Why does metabolism scale with temperature?

Abstract

At a fundamental level, all of ecology is underpinned by the laws of thermodynamics, the conservation of matter and the general physical principles that dictate how gases and liquids move. Taken altogether, this indicates that there is nothing special about the way organisms function; physiology and ecology are simply physics and chemistry writ complex. In a stimulating review, Lawton (1999) argued that ecology has no laws comparable to physics, but does have what he called widely observable tendencies. These provide a structure for ecology, but they cannot be deduced from first principles. The complication here is scale. At small scales organisms do things that can be analysed, understood and relatively easily predicted. At very large scales (typically continental or global) patterns emerge that can be described statistically; explanations for these global patterns are proving more elusive and this is the challenge of the rapidly developing field of macroecology (Brown 1995). At intermediate scales we are faced with a mixture of contingent case studies and weak generalizations (Lawton 1999). The emerging field of complexity has much to offer here (Maurer 1999), but as yet its impact on mainstream ecology has been small. Organism size has long been recognized as a major factor in ecology and in the 1980s a number of attempts were made to use allometric or scaling techniques to provide a theoretical framework for understanding ecology (Peters 1983; Calder 1984; Schmidt-Nielsen 1984). Despite the stronger claims that allometry provided a theory of size (Peters 1983), the field of scaling has not provided the conceptual framework that is needed, although it has supplied useful analytical tools for studies of energy flow through aquatic food webs (Kerr & Dickie 2001). The problem we face is that a statistical description of phenomena is of limited use if we do not also have a sound understanding of the underlying processes that produce the patterns we observe and describe. Recently Brown, West and a series of colleagues have looked again at scaling properties in an attempt to build ecological laws from first principles. This research programme has had three main phases to date: To explain the size scaling properties of organismal physiology through the fractal-like design of exchange surfaces and distribution networks in animals and plants (West, Brown & Enquist 1997; West et al. 1999). To include the effect of temperature by incorporation of the temperature-dependence of biochemical reaction rate through the Boltzmann factor, which they termed the Universal Temperature Dependence (UTD) of metabolism (Gillooly et al. 2001). To extend this model of metabolism to other aspects of energetics such as development (Gillooly et al. 2002) as well as macroecological features such as global patterns in diversity (Allen, Brown & Gillooly 2002). The combination of the mass scaling and temperature components led Gillooly et al. (2001) to propose a simple equation describing the variation of metabolic rate (Q) of all organisms: Q = b0M3/4e −E/kT, where M is body mass, T is absolute temperature, k is Boltzmann's constant, E is the activation energy of metabolism (defined as the average activation energy for the rate-limiting enzyme-catalysed biochemical reactions of metabolism) and b0 is a scaling constant independent of M and T. This equation has attracted a great deal of attention from ecologists, and the fractal explanation of the widely described 3/4 mass scaling property of metabolism has been questioned (see for example Dodds, Rothman & Weitz 2001). The formulation of the relationship between metabolic rate and temperature is identical mathematically to the treatment of the thermal behaviour of reaction rate and the equilibrium constant by the early physical chemists (Arrhenius 1889, 1915; van't Hoff 1896). The proposition of the UTD is that the metabolic rate of organisms is driven directly by the kinetic energy of the cell; in other words a higher temperature leads automatically to a higher metabolic rate, whether this is an acute temperature change within an individual organism or in different species which have adapted to divergent thermal environments over evolutionary time. In this mechanistic form, the UTD thus makes no provision for acclimatization or evolutionary adaptation. This could theoretically be achieved to some extent by variations in E (the 'activation energy of metabolism'), and Gillooly et al. (2001) acknowledge that the residual variance about the fitted UTD model is probably related to differences in ecology between species. The key assumption underlying the UTD, that metabolic rate is driven mechanistically by temperature, is incompatible with what we know of cellular physiology and the molecular mechanisms of evolutionary adaptation to temperature (Clarke 2004). Nevertheless resting metabolic rate in ectotherms is widely (though not universally) observed to co-vary with environmental temperature,