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AbstractResident temperate passerines adjust their phenotypes to cope with winter constraints, with peak performance in metabolic traits typically occurring during the coldest months. However, it is sparsely known whether cold-adapted northern species make similar adjustments when faced with variable seasonal environments. Life in near-constant cold could be associated with limited flexibility in traits underlying cold endurance. We investigated this by tracking individual physiological changes over five consecutive winters in snow buntings ( Plectrophenax nivalis ), an Arctic-breeding migratory passerine typically confronted with nearly constant cold. Buntings were held in an outdoor aviary and exposed to seasonal temperature variation typical of temperate zone climates. We measured phenotypic changes in body composition (body, fat, and lean mass, pectoralis muscle thickness), oxygen transport capacity (hematocrit), metabolic performance (basal metabolic rate [BMR] and summit metabolic rate [ M sum ]), thermogenic endurance (time to reach M sum ), and cold tolerance (temperature at M sum ). Snow buntings showed flexibility in functions underlying thermogenic capacity and cold endurance comparable to that observed in temperate resident passerines wintering at similar latitudes. Specifically, they increased body mass (13%), fat mass (246%), hematocrit (23%), pectoralis muscle thickness (8%), and M sum (27%). We also found remarkable cold tolerance in these birds, with individuals reaching M sum in helox at temperatures equivalent to less than -90°C in air. However, in contrast with resident temperate passerines, lean mass decreased by 12%, and there was no clear increase in maintenance costs (BMR). Our results show that the flexibility of traits underlying thermal acclimatization in a cold-adapted northern species is comparable to that of temperate resident species living at lower latitudes and is therefore not limited by life in near-constant cold.

Food availability might sometimes be unpredictable for wild birds. To alleviate this possible food limitation, millions of households in North America provide food supplementation to bird populations. However, the ecoimmunological impacts of this supplementation on free-living birds are largely unclear. Therefore, we compared immune function and body composition of three groups of free-living black-capped chickadees (Poecile atricapillus) that were provided either constant food supplementation ("supplemented"), interrupted food supplementation ("interrupted"), or no food supplementation ("unsupplemented"). At capture, all three groups had similar body mass and fat scores. All three groups also had similar levels of circulating immunoglobulin Y antibodies and complement lysis ability, two measures of constitutive immune function. Supplemented and interrupted groups mounted a somewhat similar body mass and temperature response to injection with lipopolysaccharide; however, the supplemented group had a higher haptoglobin (acute-phase protein) response to lipopolysaccharide injection compared to the interrupted group. This study demonstrates that birds maintained similar levels of fat despite their level of food supplementation; however, sudden removal of supplemental food might elicit a short-term decline in aspects of immunity. Future studies should investigate how food supplementation might impact induced or adaptive aspects of immune function to add to our understanding of immunology in free-living animals.

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.

In winter, temperate resident birds are often faced with periodic low natural food availability. This reduction or unpredictability in resource availability might then have a negative impact on immune function, given that immune system support is highly resource dependent. We investigated the balance between energetic and immune management in captive black-capped chickadees (Poecile atricapilus) by manipulating the predictability of resources. The control group received food ad lib. every day, while the experimental group received a reduced amount of food on random days and food ad lib. on all other days. We measured two key metrics of energetic management (body and fat mass) as well as a suite of immune system components. Compared with control birds, experimental birds maintained significantly higher total body and fat mass, had lower acute phase protein concentrations, and had decreased body temperature and lost more body mass during the fever response following injection with lipopolysaccharides. Interestingly, birds in both groups had similar levels of complement lysis, delayed-type hypersensitivity response (phytohemagglutinin), and primary antibody production (keyhole limpet hemocyanin). This experiment demonstrates that black-capped chickadees strategically increase their fat mass in response to decreased food availability and that this might allow the birds to maintain most of the immune system unaltered, except some of the most costly immune components.

Avian basal metabolic rate (BMR) and summit metabolic rate (M sum ) vary in parallel during cold acclimation and acclimatization, which implies a functional link between these variables. However, evidence suggests that these parameters may reflect different physiological systems acting independently. We tested this hypothesis in white-throated sparrows (Zonotrichia albicollis) acclimated to two temperatures (-8° and 28°C) and two diets (0% and 30% cellulose). We expected to find an uncoupling of M sum and BMR where M sum , a measure of maximal shivering heat production, would reflect muscle and heart mass variation and would respond only to temperature, while BMR would reflect changes in digestive and excretory organs in response to daily food intake, responding to both temperature and diet. We found that the gizzard, liver, kidneys, and intestines responded to treatments through a positive relationship with food intake. BMR was 15% higher in cold-acclimated birds and, as expected, varied with food intake and the mass of digestive and excretory organs. In contrast, although M sum was 19% higher in cold-acclimated birds, only heart mass responded to temperature (+18% in the cold). Pectoral muscles did not change in mass with temperature but were 8.2% lighter on the cellulose diet. Nevertheless, M sum varied positively with the mass of heart and skeletal muscles but only in cold-acclimated birds. Our results therefore suggest that an upregulation of muscle metabolic intensity is required for cold acclimation. This study increases support for the hypothesis that BMR and M sum reflect different physiological systems responding in parallel to constraints associated with cold environments.

Ultrasonography has proven to be a valuable noninvasive method of measure of muscle size in birds, but validation of its use in birds as small as black-capped chickadees (Poecile atricapillus; 11 g) is scarce. The effect of observers and life state (dead or alive) of models used for calibration on measurement quality is also poorly documented. Using 31 dead and 22 live chickadees, linear regressions between ultrasound and dissection measurements of pectoral and thigh muscles were fitted and compared between five different observers. R(2) values varied greatly between observers and were generally weaker in live birds, ranging between 0.02 and 0.59, despite high repeatability of measurement. Using equations calculated from dead birds to estimate muscle mass of live birds yielded much higher measurement errors (9%-18%) than when using equations calculated from live birds (5%-8%). Our results suggest that with careful training and using only calibration from live birds, ultrasonography can be a useful but limited tool to estimate muscle size of birds as small as the black-capped chickadee.

Abstract Small avian species wintering at northern latitudes typically show increases in basal metabolic rate (BMR) and maximal thermogenic capacity (Msum). Those are widely assumed to reflect changes in body composition, with enlargement of digestive and excretory organs resulting in elevated winter BMR and larger body muscles driving the increase in Msum. Using free-living black-capped chickadees (Poecile atricapillus) as our model species, we investigated seasonal changes in body composition and tested for relationships between mass variations of body organs and variability of both BMR and Msum. Our results confirmed the expected winter increase in mass of body muscles and cardiopulmonary organs (heart + lungs) and showed that 64% of the observed Msum variations throughout the year were explained by changes in these organs. In contrast, we found little support for an effect of the digestive organs (gizzard + intestines) on BMR seasonal changes. Instead, this variable was mainly influenced by variations in mass of body muscles and excretory organs (liver + kidney), explaining up to 35% of its variability.

Previous experiments showed reduction of basal metabolic rate (BMR) in birds facing energetic challenges. We alternately exposed two groups of red knots (Calidris canutus) to either 6 h or 22 h of food availability for periods of 22 d. Six h of access to food led to a 6%-10% loss of body mass over the first 8 d, with nearly all of the birds' daily energy expenditures supported by body nutrient stores during the first 2 d. Birds responded by increasing feeding behavior and food intake, but the response was slow. There were no gains of mass before day 15, which suggests a digestive bottleneck and a period of physiological adjustment. Food-restricted birds exhibited decreases in pectoral-muscle thickness and BMR in association with a loss of body mass. Although a decrease in BMR saves energy, savings represented only 2%-7% of the daily energy spent in excess of that acquired during the deficit period. Red knots did not downregulate mass-independent BMR. On the bases of recent independent findings and the pattern of mass gain observed when food access was switched from 6 h to 22 h, we suggest that these birds routinely maintain nutrient stores as a buffer against periods of energy shortages, thereby precluding the need for downregulation of mass-independent BMR.

In response to unbalanced energy budgets, animals must allocate resources among competing physiological systems to maximize fitness. Constraints can be imposed on energy availability or energy expenditure, and adjustments can be made via changes in metabolism or trade-offs with competing demands such as body-mass maintenance and immune function. This study investigates changes in constitutive immune function and the acute-phase response in shorebirds (red knots) faced with limited access time to food. We separated birds into two experimental groups receiving either 6 h or 22 h of food access and measured constitutive immune function. After 3 wk, we induced an acute-phase response, and after 1 wk of recovery, we switched the groups to the opposite food treatment and measured constitutive immune function again. We found little effect of food treatment on constitutive immune function, which suggests that even under resource limitation, a baseline level of immune function is maintained. However, birds enduring limited access to food suppressed aspects of the acute-phase response (decreased feeding and mass loss) to maintain energy intake, and they downregulated thermoregulatory adjustments to food treatment to maintain body temperature during simulated infection. Thus, under resource-limited conditions, birds save energy on the most costly aspects of immune defense.

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.

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.

Body composition in vertebrates is known to show phenotypic plasticity, and changes in organ masses are usually rapid and reversible. One of the most rapid and reversible changes is the transformation of the female avian reproductive organs before breeding. This provides an excellent system to investigate the effects of plasticity in organ size on basal metabolic rate (BMR) through relationships between organ masses and BMR. We compared body composition of female European starlings (Sturnus vulgaris) during various reproductive stages over 3 yr and investigated the pattern of changes in reproductive and nonreproductive organ mass during follicular development and ovulation. Furthermore, we analyzed the relationship between organ mass and resting metabolic rate (RMR) in nonbreeding, laying, and chick-rearing females. Our analysis revealed marked variation in organ masses between breeding stages but no consistent pattern among years except for kidney and pectoralis muscle. Furthermore, changes in nonreproductive organs did not parallel the cycle of growth and regression of the reproductive organs. The oviduct gained 62% of its 22-fold increase in mass in only 3 d, and oviduct regression was just as rapid and began even before the final egg of the clutch was laid, with 42% of the oviduct mass lost before laying of the final egg. In laying females, 18% of variation in mass-corrected RMR was explained by the mass of the oviduct (r2=0.18, n=80, P<0.0005), while pectoralis muscle mass in nonbreeding individuals and liver and gizzard mass in chick-rearing females were the only organs significantly related to RMR (r2=0.31-0.44). We suggest that the nonreproductive organs are affected more by changes in local ecological conditions than the reproductive state itself and that the activity and maintenance cost of the oviduct is high enough that selection has led to a very tight size-function relationship for this organ.

The energy cost of egg production in passerine birds has typically been estimated to be 45%-60% of basal metabolic rate (BMR), but this is based on theoretical models using data on energy content of eggs and reproductive tissue; there are still very few empirical data on egg production costs. In this study, we directly measured resting metabolic rate (RMR) in egg-laying female European starlings (Sturnus vulgaris) over 3 yr. We compared these data with RMR of nonbreeding and chick-rearing birds and with estimated energy expenditure generated from a typical energy content model by using empirically derived data from body composition analysis for this species. We found marked variation in RMR between years and between reproductive stages, which complicates comparisons among breeding stages for the assessment of relative egg production costs. On the basis of this method, RMR during egg laying varied from +74% to -13% of nonbreeding RMR and from +20% to -7% of chick-rearing RMR. We therefore used an alternate approach: measuring changes in RMR through the complete cycle of follicle development and ovulation. The increase in RMR from the beginning of prelaying to the six-follicle stage (before first ovulation) when birds have a complete developing follicle hierarchy was 22.4%. This value is still much lower than that estimated from our energy content model. We discuss conceptual problems associated with the theoretical energy content approach but also suggest, on the basis of earlier work done in our lab, that the measured increase in RMR might still underestimate the actual cost of egg production if birds reallocate energy between different physiological systems.

We investigated the quantitative matching of plasma yolk precursor supply (the plasma pool) to follicle demand during yolk formation in European starlings (Sturnus vulgaris). Plasma concentrations of the two yolk precursors, vitellogenin (VTG) and very low density lipoprotein (VLDL), were only elevated coincident with rapid yolk development (RYD) and matched variation in total yolky follicle mass. VTG and VLDL were low (<0.4 microg/mL and <4.2 mg/mL, respectively) in nonbreeders and prebreeders with no yolky follicles, and at clutch completion. They increased to 4.02 microg/mL and 19.4 mg/mL in birds with a full follicle hierarchy (F1-F4), and concentrations then remained high and actually increased up to the point where only a single, yolky (F1) follicle remained. However, there was some evidence for mismatching of supply and demand: (a) precursor concentrations increased throughout the laying cycle even though the number of developing follicles decreased. We suggest that this is because of a requirement to maintain a large precursor pool to maintain high uptake rates; and (b) in birds with a full follicle hierarchy, precursor concentrations were negatively correlated with total follicle mass. This suggests that high uptake rates in large follicles can actually deplete circulating precursor concentrations. Plasma concentrations of both yolk precursors increased rapidly in the early morning with (predicted) time after ovulation, consistent with a lack of fine control of precursor concentrations. However, mean plasma VTG concentrations did not differ between morning or evening samples. In contrast, plasma VLDL concentrations were lower in the morning (16.8 mg/mL) than in the evening (22.9 mg/mL). Although there is marked individual variation in plasma VTG and VLDL (four- to eightfold), both precursors were repeatable in the short term (24 h), and plasma VTG was repeatable over a 14-d interval between successive breeding attempts.

Studies of wintering birds have demonstrated a correlation between social rank and energy expenditures. It is assumed that dominance is energetically costly because of increased activity, possibly caused by elevated androgen levels. As winter acclimatization leads to an increase in metabolic rate, maintaining dominance status in a cold climate can be a substantial challenge. We measured resting metabolic rates in dominant and subordinate dark-eyed juncos (Junco hyemalis) living in small groups in a controlled winter environment. We found no significant effect of social rank when controlling for body size. It has been shown previously that high testosterone levels during the nonbreeding season can lead to higher body conductance, fat loss, and higher nocturnal body temperature. A hypothesis explaining our result is that for juncos it is preferable to maintain low androgen levels during winter and to maintain social rank using a mechanism other than higher agonistic activity.