How does mitochondrial function relate to thermogenic capacity and basal metabolic rate in small birds?

We investigated the role of mitochondrial function in the avian thermoregulatory response to a cold environment. Using black-capped chickadees (Poecile atricapillus) acclimated to cold (-10°C) and thermoneutral (27°C) temperatures, we expected to observe an upregulation of pectoralis muscle and liver respiratory capacity that would be visible in mitochondrial adjustments in cold-acclimated birds. We also predicted that these adjustments would correlate with thermogenic capacity (Msum) and basal metabolic rate (BMR). Using tissue high-resolution respirometry, mitochondrial performance was measured as respiration rate triggered by proton leak and the activity of complex I (OXPHOSCI) and complex I+II (OXPHOSCI+CII) in the liver and pectoralis muscle. The activity of citrate synthase (CS) and cytochrome c oxidase (CCO) was also used as a marker of mitochondrial density. We found 20% higher total CS activity in the whole pectoralis muscle and 39% higher total CCO activity in the whole liver of cold-acclimated chickadees relative to that of birds kept at thermoneutrality. This indicates that cold acclimation increased overall aerobic capacity of these tissues. Msum correlated positively with mitochondrial proton leak in the muscle of cold-acclimated birds while BMR correlated with OXPHOSCI in the liver with a pattern that differed between treatments. Consequently, this study revealed a divergence in mitochondrial metabolism between thermal acclimation states in birds. Some functions of the mitochondria covary with thermogenic capacity and basal maintenance costs in patterns that are dependent on temperature and body mass.

Wintering Snow Buntings Elevate Cold Hardiness to Extreme Levels but Show No Changes in Maintenance Costs.

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 [Msum]), thermogenic endurance (time to reach Msum), and cold tolerance (temperature at Msum). 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 Msum (27%). We also found remarkable cold tolerance in these birds, with individuals reaching Msum 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.

Large muscles are beneficial but not required for improving thermogenic capacity in small birds.

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 (Msum) 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 Msum, 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, Msum 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.

Estimation of Muscle Mass by Ultrasonography Differs between Observers and Life States of Models in Small Birds.

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.

Individual inconsistencies in basal and summit metabolic rate highlight flexibility of metabolic performance in a wintering passerine.

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.

Lipid metabolites as markers of fattening rate in a non-migratory passerine: effects of ambient temperature and individual variation.

Plasma lipid metabolites triglycerides (TRIG) and glycerol (GLY) are used as indicators of fattening rate and nutritional condition in migratory birds. Requiring only one blood sample, they could also be used for studying daily and seasonal fattening rates in relation with habitat quality or weather variations in species wintering in cold climates. Using black-capped chickadees exposed to three experimental temperatures (0 °C, 15 °C, and 30 °C), the goal of this experiment was to determine the relationship between plasma levels of TRIG and GLY and fattening rate measured over periods from a few hours to the previous two days. Results showed that birds maintained in the cold had metabolite levels 39-81% higher than those at thermoneutrality, likely reflecting the size of their fat reserves, and that TRIG and total GLY were highly correlated across treatments. Fattening rate was also higher at 0 °C (+35%) and 30 °C (+24%) relative to that measured at 15 °C and, as expected, was positively correlated with metabolite levels across treatments. However, despite fattening rates similar to that observed at the other temperatures, the relationships were uncoupled at 30 °C, implying that the technique may not be easily applicable at temperatures within or close to thermoneutrality. We also found a strong individual effect in the relationships between fattening rate and TRIG levels, suggesting high individual consistency in these parameters in conditions of unrestricted food access such as in captivity. Our study confirms that plasma TRIG and GLY levels can be used as relative indexes of condition and fattening rates in wintering passerines.

Energy expenditure of freely swimming adult green turtles (Chelonia mydas) and its link with body acceleration.

Marine turtles are globally threatened. Crucial for the conservation of these large ectotherms is a detailed knowledge of their energy relationships, especially their at-sea metabolic rates, which will ultimately define population structure and size. Measuring metabolic rates in free-ranging aquatic animals, however, remains a challenge. Hence, it is not surprising that for most marine turtle species we know little about the energetic requirements of adults at sea. Recently, accelerometry has emerged as a promising tool for estimating activity-specific metabolic rates of animals in the field. Accelerometry allows quantification of the movement of animals (ODBA/PDBA, overall/partial dynamic body acceleration), which, after calibration, might serve as a proxy for metabolic rate. We measured oxygen consumption rates (V(O(2))) of adult green turtles (Chelonia mydas; 142.1±26.9 kg) at rest and when swimming within a 13 m-long swim channel, using flow-through respirometry. We investigated the effect of water temperature (T(w)) on turtle and tested the hypothesis that turtle body acceleration can be used as a proxy for V(O(2)). Mean mass-specific V(O(2)) (sV(O(2))) of six turtles when resting at a T(w) of 25.8±1.0°C was 0.50±0.09 ml min(-1) kg(-0.83). sV(O(2))increased significantly with T(w) and activity level. Changes in sV(O(2)) were paralleled by changes in respiratory frequency (f(R)). Deploying bi-axial accelerometers in conjunction with respirometry, we found a significant positive relationship between sV(O(2)) and PDBA that was modified by T(w). The resulting predictive equation was highly significant (r(2)=0.83, P<0.0001) and associated error estimates were small (mean algebraic error 3.3%), indicating that body acceleration is a good predictor of V(O(2)) in green turtles. Our results suggest that accelerometry is a suitable method to investigate marine turtle energetics at sea.