Why does metabolism scale with temperature?
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, and this requires explanation. Here we present an alternative explanation for the relationship between resting metabolic rate and environmental temperature in ectotherms. A glance at any biochemistry textbook will indicate the intense complexity of cellular metabolism. Complexity theory is now providing a glimpse at the underlying structure of metabolism (Jeong et al. 2000; Wagner & Fell 2001) but in energetic terms there is a common theme in that all these reactions involve water either as reactant or product (Clarke 2003a) and most require ATP. The production of ATP from glycolysis and the tricarboxylic acid (TCA) cycle is thus the central process in cellular metabolism. Metabolic rate is a measure of the power utilization of an organism, and is traditionally measured as the rate of oxygen consumption. This is a reasonable approximation for in most organisms ATP is generated aerobically using oxygen as the final electron acceptor. Some organisms do generate ATP anaerobically, and this can be important in low oxygen environments, or when large amounts of ATP are needed rapidly such as during intense muscular activity. Typically the accumulation of anaerobic end products is temporary and these are cleared later when oxygen is available once more. The stoichiometry of oxygen utilized to ATP generated is, however, not constant for it depends on the metabolic substrate being oxidized. A critical factor for any ecological discussion of metabolic rate is that the generation of ATP, and hence uptake of oxygen, does not proceed regardless; it is under complex and subtle feedback control. The most important control stems from the concentration of ATP itself. When ATP concentration is high, synthesis of ATP from ADP slows, and when ATP concentration drops because it is being utilized rapidly, synthesis of ATP is stimulated. There are also many other feedback mechanisms, such as inhibition of glycolysis by increase in the concentration of citric acid cycle intermediates. This leads to a simple ecological picture of metabolism (Fig. 1) which emphasizes that the synthesis of ATP, and hence the utilization of oxygen and metabolic substrate (food or reserves), is driven by demand for ATP. Synthesis of new macromolecules also requires a supply of reducing power (typically NADPH) and a limited suite of small molecular weight intermediaries to provide carbon skeletons (Fig. 1a), but in simply ecological terms the synthesis of ATP is driven by the demand for physiological work (Fig. 1b). This control of ATP synthesis (and hence oxygen consumption) is central to any ecological discussion of metabolic rate. In ectotherms there is no mechanism for a purely temperature-driven synthesis of ATP, which would anyway be needlessly wasteful of valuable resources: once ATP concentration has reached a high level, ATP synthesis stops. Since any living organism continues to require oxygen, the ecological question thus becomes, what is the ATP needed for? A conceptual model of metabolism. (a) Schematic diagram of the relationship between catabolic processes generating ATP, reducing power and a range of small molecular weight intermediates to provide carbon skeletons, and anabolic processes plus maintenance. (b) A further simplification to emphasize the role of physiological work, and not temperature, in regulating the rate at which ATP is synthesized, and hence oxygen and food or reserves utilized. Diagrams modified from Clarke (1991, 1993). It has long been recognized that there are a number of ATP-requiring processes which are essential for the cell to remain alive. These are often grouped together as basal metabolism. A simple functional definition of basal metabolism is shown in Fig. 2(a). Here basal metabolism is defined as the metabolic rate of an organism whose food intake is such that there is no net change in body mass. Higher food intake results in positive growth, a lower food intake in loss of mass as tissue is utilized to provide energy. The balance point is that food intake which just maintains body mass (hence the alternative term of maintenance metabolism), and this has been determined experimentally in many organisms by measuring growth rate as a function of food intake. This functional definition of basal metabolism reflects the early history of energetics, for which studies of domesticated mammals and birds were central (Brody 1945; Blaxter 1967). This approach is, however, neither suitable nor perhaps meaningful for many invertebrate organisms, particularly during larval development. A pragmatic alternative is to estimate basal metabolism by the oxygen consumption of an inactive, postabsorbtive, non-growing and non-reproducing individual. This is often termed resting metabolism and in many cases provides our best practical estimate of basal metabolism (Fig. 2b). Fish physiologists have introduced a related (but not identical) concept of standard metabolism, which is the lowest metabolic rate sustained for short periods; this is typically lower than maintenance or resting metabolism (Brett & Groves 1979). A definition of basal metabolism. (a) The relationship between growth rate and ration, illustrating a functional definition of maintenance ration. Maintenance metabolism (basal metabolic rate) is defined operationally as the resting metabolic rate of an organism fed at maintenance levels. Data for larval Sepia officinalis (Clarke et al. 1989). (b) Diagrammatic representation of relationship between basal metabolic rate and active respiration, showing the definition of metabolic This diagram also emphasizes that although resting metabolic rate is the best practical estimate we can of basal metabolic rate, the are not = metabolic rate. the concept of basal metabolism has a long it is that we have to an understanding of what cellular processes are have from studies of cell and These indicate that a of basal metabolism is made from synthesis and work to energy important is the the which is the for ATP and the of this is an important of basal metabolism. some ectotherms are to more energy in than they in either growth or The of the different components of basal metabolism are to be the in all of all any tissue the absolute rate of basal metabolism, and the of the will on such as for synthesis and on et al. the basal metabolic rate of a of or will the basal metabolic rate of a organism will on the of with of basal metabolism & and it will also during development. This variation in the of different explain differences in basal metabolism between (Clarke & 1999). There however, also differences in basal metabolism within with ecology or within more active species to have higher basal metabolic & 1984; & and in have a higher standard metabolic rate than species & 2002). These differences be for by variation in concentration or but also by higher of work or metabolism thus a complex suite of very different processes all require ATP and hence oxygen consumption. Since the absolute and of these processes from tissue to and hence from organism to organism, the important question is, how do these in organisms living at different in the metabolic rate of organisms with body size and temperature have long been with the work in this field being that of of with ectotherms living over a range of a conceptual problem for this and the pragmatic approach either to to made at a temperature, or to the for ectotherms to a common temperature, using an for the temperature of basal metabolism. the of resting metabolic rate as a function of the temperature at which the organism living to the work of & it is relatively that this approach has been in The positive relationship between resting metabolic rate and temperature (Fig. is of all studies of organisms to Clarke & & 2000; et al. 2001). There are no comparable studies of organisms over the a being that of et al. This of standard metabolism in species of a weak but relationship with This different a fundamental between the physiology of and or the more complex thermal by The of this to be for other and for the of this we will on the where the is stronger and The relationship between temperature and metabolic rate. (a) The relationship determined by & for a The resting metabolism, and the oxygen consumption of the individual under The have been from in & from representation and This the and of the of resting metabolic rate to temperature in any (b) The relationship for species of with resting metabolic rate for the temperature at which the This is the from Clarke & The in of the rate as a function of which the features of the relationship between metabolic rate and temperature are of The first is that there is a between the (Fig. and the (Fig. The is that the variance also with There are three of explanation for the relationship between resting metabolic rate and temperature resting metabolic rate in a mechanistic The most such explanation is the temperature (UTD) of metabolism by Gillooly et al. In its be termed the UTD Clarke metabolic rate is to be mechanistically by temperature, driven by the kinetic energy of cellular This mechanism to an individual organism to an acute temperature and to organisms adapted over evolutionary to at different (see discussion in Clarke 2004). temperature the of the relationship between resting metabolic rate and temperature in organisms adapted to at different but its is through a combination of energetic and evolutionary temperature adaptation. This is the evolutionary of Clarke 2004). temperature has no on resting metabolic rate and the relationship is being the of on other has this but the it is very to know how to do other than by of all other or temperature Gillooly et al. (2001) propose that the higher kinetic energy of cellular components at higher leads directly to higher resting metabolic rate. Gillooly et al. (2001) do acknowledge that there is residual variance about the UTD and that this is related to ecological The of the UTD relationship is, however, a mechanistic relationship between resting metabolic rate and In other an organism living at a higher temperature has no but to more ATP and more There are with a purely relationship between temperature and resting metabolic rate. The first is the evolutionary question a higher temperature an organism to produce more ATP, and hence food or for no ecological There are ecological to be from a high resting metabolic rate the to generate a higher absolute and a more active Clarke 2004). The of such a high resting metabolic rate is, however, the of and evolutionary it is not the of a simple mechanistic to the higher for the from the at the environmental temperature of organisms with high and low resting metabolic (Fig. The most critical problem for the mechanistic however, on the evolutionary adaptation of to The combination of the distribution of energy in a of together with the concept of activation energy introduced by provides a mechanistic explanation of the thermal of reaction rate of simple in under equilibrium and where nothing in the from now however, that the rate-limiting in is not the and of to product to be relatively because of the structure and of the active it is the and of and These to be relatively and the of cellular to the energy change is not constant the temperature range by organisms & 2002). In simple from organisms living at different to differences in structure from the active which relatively independent of temperature 1995). the variation in concentration of and of the kinetic of the the for the of statistical to of the thermal behaviour of resting metabolic rate. The of evolutionary temperature adaptation is thus to key aspects of organismal physiology independent of cellular has to the of the work in this & and & 1997; for a of the field & These are in more in Clarke the of key metabolic can be relatively independent of temperature when organisms adapted to in different thermal environments are does the of living (basal metabolism) with The in the of temperature on cellular metabolism. we can a mechanistic of temperature on resting metabolic rate, it is that the are in some way (Fig. in our understanding of the processes in basal metabolic rate are to what these A key of basal metabolic rate is it has long been from studies of that individual at higher studies of from organisms living at different have shown that from organisms to be more than from or organisms 2000; & 2002). This a for in animals living at lower and yet the relationship between resting metabolic rate and temperature (Fig. would that absolute of synthesis major to basal metabolic 1) are in animals living at than that is, the The of this is that studies of thermal to be all at the temperature, the are adapted to work at different The important are and at the temperature at which the organism The rate at which a to be over is thus the of an evolutionary between function and the net being lower absolute of resting synthesis at low and higher in organisms living at (Clarke 1993). This for the relationship between function and is on studies of a small number of and to the of the know nothing of the thermal and kinetic of most of the and it is that and of cellular are by other in cellular or et al. Clarke The of the with and temperature & with discussion of any physiological to temperature, however, we cannot from the effect of temperature within species to the evolutionary The acute of a to a change in temperature is driven by thermodynamics, in between species much more than temperature in the case of organisms living at different will probably have that in and and The concentration of within also & of these are to & and hence we cannot from results from within species to the evolutionary species. To some extent is under evolutionary control example in the of and of & Brown and all we can do is at the end of the evolutionary to for and can be for the other components of basal metabolic rate, although here the are however, to a conceptual model of how and resting metabolic rate with temperature, and this is in Fig. This model has key A conceptual model of the relationship between resting metabolic rate and temperature in ectotherms. Data are shown for organisms, living at a temperature, at a temperature and at a high The the acute effect of temperature on species. The the resting metabolic rate for species at its living The relationship is different in from the It is also different in being a statistical of individual evolutionary (a) (b) which emphasizes the in between the within and The relationship between resting metabolic rate and temperature reflects the acute effect of temperature on the temperature more ATP is to processes driven by higher cellular kinetic at processes The resting metabolic rate of any species at its environmental temperature an evolutionary for that by temperature, ecology and This is the evolutionary (Clarke 2004). The complexity of cellular structure and metabolism that the acute to temperature cannot be from first principles. It would however, that this is determined to a extent by the temperature of weak and are & 2002). A of within species for the acute effect of temperature on resting metabolic rate in a of = (Clarke & 1999). the relationship between resting metabolic rate and temperature is the of evolutionary it cannot be from first principles. It can be described however, what evolutionary are to the resting metabolic rate of a species. The of basal metabolic rate be from food or and it would be that environments with or acute food would for a basal metabolic rate and an metabolism a of food for the synthesis of this can the of a higher basal metabolic rate in of in organisms are by a very low resting metabolic rate and not to energy reserves the long when is or In organisms whose the energetic of in the water do reserves for (Clarke & a higher basal metabolic rate is it also In it would that to be constant the range of physiological at within related Clarke & This that a higher basal metabolic rate a absolute and hence more active (Clarke alternative way of at this is that an energetic with it a high basal metabolic rate. A higher basal metabolic rate also a more to an environmental through more cellular The basal metabolic rate of an organism thus depends on its ecology, with the being by an evolutionary between and A of with indicates that when ecology is there a positive relationship between resting metabolic rate and temperature et al. The variance in resting metabolic rate at higher when all are a range of evolutionary at with lower It is not this is important be temperature related on ATP generation by or on the power that can be by (Clarke important question is whether the basal metabolic rate at a higher temperature, or a more energetic a general of all or whether some processes increase more with temperature than work on the has that at low absolute of synthesis are but a lower of this is as growth This that at low a of is perhaps because of these are for they do that the balance of processes basal metabolic rate the physiological temperature This is an important for particularly in of and function (Clarke Since individual species a more or independent evolutionary the relationship between resting metabolic rate and temperature can be described as a statistical are independent because of more related species to have more and than more related The energetic however, that the would be than the acute (Fig. in other words the between species. The of the UTD of metabolic rate by temperature, would that these would be identical (Clarke 2004). In the case of the of the evolutionary is in that the of the of the for studies (Clarke & 1999). The is, however, small and cannot be as a of by temperature (the or UTD however, our understanding of the physiological processes basal metabolic rate, and the mechanisms of evolutionary adaptation to temperature, indicate that the relationship between temperature and resting metabolic rate is of A of resting metabolic rate as a function of temperature (Fig. is and variance with This is a common in macroecology and the of more than however, to work with where generalizations are needed for incorporation in The for can be by any of statistical and of metabolic rate as a function of (Clarke & 1999). studies but more the model has perhaps because of its in statistical The for are in in Fig. three to the variance the temperature and they are at There is thus to between although the fitted do different for thermal It has long been that in organisms basal metabolic rate, as by resting metabolic rate, with mechanistic explanations have been that temperature resting metabolic rate higher at simply as a of thermodynamics, energetic and evolutionary this is not an resting metabolic rate to be by an evolutionary between and ecological The resting metabolic rate thus be as the energetic of evolutionary temperature in the of the energetic demand of cellular adapted to at a temperature (Clarke a picture of the of the relationship between temperature and resting metabolic rate is emerging for organisms, this is not yet the case for ectotherms. At present we cannot whether the more complex thermal of many has led to the of a different thermal or whether the of the simply makes the evolutionary to A more understanding of the processes of basal metabolic rate, and these with temperature, is important to physiology to ecology in what has been termed evolutionary physiology et al. and for the to this also and for useful aspects of the in this