A comparative meta-analysis of maximal aerobic metabolism of vertebrates: implications for respiratory and cardiovascular limits to gas exchange

Hillman, Stanley S.; Hancock, Thomas V.; Hedrick, Michael S.

doi:10.1007/s00360-012-0688-1

Cited by 64 publications

(52 citation statements)

References 66 publications

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“…The concept of symmorphosis (Weibel et al, 1991;Weibel, 2000) suggested there was no rate-limiting step to maximal O 2 transport because it was assumed that natural selection would eliminate excess capacity in a complex pathway such as O 2 transport (Weibel et al, 1991). The problem with the symmorphosis concept as applied to rate-limitation analysis is that is focuses solely on O 2 and ignores the role that these same transport processes play in eliminating CO 2 produced by the mitochondria (see Hillman et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

A meta-analysis ofin vivovertebrate cardiac performance: implications for cardiovascular support in the evolution of endothermy

Hillman

Hedrick

2015

Journal of Experimental Biology

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Endothermy in birds and mammals is associated with high body temperatures, and high rates of metabolism that are aerobically supported by elevated rates of cardiovascular O 2 transport. The purpose of this meta-analysis was to examine cardiovascular data from ectothermic and endothermic vertebrates, at rest and during exercise, with the goal of identifying key variables that may have contributed to the role of the cardiovascular system in supporting high rates of O 2 transport associated with endothermy. Vascular conductance, cardiac power and stroke work were summarized and calculated from a variety of studies at rest and during exercise for five classes of vertebrates where data were available. Conductance and cardiac power were linearly related to cardiac output from rest to exercise and also interspecifically. Exercise cardiac power and stroke work were greater in the endothermic species, owing to increased flow resulting from increased heart rate and increased pressure. Increased relative ventricle mass (RVM) was related to increased stroke volume in both groups. However, the increased RVM of endotherms was related to the increased pressure, as stroke work per gram of ventricle during exercise was equivalent between the groups. Cardiac power was linearly related to aerobic metabolic power, with 158 mW aerobic power output achieved per mW of cardiac power input. This analysis indicates that the greatly increased heart rate and cardiac stroke work leading to increased blood flow rate and blood pressure was necessary to support the metabolic requirements of endothermy.

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Section: Discussionmentioning

confidence: 99%

A meta-analysis ofin vivovertebrate cardiac performance: implications for cardiovascular support in the evolution of endothermy

Hillman

Hedrick

2015

Journal of Experimental Biology

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“…It is perhaps no coincidence that species with thicker respiratory barriers (e.g., salamanders, lungfish, and tortoises) also tend to have larger cells (77). Passive diffusion may be just one of many colimiting steps on oxygen consumption (78).…”

Section: Discussionmentioning

confidence: 99%

Body mass scaling of passive oxygen diffusion in endotherms and ectotherms

Gillooly

Gómez

Mavrodiev

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The area and thickness of respiratory surfaces, and the constraints they impose on passive oxygen diffusion, have been linked to differences in oxygen consumption rates and/or aerobic activity levels in vertebrates. However, it remains unclear how respiratory surfaces and associated diffusion rates vary with body mass across vertebrates, particularly in relation to the body mass scaling of oxygen consumption rates. Here we address these issues by first quantifying the body mass dependence of respiratory surface area and respiratory barrier thickness for a diversity of endotherms (birds and mammals) and ectotherms (fishes, amphibians, and reptiles). Based on these findings, we then use Fick's law to predict the body mass scaling of oxygen diffusion for each group. Finally, we compare the predicted body mass dependence of oxygen diffusion to that of oxygen consumption in endotherms and ectotherms. We find that the slopes and intercepts of the relationships describing the body mass dependence of passive oxygen diffusion in these two groups are statistically indistinguishable from those describing the body mass dependence of oxygen consumption. Thus, the area and thickness of respiratory surfaces combine to match oxygen diffusion capacity to oxygen consumption rates in both air-and water-breathing vertebrates. In particular, the substantially lower oxygen consumption rates of ectotherms of a given body mass relative to those of endotherms correspond to differences in oxygen diffusion capacity. These results provide insights into the long-standing effort to understand the structural attributes of organisms that underlie the body mass scaling of oxygen consumption.allometry | metabolic theory | respiration rate | metabolism | oxygen consumption S ince the classic debates of Krogh and Bohr (1), the relationship of passive oxygen diffusion to oxygen consumption has remained the focus of considerable research (2). Still, we have much to learn about how oxygen diffusion across respiratory surfaces relates to whole-organism oxygen consumption (3). In particular, we have much to learn about how the structural constraints on oxygen diffusion capacity, namely the thickness and area of respiratory surfaces, relate to the body mass scaling of oxygen consumption in vertebrates-a pattern that reflects the scaling of species' energy use (3).Studies on the body mass dependence of oxygen diffusion have been undertaken over the last century in all major classes of vertebrates, typically using respiratory surface area as a metric of diffusion capacity (2, 3). Less commonly, studies have also considered potentially relevant changes in respiratory barrier thickness with mass (4). In many cases, these studies have concluded that the body mass scaling of oxygen diffusion relative to that of oxygen consumption differs between endotherms and ectotherms (3,5,6). This has led to very different conclusions regarding the structure and function of respiratory systems among classes of vertebrates, as explained below.Among endotherms, particularly...

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“…As with birds and mammals, increased RMR gives rise to elevated body temperatures which, in turn, enhances energy turnover rates and aerobic performance (Clarke and Pörtner 2010). Even though the cost of transport for swimming animals is low compared to those that walk or fly (Schmidt-Nielsen 1972), which probably explains why many fish species exhibit a broad range of aerobically supported locomotory speeds with a relatively low MMR (Bennett and Ruben 1979;Hillman et al 2013), it appears that in temperate waters there is also strong selection on the capacity for remaining active.…”

Section: Selection For Increased Locomotor Capacitymentioning

confidence: 99%

Ecological Influences and Morphological Correlates of Resting and Maximal Metabolic Rates across Teleost Fish Species

Killen

Glazier

Rezende

et al. 2016

The American Naturalist

208

259

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Rates of aerobic metabolism vary considerably across evolutionary lineages, but little is known about the proximate and ultimate factors that generate and maintain this variability.Using data for 131 teleost fish species, we performed a large-scale phylogenetic comparative analysis of how interspecific variation in resting and maximum metabolic rates (RMR and MMR, respectively) is related to several ecological and morphological variables. Mass-and temperature-adjusted RMR and MMR are highly correlated along a continuum spanning a 30-to 40-fold range. Phylogenetic generalized least squares models suggest RMR and MMR are higher in pelagic species and that species with higher trophic levels exhibit elevated MMR. This variation is mirrored at various levels of structural organization: gill surface area, muscle protein content, and caudal fin aspect ratio (a proxy for activity) are positively related with aerobic capacity. Muscle protein content and caudal fin aspect ratio are also positively correlated with RMR. Hypoxia-tolerant lineages fall at the lower end of the metabolic continuum. Different ecological lifestyles are associated with contrasting levels of aerobic capacity, possibly reflecting the interplay between selection for increased locomotor performance on one hand and tolerance to low resource availability, particularly oxygen, on the other. These results support the aerobic capacity model of the evolution of endothermy, suggesting elevated body temperatures evolved as correlated responses to selection for high activity levels.

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A comparative meta-analysis of maximal aerobic metabolism of vertebrates: implications for respiratory and cardiovascular limits to gas exchange

Cited by 64 publications

References 66 publications

A meta-analysis ofin vivovertebrate cardiac performance: implications for cardiovascular support in the evolution of endothermy

A meta-analysis ofin vivovertebrate cardiac performance: implications for cardiovascular support in the evolution of endothermy

Body mass scaling of passive oxygen diffusion in endotherms and ectotherms

Ecological Influences and Morphological Correlates of Resting and Maximal Metabolic Rates across Teleost Fish Species

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