Multi-level variation of instantaneous metabolism across activity and time in a songbird

ROSENMANN, MARIO, AND PETER MORRISON. Maximum oxygen consumption and heat loss facilitation in small homeotherms by He-02 . Am. J. Physiol. 226(3) : 490495. 1974.-The high thermal conductance of an 80% He-20y0 02 atmosphere was used to elicit maximum metabolism (Mmax) in moderate cold in species ranging from 7-g pygmy mice (Baiomys taylori) to 250-g white rats, including redpolls (Acanthis J?ammea), two vesper mice (Calomys d&la, C. callosus), tundra voles (Microtus oeconomus), and four strains of Mus musculus. Values slightly exceeded those in similar animals using other methods to confirm the low metabolic ratio (Mmax/M, in) in rodents (4-8 X). Submaximal values at higher temperatures defined thermal conductance in He-02 and air. In different species the ratios of these conductances ranged from 1.4 to 2.6, differences which relate to the extent and quality of the respective insulation. M,,, was obtained at 13-70°C warmer in He-02 than required in air for the same metabolic effort. Avoidance of low-temperature technology and freezing injury, elimination of treadmills and training in running, prompt attainment of M,,., (3-10 min after He-02 exposure), and obviation of shaving or wetting procedures are advantages of the present technique.

Physiological processes vary widely across individuals and can influence how individuals respond to environmental change. Repeatability in how metabolic rate changes across temperatures (i.e. metabolic thermal plasticity) can influence mass‐scaling exponents in different thermal environments. Moreover, repeatable plastic responses are necessary for reaction norms to respond to selective forces which is important for populations living in fluctuating environments. Nonetheless, only a small number of studies have explicitly quantified repeatability in metabolic plasticity, and fewer have explored how it can impact mass‐scaling. We repeatedly measured standard metabolic rate of n = 42 delicate skinks Lampropholis delicata at six temperatures over the course of four months ( N [observations] = 4952). Using hierarchical statistical techniques, we accounted for multi‐level variation and measurement error in our data in order to obtain more precise estimates of reaction norm repeatability and mass‐scaling exponents at different acute temperatures. Our results show that individual differences in metabolic thermal plasticity were somewhat consistent over time (R slope = 0.25, 95% CI = 2.48 × 10 −8 – 0.67), however estimates were associated with a large degree of error. After accounting for measurement error, which decreased steadily with temperature, we show that among individual variance remained consistent across all temperatures. Congruently, temperature specific repeatability of average metabolic rate was stable across temperatures. Cross‐temperature correlations were positive but were not uniform across the reaction norm. After taking into account multiple sources of variation, our estimates for mass‐scaling did not change with temperature and were in line with published values for snakes and lizards. This implies that repeatable plastic responses may promote thermal stability of scaling exponents. Our work contributes to understanding how energy expenditure scales with abiotic and biotic factors and the capacity for reaction norms to respond to selection.

Summary 1 Classical evolutionary theory states that senescence should arise as a consequence of the declining force of selection late in life. Although the quantitative genetic predictions of hypotheses derived from this theory have been extensively tested in laboratory studies of invertebrate systems, relatively little is known about the genetics of ageing in the wild. 2 Data from long-term ecological studies is increasingly allowing quantitative genetic approaches to be used in studies of senescence in free-living populations of vertebrates. We review work to date and argue that the patterns are broadly consistent with theoretical predictions, although there is also a clear need for more empirical work. 3 We argue that further advances in this field of research might be facilitated by increased use of reaction norm models, and a decreased emphasis on attempting to discriminate between mutation accumulation and antagonistic pleiotropy models of senescence. We also suggest a framework for the better integration of environmental and genetic effects on ageing. 4 Finally, we discuss some of the difficulties in applying quantitative genetic models to studies of senescence outside the laboratory. In particular we highlight the problems that viability selection can cause for an accurate estimation of parameters used in the prediction of age-trajectory evolution.

The Relationship between Summated Tissue Respiration and Metabolic Rate in the Mouse and Dog

SummaryLife history theory predicts that available energy is limited and needs to be allocated among different processes such as growth, reproduction and self‐maintenance. Basal metabolic rate (BMR), a common measure of an animal's maintenance cost, is therefore believed to be a trait of ecological and evolutionary significance. However, althoughBMRis often assumed to be correlated with fitness, its association with individual variation in fitness in free‐living populations is virtually unknown.We examined the relationship betweenBMRin late winter prior to the breeding season and recruit production (number of offspring recorded the subsequent year), as well as adult survival, in two populations of house sparrow (Passer domesticus) on the islands Leka and Vega in northern Norway.Number of recruits tended to be negatively related toBMR. However, analysing the data for each sex within the two populations revealed that the negative effect ofBMRon recruit production was significant only for females in the Vega population.Survival probability was associated withBMR, but the relationship differed both between sexes and populations. In the Leka population, we found evidence for stabilizing selection in the females and disruptive selection in the males. In contrast, there was no effect ofBMRon survival in the Vega population.Body mass influenced adult survival, but not recruit production. Furthermore, the relationship betweenBMRand fitness in females remained significant after controlling for body mass. Thus, the selection onBMRin females was not driven by aBMR‐body mass correlation.Basal metabolic rate was significantly related to fitness in both populations. However, the results in the present study show spatial variation as well as sex specific differences in the influence ofBMRon fitness in house sparrows.

Synopsis The climatic variability hypothesis (CVH) posits that more flexible phenotypes should provide a fitness advantage for organisms experiencing more variable climates. While typically applied across geographically separated populations, whether this principle applies across seasons or other conditions (e.g., open vs. sheltered habitats) which differ in climatic variability remains essentially unstudied. In north-temperate climates, climatic variability in winter usually exceeds that in summer, so extending the CVH to within-population seasonal variation predicts that winter phenotypes should be more flexible than summer phenotypes. We tested this prediction of the within-season extension of the CVH by acclimating summer and winter-collected house sparrows (Passer domesticus) to 24, 5, and −10°C and measuring basal metabolic rate (BMR) and summit metabolic rate (Msum = maximum cold-induced metabolic rate) before and after acclimation (Accl). To examine mechanistic bases for metabolic variation, we measured flight muscle and heart masses and citrate synthase and β-hydroxyacyl coA-dehydrogenase activities. BMR and Msum were higher for cold-acclimated than for warm-acclimated birds, and BMR was higher in winter than in summer birds. Contrary to our hypothesis of greater responses to cold Accl in winter birds, metabolic rates generally decreased over the Accl period for winter birds at all temperatures but increased at cold temperatures for summer birds. Flight muscle and heart masses were not significantly correlated with season or Accl treatment, except for supracoracoideus mass, which was lower at −10°C in winter, but flight muscle and heart masses were positively correlated with BMR and flight muscle mass was positively correlated with Msum. Catabolic enzyme activities were not clearly related to metabolic variation. Thus, our data suggest that predictions of the CVH may not be relevant when extended to seasonal temperature variability at the within-population scale. Indeed, these data suggest that metabolic rates are more prominently upregulated in summer than in winter in response to cold. Metabolic rates tended to decrease during Accl at all temperatures in winter, suggesting that initial metabolic rates at capture (higher in winter) influence metabolic Accl for captive birds.

We evaluated the relationship between organ mass and the limits to aerobic metabolism in house sparrows Passer domesticus. The results were used to test three models of performance limitation (the central limitation, peripheral limitation and symmorphosis concepts). Basal metabolic rate (BMR) was determined during the rest phase. The maximum rate of oxygen consumption during exercise ( v_dot (O2max)) was measured in an enclosed wheel that allowed limited hovering flight. Neither BMR nor v_dot (O2max) was affected by gender, but adults had significantly higher v_dot (O2max) and lower BMR than juveniles. The masses of most central organs (gut, gizzard, liver, heart, kidney and reproductive organs) differed significantly between ages. There were no gender differences in organ mass among juveniles, but liver mass differed between male and female adults. In the pooled data, BMR was positively correlated with the mass of three central organs (gut, liver and kidney) and with one peripheral effector (breast muscle); together, these explained more than half the variance in BMR (r(2)=0.57). In adults, BMR was positively correlated with the mass of reproductive tissue. The masses of one peripheral effector (breast muscle) and one central organ (the heart) were positively correlated with v_dot (O2max) (r(2)=0.17 for the pooled data set). These results are consistent with a symmorphosis model of aerobic capacity. We found a significant positive relationship between BMR and v_dot (O2max) in juveniles, but not in adults. Taken together, our data indicate that house sparrows can achieve elevated v_dot (O2max) without paying a 'penalty' (fitness trade-off) in the form of an increased BMR.

Phenotypic plasticity is an important mechanism that allows populations to adjust to changing environments. Early life experiences can have lasting impacts on how individuals respond to environmental variation later in life (i.e., individual reaction norms), altering the capacity for populations to respond to selection. Here, we incubated lizard embryos (Lampropholis delicata) at two fluctuating developmental temperatures (cold = 23 ºC + / − 3 ºC, hot = 29 ºC + / − 3 ºC, ncold = 26, nhot = 25) to understand how it affected metabolic plasticity to temperature later in life. We repeatedly measured individual reaction norms across six temperatures 10 times over ~ 3.5 months (nobs = 3,818) to estimate the repeatability of average metabolic rate (intercept) and thermal plasticity (slope). The intercept and the slope of the population-level reaction norm was not affected by developmental temperature. Repeatability of average metabolic rate was, on average, 10% lower in hot incubated lizards but stable across all temperatures. The slope of the thermal reaction norm was overall moderately repeatable (R = 0.44, 95% CI = 0.035 – 0.93) suggesting that individual metabolic rate changed consistently with short-term changes in temperature, although credible intervals were quite broad. Importantly, reaction norm repeatability did not depend on early developmental temperature. Identifying factors affecting among-individual variation in thermal plasticity will be increasingly more important for terrestrial ectotherms living in changing climate. Our work implies that thermal metabolic plasticity is robust to early developmental temperatures and has the capacity to evolve, despite there being less consistent variation in metabolic rate under hot environments.

Summary Metabolic rates can vary as much as threefold among individuals of the same size and age in a population, but why such variation persists is unclear given that they determine the energetic cost of living. Relationships between standard metabolic rate (SMR), growth and survival can vary with environmental conditions, suggesting that the fitness consequences of a given metabolic phenotype may be context‐dependent. Less attention has focused on the link between absolute aerobic scope (AS, the difference between standard and maximum metabolic rate) and fitness under different environmental conditions, despite the importance of aerobic scope to an organism's total energetic capacity. We examined the links between individual variation in both SMR and AS and somatic growth rates of brown trout (Salmo trutta) under different levels of food availability. Standard metabolic rate and AS were uncorrelated across individuals. However, SMR and AS not only had interactive effects on growth, but these interactions depended on food level: at ad libitum food levels, AS had a positive effect on growth whose magnitude depended on SMR; at intermediate food levels, AS and SMR had interactive effects on growth, but at the low food level, there was no effect of either AS or SMR on growth. As a result, there was no metabolic phenotype that performed best or worst across all food levels. These results demonstrate the importance of aerobic scope in explaining somatic growth rates and support the hypothesis that links between individual variation in metabolism and fitness are context‐dependent. The larger metabolic phenotype and the environmental context in which performance is evaluated both need to be considered in order to better understand the link between metabolic rates and fitness and thereby the persistence of individual variation in metabolic rates.

High levels of anthropogenic noise produced in urban areas are known to negatively affect wildlife. Although most research has been focused on the disturbances of communication systems, chronic noise exposure can also lead to physiological and behavioural changes that have strong consequences for fitness. For instance, behavioural changes mediated by anthropogenic noise (e.g. quality of parental care) may alter development and could influence nestling phenotype. We tested if nestling metabolism was influence by traffic noise in an urban exploiter, the house sparrow Passer domesticus . We experimentally exposed breeding house sparrows from a rural area to a playback of traffic noise and we examined the impacts of this experimental procedure on metabolic rates and morphology of nestlings. We did not find an effect of traffic noise on the morphology of nestlings. Surprisingly, we found that disturbed nestlings had overall lower metabolic rates and mass‐adjusted metabolic rates than undisturbed birds. Our results suggest a specific effect of noise exposure per se, rather than an indirect effect of anthropogenic noise through the quality of parental care. Both the proximate mechanisms and the ultimate consequences of such metabolic changes on nestlings remain unknown and deserve future experimental studies.

Two classes of explanations for covariation between activity level and metabolic rate among conspecifics have been proposed. First, individual-level variation in activity exhibited during the measurement of metabolic rate should covary with routine metabolic rate because movement increases respiration (a methodological relationship). Second, energetic-based hypotheses posit relationships between individual activity measured under more natural conditions and baseline measures of metabolic rate, among other behavioral, physiological, and life-history traits (functional relationships). Here, we examined these potential relationships between individual behavior and metabolic rate in the mud crab (Panopeus herbstii). Specifically, we tested for (1) an effect of crab activity in metabolic chambers (activitychamber) on routine metabolic rate (RMR), and (2) an effect of crab activity in mesocosms that mimicked field conditions (activitymesocosm) on standard metabolic rate (SMR). To test for context dependence, we assessed both activity-metabolic rate relationships in the absence and presence of predation threat from toadfish (Opsanus tau) in the form of waterborne chemical cues. Individual variation in activitymesocosm and RMR was repeatable over time. In support of a methodological relationship, individual differences in RMR were partially explained by crab activitychamber. After accounting for this methodological relationship, individual SMR was inversely related to activitymesocosm, supporting an allocation model that predicts behavior and baseline metabolic rate compete for finite energy reserves. We found no evidence of context dependence in either activity-metabolic rate relationship. Thus, our study emphasizes the importance of considering methodological artifacts in elucidating functional relationships between individual behavior and energetics.

Physiological diversity: listening to the large‐scale signal

We investigated inter-individual variation in metabolism, swimming performance and the relationship between metabolism and swimming performance under normoxic and hypoxic oxygen conditions ([O2]) in juvenile black carp (Mylopharyngodon piceus). We measured the standard metabolic rate (SMR), critical swimming speed (Ucrit), active metabolic rate (AMR) and aerobic scope (AS) of 40 fish (body weight, 9.7–11.0 g; body length, 8.4–8.8 cm) at 20 °C under normoxic (100% air saturation) and hypoxic (30% air saturation) conditions. Hypoxia resulted in a significant decrease in all the investigated parameters (p < 0.05). The SMR, Ucrit and AMR exhibited consistent individual differences (repeatability) (p ≤ 0.022), whereas the AS had no consistency across different water [O2] conditions (p = 0.088). The SMR was positively correlated with the Ucrit, AMR and AS (p ≤ 0.002) under normoxic conditions. The SMR was also positively correlated with the Ucrit and AMR under hypoxic conditions (p ≤ 0.003) but there was no correlation between the SMR and AS (p = 0.141). The slope of the correlation between the SMR and Ucrit was shallower under hypoxic conditions than under normoxic conditions (F1,76 = 13.844, p < 0.001), which indicated that the swimming performance decreased more profoundly under hypoxic conditions in individuals with a high SMR.

Repeatability is an important concept in evolutionary analyses because it provides information regarding the benefit of repeated measurements and, in most cases, a putative upper limit to heritability estimates. Repeatability (R) of different aspects of energy metabolism and behavior has been demonstrated in a variety of organisms over short and long time intervals. Recent research suggests that consistent individual differences in behavior and energy metabolism might covary. Here we present new data on the repeatability of body mass, standard metabolic rate (SMR), voluntary exploratory behavior, and feeding rate in a semiaquatic salamander and ask whether individual variation in behavioral traits is correlated with individual variation in metabolism on a whole-animal basis and after conditioning on body mass. All measured traits were repeatable, but the repeatability estimates ranged from very high for body mass (R = 0.98), to intermediate for SMR (R = 0.39) and food intake (R = 0.58), to low for exploratory behavior (R = 0.25). Moreover, repeatability estimates for all traits except body mass declined over time (i.e., from 3 to 9 wk), although this pattern could be a consequence of the relatively low sample size used in this study. Despite significant repeatability in all traits, we find little evidence that behaviors are correlated with SMR at the phenotypic and among-individual levels when conditioned on body mass. Specifically, the phenotypic correlations between SMR and exploratory behavior were negative in all trials but significantly so in one trial only. Salamanders in this study showed individual variation in how their exploratory behavior changed across trials (but not body mass, SMR, and feed intake), which might have contributed to observed changing correlations across trials.

Seasonal variation in the metabolism-temperature relation of House Sparrows ( Passer domesticus) in KwaZulu-Natal, South Africa