Approaches for testing hypotheses for the hypometric scaling of aerobic metabolic rate in animals

Abstract

Hypometric scaling of aerobic metabolism (larger organisms have lower mass-specific metabolic rates (MR/g)), is nearly universal for interspecific comparisons among animals, yet we lack an agreed upon explanation for this pattern. If physiological constraints on the function of larger animals occur and limit MR/g, these should be observable as direct constraints on animals of extant species, and/or as evolved responses to compensate for the proposed constraint. There is evidence for direct constraints and compensatory responses to oxygen-supply constraint in skin-breathers but not vertebrates with gas exchange organs. Larger birds and mammals retain food in the gut for longer, consistent with a direct constraint on nutrient uptake across the gut wall, but there is little evidence for larger animals evolving compensatory responses to gut transport constraints. Larger placental mammals (but not marsupials or birds) show evidence of greater challenges with heat dissipation, but there is little evidence for compensatory adaptations to enhance heat loss in larger endotherms, suggesting MR more generally balances heat loss for thermoregulation in endotherms. Size-dependent patterns in many molecular, physiological and morphological properties are consistent with size-dependent natural selection, such as stronger selection on neurolocomotory performance and growth rate in smaller animals, and stronger selection for safety and longevity in larger. Hypometric scaling of MR very likely arises by different mechanisms in different taxa and conditions, consistent with the diversity of scaling slopes for MR.

The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy

“…Differences among life-stages in breathing patterns and modulation thereof were expected to result from structural differences in the tracheal system. Indeed, in other insect species investigated to date (mainly Lepidoptera), the larval internal air volume stays constant within an instar, with increasing larval mass (Callier and Nijhout, 2011; Harrison, 2018). This unchanging internal air volume probably leads to an increasing mismatch between their resting metabolic rate and oxygen supply as the larvae grow, before molting (see e.g., Greenlee and Harrison, 2005 for Lepidopteran larvae, but see Kivelä et al, 2016, 2019), as suggested by the negative correlations between CT max and body mass we observed.…”

“…Major remodeling or change in these relationships, within and across taxa, should produce predictable variation in the impacts of oxygen limitation on thermal tolerance. Depending on the type of metabolic theory and its mechanistic underpinnings (see e.g., Chown et al, 2007; Snelling et al, 2011a, b; Maino and Kearney, 2014; Harrison, 2018; Harrison et al, 2018) there may be considerable variation predicted in how the respiratory structure scales with body size. This scaling, in turn, is expected to have functional consequences for respiratory and athletic performance of a species (White et al, 2008; Snelling et al, 2011a, b).…”

Coevolution of body size and metabolic rate in vertebrates: a life‐history perspective

“…Reviewing mechanistic theories that address the hypoallometric mass scaling of MR is not our aim because many such reviews are available (e.g. Suarez, Darveau, & Childress, 2004;Glazier, 2005Glazier, , 2014Kearney & White, 2012;White & Kearney, 2014;Harrison, 2018a). Most of these theories ignore the coevolution between MR and body size and the driving force of mortality in this coevolution (but see Harrison, 2017Harrison, , 2018a.…”

Scaling of organ masses in mammals and birds: phylogenetic signal and implications for metabolic rate scaling

“…Although the existence of a universal value for b has been contradicted in recent decades (e.g. Harrison 2018 and citations there), the ubiquity of the hypoallometric scaling requires explanation on two levels: ultimate and proximate. There is no agreement on the ultimate causes ( Kozłowski et al 2020 ), whereas the proximate mechanism is clear but not always invoked: the relative size of metabolically relatively inert parts must increase with body mass or the relative size of energy-demanding organs must decrease with body mass or the mass-specific metabolic rate of energy-demanding organs must decrease with body mass or, most likely, some of these three phenomena occur simultaneously ( Krebs 1950 ; Wang et al 2001 ).…”