Rediscovering and Reviving Old Observations and Explanations of Metabolic Scaling in Living Systems

Abstract

Why the rate of metabolism varies (scales) in regular, but diverse ways with body size is a perennial, incompletely resolved question in biology. In this article, I discuss several examples of the recent rediscovery and (or) revival of specific metabolic scaling relationships and explanations for them previously published during the nearly 200-year history of allometric studies. I carry out this discussion in the context of the four major modal mechanisms highlighted by the contextual multimodal theory (CMT) that I published in this journal four years ago. These mechanisms include metabolically important processes and their effects that relate to surface area, resource transport, system (body) composition, and resource demand. In so doing, I show that no one mechanism can completely explain the broad diversity of metabolic scaling relationships that exists. Multi-mechanistic models are required, several of which I discuss. Successfully developing a truly general theory of biological scaling requires the consideration of multiple hypotheses, causal mechanisms and scaling relationships, and their integration in a context-dependent way. A full awareness of the rich history of allometric studies, an openness to multiple perspectives, and incisive experimental and comparative tests can help this important quest.

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

“…Others claim that heterogeneous contingent factors are importantly involved in determining both the slopes and elevations of metabolic scaling relationships [10,16,23,32,[50][51][52]. As a point of departure for my discussion about the contingency versus constraints debate, I focus on published data showing that an extrinsic factor, namely ambient temperature, not only significantly affects the scaling of metabolic rate, but also does so in fundamentally different ways in ectothermic and endothermic animals.…”

“…It invokes effects of T a on growth rate, which cannot explain negative associations between T a and the metabolic scaling exponent commonly observed in ectothermic organisms. Decreasing T a inhibits growth rate, and decreased growth rates are associated with lower, not higher metabolic scaling exponents (see [10,32,44,96]). …”

“…As further evidence, when the effects of activity are removed in an actively mobile species, such as the fish Coregonus albula, T a and the resting metabolic scaling exponent are strongly negatively correlated [115], as predicted by the MLBH [16,26]. Further studies of the effects of various abiotic and biotic ecological factors on metabolic scaling would also be worthwhile (see also [10,16,22,26,32,41,[44][45][46]48]). …”

“…I recommend future research that attempts to explain the diversity of metabolic scaling and its sensitivity to a variety of intrinsic and extrinsic factors, rather than a non-existent universal metabolic scaling law (e.g., 3/4-power law) (see [10,16,23,32,105]). Potentially productive approaches include comparative and experimental studies exploring how various intrinsic and extrinsic factors interact to produce a variety of metabolic scaling relationships, and how biological regulation mediates these interactions.…”

“…However, in the 1930s, animal scientists such as Kleiber and Brody discovered that the interspecific scaling of basal (resting) metabolic rate in mammals more closely matched a 3/4-power relationship than a 2/3-power relationship [17,18]. In 1960, Hemmingsen [19] claim that heterogeneous contingent factors are importantly involved in determining both the slopes and elevations of metabolic scaling relationships [10,16,23,32,[50][51][52].…”