Biochemical universality of living matter and its metabolic implications

Summary 1. Recent discussions of metabolic scaling laws focus on the model of West, Brown & Enquist (WBE). The core assumptions of the WBE model are the size-invariance of terminal units at which energy is consumed by living matter and the size-invariance of the rate of energy supply to these units. Both assumptions are direct consequences of the biochemical universality of living matter. However, the second assumption contradicts the central prediction of the WBE model that mass-specific metabolic rate q should decrease with body mass with a scaling exponent µ = − 1 / 4 , thus making the model logically inconsistent. 2. Examination of evidence interpreted by WBE and colleagues in favour of a universal µ = − 1 / 4 across 15 and more orders of magnitude range in body mass reveals that this value resulted from methodological errors in data assortment and analysis. 3. Instead, the available evidence is shown to be consistent with the existence of a size-independent mean value of mass-specific metabolic rate common to most taxa. Plotted together, q -values of non-growing unicells, insects and mammals in the basal state yield µ ≈ 0. Estimated field metabolic rates of bacteria and vertebrates are also size-independent. 4. Standard mass-specific metabolic rates of most unicells, insects and mammals studied are confined between 1 and 10 W kg − 1 . Plant leaves respire at similar rates. This suggests the existence of a metabolic optimum for living matter. With growing body size and diminishing surface-to-volume ratio organisms have to change their physiology and perfect their distribution networks to keep their q in the vicinity of the optimum.

[1]  C. Lusk,et al.  Survival and growth of seedlings of 12 Chilean rainforest trees in two light environments: Gas exchange and biomass distribution correlates , 2002 .

[2]  James H. Brown,et al.  A general model for ontogenetic growth , 2001, Nature.

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

[4]  Bai-lian Li,et al.  Ontogenetic growth: models and theory , 2004 .

[5]  Comparative studies on phenotypic plasticity of two herbs,Changium smyrnioides andAnthriscus sylvestris , 2004 .

[6]  S. Chown,et al.  Discontinuous gas-exchange in centipedes and its convergent evolution in tracheated arthropods. , 2002, The Journal of experimental biology.

[7]  Anastassia M. Makarieva,et al.  Body size, energy consumption and allometric scaling: a new dimension in the diversity–stability debate , 2004 .

[8]  J. Lighton,et al.  STANDARD AND EXERCISE METABOLISM AND THE DYNAMICS OF GAS EXCHANGE IN THE GIANT RED VELVET MITE, DINOTHROMBIUM MAGNIFICUM , 1995 .

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

[10]  Comparative studies on phenotypic plasticity of two herbs, Changium smyrnioides and Anthriscus sylvestris. , 2004, Journal of Zhejiang University. Science.

[11]  Hans W. Paerl,et al.  Nitrogen, Carbon, and Sulfur Metabolism in NaturalThioploca Samples , 1999, Applied and Environmental Microbiology.

[12]  Mikael Akke,et al.  Global Allocation Rules for Patterns of Biomass Partitioning , 2002, Science.

[13]  T. Berman,et al.  Metabolically active bacteria in Lake Kinneret , 2001 .

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

[15]  N. Revsbech,et al.  Colorless Sulfur Bacteria, Beggiatoa spp. and Thiovulum spp., in O2 and H2S Microgradients , 1983, Applied and environmental microbiology.

[16]  G. Perry,et al.  The densest terrestrial vertebrate , 2001, Journal of Tropical Ecology.

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

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

[19]  R. Porter,et al.  Allometry of mammalian cellular oxygen consumption , 2001, Cellular and Molecular Life Sciences CMLS.

[20]  Bai-lian Li,et al.  ENERGY PARTITIONING BETWEEN DIFFERENT-SIZED ORGANISMS AND ECOSYSTEM STABILITY , 2004 .

[21]  G. Nilsson,et al.  Brain and body oxygen requirements of Gnathonemus petersii, a fish with an exceptionally large brain , 1996, The Journal of experimental biology.

[22]  R. Peters,et al.  The effects of body size and temperature on metabolic rate of organisms , 1983 .

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

[24]  Philip L. Altman,et al.  Biology Data Book , 1964 .

[25]  T. J. Chandler,et al.  The Climate of the British Isles , 1976 .

[26]  Bai-lian Li,et al.  A note on metabolic rate dependence on body size in plants and animals. , 2003, Journal of theoretical biology.

[27]  Y. Prairie,et al.  Bacterial metabolism and growth efficiency in lakes: The importance of phosphorus availability , 2004 .

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

[29]  Ewald R. Weibel,et al.  Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor , 2004, Respiratory Physiology & Neurobiology.

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

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

[32]  J. Steffensen,et al.  Metabolic cold adaptation of polar fish based on measurements of aerobic oxygen consumption: fact or artefact? Artefact! , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[33]  J. Cole,et al.  BACTERIAL GROWTH EFFICIENCY IN NATURAL AQUATIC SYSTEMS , 1998 .

[34]  A. F. Bennett,et al.  Population density and energetics of lizards on a tropical island , 1979, Oecologia.

[35]  T. Fenchel,et al.  Respiration rates in heterotrophic, free-living protozoa , 1983, Microbial Ecology.

[36]  D. Brunt The Climate of the British Isles: , 1938, Nature.

[37]  K. Schleifer,et al.  The chemolithotrophic prokaryotes. , 1992 .

[38]  N. Stork,et al.  Species number, species abundance and body length relationships of arboreal beetles in Bornean lowland rain forest trees , 1988 .

[39]  S. Oikawa,et al.  Relationship between summated tissue respiration and body size in a marine teleost, the porgy Pagrus major , 2003 .

[40]  W. Ulrich Allometric ecological distributions in a local community of Hymenoptera , 2004 .

[41]  Andrea Rinaldo,et al.  Supply–demand balance and metabolic scaling , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[42]  R. Buschbom,et al.  A General Weight vs. Length Relationship for Insects , 1976 .

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

[44]  J. Lighton,et al.  Low metabolic rate in scorpions: implications for population biomass and cannibalism. , 2001, The Journal of experimental biology.

[45]  A. Heusner Energy metabolism and body size. I. Is the 0.75 mass exponent of Kleiber's equation a statistical artifact? , 1982, Respiration physiology.

[46]  Tim M. Blackburn,et al.  Abundance, body size and biomass of arthropods in tropical forest , 1993 .

[47]  K. Nagy,et al.  Energetics of free-ranging mammals, reptiles, and birds. , 1999, Annual review of nutrition.

[48]  T. Rosswall,et al.  Biomass and turnover of bacteria in a forest soil and a peat , 1980 .

[49]  Bai-lian Li,et al.  Testing the allometric scaling relationships with seedlings of two tree species , 2003 .

[50]  F. Bokma Evidence against universal metabolic allometry , 2004 .

[51]  P. Reich,et al.  Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups , 1998, Oecologia.

[52]  S. Hemmingsen,et al.  Energy metabolism as related to body size and respiratory surfaces, and its evolution , 1960 .

[53]  H. N. Schulz,et al.  Big bacteria. , 2001, Annual review of microbiology.

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

[55]  D. Henning Metabolism , 1972, Introduction to a Phenomenology of Life.

[56]  P. Reich,et al.  Relationships of leaf dark respiration to leaf nitrogen , specific and leaf life-span : a test across biomes and functional groups leaf area , 1998 .

[57]  K. Svensson,et al.  Reversible transition between active and dormant microbial states in soil. , 2001, FEMS microbiology ecology.

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