Reconsidering the mechanistic basis of the metabolic theory of ecology

Abstract

The recently proposed metabolic theory of ecology (MTE) claims to provide a mechanistic explanation for long known allometric relationships between mass and metabolic rate. The MTE postulates that these patterns of allometry are driven by the primary selective constraint of transport of energy and materials. However, recent evidence along several different lines has called into question both the adequacy and the universality of this mechanism. We review the accumulating body of literature on this subject, adding our own concerns and criticisms. In addition to other difficulties, we argue that MTE fails as a mechanistic explanation of mass versus metabolic rate allometries because: 1) circulatory cost minimization is not a tenable criterion for evolutionary optimization, 2) the Boltzmann type relationships on which MTE depends are inadequate descriptors of complex metabolic pathways, and 3) most of the hypotheses advanced by the MTE do not, in fact, depend on the proposed mechanism and therefore cannot be used to test the theory. We conclude that the MTE should be abandoned as a monolithic explanation for allometric patterns, and that a more realistic path toward a better understanding of allometry would be to consider multiple explanatory mechanisms for physiological allometries.Biologists have been intrigued by allometric scaling relationships between organismal form, function, and ecology for more than a century. Such scaling relationships are taxonomically pervasive and have inspired a literature that, by 20 years ago, resulted in three nearly simultaneous, but remarkably different, book-length reviews (Peters 1983, Calder 1984, Schmidt-Nielsen 1984. Nonetheless, there is currently no widely accepted general mechanism for these patterns. Hypothesized explanations include structural and functional factors (e.g. surface area/volume effects on exchanges of heat and metabolites; reviewed by Calder 1984, Dodds et al. 2001, biomechanical requirements for support and fracture resistance (McMahon 1973, Biewener 2005, and correlated natural selection on body size and life history (Kozlowski and Weiner 1997).Recently, West et al. and others have advanced a metabolic theory of ecology (MTE Á West et al. 1997, Brown et al. 2004a which:1. conjectures that a quasi-fractal structure of distributional networks like circulatory systems requires an allometry (e.g. metabolism 0/a mass b , where a is a ''normalization constant'' and b is a scaling exponent) in order to minimize transport costs of energy and materials 2. argues that minimizing these transport costs requires a scaling exponent of b 0/3/4, which in

The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment

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

“…The influence of adaptive evolution, as mediated by various ecological factors, on SA, SC and RD mechanisms of metabolic scaling, is schematically depicted in Figure 6 (also see Figures 4 and 5 in [20] [19,20,46,[56][57][58]60,98,99,103,105,106,212,257]. Contrary to the MTE view, metabolic rate may not always be a pacemaker for other biological and ecological processes (reviewed in [98]; also see [51,244,257,258]). Recognition of demand-side effects on metabolic scaling opens up numerous possibilities for how extrinsic (ecological) factors may affect these relationships [20].…”

Testing Metabolic Theories

“…However, vociferous debate has ensued on the universality of the empirically observed scaling (Glazier 2005;White et al 2007;Makarieva et al 2008), the empirical and statistical validity of the temperature dependence term (Clarke 2004;Irlich et al 2009), fundamental principles of the models (Makarieva et al 2004;Suarez et al 2004;Kozłowski and Konarzewski 2005;O'Connor et al 2007;Apol et al 2008;Banavar et al 2010), and their predictive capacity (Algar et al 2007).…”