma levels of thyroxine (T(4)) were correlated with individual rate of body feather renewal, confirming that T(4) is related to body molt but also showing that it is potentially regulating its rate. Across seasons, mass-independent average heat loss measured as conductance gradually declined with conductance during molt falling between measured values for summer and winter. During the molting period, however, body molting rate was positively correlated with thermal conductance, indicating that for a given ambient temperature below thermoneutrality, the fastest molting birds were losing more body heat. Across seasons, triiodothyronine (T(3)), a hormone typically upregulated in response to a cold stimulus, was correlated with individual thermal conductance and BMR. We suggest that the increased heat loss of fast-molting birds leads to a cold-acclimatization response that may be partly responsible for the elevated BMR measured during molt. This could be mediated through a stimulatory effect of T(3) on BMR in response to increased heat loss. Our interpretation is supported by a positive relationship between the individual changes in conductance and the change in BMR from summer to the molting period.

Marked interindividual variation in metabolic rate suggests considerable complexity in energy management strategies, but attempts to further our understanding of the relationship between resting metabolic rate (RMR), daily energy expenditure (DEE), and reproductive effort have been hampered by the complexity of studying this system in the field. Here, we describe energy management strategies in a captive-breeding system, using Zebra Finches (Taeniopygia guttata), to demonstrate the high level of complexity and interindividual variability in energy expenditure, food intake, locomotor activity, and reproductive effort. In particular, we investigated whether the increase in RMR associated with egg production is additive, resulting in higher DEE and a need for elevated food intake, or whether this cost is compensated by reduced expenditure in nonreproductive components of the energy budget. We found high levels of intra-individual variation in energy expenditure associated with egg production in female Zebra Finches, e.g., comparing nonbreeding stage with the one-egg stage, change in RMR varied from 4.0% and 41.3%, and change in DEE varied from -33.3% to +46.4%. This variation was systematically related to aspects of locomotor activity and reproductive effort. Females with the largest increase in RMR during egg production decreased locomotor activity the most but still had increased DEE at the one-egg stage, and females with high DEE at the one-egg stage produced larger clutches. Our study suggests that females minimize increases in DEE during egg production through behavioral energy reallocation (reduced locomotor activity) but that individuals differ in their use of this strategy, which, in turn, is related to the absolute level of reproductive investment. This suggests a very complex, individually variable system of energy management to meet the demands of egg production.

The metabolic cost of egg production in birds (passerines) has been measured as a 16-27% increase in basal or resting metabolic rate (BMR and RMR, respectively) when comparing non-breeding values with those in egg-producing individuals. However, available data to date have been obtained in free-living birds and may thus be confounded by the effect of variable ecological conditions on non-reproductive physiological machinery (organ mass or metabolic activity) which might contribute to measured variation in RMR. Here, we show that in captive, controlled conditions, the process of egg formation induces a 22% increase in RMR in female zebra finches Taeniopygia guttata. Among individuals, variation in laying RMR is independent of egg mass, clutch size or total clutch mass. Importantly, we show that individual variation in both non-breeding and laying RMR is repeatable over periods of at least 8-10 months, i.e. individual variation in RMR remained constant over time for any given physiological state. This suggests that the metabolic cost of egg formation should respond to selection. However, we also show that in males, but not females, repeatability of RMR declines over time even when birds are kept in constant controlled conditions.