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Toward a Metabolic Theory of Ecology

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Toward a Metabolic Theory of Ecology Ecology, 85(7), 2004, pp. 1771±1789 q 2004 by the Ecological Society of America TOWARD A METABOLIC THEORY OF ECOLOGY JAMES H. BROWN,1,2,4 with JAMES F. G ILLOOLY,1 ANDREW P. A LLEN,1 VAN M. SAVAGE,2,3 AND GEOFFREY B. WEST2,3 1Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131 USA 2Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, New Mexico 87501 USA 3Theoretical Division, MS B285, Los Alamos National Laboratory, Los Alamos, New Mexico 87545 USA JAMES H. BROWN, MacArthur Award Recipient, 2002 Abstract. Metabolism provides a basis for using ®rst principles of physics, chemistry, and biology to link the biology of individual organisms to the ecology of populations, communities, and ecosystems. Metabolic rate, the rate at which organisms take up, transform, and expend energy and materials, is the most fundamental biological rate. We have developed a quantitative theory for how metabolic rate varies with body size and temperature. Metabolic theory predicts how metabolic rate, by setting the rates of resource uptake from the environment and resource allocation to survival, growth, and reproduction, controls ecological processes at all levels of organization from individuals to the biosphere. Examples include: (1) life history attributes, including devel- opment rate, mortality rate, age at maturity, life span, and population growth rate; (2) population interactions, including carrying capacity, rates of competition and predation, and patterns of species diversity; and (3) ecosystem processes, including rates of biomass production and respiration and patterns of trophic dynamics. Data compiled from the ecological literature strongly support the theoretical predictions. Even- tually, metabolic theory may provide a conceptual foundation for much of ecology, just as genetic theory provides a foundation for much of evolutionary biology. Key words: allometry; biogeochemical cycles; body size; development; ecological interactions; ecological theory; metabolism; population growth; production; stoichiometry; temperature; trophic dynamics. 4 E-mail: [email protected] 1771 1772 JAMES H. BROWN ET AL. Ecology, Vol. 85, No. 7 INTRODUCTION of basic principles of biology, chemistry, and physics (e.g., Peters 1983, Sterner 1990, Elser et al. 1996, The complex, spatially and temporally varying struc- 2000a, West et al. 1997, 1999a, b, 2001, Enquist et al. tures and dynamics of ecological systems are largely 1999, Gillooly et al. 2001, 2002). Together, the older consequences of biological metabolism. Wherever they conceptual and empirical foundations and the more re- occur, organisms transform energy to power their own cent theoretical advances provide the basis for a met- activities, convert materials into uniquely organic abolic theory of ecology. This theory explicitly shows forms, and thereby create a distinctive biological, how many ecological structures and dynamics can be chemical, and physical environment. explained in terms of how body size, chemical kinetics, Metabolism is the biological processing of energy and resource supply affect metabolism. Through var- and materials. Organisms take up energetic and ma- iation in the rates and biochemical pathways of me- terial resources from the environment, convert them tabolism among different kinds of organisms and en- into other forms within their bodies, allocate them to vironmental settings, metabolic theory links the per- the ®tness-enhancing processes of survival, growth, formance of individual organisms to the ecology of and reproduction, and excrete altered forms back into populations, communities, and ecosystems. the environment. Metabolism therefore determines the demands that organisms place on their environment for Metabolism and metabolic rate all resources, and simultaneously sets powerful con- Metabolism is a complex network of biochemical straints on allocation of resources to all components of reactions that are catalyzed by enzymes, allowing the ®tness. The overall rate of these processes, the meta- concentrations of substrates and products and the rates bolic rate, sets the pace of life. It determines the rates of reactions to be regulated. A chart of the chemical of almost all biological activities. reactions of metabolism shows a bewildering number Recent progress in understanding how body size, of substrates, enzymes, and pathways. Nevertheless, temperature, and stoichiometry affect biological struc- the core of metabolism consists of a small number of ture and function at the molecular, cellular, and whole- reactions that form the basis of the TCA (tricarboxylic organism levels of organization raises the prospect of acid) cycle (Morowitz et al. 2000). The vast majority developing a metabolic theory of ecology. Metabolism of organisms use the same basic biochemistry, but the is a uniquely biological process, but it obeys the phys- rates of resource uptake, transformation, and allocation ical and chemical principles that govern the transfor- vary. mations of energy and materials; most relevant are the When we speak of energy and energetics, we refer laws of mass and energy balance, and thermodynamics. to potential energy: the energy contained in photons or Much of the variation among ecosystems, including chemical bonds. Some fraction of this energy is con- Perspectives their biological structures, chemical compositions, en- verted by the reactions of photosynthesis and respira- ergy and material ¯uxes, population processes, and spe- tion into biologically useful forms that are used to per- cies diversities, depends on the metabolic character- form the work of biosynthesis, membrane transport, istics of the organisms that are present. Much of the muscle contraction, nerve conduction, and so on. We variation among organisms, including their life history use the term kinetics to refer to kinetic energy, the characteristics and ecological roles, is constrained by energy of molecular motion. Kinetics affect biological their body sizes, operating temperatures, and chemical processes largely through the in¯uence of temperature compositions. These constraints of allometry, bio- on metabolic rate. chemical kinetics, and chemical stoichiometry lead to The metabolic rate is the fundamental biological rate, metabolic scaling relations that, on the one hand, can because it is the rate of energy uptake, transformation, be explained in terms of well-established principles of and allocation. For a heterotroph, the metabolic rate is biology, chemistry, and physics and, on the other hand, equal to the rate of respiration because heterotrophs can explain many emergent features of biological struc- obtain energy by oxidizing carbon compounds as de- ture and dynamics at all levels of organization. → scribed by the reaction: CH2O 1 O2 energy 1 CO2 1 H O. For an autotroph, the metabolic rate is equal THEORETICAL FOUNDATIONS 2 to the rate of photosynthesis because this same reaction Virtually all characteristics of organisms vary pre- is run in reverse using energy (i.e., photons) provided dictably with their body size, temperature, and chem- by the sun to ®x carbon (Farquhar et al. 1980). It has ical composition (e.g., Bartholomew 1981, Peters 1983, proven challenging to measure metabolic rate accu- Calder 1984, Schmidt-Nielsen 1984, Niklas 1994, Gil- rately and consistently. Ideally, it would be measured looly et al. 2001, 2002, Sterner and Elser 2002). For as heat loss by direct calorimetry, which would quan- more than a century, biologists have been investigating tify the energy dissipated in all biological activities. the mechanistic processes that underlie these relation- However, because of the ®xed stoichiometry of respi- ships. Recent theoretical advances have shown more ratory gas exchange, it is nearly as accurate and much explicitly how these biological characteristics can be more practical to measure the rate of carbon dioxide quanti®ed, related to each other, and explained in terms uptake in plants or the rate of oxygen consumption in July 2004 MACARTHUR AWARD LECTURE 1773 aerobic prokaryotes and eukaryotes (Withers 1992). free-living organism in nature, which ideally would Physiologists typically measure the basal or standard include allocation to growth and reproduction suf®cient metabolic rate, the minimal rate of an inactive organism to maintain a stable population; and perhaps also (3) in the laboratory. Basal rates are invariably less than maximal metabolic rate, the rate of energy ¯ux during the actual or ®eld metabolic rates of free-living organ- maximal sustained activity (Savage et al., in press b). isms, which must expend additional energy for for- Recently, West et al. (1997, 1999a, b) showed that aging, predator avoidance, physiological regulation, the distinctively biological quarter-power allometric and other maintenance processes, and still more energy scaling could be explained by models in which whole- for growth and reproduction. In most organisms, how- organism metabolic rate is limited by rates of uptake ever, the average daily energy expenditure or the long- of resources across surfaces and rates of distribution term sustained rate of biological activity is some fairly of materials through branching networks. The fractal- constant multiple, typically about two to three, of the like designs of these surfaces and networks cause their basal metabolic rate (Taylor et al. 1982, Schmidt-Niel- properties to scale as ¼ powers of body mass or vol- son 1984, Nagy 2001; Savage et al., in press b). ume, rather than the Ä powers that would be
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