Mean mass-specific metabolic rates are strikingly similar across life's major domains: Evidence for life's metabolic optimum

Abstract

A fundamental but unanswered biological question asks how much energy, on average, Earth's different life forms spend per unit mass per unit time to remain alive. Here, using the largest database to date, for 3,006 species that includes most of the range of biological diversity on the planet-from bacteria to elephants, and algae to sapling trees-we show that metabolism displays a striking degree of homeostasis across all of life. We demonstrate that, despite the enormous biochemical, physiological, and ecological differences between the surveyed species that vary over 10(20)-fold in body mass, mean metabolic rates of major taxonomic groups displayed at physiological rest converge on a narrow range from 0.3 to 9 W kg(-1). This 30-fold variation among life's disparate forms represents a remarkably small range compared with the 4,000- to 65,000-fold difference between the mean metabolic rates of the smallest and largest organisms that would be observed if life as a whole conformed to universal quarter-power or third-power allometric scaling laws. The observed broad convergence on a narrow range of basal metabolic rates suggests that organismal designs that fit in this physiological window have been favored by natural selection across all of life's major kingdoms, and that this range might therefore be considered as optimal for living matter as a whole.

Fig. 1.

Frequency distribution of log₁₀-transformed values of mass-specific metabolic rates q (W kg⁻¹) in species differing greatly in size, taxonomy, and trophic status (Table 1). (Left) Heterotrophs. (Right) Photoautotrophs. Three lowest values falling outside of the 99% C.I. are not shown for aquatic invertebrates. For vascular plants (seedlings and tree saplings), the vertical axis shows number N of individual plants studied.

Fig. 2.

Mean mass-specific metabolic rates q versus mean body mass M in the studied groups of organisms. Squares correspond to mean body mass and mean mass-specific metabolic rate in each group (Table 1); horizontal and vertical bars show 95% C.I. of body mass and mass-specific metabolic rate values, respectively, within each group. 1, heterotrophic prokaryotes; 2, heterotrophic protozoa; 3, insects; 4, aquatic invertebrates; 5, ectothermic vertebrates; 6, endothermic vertebrates; 7, cyanobacteria; 8, eukaryotic microalgae; 9, tree saplings; 10, tree seedlings. The dashed lines marked −1/4 and −1/3 describe the dependence q = q₀(M/M₀)^β, where β = −1/4 or −1/3, respectively, and M₀ = 0.2 mg and q₀ = 2.6 W kg⁻¹ are the unweighted averages of mean body masses and mean mass-specific metabolic rates of each group. Note that neither of the lines describes the studied dataset.

Fig. 3.

Body mass range of heterotrophic species that keep their mean taxonomic mass-specific metabolic rate within the proposed metabolic optimum of 1–4 × 10² W (kg N)⁻¹ or 3–9 W (kg wet mass)⁻¹ (Table 1); n is the number of species shown. This range harbors organisms of practically all sizes found on Earth. Aquatic invertebrates with body mass M ≫ 10⁻³ g and ectothermic vertebrates have lower metabolic rates outside of this range (Table 1) presumably because of the breathing costs' limitation (SI Appendix). A solid line and two dashed lines indicate the unweighted averages of the mean mass-specific metabolic rate (4.7 W kg⁻¹) and the upper and lower 95% C.I. (0.51 and 49 W kg⁻¹), respectively, across the five groups (Table 1). Species number of prokaryotes is less than in Table 1 because cell size estimates were unavailable for some species.