Scaling of Metabolic Scaling within Physical Limits

Abstract

Both the slope and elevation of scaling relationships between log metabolic rate and log body size vary taxonomically and in relation to physiological or developmental state, ecological lifestyle and environmental conditions. Here I discuss how the recently proposed metabolic-level boundaries hypothesis (MLBH) provides a useful conceptual framework for explaining and predicting much, but not all of this variation. This hypothesis is based on three major assumptions: (1) various processes related to body volume and surface area exert state-dependent effects on the scaling slope for metabolic rate in relation to body mass; (2) the elevation and slope of metabolic scaling relationships are linked; and (3) both intrinsic (anatomical, biochemical and physiological) and extrinsic (ecological) factors can affect metabolic scaling. According to the MLBH, the diversity of metabolic scaling relationships occurs within physical boundary limits related to body volume and surface area. Within these limits, specific metabolic scaling slopes can be predicted from the metabolic level (or scaling elevation) of a species or group of species. In essence, metabolic scaling itself scales with metabolic level, which is in turn contingent on various intrinsic and extrinsic conditions operating in physiological or evolutionary time. The MLBH represents a "meta-mechanism" or collection of multiple, specific mechanisms that have contingent, state-dependent effects. As such, the MLBH is Darwinian in approach (the theory of natural selection is also meta-mechanistic), in contrast to currently influential metabolic scaling theory that is Newtonian in approach (i.e., based on unitary deterministic laws). Furthermore, the MLBH can be viewed as part of a more general theory that includes other mechanisms that may also affect metabolic scaling.

Effects of Contingency versus Constraints on the Body-Mass Scaling of Metabolic Rate

“…Small cells (and organisms containing them) tend to have higher mass-specific metabolic rates than large cells (and organisms containing them) [26,[69][70][71][72][73][74][75][76][77]. Therefore, like the MTE, cell-size theory predicts that changing temperature should affect the elevation of metabolic scaling relationships, but not their slopes (but see Section 3.2.2), which again is contradicted by the results described in this study.…”

“…The model that best explains the observed results is the metabolic-level boundaries hypothesis (MLBH) [23,26]. It predicts that changes in temperature should affect both the elevation and slope of metabolic scaling relationships [26], as observed in this study and several other studies (e.g., [16,26,48,53]; also see Section 3.2.2).…”

“…It predicts that changes in temperature should affect both the elevation and slope of metabolic scaling relationships [26], as observed in this study and several other studies (e.g., [16,26,48,53]; also see Section 3.2.2). Moreover, it uniquely predicts that increasing temperature should result in decreases in the metabolic scaling exponent in ectotherms (Figures 1 and 2), but increases in the exponent in endotherms (Figures 3 and 4), again as observed.…”

“…According to the MLBH, at low metabolic levels, volume-related tissue maintenance chiefly influences metabolic scaling (scaling slope approaching 1 in organisms with uniform scaling of metabolic rate in different tissues), whereas at high metabolic levels, surface-area-related processes (such as resource uptake, metabolic waste removal, and heat dissipation) predominate (scaling slope approaching 2/3 in isomorphic organisms). In short, the scaling exponent for resting metabolic rate should vary between 2/3 and 1, depending on metabolic level [23,26].…”

“…Heat dissipation importantly affects the metabolic scaling of endotherms at all ambient temperatures (also see [23][24][25][26]28,56,58,87]), but in the thermoneutral zone, surface area is chiefly important, whereas at increasingly lower ambient temperatures outside the thermoneutral zone, insulation and the cross-surface temperature differential become increasingly important, as well. As Kendeigh and colleagues argued [56], metabolic heat production that exactly compensates for heat dissipation in the cold should scale approximately to the 0.5 power, or as (M 0.167 )(M 0.667 )/(W 0.333 ), which are the hypothesized power relations for the thermal conductivity of the surface layer of insulation (h), surface area (A), and insulation thickness (I), respectively, for endotherms.…”