Charles-A. Darveau

Allometric cascade as a unifying principle of body mass effects on metabolism

The power function of basal metabolic rate scaling is expressed as aMb, where a corresponds to a scaling constant (intercept), M is body mass, and b is the scaling exponent. The 3/4 power law (the best-fit b value for mammals) was developed from Kleibers original analysis and, since then, most workers have searched for a single cause to explain the observed allometry. Here we present a multiple-causes model of allometry, where the exponent b is the sum of the influences of multiple contributors to metabolism and control. The relative strength of each contributor, with its own characteristic exponent value, is determined by the control contribution. To illustrate its use, we apply this model to maximum versus basal metabolic rates to explain the differing scaling behaviour of these two biological states in mammals. The main difference in scaling is that, for the basal metabolic rate, the O2 delivery steps contribute almost nothing to the global b scaling exponent, whereas for the maximum metabolic rate, the O2 delivery steps significantly increase the global b value.

Energy metabolism in orchid bee flight muscles : carbohydrate fuels all

SUMMARY The widely accepted idea that bees fuel flight through the oxidation of carbohydrate is based on studies of only a few species. We tested this hypothesis as part of our research program to investigate the size-dependence of flight energetics in Panamanian orchid bees. We succeeded in measuring rates of O2 consumption and CO2 production in vivo during hovering flight, as well as maximal activities (Vmax values) in vitro of key enzymes in flight muscle energy metabolism in nine species belonging to four genera. Respiratory quotients (ratios of rates of CO2 production to O2 consumption) in all nine species are close to 1.0. This indicates that carbohydrate is the main fuel used for flight. Trehalase, glycogen phosphorylase and hexokinase activities are sufficient to account for the glycolytic flux rates estimated from rates of CO2 production. High activities of other glycolytic enzymes, as well as high activities of mitochondrial oxidative enzymes, are consistent with the estimated rates of carbohydrate-fueled oxidative metabolism. In contrast, hydroxyacylCoA dehydrogenase, an enzyme involved in fatty acid oxidation, was not detectable in any species. Thoracic homogenates displayed ADP-stimulated oxidition of pyruvate + proline, but did not oxidize palmitoyl l-carnitine + proline as substrates. A metabolic map, based on data reported herein and information from the literature, is presented. The evidence available supports the hypothesis that carbohydrate serves as the main fuel for flight in bees.

Multi-level regulation and metabolic scaling

SUMMARY Metabolic control analysis has revealed that flux through pathways is the consequence of system properties, i.e. shared control by multiple steps, as well as the kinetic effects of various pathways and processes over each other. This implies that the allometric scaling of flux rates must be understood in terms of properties that pertain to the regulation of flux rates. In contrast, proponents of models considering the scaling of branching or fractal-like systems suggest that supply rates determine metabolic rates. Therefore, the allometric scaling of supply alone provides a sufficient explanation for the allometric scaling of metabolism. Examination of empirical data from the literature of comparative physiology reveals that basal metabolic rates (BMR) are driven by rates of energy expenditure within internal organs and that the allometric scaling of BMR can be understood in terms of the scaling of the masses and metabolic rates of internal organs. Organ metabolic rates represent the sum of tissue metabolic rates while, within tissues, cellular metabolic rates are the outcome of shared regulation by multiple processes. Maximal metabolic rates (MMR, measured as maximum rates of O2 consumption, V̇O2max) during exercise also scale allometrically, are also subject to control by multiple processes, but are due mainly to O2 consumption by locomotory muscles. Thus, analyses of the scaling of MMR must consider the scaling of both muscle mass and muscle energy expenditure. Consistent with the principle of symmorphosis, allometry in capacities for supply (the outcome of physical design constraints) is observed to be roughly matched by allometry in capacities for demand (i.e. for energy expenditure). However, physiological rates most often fall far below maximum capacities and are subject to multi-step regulation. Thus, mechanistic explanations for the scaling of BMR and MMR must consider the manner in which capacities are matched and how rates are regulated at multiple levels of biological organization.

Allometric scaling of flight energetics in Panamanian orchid bees: a comparative phylogenetic approach

SUMMARY The relationship between body size and flight energetics was studied in the clade of tropical orchid bees, in order to investigate energy metabolism and evolution. Body mass, which varied from 47 to 1065 mg, was found to strongly affect hovering flight mass-specific metabolic rates, which ranged from 114 ml CO2 h-1 g-1 in small species to 37 ml CO2 h-1 g-1 in large species. Similar variation of wingbeat frequency in hovering flight occurred among small to large species, and ranged from 250 to 86 Hz. The direct relationship between such traits was studied by the comparative method of phylogenetically independent contrasts (PIC), using a new molecular phylogeny generated from the cytochrome b gene partial sequences. We found wingbeat frequency variation is satisfactorily explained by variation in wing loading, after corrections for body mass and phylogeny. The correlated evolution of mass-specific metabolic rate, wingbeat frequency and wing loading was also revealed after correcting for phylogeny and body mass. Further, the effect of body size on flight energetics can be understood in terms of a relationship between wing form and kinematics, which directly influence and explain the scaling of metabolic rate in this group of bees.

Metabolic and cardiovascular adjustments of juvenile green turtles to seasonal changes in temperature and photoperiod

SUMMARY We measured activity levels, oxygen consumption, metabolic enzyme activity, breathing frequency, heart rate and blood chemistry variables of juvenile green turtles exposed to a laboratory simulation of subtropical winter and summer temperatures (17-26°C) and photoperiod (10.25 h:13.75 h to 14 h:10 h light:dark). The activity level of turtles had a significant effect on oxygen consumption and breathing frequency but there was no significant change in activity level between the summer and winter simulations. There was a moderate 24-27% decrease in oxygen consumption during exposure to winter conditions compared with summer conditions, but this difference was not statistically significant. Likewise, there was no statistically significant difference in breathing frequency between summer and winter simulations. Exposure to winter conditions did result in a significant decrease in activity of the aerobic enzyme citrate synthase. By contrast, activities of the glycolytic enzymes pyruvate kinase and lactate dehydrogenase were significantly higher in tissue collected during exposure to winter conditions compared with summer conditions. Citrate synthase, pyruvate kinase and lactate dehydrogenase had relatively low thermal dependence over the range of assay temperatures (15-30°C; Q10=1.44-1.69). Heart rate was 46-48% lower during the winter simulation compared with the summer simulation, and this difference was statistically significant. Exposure to winter conditions resulted in a significant decrease in plasma thyroxine and plasma proteins and a significant increase in plasma creatine phosphokinase and hematocrit. Overall, our results suggest that green turtles have a relatively low thermal dependence of metabolic rate over the range of temperatures commonly experienced at tropical to subtropical latitudes, a trait which allows them to maintain activity year-round.

Allometric scaling of flight energetics in orchid bees: evolution of flux capacities and flux rates

SUMMARY The evolution of metabolic pathways involved in energy production was studied in the flight muscles of 28 species of orchid bees. Previous work revealed that wingbeat frequencies and mass-specific metabolic rates decline in parallel by threefold as body mass increases interspecifically over a 20-fold range. We investigated the correlated evolution of metabolic rates during hovering flight and the flux capacities, i.e. Vmax values, of flight muscle enzymes involved in substrate catabolism, the Krebs cycle and the electron transport chain. Vmax at the hexokinase (HK) step scales allometrically with an exponent almost identical to those obtained for wingbeat frequency and mass-specific metabolic rate. Analysis of this relationship using phylogenetically independent contrasts supports the hypothesis of correlated evolution between HK activity and mass-specific metabolic rate. Although other enzymes scale allometrically with respect to body mass, e.g. trehalase, glycogen phosphorylase and citrate synthase, no other enzyme activities were correlated with metabolic rate after controlling for phylogenetic relatedness. Pathway flux rates were used with enzyme Vmax values to estimate fractional velocities (fraction of Vmax at which enzymes operate) for various reactions to gain insights into enzyme function and how this varies with body mass. Fractional velocity is highly conserved across species at the HK step, but varied at all other steps examined. These results are discussed in the context of the regulation and evolution of pathways of energy metabolism.

Morphological and physiological idiosyncrasies lead to interindividual variation in flight metabolic rate in worker bumblebees (Bombus impatiens).

Although intraspecific variation in metabolic rate is associated with variation in body size, similarly sized individuals nonetheless vary greatly. At similar masses, hovering bumblebee workers (Bombus impatiens) can differ in metabolic rate up to twofold. We examined how such interindividual variation arises by studying covariation of flight metabolic rate with morphological and other physiological parameters. Body size alone explained roughly half the variation in flight metabolic rate. The remaining variation could be explained as the outcome of variation in wing morphology and possibly an association with variation in flight muscle metabolic enzyme activities. As shown using statistical models, for a given mass, higher metabolic rate was correlated with both higher thoracic temperature and higher wing stroke frequency, in turn resulting from smaller wing surface area. When organismal and cellular metabolism for a given mass were linked, variation in metabolic rate was positively correlated with the activities of trehalase and hexokinase. Altogether, covariation with morphology and other physiological parameters explains up to 75% of the variation in metabolic rate. We also investigated the role of flight experience and show that neither flight restriction nor the number of lifetime flights affected flight energetics or flight muscle phenotype. Additionally, manipulating the level of wing asymmetry increased flight wing stroke frequency, metabolic rate, and thoracic temperature, but it did not alter enzyme activity. We conclude that idiosyncrasies in body morphology largely explained interindividual variation in flight metabolic rate but flight muscle metabolic phenotype shows little variation associated with differences in flight experience.

Behavioural, morphological, and metabolic maturation of newly emerged adult workers of the bumblebee, Bombus impatiens.

Newly emerged adult holometabolous insects must still complete considerable morphological, metabolic, and neural maturation. Despite this, adults have frequently been documented to fly prior to finishing maturation and attaining peak physiological capacity. In some species, flight is limited by the unfurling of the wing, while in other species it may be limited by biochemical capacity. We charted maturation trajectories of adult bumblebee workers (Bombus impatiens) for both morphological and flight muscle metabolic capacities, and compared these to the first age at flight. Workers began regular flights as soon as two days after emergence. The unfurling of the wings was completed well before first flights and before any other studied factor, suggesting this did not initially limit flight. Wing beat frequencies, measured as a struggling response to grasping the hindlegs, were about 90% mature by two days old, and did not significantly change after three days. Conversely, by the initiation of flight, the mean enzyme maturation was only 63% completed relative to adult enzyme capacity, though specific enzyme profiles ranged from 42% to 73%. Maximum ADP-stimulated mitochondrial respiratory activity on pyruvate and proline matured along a similar time frame to glycolytic capacity, reaching its maximum three days after emergence. Bumblebees, as other adult insects, thus begin flights prior to fully maturing.

Physiology (communication arising (reply)): Why does metabolic rate scale with body size?/Allometric cascades

Physiology (communication arising (reply)): Why does metabolic rate scale with body size?/Allometric cascades

Variation in cricket acoustic mate attraction signalling explained by body morphology and metabolic differences

Males often signal to attract mates and can show extensive variation in how much time they spend signalling. In crickets, some males signal extensively, spending over 50% of their adult lives attempting to attract a mate. At the other end of the continuum, some males are rarely observed to signal. Given that signalling efforts are usually correlated with mating success, all individuals should be selected to signal with high effort. Why then, do males show such variability? Signalling effort variation may stem from differences in physiological capacity that result from disparities in energy stores, metabolic capacities of the muscles used for sexual signalling, the comparative size of the signalling organs, or overall differences in body size. To address the proximate causes underlying variation in signalling effort, we quantified the morphological, physiological and biochemical variation among male European house crickets, Acheta domesticus, and assessed whether it correlated with signalling effort variation. Surprisingly, we found no correlation between signalling effort and activity of the β-oxidation enzyme HOAD, suggesting that the capacity for lipid metabolism is not associated with signalling effort. Instead, signalling effort variation was associated with differences in overall body size and differences in the activity of the glycolytic enzyme pyruvate kinase. Together our findings suggest that the ability to locate and assimilate high-quality diets both during development (to grow large) and into adulthood (capacity for carbohydrate catabolism) may explain some of the variation in signalling effort in this species.