Reconsidering the mechanistic basis of the metabolic theory of ecology

O’Connor, Michael; Kemp, Stanley J.; Agosta, Salvatore J.; Hansen, Frank C; Sieg, Annette E.; Wallace, Bryan P.; McNair, James N.; Dunham, Arthur E.

doi:10.1111/j.2006.0030-1299.15534.x

Cited by 29 publications

(56 citation statements)

References 104 publications

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“…In particular, the metabolic theory of ecology (MTE), which is largely a synthesis of pre-existing ideas and empirical data (O'Connor et al, 2007;Price et al, 2012;Glazier, 2013b), has been proposed as a basis for understanding the rates of various biological and ecological processes (Brown et al, 2004;Price et al, 2010;Sibly et al, 2012). In particular, the metabolic theory of ecology (MTE), which is largely a synthesis of pre-existing ideas and empirical data (O'Connor et al, 2007;Price et al, 2012;Glazier, 2013b), has been proposed as a basis for understanding the rates of various biological and ecological processes (Brown et al, 2004;Price et al, 2010;Sibly et al, 2012).…”

Section: Metabolic Theory: Scaling the Fire Of Life (1) The Metamentioning

confidence: 99%

“…Although it has been assumed that metabolism dictates the rates of other processes, this has not been clearly demonstrated in a mechanistic way (O'Connor et al, 2007). First, it is based empirically almost entirely on correlational analyses, which by themselves do not specify what is cause or effect.…”

Section: Metabolic Theory: Scaling the Fire Of Life (1) The Metamentioning

confidence: 99%

“…Rates of metabolism and other processes may not merely passively respond to changes in temperature, nor do so similarly as specified by the metabolic pacemaker assumption (see below), but also may be adaptively adjusted in specific environmentally sensitive ways (Penick et al, 1998;Clarke, 2004Clarke, , 2006Clarke & Fraser, 2004;O'Connor et al, 2007;Dell et al, 2011;; also see Section V). Rates of metabolism and other processes may not merely passively respond to changes in temperature, nor do so similarly as specified by the metabolic pacemaker assumption (see below), but also may be adaptively adjusted in specific environmentally sensitive ways (Penick et al, 1998;Clarke, 2004Clarke, , 2006Clarke & Fraser, 2004;O'Connor et al, 2007;Dell et al, 2011;; also see Section V).…”

Section: Metabolic Theory: Scaling the Fire Of Life (1) The Metamentioning

confidence: 99%

“…They may adaptively adjust their activities to temperature changes in ways that are not predicted by simple Boltzmann-Arrhenius kinetics. These and other examples of temperature compensation (Clarke, 2004(Clarke, , 2006O'Connor et al, 2007;Terblanche et al, 2009;Hare et al, 2010;White, Alton & Frappell, 2011;Dymowska et al, 2012;Pyl et al, 2012) suggest that even when the rates of biological processes increase with increasing temperature as predicted by the MTE, biological systems may be actively permitting (rather than merely passively succumbing to) such responses, at least to some extent, because they increase the rates of fitness-related processes (e.g. Furthermore, temperature influences the locomotor activity of this snail in a markedly different way than its metabolic rate , which also contradicts the metabolic pacemaker view (also see Section III for citations of other examples of temperature-induced dissociations between metabolic rate and the rates of other biological processes).…”

Section: (8) Temperature Effectsmentioning

confidence: 99%

“…Although the pace of life involves numerous biochemical, developmental, physiological, behavioural, and life-history processes with rates that often appear to be associated as a 'syndrome' (Ricklefs & Wikelski, 2002) or along a 'single slow-fast axis' (Versteegh et al, 2012), it is usually quantified as the rate of metabolism, which is most often estimated by the rate of oxygen consumption or carbon dioxide production, i.e. However, and somewhat surprisingly, unlike other assumptions and predictions of the MTE, this fundamental assumption has received little or no critical analysis, including in several recent major reviews and forums concerning the MTE (Agrawal, 2004;O'Connor et al, 2007;Price et al, 2010Price et al, , 2012Sibly, Brown & Kodric-Brown, 2012). Moreover, it has long been assumed by many biologists that metabolic rate is the driver or 'pacemaker' for other biological processes (see e.g.…”

Section: Introductionmentioning

confidence: 99%

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Is metabolic rate a universal ‘pacemaker’ for biological processes?

2014

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A common, long-held belief is that metabolic rate drives the rates of various biological, ecological and evolutionary processes. Although this metabolic pacemaker view (as assumed by the recent, influential 'metabolic theory of ecology') may be true in at least some situations (e.g. those involving moderate temperature effects or physiological processes closely linked to metabolism, such as heartbeat and breathing rate), it suffers from several major limitations, including: (i) it is supported chiefly by indirect, correlational evidence (e.g. similarities between the body-size and temperature scaling of metabolic rate and that of other biological processes, which are not always observed) - direct, mechanistic or experimental support is scarce and much needed; (ii) it is contradicted by abundant evidence showing that various intrinsic and extrinsic factors (e.g. hormonal action and temperature changes) can dissociate the rates of metabolism, growth, development and other biological processes; (iii) there are many examples where metabolic rate appears to respond to, rather than drive the rates of various other biological processes (e.g. ontogenetic growth, food intake and locomotor activity); (iv) there are additional examples where metabolic rate appears to be unrelated to the rate of a biological process (e.g. ageing, circadian rhythms, and molecular evolution); and (v) the theoretical foundation for the metabolic pacemaker view focuses only on the energetic control of biological processes, while ignoring the importance of informational control, as mediated by various genetic, cellular, and neuroendocrine regulatory systems. I argue that a comprehensive understanding of the pace of life must include how biological activities depend on both energy and information and their environmentally sensitive interaction. This conclusion is supported by extensive evidence showing that hormones and other regulatory factors and signalling systems coordinate the processes of growth, metabolism and food intake in adaptive ways that are responsive to an organism's internal and external conditions. Metabolic rate does not merely dictate growth rate, but is coadjusted with it. Energy and information use are intimately intertwined in living systems: biological signalling pathways both control and respond to the energetic state of an organism. This review also reveals that we have much to learn about the temporal structure of the pace of life. Are its component processes highly integrated and synchronized, or are they loosely connected and often discordant? And what causes the level of coordination that we see? These questions are of great theoretical and practical importance.

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Section: Metabolic Theory: Scaling the Fire Of Life (1) The Metamentioning

confidence: 99%

Section: Metabolic Theory: Scaling the Fire Of Life (1) The Metamentioning

confidence: 99%

Section: Metabolic Theory: Scaling the Fire Of Life (1) The Metamentioning

confidence: 99%

Section: (8) Temperature Effectsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Is metabolic rate a universal ‘pacemaker’ for biological processes?

2014

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The combined effects of reactant kinetics and enzyme stability explain the temperature dependence of metabolic rates

DeLong

Gibert

Luhring

et al. 2017

Ecology and Evolution

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A mechanistic understanding of the response of metabolic rate to temperature is essential for understanding thermal ecology and metabolic adaptation. Although the Arrhenius equation has been used to describe the effects of temperature on reaction rates and metabolic traits, it does not adequately describe two aspects of the thermal performance curve (TPC) for metabolic rate—that metabolic rate is a unimodal function of temperature often with maximal values in the biologically relevant temperature range and that activation energies are temperature dependent. We show that the temperature dependence of metabolic rate in ectotherms is well described by an enzyme‐assisted Arrhenius (EAAR) model that accounts for the temperature‐dependent contribution of enzymes to decreasing the activation energy required for reactions to occur. The model is mechanistically derived using the thermodynamic rules that govern protein stability. We contrast our model with other unimodal functions that also can be used to describe the temperature dependence of metabolic rate to show how the EAAR model provides an important advance over previous work. We fit the EAAR model to metabolic rate data for a variety of taxa to demonstrate the model's utility in describing metabolic rate TPCs while revealing significant differences in thermodynamic properties across species and acclimation temperatures. Our model advances our ability to understand the metabolic and ecological consequences of increases in the mean and variance of temperature associated with global climate change. In addition, the model suggests avenues by which organisms can acclimate and adapt to changing thermal environments. Furthermore, the parameters in the EAAR model generate links between organismal level performance and underlying molecular processes that can be tested for in future work.

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What controls microzooplankton biomass and herbivory rate across marginal seas of China?

Liu

Chen

Zheng

et al. 2020

Limnology & Oceanography

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Microzooplankton are the primary herbivores and nutrient regenerators in the marine food web, but their importance is often underestimated, and the quantitative relationships between environmental factors and the biomass and herbivory rate of microzooplankton remain obscure. To fill this gap, we conducted 224 dilution experiments to measure microzooplankton biomass and herbivory rate across a vast area of the marginal seas of China. To gain the potential mechanisms controlling microzooplankton herbivory, we also use a model that combines the Metabolic Theory of Ecology and the functional responses of grazing to quantify the effects of temperature, phytoplankton biomass, and microzooplankton biomass on microzooplankton grazing rate. We estimate an activation energy of 0.51 eV of microzooplankton and found that the Holling III function best described the functional response of microzooplankton grazing with a maximal ingestion rate of 4.76 d −1 at 15 C and a half-saturation constant of 0.27 μM N. We also find that microzooplankton biomass scales with phytoplankton biomass with an exponent of 0.77, consistent with the general 3/4 scaling law found in other ecosystems. This scaling relationship is accompanied by a shift from ciliates to heterotrophic dinoflagellates with increasing phytoplankton biomass. Our results provide empirical patterns that will be vital to parameterize and validate marine ecosystem models, particularly in China seas.

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Reconsidering the mechanistic basis of the metabolic theory of ecology

Cited by 29 publications

References 104 publications

Is metabolic rate a universal ‘pacemaker’ for biological processes?

Is metabolic rate a universal ‘pacemaker’ for biological processes?

The combined effects of reactant kinetics and enzyme stability explain the temperature dependence of metabolic rates

What controls microzooplankton biomass and herbivory rate across marginal seas of China?

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