Reconsidering the mechanistic basis of the metabolic theory of ecology

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.

[1]  Joseph Heijnen,et al.  Metabolic Control Analysis , 2009 .

[2]  David W. Stephens,et al.  Optimal Foraging Theory , 2008 .

[3]  A. P. Allen,et al.  The mechanistic basis of the metabolic theory of ecology , 2007 .

[4]  J. Stuart,et al.  Metabolic rate does not scale with body mass in cultured mammalian cells. , 2007, American journal of physiology. Regulatory, integrative and comparative physiology.

[5]  Karl J. Niklas,et al.  Biological scaling: Does the exception prove the rule? , 2007, Nature.

[6]  Benjamin S. Halpern,et al.  Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation , 2007, Proceedings of the National Academy of Sciences.

[7]  A. P. Allen,et al.  Changes in body temperature influence the scaling of VO2max and aerobic scope in mammals. , 2007, Biology letters.

[8]  A. Dunham,et al.  Linking physiological effects on activity and resource use to population level phenomena. , 2006, Integrative and comparative biology.

[9]  R. Huey,et al.  Thermodynamics Constrains the Evolution of Insect Population Growth Rates: “Warmer Is Better” , 2006, The American Naturalist.

[10]  James H. Brown,et al.  Kinetic effects of temperature on rates of genetic divergence and speciation. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Stephanie A. Bohlman,et al.  Testing metabolic ecology theory for allometric scaling of tree size, growth and mortality in tropical forests. , 2006, Ecology letters.

[12]  Geoffrey B. West,et al.  Response to Clarke and Fraser: effects of temperature on metabolic rate , 2006 .

[13]  Mark G. Tjoelker,et al.  Universal scaling of respiratory metabolism, size and nitrogen in plants , 2006, Nature.

[14]  Tommaso Anfodillo,et al.  Convergent tapering of xylem conduits in different woody species. , 2006, The New phytologist.

[15]  Matthew W. Hahn,et al.  Ancient and Recent Positive Selection Transformed Opioid cis-Regulation in Humans , 2005, PLoS biology.

[16]  Bai-Lian Li,et al.  Energetics of the smallest: do bacteria breathe at the same rate as whales? , 2005, Proceedings of the Royal Society B: Biological Sciences.

[17]  D. S. Glazier,et al.  Beyond the ‘3/4‐power law’: variation in the intra‐and interspecific scaling of metabolic rate in animals , 2005, Biological reviews of the Cambridge Philosophical Society.

[18]  James H. Brown,et al.  The metabolic basis of whole-organism RNA and phosphorus content. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Geoffrey B. West,et al.  Yes, West, Brown and Enquist"s model of allometric scaling is both mathematically correct and biologically relevant , 2005 .

[20]  J. Kozłowski,et al.  West, Brown and Enquist's model of allometric scaling again: the same questions remain , 2005 .

[21]  N. Gotelli,et al.  ALLOMETRIC EXPONENTS SUPPORT A 3/4-POWER SCALING LAW , 2005 .

[22]  James H. Brown,et al.  The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization , 2005, Journal of Experimental Biology.

[23]  A. Biewener Biomechanical consequences of scaling , 2005, Journal of Experimental Biology.

[24]  Adrian Bejan,et al.  The constructal law of organization in nature: tree-shaped flows and body size , 2005, Journal of Experimental Biology.

[25]  C. Navas,et al.  Control of metabolic rate is a hidden variable in the allometric scaling of homeotherms , 2005, Journal of Experimental Biology.

[26]  K. Nagy Field metabolic rate and body size , 2005, Journal of Experimental Biology.

[27]  Thomas H Dawson,et al.  Modeling of vascular networks , 2005, Journal of Experimental Biology.

[28]  C. Moyes,et al.  Control of muscle bioenergetic gene expression: implications for allometric scaling relationships of glycolytic and oxidative enzymes , 2005, Journal of Experimental Biology.

[29]  E. Weibel,et al.  Exercise-induced maximal metabolic rate scales with muscle aerobic capacity , 2005, Journal of Experimental Biology.

[30]  A. J. Hulbert,et al.  Membranes and the setting of energy demand , 2005, Journal of Experimental Biology.

[31]  J. Speakman,et al.  Body size, energy metabolism and lifespan , 2005, Journal of Experimental Biology.

[32]  Craig R. White,et al.  Allometric scaling of mammalian metabolism , 2005, Journal of Experimental Biology.

[33]  C. Hemelrijk,et al.  Problems of allometric scaling analysis: examples from mammalian reproductive biology , 2005, Journal of Experimental Biology.

[34]  R. Suarez,et al.  Multi-level regulation and metabolic scaling , 2005, Journal of Experimental Biology.

[35]  James H. Brown,et al.  Linking the global carbon cycle to individual metabolism , 2005 .

[36]  N. Whiteley,et al.  Temperature Influences Whole‐Animal Rates of Metabolism but Not Protein Synthesis in a Temperate Intertidal Isopod , 2005, Physiological and Biochemical Zoology.

[37]  S. Austad Diverse aging rates in metazoans: targets for functional genomics , 2005, Mechanisms of Ageing and Development.

[38]  James H. Brown,et al.  The rate of DNA evolution: effects of body size and temperature on the molecular clock. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Michael Textbook of Medical Physiology , 2005 .

[40]  J. Rogers,et al.  Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  A. Sugden ECOLOGY/EVOLUTION: Phenotypic Plasticity , 2004 .

[42]  Walter Jetz,et al.  The Scaling of Animal Space Use , 2004, Science.

[43]  W. V. Van Voorhies Live fast – live long? A commentary on a recent paper by Speakman et al. , 2004, Aging cell.

[44]  James H. Brown,et al.  Toward a metabolic theory of ecology , 2004 .

[45]  P. Marquet,et al.  METABOLIC ECOLOGY: LINKING INDIVIDUALS TO ECOSYSTEMS , 2004 .

[46]  J. Fargione,et al.  DOES METABOLIC THEORY APPLY TO COMMUNITY ECOLOGY? IT'S A MATTER OF SCALE , 2004 .

[47]  M. Kaspari USING THE METABOLIC THEORY OF ECOLOGY TO PREDICT GLOBAL PATTERNS OF ABUNDANCE , 2004 .

[48]  K. L. Cottingham,et al.  METABOLIC RATE OPENS A GRAND VISTA ON ECOLOGY , 2004 .

[49]  H. Cyr,et al.  AN ILLUSION OF MECHANISTIC UNDERSTANDING , 2004 .

[50]  M. Koehl,et al.  CAN FUNCTION AT THE ORGANISMAL LEVEL EXPLAIN ECOLOGICAL PATTERNS , 2004 .

[51]  James H. Brown,et al.  RESPONSE TO FORUM COMMENTARY ON “TOWARD A METABOLIC THEORY OF ECOLOGY” , 2004 .

[52]  P. Redman,et al.  Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer , 2004, Aging cell.

[53]  A. Clarke Is there a Universal Temperature Dependence of metabolism , 2004 .

[54]  Geoffrey B. West,et al.  The predominance of quarter-power scaling in biology , 2004 .

[55]  A. Clarke,et al.  Why does metabolism scale with temperature , 2004 .

[56]  Jan Kozłowski,et al.  Is West, Brown and Enquist's model of allometric scaling mathematically correct and biologically relevant? , 2004 .

[57]  James H. Brown,et al.  Growth models based on first principles or phenomenology , 2004 .

[58]  M. Lesser,et al.  Seasonal temperature compensation in the horse mussel, Modiolus modiolus: metabolic enzymes, oxidative stress and heat shock proteins. , 2004, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[59]  Geoffrey B. West,et al.  Effects of Body Size and Temperature on Population Growth , 2004, The American Naturalist.

[60]  H. Pörtner,et al.  Effects of temperature acclimation on lactate dehydrogenase of cod (Gadus morhua): genetic, kinetic and thermodynamic aspects , 2004, Journal of Experimental Biology.

[61]  Pat Langley,et al.  Editorial: On Machine Learning , 1986, Machine Learning.

[62]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[63]  THE VALUE OF NULL THEORIES IN ECOLOGY , 2004 .

[64]  A. J. Hulbert,et al.  An allometric comparison of the mitochondria of mammalian and reptilian tissues: The implications for the evolution of endothermy , 2004, Journal of Comparative Physiology B.

[65]  M. Tatar,et al.  Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster , 2003, Aging cell.

[66]  J. Speakman,et al.  Age‐related changes in the metabolism and body composition of three dog breeds and their relationship to life expectancy , 2003, Aging cell.

[67]  Evan P. Economo,et al.  Scaling metabolism from organisms to ecosystems , 2003, Nature.

[68]  Lloyd Demetrius,et al.  Quantum statistics and allometric scaling of organisms , 2003 .

[69]  Russel D. Andrews,et al.  Allometric cascade: a model for resolving body mass effects on metabolism. , 2003, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[70]  C. R. White,et al.  Mammalian basal metabolic rate is proportional to body mass2/3 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[71]  A. Maritan,et al.  Physiology (communication arising): Allometric cascades , 2003, Nature.

[72]  Russel D. Andrews,et al.  Physiology (communication arising (reply)): Why does metabolic rate scale with body size?/Allometric cascades , 2003, Nature.

[73]  Geoffrey B. West,et al.  Physiology (communication arising): Why does metabolic rate scale with body size? , 2003, Nature.

[74]  O. Reichman,et al.  Physiology on a Landscape Scale: Plant-Animal Interactions1 , 2002, Integrative and comparative biology.

[75]  Kevin J. Gaston,et al.  Metabolic cold adaptation in insects: a large‐scale perspective , 2002 .

[76]  Raul K. Suarez,et al.  Allometric cascade as a unifying principle of body mass effects on metabolism , 2002, Nature.

[77]  James H. Brown,et al.  Effects of size and temperature on developmental time , 2002, Nature.

[78]  James H Brown,et al.  Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[79]  James H. Brown,et al.  Effects of Size and Temperature on Metabolic Rate , 2001, Science.

[80]  K J Niklas,et al.  Invariant scaling relationships for interspecific plant biomass production rates and body size , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[81]  T. Dawson Similitude in the cardiovascular system of mammals. , 2001, The Journal of experimental biology.

[82]  J. Weitz,et al.  Re-examination of the "3/4-law" of metabolism. , 2000, Journal of theoretical biology.

[83]  H V Westerhoff,et al.  A metabolic control analysis of kinetic controls in ATP free energy metabolism in contracting skeletal muscle. , 2000, American journal of physiology. Cell physiology.

[84]  J. Li Scaling and invariants in cardiovascular biology , 2000 .

[85]  J. Kozłowski Does body size optimization alter the allometries for production and life history traits , 2000 .

[86]  S. Dodson,et al.  The relationship of neonate mass and incubation temperature to embryonic development time in a range of animal taxa , 2000 .

[87]  Geoffrey B. West,et al.  Scaling in Biology , 2000 .

[88]  T. Jukes,et al.  The neutral theory of molecular evolution. , 2000, Genetics.

[89]  A. J. Hulbert,et al.  Mechanisms underlying the cost of living in animals. , 2000, Annual review of physiology.

[90]  Kenneth Petren,et al.  Experimental Ecology: Issues and Perspectives , 1999 .

[91]  James H. Brown,et al.  A general model for the structure and allometry of plant vascular systems , 1999, Nature.

[92]  M. O’connor,et al.  Biophysical constraints on the thermal ecology of dinosaurs , 1999, Paleobiology.

[93]  James H. Brown,et al.  The fourth dimension of life: fractal geometry and allometric scaling of organisms. , 1999, Science.

[94]  K. Wells Principles of Animal Design: The Optimization and Symmorphosis Debate. Ewald R. Weibel , C. Richard Taylor , Liana Bolis , 1999 .

[95]  Roderick C. Dewar,et al.  Acclimation of the respiration/photosynthesis ratio to temperature: insights from a model , 1999 .

[96]  Amos Maritan,et al.  Size and form in efficient transportation networks , 1999, Nature.

[97]  M. O’connor Physiological and ecological implications of a simple model of heating and cooling in reptiles , 1999 .

[98]  Hilan Bensusan,et al.  God Doesn't Always Shave with Occam's Razor - Learning When and How to Prune , 1998, ECML.

[99]  C. R. Taylor,et al.  Principles of Animal Design: The Optimization And Symmorphosis Debate , 1998 .

[100]  S. Vogel,et al.  Life in Moving Fluids , 2020 .

[101]  K. Dill,et al.  Protein folding in the landscape perspective: Chevron plots and non‐arrhenius kinetics , 1998, Proteins.

[102]  G. Brown,et al.  Cellular energy utilization and molecular origin of standard metabolic rate in mammals. , 1997, Physiological reviews.

[103]  L. Glickman,et al.  Comparative longevity of pet dogs and humans: implications for gerontology research. , 1997, The journals of gerontology. Series A, Biological sciences and medical sciences.

[104]  James H. Brown,et al.  A General Model for the Origin of Allometric Scaling Laws in Biology , 1997, Science.

[105]  J. Weiner,et al.  Interspecific Allometries Are by-Products of Body Size Optimization , 1997, The American Naturalist.

[106]  Geoffrey I. Webb Further Experimental Evidence against the Utility of Occam's Razor , 1996, J. Artif. Intell. Res..

[107]  A. F. Bennett,et al.  Animals and Temperature: List of contributors , 1996 .

[108]  H. Guderley,et al.  Animals and Temperature: Phenotypic plasticity and evolutionary adaptations of mitochondria to temperature , 1996 .

[109]  E. C. Beyer,et al.  Seasonal variation in metabolic rates and maintenance costs of the eastern fence lizard, Sceloporus undulatus , 1994 .

[110]  A. Dunham,et al.  THE EVOLUTION OF REPRODUCTIVE EFFORT IN SQUAMATE REPTILES: COSTS, TRADE‐OFFS, AND ASSUMPTIONS RECONSIDERED , 1994, Evolution; international journal of organic evolution.

[111]  Michael L. Pace,et al.  Allometric Theory: Extrapolations from Individuals to Communities , 1993 .

[112]  J. Bentz Intermediates and kinetics of membrane fusion. , 1992, Biophysical journal.

[113]  Lawrence B. Slobodkin,et al.  A Critique for Ecology , 1991 .

[114]  C. Gans,et al.  A Critique of Symmorphosis and Optimality Models in Physiology , 1991, Physiological Zoology.

[115]  Raymond L. Lindeman The trophic-dynamic aspect of ecology , 1942 .

[116]  T. Creighton,et al.  Protein Folding , 1992 .

[117]  D. Fell,et al.  Metabolic control analysis. The effects of high enzyme concentrations. , 1990, European journal of biochemistry.

[118]  J. N. Cameron The Respiratory Physiology of Animals , 1989 .

[119]  Arthur E. Dunham,et al.  Interfaces between Biophysical and Physiological Ecology and the Population Ecology of Terrestrial Vertebrate Ectotherms , 1989, Physiological Zoology.

[120]  Steven Vogel,et al.  Life's Devices: The Physical World of Animals and Plants , 1988 .

[121]  W. Calder Size, Function, and Life History , 1988 .

[122]  J. Szulmajster Protein folding , 1988, Bioscience reports.

[123]  R. Huey,et al.  PHYLOGENETIC STUDIES OF COADAPTATION: PREFERRED TEMPERATURES VERSUS OPTIMAL PERFORMANCE TEMPERATURES OF LIZARDS , 1987, Evolution; international journal of organic evolution.

[124]  G. Pierce,et al.  Eight Reasons Why Optimal Foraging Theory Is a Complete Waste of Time , 1987 .

[125]  W. Calder Scaling energetics of homeothermic vertebrates: an operational allometry. , 1987, Annual review of physiology.

[126]  J. Kingsolver,et al.  Mechanistic Constraints and Optimality Models: Thermoregulatory Strategies in Colias Butterflies , 1984 .

[127]  K. Schmidt-Nielsen,et al.  Scaling, why is animal size so important? , 1984 .

[128]  G. Pyke Optimal Foraging Theory: A Critical Review , 1984 .

[129]  Jonathan Roughgarden,et al.  Competition and Theory in Community Ecology , 1983, The American Naturalist.

[130]  Donald R. Strong,et al.  Natural Variability and the Manifold Mechanisms of Ecological Communities , 1983, The American Naturalist.

[131]  James F. Quinn,et al.  On Hypothesis Testing in Ecology and Evolution , 1983, The American Naturalist.

[132]  Joseph H. Connell,et al.  On the Prevalence and Relative Importance of Interspecific Competition: Evidence from Field Experiments , 1983, The American Naturalist.

[133]  R. Peters The Ecological Implications of Body Size , 1983 .

[134]  A. Hulbert,et al.  Comparison of the "mammal machine" and the "reptile machine": energy use and thyroid activity. , 1981, The American journal of physiology.

[135]  C. R. Taylor,et al.  Design of the mammalian respiratory system. I. Problem and strategy. , 1981, Respiration physiology.

[136]  E R Weibel,et al.  Design of the mammalian respiratory system. III Scaling maximum aerobic capacity to body mass: wild and domestic mammals. , 1981, Respiration physiology.

[137]  C. R. Taylor,et al.  Design of the mammalian respiratory system. , 1981, Respiration physiology.

[138]  F. H. Pough The Advantages of Ectothermy for Tetrapods , 1980, The American Naturalist.

[139]  S. Gould,et al.  The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[140]  舟木 広,et al.  Metabolic Rateと比表面積〔英文〕 , 1976 .

[141]  T. McMahon Using body size to understand the structural design of animals: quadrupedal locomotion. , 1975, Journal of applied physiology.

[142]  T. McMahon,et al.  Size and Shape in Biology , 1973, Science.

[143]  L. Boltzmann Weitere Studien über das Wärmegleichgewicht unter Gasmolekülen , 1970 .

[144]  Carl Gans,et al.  Biology of the Reptilia , 1969 .

[145]  Max Kleiber,et al.  The Fire of Life: An Introduction to Animal Energetics , 1975 .

[146]  W. Dawson,et al.  Relation of Oxygen Consumption to Body Weight, Temperature, and Temperature Acclimation in Lizards Uta stansburiana and Sceloporus occidentalis , 1956, Physiological Zoology.

[147]  W. Snodgrass Physiology , 1897, Nature.

[148]  W. Crozier On the Possibility of Identifying Chemical Processes in Living Matter. , 1924, Proceedings of the National Academy of Sciences of the United States of America.

[149]  A. Krogh,et al.  The Respiratory Exchange of Animals and Man , 2009, Nature.

[150]  Albert Y. Kim,et al.  Hypothesis Testing , 2019, Encyclopedic Dictionary of Archaeology.