Active and resting metabolism in birds: allometry, phylogeny and ecology

Variation in resting metabolic rate is strongly correlated with differences in body weight among birds. The lowest taxonomic level at which most of the variance in resting metabolic rate and body weight is evident for the sample is among families within orders. The allometric exponent across family points is 0.67. This exponent accords with the surface area interpretation of metabolic scaling based on considerations of heat loss. Deviations of family points from this allometric line are used to examine how resting metabolic rates differ among taxa, and whether variation in resting metabolic rate is correlated with broad differences in ecology and behaviour. Despite the strong correlation between resting metabolic rate and body weight, there is evidence for adaptive departures from the allometric line, and possible selective forces are discussed.
The allometric scaling of active metabolic rate is compared with that of resting metabolic rate. The allometric exponents for the two levels of energy expenditure differ, demonstrating that active small-bodied birds require proportionately more energy per unit time above resting levels than do active large-bodied birds. No consistent evidence was found to indicate that the different methods used to estimate active metabolic rate result in systematic bias. Birds require more energy relative to body size when undertaking breeding activities than at other stages of the annual cycle.     

A new similarity principle for cardiac energetics

Similarity criteria of the functional design of the mammalian cardiovascular system are scant. For the analysis of mammalian cardiac energetics physiological parameters such as mean arterial blood pressure, stroke volume, heart rate, metabolic rate and heart and body weights are considered pertinent. Based on these parameters, a new similarity principle is established via allometric equations, dimensional analysis and Buckingham's pi-theorem. The principle states that the ratio of left ventricular external work to metabolic rate is inversely proportional to resting heart rates of mammals. The proportionality constant is dimensionless and is invariant of mammalian body weights.     

Hemodynamic significance of metabolic turn-over rate

Method in establishing mammalian hemodynamic similarity criteria via the classical allometric approach was examined. Metabolic rate (MR) per unit body weight (w), termed the metabolic turn-over rate (MTR), was found to be linearly related to mammalian resting heart rate (fh). The external ventricular work (EW) per unit body weight was found to be constant among mammalian species. The ratio of (EW/w)/(MTR/fh) is dimensionless, and is about 1/70. This latter qualifies as a new similarity principle. It states that the external ventricular work intensity during each cardiac cycle is directly proportional to the metabolic turn-over rate.     

Does basal metabolic rate contain a useful signal? Mammalian BMR allometry and correlations with a selection of physiological, ecological, and life-history variables

Basal metabolic rate (BMR, mL O2 h(-1)) is a useful measurement only if standard conditions are realised. We present an analysis of the relationship between mammalian body mass (M, g) and BMR that accounts for variation associated with body temperature, digestive state, and phylogeny. In contrast to the established paradigm that BMR proportional to M3/4, data from 619 species, representing 19 mammalian orders and encompassing five orders of magnitude variation in M, show that BMR proportional to M2/3. If variation associated with body temperature and digestive state are removed, the BMRs of eutherians, marsupials, and birds do not differ, and no significant allometric exponent heterogeneity remains between orders. The usefulness of BMR as a general measurement is supported by the observation that after the removal of body mass effects, the residuals of BMR are significantly correlated with the residuals for a variety of physiological and ecological variables, including maximum metabolic rate, field metabolic rate, resting heart rate, life span, litter size, and population density.     

Ontogenic growth of the haemopoietic stem cell pool in humans

Recently, the size of the active stem cell pool has been predicted to scale allometrically with the adult mass of mammalian species with a 3/4 power exponent, similar to what has been found to occur for the resting metabolic rate across species. Here we investigate the allometric scaling of human haemopoietic stem cells (HSCs) during ontogenic growth and predict a linear scaling with body mass. We also investigate the allometric scaling of resting metabolic rate during growth in humans and find a linear scaling with mass similar to that of the haemopoietic stem cell pool. Our findings suggest a common underlying organizational principle determining the linear scaling of both the stem cell pool and resting metabolic rate with mass during ontogenic growth within the human species, combined with a 3/4 scaling with adult mass across mammalian species. It is possible that such common principles remain valid for haemopoiesis in other mammalian species.     

Effects of different rates of cardiac pacing on rat myocardial energy status

The energy status of mammalian cells is a finely regulated phenomenon. This is especially true in cardiac muscle cells in which energy requirements are high and the system must provide rapid turnover of the adenine nucleotides and instant response to changes in energetic demands. We have examined the acute response of the rat myocardium to ventricular pacing up to 2.5 times the resting heart rate. The purpose of this study was to determine at what level of pacing the normal energy status could be maintained and at what point it was compromised. Myocardial energy charge (EC = (ATP + 0.5 ADP)/(ATP + ADP + AMP)) was maintained at 1, 1.5 and 2 times the resting heart rate but declined significantly at 2.5 times. In contrast, phosphorylation potential (PP = ATP/ADP₁ × Pi) was drastically altered in hearts paced at 1.5, 2 and 2.5 times the resting rate. Tissue lactate increased and glycogen decreased in a linear fashion as pacing rate increased, indicating that the metabolic challenge was proportional to the pacing rate. EC seems to reflect the overall status of the cell and its ability to maintain a dynamic equilibrium. PP may reflect the immediate and necessary driving force for mitochondrial respiration in times of increased demand. These data suggest that the myocardium may meet the increased energy demands of acute ventricular pacing by shifting the molar ratio of ATP to ADP times Pi in favour of driving phosphorylation.     

Scaling of brain metabolism and blood flow in relation to capillary and neural scaling

Brain is one of the most energy demanding organs in mammals, and its total metabolic rate scales with brain volume raised to a power of around 5/6. This value is significantly higher than the more common exponent 3/4 relating whole body resting metabolism with body mass and several other physiological variables in animals and plants. This article investigates the reasons for brain allometric distinction on a level of its microvessels. Based on collected empirical data it is found that regional cerebral blood flow CBF across gray matter scales with cortical volume V as CBF ~ V(-1/6), brain capillary diameter increases as V(1/12), and density of capillary length decreases as V(-1/6). It is predicted that velocity of capillary blood is almost invariant (~V(ε)), capillary transit time scales as V(1/6), capillary length increases as V(1/6+ε), and capillary number as V(2/3-ε), where ε is typically a small correction for medium and large brains, due to blood viscosity dependence on capillary radius. It is shown that the amount of capillary length and blood flow per cortical neuron are essentially conserved across mammals. These results indicate that geometry and dynamics of global neuro-vascular coupling have a proportionate character. Moreover, cerebral metabolic, hemodynamic, and microvascular variables scale with allometric exponents that are simple multiples of 1/6, rather than 1/4, which suggests that brain metabolism is more similar to the metabolism of aerobic than resting body. Relation of these findings to brain functional imaging studies involving the link between cerebral metabolism and blood flow is also discussed.     

High-Throughput Tissue Bioenergetics Analysis Reveals Identical Metabolic Allometric Scaling for Teleost Hearts and Whole Organisms

Organismal metabolic rate, a fundamental metric in biology, demonstrates an allometric scaling relationship with body size. Fractal-like vascular distribution networks of biological systems are proposed to underlie metabolic rate allometric scaling laws from individual organisms to cells, mitochondria, and enzymes. Tissue-specific metabolic scaling is notably absent from this paradigm. In the current study, metabolic scaling relationships of hearts and brains with body size were examined by improving on a high-throughput whole-organ oxygen consumption rate (OCR) analysis method in five biomedically and environmentally relevant teleost model species. Tissue-specific metabolic scaling was compared with organismal routine metabolism (RMO₂), which was measured using whole organismal respirometry. Basal heart OCR and organismal RMO₂ scaled identically with body mass in a species-specific fashion across all five species tested. However, organismal maximum metabolic rates (MMO₂) and pharmacologically-induced maximum cardiac metabolic rates in zebrafish Danio rerio did not show a similar relationship with body mass. Brain metabolic rates did not scale with body size. The identical allometric scaling of heart and organismal metabolic rates with body size suggests that hearts, the power generator of an organism’s vascular distribution network, might be crucial in determining teleost metabolic rate scaling under routine conditions. Furthermore, these findings indicate the possibility of measuring heart OCR utilizing the high-throughput approach presented here as a proxy for organismal metabolic rate—a useful metric in characterizing organismal fitness. In addition to heart and brain OCR, the current approach was also used to measure whole liver OCR, partition cardiac mitochondrial bioenergetic parameters using pharmacological agents, and estimate heart and brain glycolytic rates. This high-throughput whole-organ bioenergetic analysis method has important applications in toxicology, evolutionary physiology, and biomedical sciences, particularly in the context of investigating pathogenesis of mitochondrial diseases.     

Resting metabolic rates of two orbweb spiders: a first approach to evolutionary success of ecribellate spiders

Spiders are considered conservative with regard to their resting metabolic rate, presenting the same allometric relation with body mass as the majority of land-arthropods. Nevertheless, web-building is thought to have a great impact on the energetic metabolism, and any modification that affects this complex behavior is expected to have an impact over the daily energetic budget. We analyzed the possibility of the presence of the cribellum having an effect on the allometric relation between resting metabolic rate and body mass for an ecribellate species (Zosis geniculata) and a cribellate one (Metazygia rogenhoferi), and employed a model selection approach to test if these species had the same allometric relationship as other land-arthropods. Our results show that M. rogenhoferi has a higher resting metabolic rate, while Z. geniculata fitted the allometric prediction for land arthropods. This indicates that the absence of the cribellum is associated with a higher resting metabolic rate, thus explaining the higher promptness to activity found for the ecribellate species. If our result proves to be a general rule among spiders, the radiation of Araneoidea could be connected to a more energy-consuming life style. Thus, we briefly outline an alternative model of diversification of Araneoidea that accounts for this possibility.     

Bioenergetics in aging: mitochondrial proton leak in aging rat liver, kidney and heart

Aging is associated with a decline in performance in many organs and loss of physiological performance can be due to free radicals. Mitochondria are incompletely coupled: during oxidative phosphorylation some of the redox energy is dissipated as natural proton leak across the inner membrane. To verify whether proton leak occurs in mitochondria during aging, we measured the mitochondrial respiratory chain activity, membrane potential and proton leak in liver, kidneys and heart of young and old rats. Mitochondria from old rats showed normal rates of Complex I and Complex II respiration. However, they had a lower membrane potential compared to mitochondria from younger rats. In addition, they exhibited an increased rate of proton conductance which partially dissipated the mitochondrial membrane potential when the rate of electron transport was suppressed. This could compromise energy homeostasis in aging cells in conditions that require additional energy supply and could minimize oxidative damage to DNA.     

Do the high energy lifestyles of shorebirds result in high maximal metabolic rates? Basal and maximal metabolic rates in least and pectoral sandpipers during migration

Shorebirds have high resting and field metabolic rates relative to many other bird groups, and this is posited to be related to their high‐energy lifestyle. Maximum metabolic outputs for cold or exercise are also often high for bird groups with energetically demanding lifestyles. Moreover, shorebirds demonstrate flexible basal and maximal metabolic rates, which vary with changing energy demands throughout the annual cycle. Consequently, shorebirds might be expected to have high maximum metabolic rates, especially during migration periods. We captured least Calidris minutilla and pectoral C. melanotos sandpipers during spring and fall migration in southeastern South Dakota and measured maximal exercise metabolic rate (MMR; least sandpipers only), summit metabolic rate (M_sum, maximal cold‐induced metabolic rate) and basal metabolic rate (BMR, minimum maintenance metabolic rate) with open‐circuit respirometry. BMR for both least and pectoral sandpipers exceeded allometric predictions by 3–14%, similar to other shorebirds, but M_sum and MMR for both species were either similar to or lower than allometric predictions, suggesting that the elevated BMR in shorebirds does not extend to maximal metabolic capacities. Old World shorebirds show the highest BMR during the annual cycle on the Arctic breeding grounds. Similarly, least sandpiper BMR during migration was lower than on the Arctic breeding grounds, but this was not the case for pectoral sandpipers, so our data only partially support the idea of similar seasonal patterns of BMR variation in New World and Old World shorebirds. We found no correlations of BMR with either M_sum or MMR for either raw or mass‐independent data, suggesting that basal and maximum aerobic metabolic rates are modulated independently in these species.     

Phylogenetic analysis of the allometric scaling of therapeutic regimes for birds

The use of allometric scaling to estimate drug doses, regimes, and clearance rates (metabolic dosing) is based on the principle that the amount of drug to be administered is more closely related to daily energy use than to body mass (kg). Thus, by using the allometric estimations of minimal energy consumption (MEC) in kcal day⁻¹ based on the formula MEC= kM _b ^b , where b =3, it is thought to be possible to extrapolate appropriate drug dosage regimens to species for which direct MEC data are unavailable. However, the allometric equations for respiratory variables in birds were developed 30 years ago, and were based on a very small sample size, while the appropriate scaling exponent for the allometry of energy use is a matter of considerable debate. Hence, we revisit the issue of the scaling of therapeutic regimes in birds using the most current expanded database available (resting metabolic rate data for 296 species across 17 bird orders), taking account of the non-independence of species in this process using a phylogenetically independent approach. We show that the use of caloric values to estimate daily energy consumption introduces significant error into the formula, as there are a number of assumptions that are made when converting rate of oxygen consumption to a caloric value. We also show that there are significant differences in the proportionality or Hainsworth coefficients k across taxa when the data are examined in a phylogenetic context, although the allometric scaling exponent does not vary. We therefore recommend the use of only data based on oxygen consumption values, and not caloric values, and a multi-order phylogenetic model when calculating the appropriate drug dosage regime.     

Proteomic analysis of succinate dehydrogenase and ubiquinol-cytochrome c reductase (Complex II and III) isolated by immunoprecipitation from bovine and mouse heart mitochondria

The oxidative phosphorylation system (OXPHOS) consists of five multi-enzyme complexes, Complexes I-V, and is a key component of mitochondrial function relating to energy production, oxidative stress, cell signaling and apoptosis. Defects or a reduction in activity in various components that make up the OXPHOS enzymes can cause serious diseases, including neurodegenerative disease and various metabolic disorders. Our goal is to develop techniques that are capable of rapid and in-depth analysis of all five OXPHOS complexes. Here, we describe a mild, micro-scale immunoisolation and mass spectrometric/proteomic method for the characterization of Complex II (succinate dehydrogenase) and Complex III (ubiquinol-cytochrome c reductase) from bovine and rodent heart mitochondria. Extensive protein sequence coverage was obtained after immunocapture, 1D SDS PAGE separation and mass spectrometric analysis for a majority of the 4 and 11 subunits, respectively, that make up Complexes II and III. The identification of several posttranslational modifications, including the covalent FAD modification of flavoprotein subunit 1 from Complex II, was possible due to high mass spectrometric sequence coverage.     

Relationships between heart rate and metabolic rate of pike: integration of existing data

The percentage contribution of heart rate ( f _H) to change in oxygen consumption ( V o₂) was examined in relation to body weight and across the metabolic scope of pike. Also the consequences of variability around the regression relating V o₂ and f _H for estimating V o₂ were considered. The percentage contribution of f _H was calculated using two equations, one that ignored and one that included an estimate for oxygen consumed by the gills and absorbed across the skin ( V o_2s). Using both equations the percentage contribution of f _H calculated using maximum and resting values for f _H and V o₂ decreased with weight of pike. The omission of V o_2s, resulted in erroneously high estimates of the percentage contribution of f _H for pike of any given weight. The omission of V o_2s resulted in erroneously high estimates of the percentage contribution of f _H over the region of the metabolic scope where f _H is related linearly to V o₂, whereas the equation that included V o_2s resulted in the expected value of 100%. Assuming zero experimental error and under normoxic conditions, the 95% confidence limits for single estimates of V o₂ from 30–60-min readings of heart rate are ±39% at a heart rate of 30 beats min ⁻¹. Averaged over longer periods the error decreases, and used over several days to estimate meal size the error is of the order of 1%.     

HEART RATE AND ELECTROCARDIOGRAM CHARACTERISTICS OF A YOUNG CALIFORNIA GRAY WHALE (ESCHRICHTIUS ROBUSTUS)1

Electrocardiogram (ECG) analyses of Holter monitor recordings from a young California gray whale were performed to determine ECG waveform characteristics, evaluate the heart rate pattern for sinus arrhythmia, obtain resting heart rates at known body masses as the whale increased in size, and compare those heart rates with predicted heart rates from allometric equations. The PR and QRS intervals (475 ± 35 msec, 208 ± 24 msec, respectively, n= 20) support the concept (Meijler et al. 1992) that atrioventricular transmission and ventricular excitation times do not increase linearly in very large mammals. A sinus arrhythmia pattern at rest (apneic heart rates of 15–25 beats per min [bpm] and eupneic heart rates of 34–40 bpm) is consistent with a relative eupneic tachycardia and apneic bradycardia during diving activity of whales. The heart rate-body mass measurements (35–24 bpm at body masses of 3,591-8,200 kg) in this study (1) extend the range of allometric heart rate and body mass data in mammals a full order of magnitude, to almost 10,000 kg, (2) support the use of allometric equations (based primarily on mammals <1,000 kg in body mass) in estimating resting heart rates in whales, and (3) demonstrate that previously reported heart rates in large whales are not representative of resting heart rate, probably secondary to circumstances during measurement.     

Studies on the immunological properties of complex V (mitochondrial ATP synthetase complex)

Antibody raised in rabbits against Complex V (miochondrial ATP synthetase complex) purified from beef heart mitochondria cross-reacted with Complex V and submitochondrial particles from beef heart, beef adrenals, and rat liver as shown by double-diffusion and rocket immunoelectrophoresis analysis. Of the various isolated and purified components of Complex V, only the oligomycin sensitivity-conferring protein showed strong reactivity with the anti-Complex V antibody, soluble F₁-ATPase reacted very faintly, while F₆ and ATPase inhibitor protein showed no precipitin lines. Crossed immunoelectrophoresis indicated that antigenic determinants recognized by the antibody were present on OSCP and possibly on the dicyclohexylcarbodiimide-binding protein. The components of Complex V could be precipitated from beef heart submitochondrial particles dissolved in Triton X-100 and pretreated with control IgG. When the composition of the immunoprecipitate was compared to that of purified Complex V, all the constituent polypeptides of the latter were present in the immunoprecipitate, except for one polypeptide in the low-molecular-weight region. Incubation of Complex V or submitochondrial particles with the anti-Complex V antibody in the absence of Triton X-100 caused inhibition of ATP-P_i exchange but not of ATPase activity. In the presence of Triton X-100, oligomycin sensitivity of Complex V was lost and the antibody was able to inhibit also the ATPase activity. The enzymic activity of soluble F₁-ATPase was unaffected by the antibody in the absence or presence of Triton X-100. These results suggest that the anti-Complex V antibody might be a useful tool for identifying and probing the role of Complex V components involved in energy transduction.     

Energetically costly behaviour and the evolution of resting metabolic rate in insects

1. A general hypothesis is presented to explain interspecific differences in size-independent resting metabolic rate. This hypothesis is based on a presumed trade-off between a low resting metabolism and adaptations of metabolism during activity.
2. With such a trade-off, selection to reduce resting metabolism is less intense in active species than in species where resting metabolism constitutes a large proportion of the daily metabolic costs. Those animals that spend more energy on activity should therefore have a higher resting metabolic rate than animals that spend less energy on activity.
3. A literature review reveals that flying insects have higher resting metabolic rates than species that use energetically less demanding types of locomotion.
4. Insects producing acoustic advertisement signals can be shown to have higher mass-independent resting metabolic rates than closely related species without this energetically demanding behaviour.
5. Literature data on vertebrate resting metabolic rates are also consistent with the presented hypothesis: the more energy animals spend on activity, the higher the mass-independent resting metabolic rate.     

Cardiac metabolism in high performance fish

In aerobic tissues, such as cardiac and skeletal muscle, short term increases in energy demand are met primarily by acute regulation of mitochondrial pathways. Chronic increases in time-average metabolic rate of an individual or tissue can lead to modest “physiological adaptations” that may result in increased metabolic capacities and more efficient energy production and utilization. These physiological adaptations differ fundamentally from those which alter metabolic rate acutely. Analysis of the metabolic strategies used by an individual to chronically elevate cardiac metabolic rates may help identify the components of cardiac metabolism which may be constrained or malleable over evolutionary time. While pronounced physiological differences in cardiac energy transduction are apparent across species, the evolutionary origins of such differences are difficult to assess. However, the functional consequences of such differences in homologous tissues across species can be discussed with more certainty. Both chronic hypermetabolic challenges and interspecies comparisons suggest highly oxidative tissues such as heart are restricted to strategies which a) elevate the functional mass b) make more efficient use of intracellular space devoted to mitochondria and c) shift toward more efficient metabolic fuels, primarily fatty acids if oxygen delivery is not a factor.     

Switching of metabolic-rate scaling between allometry and isometry in colonial ascidians

The metabolic rate and its scaling relationship to colony size were studied in the colonial ascidian Botrylloides simodensis. The colonial metabolic rate, measured by the oxygen consumption rate (V(O2) in millilitres of O(2) per hour) and the colony mass (wet weight M(w) in grams) showed the allometric relationship (V(O2) = 0.0412 M(w)(0.799). The power coefficient was statistically not different from 0.75, the value for unitary organisms. The size of the zooids and the tunic volume fraction in a colony were kept constant irrespective of the colonial size. These results, together with the two-dimensional colonial shape, excluded shape factors and colonial composition as possible causes of allometry. Botryllid ascidians show a takeover state in which all the zooids of the parent generation in a colony degenerate and zooids of a new generation develop in unison. The media for connection between zooids such as a common drainage system and connecting vessels to the common vascular system experienced reconstruction. The metabolic rate during the takeover state was halved and was directly proportional to the colonial mass. The scaling thus changed from being allometric to isometric. The alteration in the scaling that was associated with the loss of the connection between the zooids strongly support the hypothesis that the allometry was derived from mutual interaction among the zooids. The applicability of this hypothesis to unitary organisms is discussed.     

Differential energy costs of winter acclimatized common spiny mice Acomys cahirinus from two adjacent habitats

The common spiny mouse Acomys cahirinus, of Ethiopian origin, has a widespread distribution across arid, semi-arid and Mediterranean parts of the Arabian sub-region. We compared the daily energy expenditure (DEE), water turnover (WTO) and sustained metabolic scope (SusMS=DEE/resting metabolic rate) of two adjacent populations during the winter. Mice were captured from North- and South- facing slopes (NFS and SFS) of the same valley, comprising mesic and xeric habitats, respectively. Both DEE and SusMS winter values were greater in NFS than SFS mice and were significantly greater than values previously measured in the summer for these two populations in the same environments. However, WTO values were consistent with previously established values and were not significantly different from allometric predictions for desert eutherians. We suggest that physiological plasticity in energy expenditure, which exists both temporally and spatially, combined with stable WTO, perhaps reflecting a xeric ancestry, has enabled A. cahirinus to invade a wide range of habitats.