Resting vs. active: a meta-analysis of the intra- and inter-specific associations between minimum, sustained, and maximum metabolic rates in vertebrates

Abstract

Variation in aerobic capacity has far reaching consequences for the physiology, ecology, and evolution of vertebrates. Whether at rest or active, animals are constrained to operate within the energetic bounds determined by their minimum (minMR) and sustained or maximum metabolic rates (upperMR). MinMR and upperMR can differ considerably among individuals and species but are often presumed to be mechanistically linked to one another. Specifically, minMR is thought to reflect the idling cost of the machinery needed to support upperMR. However, previous analyses based on limited datasets have come to conflicting conclusions regarding the generality and strength of their association.Here we conduct the first comprehensive assessment of their relationship, based on a large number of published estimates of both the intra-specific (n = 176) and inter-specific (n = 41) phenotypic correlations between minMR and upperMR, estimated as either exercise-induced maximum metabolic rate (VO ₂max), cold-induced summit metabolic rate (Msum), or daily energy expenditure (DEE).Our meta-analysis shows that there is a general positive association between minMR and upperMR that is shared among vertebrate taxonomic classes. However, there was stronger evidence for intra-specific correlations between minMR and Msum and between minMR and DEE than there was for a correlation between minMR and VO ₂max across different taxa. As expected, inter-specific correlation estimates were consistently higher than intra-specific estimates across all traits and vertebrate classes.An interesting exception to this general trend was observed in mammals, which contrast with birds and exhibit no correlation between minMR and Msum. We speculate that this is due to the evolution and recruitment of brown fat as a thermogenic tissue, which illustrates how some species and lineages might circumvent this seemingly general association.We conclude that, in spite of some variability across taxa and traits, the contention that minMR and upperMR are positively correlated generally holds true both within and across vertebrate species. Ecological and comparative studies should therefore take into consideration the possibility that variation in any one of these traits might partly reflect correlated responses to selection on other metabolic parameters. A lay summary is available for this article.

Keywords: aerobic capacity; daily energy expenditure; locomotion; maximum thermogenesis; resting metabolic rate; standard metabolic rate.

Figure 1

(a) Conceptual model: The strength of association between minMR and upperMR should vary predictably with factorial aerobic scope (FAS = upperMR/minMR), as shown with the coil spring model, either because species with high FAS are near a physiological limit (stretched spring) or due to part‐whole correlation because minMR encompasses an increasingly large fraction of upperMR in species with lower FAS (compressed spring). (b) Empirical evaluation: Z‐scores of the correlation between minMR and each of exercise‐induced maximum metabolic rate (black), cold‐induced summit metabolic rate (grey) and daily energy expenditure (white). Data are from this study. Correlations were assessed using different measures of minMR: standard and basal metabolic rate (circles) or resting metabolic rate (squares). Our analyses support the later alternative for correlations involving DEE, as shown by the dotted line.

Figure 2

Phylogeny and distribution of effect sizes for the intra‐specific correlation between minMR and exercise‐induced maximum metabolic rate (VO ₂max), cold‐induced summit metabolic rate (Msum), and daily energy expenditure (DEE). Correlations were assessed using different measures of minMR: standard and basal metabolic rate (circles) or resting metabolic rate (squares). See Appendix S1 for details on species and their phylogenetic relationships and Appendix S2 for species’ correlations and references.

Figure 3

Effect sizes for the inter‐specific correlation between minimum metabolic rate and exercise‐induced maximum metabolic rate (VO ₂max), cold‐induced summit metabolic rate (Msum) or daily energy expenditure (DEE). Correlations in original studies were assessed with phylogenetic (squares) and non‐phylogenetic analyses (circles). See Appendix S3 for details of taxonomic classes and references.

Figure 4

Frequency distributions of the intra‐ and inter‐specific correlations between minimum metabolic rate (standard, basal, and resting) and each of exercise‐induced maximum metabolic rate (VO ₂max = black), cold‐induced maximum metabolic rate (Msum = grey), and daily energy expenditure (DEE = white) in vertebrates.

Figure 5

Means and 95% confidence intervals for effect sizes of the intra‐ and inter‐specific correlation between minimum metabolic rate and exercise‐induced maximum metabolic rate (VO ₂max), cold‐induced summit metabolic rate (Msum), and daily energy expenditure (DEE). Because inter‐specific estimates often differed between phylogenetic vs. non‐phylogenetic analyses (see Results), adjusted effect sizes were calculated for phylogenetic analyses.