Mammalian metabolism: insights from arid zone reptiles.

2004 ◽  
Vol 26 (1) ◽  
pp. 111
Author(s):  
AJ Hulbert ◽  
PL Else

Mammals, being endotherms have very high metabolic rates compared to ectothermic reptiles. Similarly, small mammals have high rates of mass-specific metabolism compared to larger mammals. This review examines the mechanistic basis of why particular mammal species have a specific metabolic rate. Initial studies compared mammals with arid zone reptile species of the same size and Tb. Mammals have larger internal organs, with more mitochondrial membrane surface area than the reptiles. The cells of mammals are leakier to Na+ ions and their mitochondrial membranes are leakier to H+ ions than in reptile cells. These leakier membranes have membrane lipids that are polyunsaturated and less monounsaturated than their less leaky counterparts. Examination of the cellular basis of allometric variation in metabolism in mammals reveals very similar findings with polyunsaturated membranes associated with the high mass-specific metabolic rates of small mammal species and monounsaturated membranes with low rates of metabolism of large mammals. These findings have resulted in the development of the ?membrane pacemaker? theory of metabolism, which proposes that membrane bilayer composition is regulated in animals and that highly polyunsaturated membranes result in enhanced molecular activity of membrane proteins and in turn this results in an elevated metabolic rate of cells, tissues and consequently whole animals. This theory is also supported by the recent examination of the basis of body-size variation in the metabolic rates of birds. The ?membrane pacemaker? theory of metabolism is currently the only explanation of the mechanisms determining the metabolic rate and thus the cost of living of animals. It has implications for the effect of food habits on metabolism and the relationship between metabolism and lifespan.

2019 ◽  
Vol 286 (1911) ◽  
pp. 20191693 ◽  
Author(s):  
Boël Mélanie ◽  
Romestaing Caroline ◽  
Voituron Yann ◽  
Roussel Damien

Metabolic activity sets the rates of individual resource uptake from the environment and resource allocations. For this reason, the relationship with body size has been heavily documented from ecosystems to cells. Until now, most of the studies used the fluxes of oxygen as a proxy of energy output without knowledge of the efficiency of biological systems to convert oxygen into ATP. The aim of this study was to examine the allometry of coupling efficiency (ATP/O) of skeletal muscle mitochondria isolated from 12 mammal species ranging from 6 g to 550 kg. Mitochondrial efficiencies were measured at different steady states of phosphorylation. The efficiencies increased sharply at higher metabolic rates. We have shown that body mass dependence of mitochondrial efficiency depends on metabolic intensity in skeletal muscles of mammals. Mitochondrial efficiency positively depends on body mass when mitochondria are close to the basal metabolic rate; however, the efficiency is independent of body mass at the maximum metabolic rate. As a result, it follows that large mammals exhibit a faster dynamic increase in ATP/O than small species when mitochondria shift from basal to maximal activities. Finally, the invariant value of maximal coupling efficiency across mammal species could partly explain why scaling exponent values are very close to 1 at maximal metabolic rates.


2011 ◽  
Vol 278 (1721) ◽  
pp. 3135-3141 ◽  
Author(s):  
Montserrat Gomendio ◽  
Maximiliano Tourmente ◽  
Eduardo R. S. Roldan

The hypothesis that sperm competition should favour increases in sperm size, because it results in faster swimming speeds, has received support from studies on many taxa, but remains contentious for mammals. We suggest that this may be because mammalian lineages respond differently to sexual selection, owing to major differences in body size, which are associated with differences in mass-specific metabolic rate. Recent evidence suggests that cellular metabolic rate also scales with body size, so that small mammals have cells that process energy and resources from the environment at a faster rate. We develop the ‘metabolic rate constraint hypothesis’ which proposes that low mass-specific metabolic rate among large mammals may limit their ability to respond to sexual selection by increasing sperm size, while this constraint does not exist among small mammals. Here we show that among rodents, which have high mass-specific metabolic rates, sperm size increases under sperm competition, reaching the longest sperm sizes found in eutherian mammals. By contrast, mammalian lineages with large body sizes have small sperm, and while metabolic rate (corrected for body size) influences sperm size, sperm competition levels do not. When all eutherian mammals are analysed jointly, our results suggest that as mass-specific metabolic rate increases, so does maximum sperm size. In addition, species with low mass-specific metabolic rates produce uniformly small sperm, while species with high mass-specific metabolic rates produce a wide range of sperm sizes. These findings support the hypothesis that mass-specific metabolic rates determine the budget available for sperm production: at high levels, sperm size increases in response to sexual selection, while low levels constrain the ability to respond to sexual selection by increasing sperm size. Thus, adaptive and costly traits, such as sperm size, may only evolve under sexual selection when metabolic rate does not constrain cellular budgets.


2001 ◽  
Vol 204 (13) ◽  
pp. 2301-2311 ◽  
Author(s):  
Joseph B. Williams ◽  
Stéphane Ostrowski ◽  
Eric Bedin ◽  
Khairi Ismail

SUMMARY We report on the energy expenditure and water flux, measured in the laboratory and in the field, of the Arabian oryx Oryx leucoryx, the largest desert ruminant for which measurements of the field metabolic rate of free-living individuals have been made using doubly labeled water. Prior to extirpation of this species in the wild in 1972, conservationists sequestered a number of individuals for captive breeding; in 1989, oryx were reintroduced in Saudi Arabia into Mahazat as-Sayd (2244km2). Apart from small pools of water available after rains, oryx do not have free-standing water available for drinking and therefore rely on grasses that they eat for preformed water intake as well as their energy needs. We tested whether oryx have a reduced fasting metabolic rate and total evaporative water loss (TEWL) in the laboratory, as do some other arid-adapted mammals, and whether oryx have high field metabolic rates (FMRs) and water influx rates (WIRs), as predicted by allometric equations for large arid-zone mammals. We measured FMR and WIR during the hot summer, when plant moisture content was low and ambient temperatures were high, and after winter rains, when the water content of grasses was high. For captive oryx that weighed 84.1kg, fasting metabolic rate averaged 8980kJday−1, 16.7% lower than predictions for Artiodactyla. Our own re-analysis of minimal metabolic rates among Artiodactyla yielded the equation: logV̇O2=−0.153+0.758logM, where V̇O2 is the rate of oxygen uptake in lh−1 and M is body mass in kg. Fasting metabolic rate of oryx was only 9.1% lower than predicted, suggesting that they do not have an unusually low metabolic rate. TEWL averaged 870.0mlday−1, 63.9% lower than predicted, a remarkably low value even compared with the camel, but the mechanisms that contribute to such low rates of water loss remain unresolved. For free-living oryx, FMR was 11076kJday−1 for animals with a mean body mass of 81.5kg during summer, whereas it was 22081kJday−1 for oryx in spring with a mean body mass of 89.0kg, values that were 48.6% and 90.4% of allometric predictions, respectively. During summer, WIR averaged 1310mlH2Oday−1, whereas in spring it was 3438mlH2Oday−1. Compared with allometric predictions, WIR was 76.9% lower than expected in summer and 43.6% lower in spring. We found no evidence to support the view that the WIR of large desert ungulates is higher than that of their mesic counterparts. On the basis of the WIR of the oryx averaged over the year and the water contents of plants in their diet, we estimated that an oryx consumes 858kg of dry matter per year.


2019 ◽  
Vol 69 (2) ◽  
pp. 199-212
Author(s):  
Yun-Tao Yao ◽  
Yu Du ◽  
Meng-Chao Fang ◽  
Long-Hui Lin ◽  
Xiang Ji

Abstract We have studied resting metabolic rate (RMR) of the water monitor lizard (Varanus salvator) at different developmental stages (hatchling, juvenile and adult) to test whether individuals at different ages differ in RMR when controlling for the effects of body mass. We found that: 1) resting metabolic rates of hatchlings, juveniles and adults were all positively related to their body mass with the same coefficients and that 2) developmental stage had a non-significant influence on the resting metabolic rate when controlling for the effects of body mass. Our results suggest that variation in resting metabolic rate for V. salvator is directly caused by body mass differences, which conforms to previous findings in mammal species and birds.


2013 ◽  
Vol 280 (1754) ◽  
pp. 20122636 ◽  
Author(s):  
Cynthia J. Downs ◽  
Jessi L. Brown ◽  
Bernard Wone ◽  
Edward R. Donovan ◽  
Kenneth Hunter ◽  
...  

Both appropriate metabolic rates and sufficient immune function are essential for survival. Consequently, eco-immunologists have hypothesized that animals may experience trade-offs between metabolic rates and immune function. Previous work has focused on how basal metabolic rate (BMR) may trade-off with immune function, but maximal metabolic rate (MMR), the upper limit to aerobic activity, might also trade-off with immune function. We used mice artificially selected for high mass-independent MMR to test for trade-offs with immune function. We assessed (i) innate immune function by quantifying cytokine production in response to injection with lipopolysaccharide and (ii) adaptive immune function by measuring antibody production in response to injection with keyhole limpet haemocyanin. Selection for high mass-independent MMR suppressed innate immune function, but not adaptive immune function. However, analyses at the individual level also indicate a negative correlation between MMR and adaptive immune function. By contrast BMR did not affect immune function. Evolutionarily, natural selection may favour increasing MMR to enhance aerobic performance and endurance, but the benefits of high MMR may be offset by impaired immune function. This result could be important in understanding the selective factors acting on the evolution of metabolic rates.


2020 ◽  
Vol 8 (1) ◽  
Author(s):  
Louise C Archer ◽  
Stephen A Hutton ◽  
Luke Harman ◽  
W Russell Poole ◽  
Patrick Gargan ◽  
...  

Abstract Metabolic rates vary hugely within and between populations, yet we know relatively little about factors causing intraspecific variation. Since metabolic rate determines the energetic cost of life, uncovering these sources of variation is important to understand and forecast responses to environmental change. Moreover, few studies have examined factors causing intraspecific variation in metabolic flexibility. We explore how extrinsic environmental conditions and intrinsic factors contribute to variation in metabolic traits in brown trout, an iconic and polymorphic species that is threatened across much of its native range. We measured metabolic traits in offspring from two wild populations that naturally show life-history variation in migratory tactics (one anadromous, i.e. sea-migratory, one non-anadromous) that we reared under either optimal food or experimental conditions of long-term food restriction (lasting between 7 and 17 months). Both populations showed decreased standard metabolic rates (SMR—baseline energy requirements) under low food conditions. The anadromous population had higher maximum metabolic rate (MMR) than the non-anadromous population, and marginally higher SMR. The MMR difference was greater than SMR and consequently aerobic scope (AS) was higher in the anadromous population. MMR and AS were both higher in males than females. The anadromous population also had higher AS under low food compared to optimal food conditions, consistent with population-specific effects of food restriction on AS. Our results suggest different components of metabolic rate can vary in their response to environmental conditions, and according to intrinsic (population-background/sex) effects. Populations might further differ in their flexibility of metabolic traits, potentially due to intrinsic factors related to life history (e.g. migratory tactics). More comparisons of populations/individuals with divergent life histories will help to reveal this. Overall, our study suggests that incorporating an understanding of metabolic trait variation and flexibility and linking this to life history and demography will improve our ability to conserve populations experiencing global change.


1978 ◽  
Vol 35 (6) ◽  
pp. 816-821 ◽  
Author(s):  
J. R. Brett ◽  
J. M. Blackburn

The metabolic rate of spiny dogfish, Squalus acanthias, was determined in both a tunnel respirometer and a large, covered, circular tank (mass respirometer). Swimming performance was very poor in the respirometer, so that a power–performance curve could not be established. Instead, resting metabolic rates were determined, with higher rates induced by causing heavy thrashing (active metabolism). Routine metabolic rates were measured for the spontaneous activity characterizing behavior in the circular tank. For fish of 2 kg mean weight, the metabolic rates at 10 °C were 32.4 ± 2.6 SE (resting), 49.2 ± 5.0 SE (routine), and 88.4 ± 4.6 SE (active) mg O2∙kg−1∙h−1. Assuming that the routine rate represents a general energy expenditure in nature, this is equivalent to metabolizing about 3.8 kcal∙kg−1∙d−1 (15.9 × 103 J∙kg−1∙d−1). Key words: dogfish, metabolic rates, energetics, respiration


2018 ◽  
Vol 75 (6) ◽  
pp. 2117-2128 ◽  
Author(s):  
Samuel P S Rastrick ◽  
Victoria Collier ◽  
Helen Graham ◽  
Tore Strohmeier ◽  
Nia M Whiteley ◽  
...  

Abstract Climate change driven alterations in salinity and carbonate chemistry are predicted to have significant implications particularly for northern costal organisms, including the economically important filter feeders Mytilus edulis and Ciona intestinalis. However, despite a growing number of studies investigating the biological effects of multiple environmental stressors, the combined effects of elevated pCO2 and reduced salinity remain comparatively understudied. Changes in metabolic costs associated with homeostasis and feeding/digestion in response to environmental stressors may reallocate energy from growth and reproduction, affecting performance. Although these energetic trade-offs in response to changes in routine metabolic rates have been well demonstrated fewer studies have investigated how these are affected by changes in feeding plasticity. Consequently, the present study investigated the combined effects of 26 days’ exposure to elevated pCO2 (500 µatm and 1000 µatm) and reduced salinity (30, 23, and 16) on the energy available for growth and performance (Scope for Growth) in M. edulis and C. intestinalis, and the role of metabolic rate (oxygen uptake) and feeding plasticity [clearance rate (CR) and absorption efficiency] in this process. In M. edulis exposure to elevated pCO2 resulted in a 50% reduction in Scope for Growth. However, elevated pCO2 had a much greater effect on C. intestinalis, with more than a 70% reduction in Scope for Growth. In M. edulis negative responses to elevated pCO2 are also unlikely be further affected by changes in salinity between 16 and 30. Whereas, under future predicted levels of pCO2C. intestinalis showed 100% mortality at a salinity of 16, and a >90% decrease in Scope for Growth with reduced biomass at a salinity of 23. Importantly, this work demonstrates energy available for production is more dependent on feeding plasticity, i.e. the ability to regulate CR and absorption efficiency, in response to multiple stressors than on more commonly studied changes in metabolic rates.


2000 ◽  
Vol 203 (5) ◽  
pp. 905-911 ◽  
Author(s):  
R.K. Suarez ◽  
J.F. Staples ◽  
J.R. Lighton ◽  
O. Mathieu-Costello

The biochemical bases for the high mass-specific metabolic rates of flying insects remain poorly understood. To gain insights into mitochondrial function during flight, metabolic rates of individual flying honeybees were measured using respirometry, and their thoracic muscles were fixed for electron microscopy. Mitochondrial volume densities and cristae surface densities, combined with biochemical data concerning cytochrome content per unit mass, were used to estimate respiratory chain enzyme densities per unit cristae surface area. Despite the high content of respiratory enzymes per unit muscle mass, these are accommodated by abundant mitochondria and high cristae surface densities such that enzyme densities per unit cristae surface area are similar to those found in mammalian muscle and liver. These results support the idea that a unit area of mitochondrial inner membrane constitutes an invariant structural unit. Rates of O(2) consumption per unit cristae surface area are much higher than those estimated in mammals as a consequence of higher enzyme turnover rates (electron transfer rates per enzyme molecule) during flight. Cytochrome c oxidase, in particular, operates close to its maximum catalytic capacity (k(cat)). Thus, high flux rates are achieved via (i) high respiratory enzyme content per unit muscle mass and (ii) the operation of these enzymes at high fractional velocities.


1999 ◽  
Vol 202 (18) ◽  
pp. 2485-2493
Author(s):  
R.E. Bishop ◽  
J.J. Torres

Leptocephali are the unusual transparent larvae that are typical of eels, bonefish, tarpon and ladyfish. Unlike the larvae of all other fishes, leptocephali may remain in the plankton as larvae for several months before metamorphosing into the juvenile form. During their planktonic phase, leptocephali accumulate energy reserves in the form of glycosaminoglycans, which are then expended to fuel metamorphosis. The leptocephalus developmental strategy is thus fundamentally different from that exhibited in all other fishes in two respects: it is far longer in duration and energy reserves are accumulated. It was anticipated that the unusual character of leptocephalus development would be reflected in the energy budget of the larva. This study describes the allocation of energy to metabolism and excretion, two important elements of the energy budget. Metabolic rates were measured directly in four species of leptocephali, Paraconger caudilimbatus, Ariosoma balearicum, Gymnothorax saxicola and Ophichthus gomesii, using sealed-jar respirometry at sea. Direct measurements of metabolic rates were corroborated by measuring activities of lactate dehydrogenase and citrate synthase, two key enzymes of intermediary metabolism, in addition to that of Na(+)/K(+)-ATPase, a ubiquitous ion pump important in osmotic regulation. Excretion rates were determined by subsampling the sea water used in the respiratory incubations. The entire premetamorphic size range for each species was used in all assays. Mass-specific oxygen consumption rate, excretion rate and all enzyme activities (y) declined precipitously with increasing mass (M) according to the equation y=aM(b), where a is a species-specific constant and −1.74<b<-0.44. In leptocephali, the highly negative slope of the familiar allometric equation describing the relationship between mass-specific metabolic rate and mass, normally between −0.33 and 0, showed that a massive decline in metabolic rate occurs with increasing size. The result suggests that the proportion of actively metabolizing tissue also declines with size, being replaced in large measure by the metabolically inert energy depot, the glycosaminoglycans. Leptocephali can thus grow to a large size with minimal metabolic penalty, which is an unusual and successful developmental strategy.


Sign in / Sign up

Export Citation Format

Share Document