Metabolic Scaling in Complex Living Systems

In this review I show that four major kinds of theoretical approaches have been used to explain the scaling of metabolic rate in cells, organisms and groups of organisms in relation to system size. They include models focusing on surface-area related fluxes of resources and wastes (including heat), internal resource transport, system composition, and various processes affecting resource demand, all of which have been discussed extensively for nearly a century or more. I argue that, although each of these theoretical approaches has been applied to multiple levels of biological organization, none of them alone can fully explain the rich diversity of metabolic scaling relationships, including scaling exponents (log-log slopes) that vary from ~0 to >1. Furthermore, I demonstrate how a synthetic theory of metabolic scaling can be constructed by including the context-dependent action of each of the above modal effects. This “contextual multimodal theory” (CMT) posits that various modulating factors (including metabolic level, surface permeability, body shape, modes of thermoregulation and resource-transport, and other internal and external influences) affect the mechanistic expression of each theoretical module. By involving the contingent operation of several mechanisms, the “meta-mechanistic” CMT differs from most metabolic scaling theories that are deterministically mechanistic. The CMT embraces a systems view of life, and as such recognizes the open, dynamic nature and complex hierarchical and interactive organization of biological systems, and the importance of multiple (upward, downward and reciprocal) causation, biological regulation of resource supply and demand and their interaction, and contingent internal (system) and external (environmental) influences on metabolic scaling, all of which are discussed. I hope that my heuristic attempt at building a unifying theory of metabolic scaling will not only stimulate further testing of all of the various subtheories composing it, but also foster an appreciation that many current models are, at least in part, complementary or even synergistic, rather than antagonistic. Further exploration about how the scaling of the rates of metabolism and other biological processes are interrelated should also provide the groundwork for formulating a general metabolic theory of biology.