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Metabolic rates of passerine birds are flexible traits that vary both seasonally and among and within winters. Seasonal variation in summit metabolic rates (M sum = maximum thermoregulatory metabolism) in birds is consistently correlated with changes in pectoralis muscle and heart masses and sometimes with variation in cellular aerobic metabolic intensity, so these traits might also be associated with shorter-term, within-winter variation in metabolic rates. To determine whether these mechanisms are associated with within-winter variation in M sum , we examined the effects of short-term (ST; 0-7 d), medium-term (MT; 14-30 d), and long-term (LT; 30-yr means) temperature variables on pectoralis muscle and heart masses, pectoralis expression of the muscle-growth inhibitor myostatin and its metalloproteinase activators TLL-1 and TLL-2, and pectoralis and heart citrate synthase (CS; an indicator of cellular aerobic metabolic intensity) activities for two temperate-zone resident passerines, house sparrows (Passer domesticus) and dark-eyed juncos (Junco hyemalis). For both species, pectoralis mass residuals were positively correlated with ST temperature variables, suggesting that cold temperatures resulted in increased turnover of pectoralis muscle, but heart mass showed little within-winter variation for either species. Pectoralis mRNA and protein expression of myostatin and the TLLs were only weakly correlated with ST and MT temperature variables, which is largely consistent with trends in muscle masses for both species. Pectoralis and heart CS activities showed weak and variable trends with ST temperature variables in both species, suggesting only minor effects of temperature variation on cellular aerobic metabolic intensity. Thus, neither muscle or heart masses, regulation by the myostatin system, nor cellular aerobic metabolic intensity varied consistently with winter temperature, suggesting that other factors regulate within-winter metabolic variation in these birds.

Because lipids are the main fuel supporting avian endurance activity, lipid transport and oxidation capacities may increase during migration. We measured enzyme activities, mRNA expression and protein levels in pectoralis and heart for several key steps of lipid transport and catabolism pathways to investigate whether these pathways were upregulated during migration. We used yellow-rumped (Setophaga coronata) and yellow (S. petechia) warblers and warbling vireos (Vireo gilvus) as study species because they all show migration-induced increases in organismal metabolic capacities. For yellow-rumped warblers, β-hydroxyacyl CoA-dehydrogenase (HOAD) activities and fatty acid transporter mRNA and/or protein levels were higher during spring than fall in pectoralis and heart, except that fatty acid translocase (FAT/CD36) protein levels showed the opposite pattern in heart. Lipid transporter protein levels, but not mRNA expression, in pectoralis and heart of warbling vireos were higher either during spring or fall than summer, but this was not true for HOAD activities. For yellow warblers, pectoralis, but not heart, protein levels of lipid transporters were upregulated during migration relative to summer, but this pattern was not evident for mRNA expression or HOAD activity. Finally, muscle and heart citrate synthase and carnitine palmitoyl transferase activities showed little seasonal variation for any species. These data suggest that pectoralis and heart lipid transport and catabolism capacities are often, but not universally, important correlates of elevated organismal metabolic capacity during migration. In contrast, migration-induced variation in cellular metabolic intensity and mitochondrial membrane transport are apparently not common correlates of the migratory phenotype in passerines.

Maximal metabolic outputs for exercise and thermogenesis in birds presumably influence fitness through effects on flight and shivering performance. Because both summit (Msum, maximum thermoregulatory metabolic rate) and maximum (MMR, maximum exercise metabolic rate) metabolic rates are functions of skeletal muscle activity, correlations between these measurements and their mechanistic underpinnings might occur. To examine whether such correlations occur, we measured the effects of experimental cold and exercise training protocols for 3 weeks on body (Mb) and muscle (Mpec) masses, basal metabolic rate (BMR), Msum, MMR, pectoralis mRNA and protein expression for myostatin, and mRNA expression of TLL-1 and TLL-2 (metalloproteinase activators of myostatin) in house sparrows (Passer domesticus). Both training protocols increased Msum, MMR, Mb and Mpec, but BMR increased with cold training and decreased with exercise training. No significant differences occurred for pectoralis myostatin mRNA expression, but cold and exercise increased the expression of TLL-1 and TLL-2. Pectoralis myostatin protein levels were generally reduced for both training groups. These data clearly demonstrate cross-training effects of cold and exercise in birds, and are consistent with a role for myostatin in increasing pectoralis muscle mass and driving organismal increases in metabolic capacities., (© 2015. Published by The Company of Biologists Ltd.)

Winter acclimatization in small birds living in cold climates produces a winter phenotype characterized by upregulation of metabolic rates to meet enhanced thermoregulatory demands. We measured several key aspects of fuel storage, mobilization and transport in summer and winter to determine whether black-capped chickadees (Poecile atricapillus), white-breasted nuthatches (Sitta carolinensis), and house sparrows (Passer domesticus) seasonally modulate these attributes to meet enhanced winter thermoregulatory demands. In addition, we exposed birds to thermoneutral (control) and severe cold exposure treatments to determine whether acute cold exposure influenced fuel storage, mobilization or transport. Carcass lipid mass and pectoralis intramuscular lipid did not vary significantly between seasons or temperature treatments for any of the study species. Muscle glycogen varied significantly seasonally only for chickadee supracoracoideus and leg muscles, and did not vary among warm or cold treatments for any species. Pectoralis fatty acid binding protein (FABPc) was significantly elevated in winter for chickadees and nuthatches, but not for sparrows. Plasma metabolites showed little consistent variation in response to season or acute cold exposure. Thus, fuel storage and mobilization do not appear to be major targets of adjustment associated with seasonal metabolic flexibility in these species, but modulation of intracellular lipid transport by FABPc may be an important contributor to seasonal phenotypes in some species of small birds., (Copyright © 2014 Elsevier Inc. All rights reserved.)

Abstract Cold tolerance and overwinter survival are positively correlated with organismal thermogenic capacity (=summit metabolic rate [Msum]) in endotherms. Msum varies seasonally in small-bird populations and may be mechanistically associated with variation in flight muscle size or cellular metabolic capacity, but the relative roles of these traits as drivers of individual variation in thermogenic performance are poorly known. We measured flight muscle size by ultrasonography, pectoralis and supracoracoideus muscle masses, and muscular activities of key aerobic enzymes (citrate synthase, carnitine palmitoyl transferase, and β-hydroxyacyl-CoA dehydrogenase) and correlated these measurements with Msum for individual American goldfinches (Spinus tristis) to test the hypotheses that muscle size and/or cellular metabolic capacity serve as prominent drivers of individual variation in organismal metabolic capacity. Ultrasonographic flight muscle size was weakly positively correlated with Msum ([Formula: see text]). Both log10-transformed Msum and flight muscle mass were significantly correlated with log10 body mass, so we calculated allometric residuals for log Msum and for log flight muscle mass to test their correlation independent of body mass. Flight muscle mass residuals were significantly positively correlated with Msum residuals, and this correlation was primarily driven by variation in pectoralis muscle mass. In contrast, none of the mass-specific activities of any enzyme in any muscle were significantly correlated with Msum. These data suggest that flight muscle size, not cellular metabolic capacity, is the primary driver of individual variation in thermogenic performance in goldfinches. This is consistent with the idea that phenotypic flexibility of flight muscle mass is a general mechanism mediating variation in metabolic performance in response to changing energy demands in birds.

Biogeographic analyses of passerine birds demonstrate that suboscines are numerically dominant in South America, whereas oscines are dominant elsewhere. This suggests that oscines generally outcompete suboscines and that suboscine dominance likely persists in South America because of its long isolation from other continents, where oscines have diversified. One hypothesis for oscine competitive superiority is that oscines possess higher metabolic capacities than suboscines, and this favors oscines in most habitats. We tested this hypothesis by comparing summit metabolic rates (M(sum), maximum thermoregulatory metabolic rate) between oscines and suboscines using conventional and phylogenetically informed statistical approaches. We predicted that if the metabolic-capacity hypothesis is valid, then oscines should have higher M(sum) than suboscines. Both conventional and phylogenetically informed ANCOVA on regressions of log M(sum) against log mass showed that oscines had higher M(sum) than suboscines: least squares mean M(sum) was 74% greater for oscines. Moreover, conventional and phylogenetically informed multiple regressions identified log mass, winter-range temperature, and clade (oscines vs. suboscines) as significant effectors of log M(sum). Thus, oscines have generally higher M(sum) than suboscines, which is consistent with the metabolic-capacity hypothesis and suggests that metabolic capacity is one factor influencing the evolution of broad biogeographical patterns in passerines.

We analyzed and compared the scaling of both basal and maximal thermogenic metabolic rates in passerine and nonpasserine birds using conventional and phylogenetic methods. In spite of the presumed adaptive importance of both metabolic traits, few studies concerning both their relationships and their ecological and evolutionary constraints have been conducted. We found no statistical differences in the scaling of maximal metabolic rate between passerines and nonpasserines; hence, we suggest the use of a single allometric regression for this trait in birds. In addition, basal and maximal metabolic rates were indeed correlated after removing the effects of body mass and phylogeny. The apparent generality of this correlation within both birds and mammals reinforces the need for general ecological and physiological explanations for the evolution of endothermy.