Phenotype manipulations confirm the role of pectoral muscles and haematocrit in avian maximal thermogenic capacity

Abstract

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 (Ṁ sum , a measure of maximal shivering thermogenic capacity). However, evidence suggesting that pectoral muscle size influences Ṁ sum is correlational and the link between haematrocrit level and Ṁ sum remains to be demonstrated. We experimentally tested the relationship between pectoral muscle size and Ṁ sum 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, Ṁ sum 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 Ṁ sum was up to 16% higher in birds expressing large pectoral muscles. Ṁ sum 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 Ṁ sum in black-capped chickadees and that oxygen carrying capacity likely supports thermogenesis in this species.

Relationships between interspecific differences in the mass of internal organs, biochemical markers of metabolic activity, and the thermogenic properties of three small passerines

“…This finding is in agreement with the results of our previous studies which show that seasonal and latitudinal variation in Eurasian Tree Sparrows was correlated not only with variation in BMR, but also in state-4 respiration and COX activity in the liver (Zheng et al 2008b(Zheng et al , 2014b. Because skeletal muscle mass comprises nearly 40 % of M b , it is an important contributor to thermogenesis via shivering, and even nonshivering thermogenesis (Bicudo et al 2001;Pitit and Vézina 2014). Furthermore, adjustment of cellular aerobic capacity in muscle potentially involves modulation of the activities of key catabolic enzymes in oxidative pathways, and, or, the activities of enzymes and transporters involved in substrate mobilization and delivery pathways (Marsh et al 1990;Swanson 2010;Zheng et al 2008bZheng et al , 2014a.…”

Reaction Norms in Natural Conditions: How Does Metabolic Performance Respond to Weather Variations in a Small Endotherm Facing Cold Environments?

“…For example, pectoral muscles could be at their maximal size preventing further increases in shivering capacity at temperatures below −10°C [16], [17]. Hence, to face temperature colder than −10°C, birds would have to use strategies such as microhabitat selection [53] or hypothermia [49], [54] to compensate for the lack of endogenous heat production.…”

“…Winter metabolic phenotypes, reflecting individual rates of energy use, are commonly studied to understand individual performance and are measured through variables such as basal and summit metabolic rates (BMR and Msum, respectively). BMR is interpreted as the minimal maintenance energy cost of an animal and is thought to reflect metabolic activity of resting muscles and internal organs [14], [15] while Msum is a measure of the cold-induced maximal heat production that is thought to reflect maximal shivering capacity of skeletal muscles [16], [17]. In small endotherms, both these parameters are typically elevated in winter relative to summer [18], [19].…”

Mechanistic Drivers of Flexibility in Summit Metabolic Rates of Small Birds

“…However, these increments may be a by-product of adjustments for endurance flight rather than for thermogenesis [22], [24], although thermogenic benefits may accrue nonetheless. Indeed, Petit and Vézina [25] recently demonstrated experimentally that increasing flight costs of black-capped chickadees ( Poecile atricapillus ) improved thermogenic performance and M sum . Collectively, these studies show that M sum is a flexible physiological trait that varies in a manner consistent with expected fitness consequences.…”

“…Several studies have examined seasonal variation in skeletal muscle and heart masses, and these studies typically find larger pectoralis and heart muscle masses in winter relative to summer [17], [27]–[31], although this generalization is not without exceptions [32], [33]. In addition, correlations of residual variation in pectoralis muscle size with residual variation in M sum for individual birds are generally positive [23]–[25], [34], [35]. Similarly, pectoralis muscle mass is also positively associated with maximum exercise-induced metabolic rates in birds [36], [37].…”