1771
Ecology, 85(7), 2004, pp. 1771­1789
2004 by the Ecological Society of America
TOWARD A METABOLIC THEORY OF ECOLOGY
JAMES H. BROWN,1,2,4
with JAMES F. GILLOOLY,1
ANDREW P. ALLEN,1
VAN M. SAVAGE,2,3
AND GEOFFREY B. WEST2,3
1
Department 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 first 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 development
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. Eventually,
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: jhbrown@unm.edu
1772 JAMES H. BROWN ET AL. Ecology, Vol. 85, No. 7
Perspectives
INTRODUCTION
The complex, spatially and temporally varying structures
and dynamics of ecological systems are largely
consequences of biological metabolism. Wherever they
occur, organisms transform energy to power their own
activities, convert materials into uniquely organic
forms, and thereby create a distinctive biological,
chemical, and physical environment.
Metabolism is the biological processing of energy
and materials. Organisms take up energetic and material
resources from the environment, convert them
into other forms within their bodies, allocate them to
the fitness-enhancing processes of survival, growth,
and reproduction, and excrete altered forms back into
the environment. Metabolism therefore determines the
demands that organisms place on their environment for
all resources, and simultaneously sets powerful constraints
on allocation of resources to all components of
fitness. The overall rate of these processes, the metabolic
rate, sets the pace of life. It determines the rates
of almost all biological activities.
Recent progress in understanding how body size,
temperature, and stoichiometry affect biological structure
and function at the molecular, cellular, and wholeorganism
levels of organization raises the prospect of
developing a metabolic theory of ecology. Metabolism
is a uniquely biological process, but it obeys the physical
and chemical principles that govern the transformations
of energy and materials; most relevant are the
laws of mass and energy balance, and thermodynamics.
Much of the variation among ecosystems, including
their biological structures, chemical compositions, energy
and material fluxes, population processes, and species
diversities, depends on the metabolic characteristics
of the organisms that are present. Much of the
variation among organisms, including their life history
characteristics and ecological roles, is constrained by
their body sizes, operating temperatures, and chemical
compositions. These constraints of allometry, biochemical
kinetics, and chemical stoichiometry lead to
metabolic scaling relations that, on the one hand, can
be explained in terms of well-established principles of
biology, chemistry, and physics and, on the other hand,
can explain many emergent features of biological structure
and dynamics at all levels of organization.
THEORETICAL FOUNDATIONS
Virtually all characteristics of organisms vary predictably
with their body size, temperature, and chemical
composition (e.g., Bartholomew 1981, Peters 1983,
Calder 1984, Schmidt-Nielsen 1984, Niklas 1994, Gillooly
et al. 2001, 2002, Sterner and Elser 2002). For
more than a century, biologists have been investigating
the mechanistic processes that underlie these relationships.
Recent theoretical advances have shown more
explicitly how these biological characteristics can be
quantified, related to each other, and explained in terms
of basic principles of biology, chemistry, and physics
(e.g., Peters 1983, Sterner 1990, Elser et al. 1996,
2000a, West et al. 1997, 1999a, b, 2001, Enquist et al.
1999, Gillooly et al. 2001, 2002). Together, the older
conceptual and empirical foundations and the more recent
theoretical advances provide the basis for a metabolic
theory of ecology. This theory explicitly shows
how many ecological structures and dynamics can be
explained in terms of how body size, chemical kinetics,
and resource supply affect metabolism. Through variation
in the rates and biochemical pathways of metabolism
among different kinds of organisms and environmental
settings, metabolic theory links the performance
of individual organisms to the ecology of
populations, communities, and ecosystems.
Metabolism and metabolic rate
Metabolism is a complex network of biochemical
reactions that are catalyzed by enzymes, allowing the
concentrations of substrates and products and the rates
of reactions to be regulated. A chart of the chemical
reactions of metabolism shows a bewildering number
of substrates, enzymes, and pathways. Nevertheless,
the core of metabolism consists of a small number of
reactions that form the basis of the TCA (tricarboxylic
acid) cycle (Morowitz et al. 2000). The vast majority
of organisms use the same basic biochemistry, but the
rates of resource uptake, transformation, and allocation
vary.
When we speak of energy and energetics, we refer
to potential energy: the energy contained in photons or
chemical bonds. Some fraction of this energy is converted
by the reactions of photosynthesis and respiration
into biologically useful forms that are used to perform
the work of biosynthesis, membrane transport,
muscle contraction, nerve conduction, and so on. We
use the term kinetics to refer to kinetic energy, the
energy of molecular motion. Kinetics affect biological
processes largely through the influence of temperature
on metabolic rate.
The metabolic rate is the fundamental biological rate,
because it is the rate of energy uptake, transformation,
and allocation. For a heterotroph, the metabolic rate is
equal to the rate of respiration because heterotrophs
obtain energy by oxidizing carbon compounds as described
by the reaction: CH2O O2  energy CO2
H2O. For an autotroph, the metabolic rate is equal
to the rate of photosynthesis because this same reaction
is run in reverse using energy (i.e., photons) provided
by the sun to fix carbon (Farquhar et al. 1980). It has
proven challenging to measure metabolic rate accurately
and consistently. Ideally, it would be measured
as heat loss by direct calorimetry, which would quantify
the energy dissipated in all biological activities.
However, because of the fixed stoichiometry of respiratory
gas exchange, it is nearly as accurate and much
more practical to measure the rate of carbon dioxide
uptake in plants or the rate of oxygen consumption in
July 2004 1773MACARTHUR AWARD LECTURE
Perspectives
aerobic prokaryotes and eukaryotes (Withers 1992).
Physiologists typically measure the basal or standard
metabolic rate, the minimal rate of an inactive organism
in the laboratory. Basal rates are invariably less than
the actual or field metabolic rates of free-living organisms,
which must expend additional energy for foraging,
predator avoidance, physiological regulation,
and other maintenance processes, and still more energy
for growth and reproduction. In most organisms, however,
the average daily energy expenditure or the longterm
sustained rate of biological activity is some fairly
constant multiple, typically about two to three, of the
basal metabolic rate (Taylor et al. 1982, Schmidt-Nielson
1984, Nagy 2001; Savage et al., in press b).
In addition, most organisms exhibit phenotypic plasticity
in the expression of metabolism. They can vary
the rate and pathways of metabolism to some extent to
adjust for variations in resource supply, such as fluctuating
quantity and quality of food resources, or in
resource demand, such as the costs of reproduction or
of maintaining homeostasis in the face of altered environmental
temperature, osmotic concentration, or elemental
chemical composition. For example, during
periods of resource shortages, many organisms are able
to lower metabolic rates and resource requirements by
reducing activity and entering some form of diapause
or torpor. Even these phenotypic variations, however,
occur within constraints on metabolic rate due to three
primary factors: body size, temperature, and stoichi-
ometry.
Body size
Since early in the 20th century, it has been known
that almost all characteristics of organisms vary predictably
with body size. Huxley (1932) is credited with
pointing out that most size-related variation can be described
by so-called allometric equations, which are
power functions of the form
bY Y M .0 (1)
They relate some dependent variable, Y, such as metabolic
rate, development time, population growth rate,
or rate of molecular evolution, to body mass, M,
through two coefficients, a normalization constant, Y0,
and an allometric exponent, b. Most of these biological
scaling exponents have the unusual property of being
multiples of , rather than the multiples of  that would
be expected from Euclidean geometric scaling. Thus,
for example, Kleiber (1932) showed that whole-organism
metabolic rate, I, scales as
3/4
I I M0 (2)
where I0 is a normalization constant independent of
body size. This same relation, with different values for
the normalization constant, describes: (1) basal metabolic
rate, the minimal rate of energy expenditure necessary
for survival under ideal conditions; (2) field metabolic
rate, the actual rate of energy expenditure by a
free-living organism in nature, which ideally would
include allocation to growth and reproduction sufficient
to maintain a stable population; and perhaps also (3)
maximal metabolic rate, the rate of energy flux during
maximal sustained activity (Savage et al., in press b).
Recently, West et al. (1997, 1999a, b) showed that
the distinctively biological quarter-power allometric
scaling could be explained by models in which wholeorganism
metabolic rate is limited by rates of uptake
of resources across surfaces and rates of distribution
of materials through branching networks. The fractallike
designs of these surfaces and networks cause their
properties to scale as  powers of body mass or volume,
rather than the  powers that would be expected
based on Euclidean geometric scaling (Savage et al.,
in press b).
Temperature
It has been known for more than a century that biochemical
reaction rates, metabolic rates, and nearly all
other rates of biological activity increase exponentially
with temperature. These kinetics are described by the
Boltzmann factor or the Van't Hoff-Arrhenius relation
E/kTe (3)
where E is the activation energy, k is Boltzmann's constant,
and T is absolute temperature in K (Boltzmann
1872, Arrhenius 1889). The Boltzmann factor specifies
how temperature affects the rate of reaction by changing
the proportion of molecules with sufficient kinetic
energy, E, which here we measure in electron volts (1
eV 23.06 kcal/mol 96.49 kJ/mol).
This relationship holds only over the temperature
range of normal activity, which for most organisms lies
between 0 and 40 C (Thompson 1942, Schmidt-Nielsen
1997). Normal operating temperature varies among
species and taxonomic or functional groups. Any given
species usually operates over some subset of this temperature
range, although there are exceptions. For example,
most aquatic organisms do not experience temperatures
above 25 ­30 C, endothermic birds and
mammals maintain relatively high and constant temperatures
(36 ­40 C), some ectotherms can tolerate
only a very narrow range of temperatures, and some
microbes from extreme environments such as hot
springs and hydrothermal vents can live at temperatures
that approach or exceed 100 C. With some qualifications,
then, the exponential form (3) describes the temperature
dependence of whole-organism metabolism of
virtually all organisms, from unicellular microbes to
multicellular plants and animals (Gillooly et al. 2001).
Nearly all other biological rates and times, including
individual and population growth rates, and development
times and life spans, show a similar temperature
dependence (Gillooly et al. 2001, 2002; Savage et al.,
in press a). Interestingly, the empirically estimated activation
energies for all of these processes are similar,
and within the range of activation energies typically
1774 JAMES H. BROWN ET AL. Ecology, Vol. 85, No. 7
Perspectives
observed for the biochemical reactions of metabolism
(0.60­0.70 eV, Gillooly et al. 2001). This suggests that
metabolism is the underlying process that governs most
biological rates.
Stoichiometry
In its narrow sense, stoichiometry is concerned with
the proportions of elements in chemical reactions. In
broader applications, such as to ecology, stoichiometry
refers to the quantities, proportions, or ratios of elements
in different entities, such as organisms or their
environments (e.g., Reiners 1986, Elser et al. 1996,
2000a, Sterner and Elser 2002). Protoplasm, and the
different structural and functional materials that comprise
living biomass, have characteristic ratios of the
common elements such as H, O, C, N, P, Na, Cl, S,
Ca, and K. N is found primarily in proteins; P in nucleic
acids, ADP and ATP, phospholipids, and skeletal structure;
Na or K in intracellular solutes, and so on. All
organisms have internal chemical compositions that
differ from those in their environment (Lotka 1925),
so they must expend metabolic energy to maintain concentration
gradients across their surfaces, to acquire
necessary elements, and to excrete waste products.
Fundamental stoichiometric relationships dictate the
quantities of elements that are transformed in the reactions
of metabolism. Biochemistry and physiology
specify the quantitative relationship between the metabolic
rate and the fluxes of elemental materials
through an organism. The metabolic rate dictates the
rates at which material resources are taken up from the
environment, used for biological structure and function,
and excreted as ``waste'' back into the environment.
Far from being distinct ecological currencies, as
some authors have implied (e.g., Reiners 1986, Sterner
and Elser 2002), the currencies of energy and materials
are inextricably linked by the chemical equations of
metabolism. These equations specify not only the molecular
ratios of elements, but also the energy yield or
demand of each reaction. Ecological stoichiometry is
concerned with the causes and consequences of variation
in elemental composition among organisms and
between organisms and their environments (Sterner and
Elser 2002). Despite the overall similarity in the chemical
makeup of protoplasm, organisms vary somewhat
in stoichiometric ratios within individuals, among individuals
of a species, and especially between different
taxonomic and functional groups. For example, in unicellular
organisms and small metazoans, which have
high rates of biosynthesis, a significant portion of total
body phosphorus is found in ribosomal RNA (Sutcliffe
1970, Elser et al. 2000b, Sterner and Elser 2002). Larger
vertebrate organisms, with lower rates of biosynthesis,
require much less RNA, but require much more
phosphorus for skeletal structure. Vertebrates, with
bones and muscles, contain proportionately more P and
N and less C than plants, which use cellulose and lignin
as primary structural materials and have high ratios of
C relative to N and P (Elser et al. 2000a).
The elemental composition of an organism is governed
by the rates of turnover within an organism and
the rates of flux between an organism and its environment.
The concentrations of elements in ecosystems
are therefore directly linked to the fluxes and turnover
rates of elements in the constituent organisms. There
may be reciprocal limitation, so that concentrations of
some elements, such as N in soils and P in lakes, are
regulated by a balance between the rate of supply from
abiotic and biotic sources and the rate of uptake by
organisms. On the one hand, environmental concentrations
can limit metabolic rates, and thereby growth
rates, reproductive rates, and standing stocks of organisms.
For example, plants can be limited by nitrogen,
water, iron, and phosphorus. Under controlled laboratory
conditions, plant growth rates have been shown
to vary linearly with N concentration (Ingestad 1979).
Similarly, fertilization and irrigation experiments have
repeatedly shown that growth rates of plants in the field
are limited by nitrogen or water (Field and Mooney
1986; see review in Tilman 1988). On the other hand,
sizes of pools and rates of turnover in organisms can
regulate environmental concentrations of elements and
compounds, sometimes within narrow limits (Vitousek
1982). This is the case for CO2 concentration in the
atmosphere, which is regulated in part by the balance
between photosynthesis and respiration in the biosphere
(Falkowski et al. 2000, Chapin et al. 2002), and
for the concentrations of C, N, and P found in the
organic matter of oceans and lakes, which is regulated
in part by nutrient metabolism of the biota (Redfield
1958).
ALTERNATIVE EXPRESSIONS FOR BIOLOGICAL RATES
The joint effects of body size, M, and temperature,
T (in K), on individual metabolic rate, I, can be described
by combining Eqs. 2 and 3 (Gillooly et al.
2001). This gives
3/4 E/kT
I i M e0 (4)
where i0 is a normalization constant independent of body
size and temperature. We can take logarithms of both sides
of this equation and rearrange terms to yield
3/4
ln(IM ) E(1/kT) ln(i ).0 (5)
Note that in Eq. 5, we have ``mass-corrected'' metabolic
rate, I, by incorporating the logarithm of mass
raised to the  power. This method facilitates quantitative
evaluation of the mass and temperature dependence
predicted by Eq. 4, by incorporating the predicted
scalings into the analysis and into the y-axis of
bivariate plots. Eq. 5 predicts that the natural logarithm
of mass-corrected whole-organism metabolic rate
should be a linear function of inverse absolute temperature
(1/kT). The slope of this relationship gives the
activation energy of metabolism, E, and the intercept
July 2004 1775MACARTHUR AWARD LECTURE
Perspectives
FIG. 1. Temperature and mass dependence of metabolic rate for several groups of organisms, from unicellular eukaryotes
to plants and vertebrates (from Gillooly et al. 2001). (A) Relationship between mass-corrected metabolic rate, ln(IM 3/4
),
measured in watts/g3/4
, and temperature, 1/kT, measured in K. The overall slope, calculated using ANCOVA, estimates the
activation energy, and the intercepts estimate the normalization constants, C ln(i0), for each group. The observed slope is
close to the predicted range of 0.60­0.70 eV (95% CI, 0.66­0.73 eV; SI conversion, 1 eV 96.49 kJ/mol). (B) Relationship
between temperature-corrected metabolic rate, ln(IeE/kT
), measured in watts, and body mass, ln(M), measured in grams.
Variables are M, body size; I, individual metabolic rate; k, Boltzmann's constant; T, absolute temperature (in K). E is the
activation energy. The overall slope, calculated using ANCOVA, estimates the allometric exponent, and the intercepts estimate
the normalization constants, C ln(i0), for each group. The observed slope is close to the predicted value of  (95% CI,
0.69­0.73). For clarity, data from endotherms (n 142), fish (n 113), amphibians (n 64), reptiles (n 105), invertebrates
(n 20), unicellular organisms (n 30), and plants (n 67) were binned and averaged for each taxonomic group to generate
the points depicted in the plot.
gives the natural logarithm of the normalization constant,
ln(i0). Plotted in this way (Fig. 1), it is clear that
data for all groups are well-fitted by a common slope,
E 0.69 eV (1 eV 96.49 kJ/mol), including endotherms
in hibernation and torpor. Excluding these
endotherms, we obtain an average value of E 0.63
eV. Both of these values are within the range (0.60­
0.70 eV) commonly reported for aerobic respiration
(Gillooly et al. 2001).
Using the value of E 0.63 eV, we can ``temperature-correct''
metabolic rates to isolate the effects of
mass:
E/kT
ln(Ie ) ()ln(M) ln(i ).0 (6)
We use this same value of E 0.63 eV for subsequent
temperature corrections. Eq. 6 predicts a linear relationship
between the logarithm of temperature-corrected
metabolic rate and the logarithm of mass. Plotting
the same metabolic rate data in this alternative
way (Fig. 1), we see that that the fitted slope (0.71) is
close to the value of  predicted by the theory, and
that different groups show consistent differences in intercepts
or normalization constants, ln(i0).
The explanatory power of Eq. 4 is substantial, with
body size predicting 100 000-fold variation in rates
over the 20 orders-of-magnitude size range from the
smallest unicellular microbes to the largest vertebrates
and trees, and with temperature predicting 30-fold
variation over the biologically relevant temperature
range from 0 to 40 C.
There are, of course, quantitative deviations of individual
data values around the regression lines and
from the predictions of the models. For example, there
exists an 20-fold variation in the normalization constants
for basal metabolism, i0, across all taxonomic
groups. The residual variation offers clues to the other
factors, in addition to body size and temperature, that
affect metabolic and ecological processes. We will
show that some of the remaining variation in ontogenetic
growth rates and litter decomposition rates is related
to elemental stoichiometry.
These methods of ``mass correction'' and ``temperature
correction'' will be applied repeatedly in subsequent
sections of the paper to investigate other biological
rates and times. Slightly different versions of
Eqs. 5 and 6 are required for mass-specific metabolic
rate and most other biological rates, which are predicted
to scale as M 1/4
, and for biological times, which
are expected to scale as M1/4
. For simplicity, in most
subsequent equations, we will use instead of and
will leave out symbols for the normalization constants.
We emphasize, however, that these coefficients are important,
because they differ in systematic ways among
different biological traits, taxa of organisms, and kinds
of environments.
1776 JAMES H. BROWN ET AL. Ecology, Vol. 85, No. 7
Perspectives
INDIVIDUAL PERFORMANCE AND LIFE HISTORY
The combined effect of body size and temperature
on whole-organism metabolic rate, I, is given in Eq.
4. Because the mass-specific rate of metabolism, B, is
simply I/M, it follows that B scales as
1/4 E/kTB M e . (7)
Other biological rates, from heart rate to development
rate, and even the rate of molecular evolution (J. F.
Gillooly and A. P. Allen, unpublished data), also vary
with mass as M 1/4 and with the Boltzmann factor. Biological
times, tB, such as turnover times for metabolic
substrates and generations of individuals, are the reciprocal
of rates and therefore scale as
1/4 E/kTt M eB (8)
(Gillooly et al. 2002). These equations express relationships
that have been studied for many decades. It
has long been known that large organisms require more
resources, but flux them through at slower rates than
do smaller organisms. Both overall resource requirements
and flux rates are higher at higher temperatures.
Elephants require more food, but reproduce more slowly
and live longer than mice. Microbial activity and
rates of litter decomposition are higher in warm, tropical
environments than cold, subarctic ones. The advantage
of this framework, however, is that the equations
combine the effects of size and temperature in a
single quantitative expression. This makes possible
precise comparisons across organisms that differ substantially
in body size and operating temperature, including
species in different taxonomic or functional
groups or diverse environments. When such comparisons
are made, the commonalities of life and their ecological
manifestations are revealed.
Individual biomass production
Organisms devote some fraction of their metabolism
to catabolism and activities associated with maintenance,
and the remainder to anabolism and activities
associated with production of new biomass for growth
and reproduction. Empirically, rates of whole-organism
and mass-specific biomass production, P and P/M, respectively,
scale similarly to whole-organism and massspecific
rates, so P M3/4
e E/kT
and P/M M 1/4
e E/kT
.
This supports the theoretical conjecture that some constant
fraction of metabolism tends to be allocated to
production. It follows that, to the extent organisms have
similar metabolic rates after adjusting for body size
and temperature, they should also have similar rates of
production. This prediction is confirmed by plotting
maximal rates of temperature-corrected whole-organism
production against body mass for a wide variety
of aerobic eukaryotes, including plants and animals,
ectotherms and endotherms (Fig. 2). Note that all values
cluster closely around the same allometric relationship,
which extends over nearly 20 orders of magnitude
in body mass and has a slope almost exactly
equal to the predicted . Trees and vertebrates of the
same body mass, operating at the same body temperature,
produce new biomass through some combination
of growth and reproduction, at very similar rates. The
same applies to fish and terrestrial insects. Of course
there is residual variation, some probably related to
stoichiometric resource requirements, and the remainder
to other taxon- or environment-specific factors. But
the degree of commonality is impressive.
Ontogenetic growth
The rate of metabolism sets the pace of life, including
the life history schedule. For example, time to
hatching of eggs in diverse animals, including zooplankton,
insects, fish, amphibians, and birds, varies
with size and temperature according to Eq. 8 (West et
al. 2001, Gillooly et al. 2002). Fig. 3 is a plot of development
rates as a function of temperature and mass
for eggs of zooplankton in the laboratory and fish in
the field. Note that the mass-corrected rates as a function
of temperature have slopes corresponding to activation
energies of 0.73 and 0.68 eV (1 eV 96.49
kJ/mol), close to the range of estimated activation energies
for aerobic metabolism (Gillooly et al. 2001).
The temperature-corrected rates as a function of mass
have slopes corresponding to allometric exponents of
0.27 and 0.24, bracketing the theoretically predicted
value of . Much of the variation within these
two groups probably can be explained by stoichiometric
resource limitation. This was shown for development
of zooplankton from hatching to maturity, in
which residuals around the regression were positively
correlated with body phosphorus concentration (Gillooly
et al. 2002), as expected from the relationships
between growth rate and RNA concentrations (Sutcliffe
1970, Elser et al. 2000b).
Survival and mortality
Ecologists have traditionally viewed survival times
and their inverse, mortality rates, as being highly variable
and consequences of extrinsic environmental conditions,
such as predation, disease, and resource competition,
rather than intrinsic properties of individual
organisms (e.g., Charnov 1993, Kozlowski and Weiner
1997, Stearns et al. 2000). However, because most populations
are neither continuously increasing nor decreasing,
mortality rates must very nearly equal fecundity
rates, and fecundity is fueled by biomass production.
Metabolic theory therefore predicts that Eq. 7
should account for much of the variation in field mortality
rates, Z. Mortality rates of free-living marine fish
stocks support this prediction (Fig. 4; see also Peterson
and Wroblewski 1984). The slope of the size-corrected
relationship between mortality rate and temperature
gives an activation energy of 0.47 eV, which is somewhat
lower than the predicted range of 0.60­0.70 eV.
The slope of temperature-corrected mortality rate as a
July 2004 1777MACARTHUR AWARD LECTURE
Perspectives
FIG. 2. Mass dependence (mass measured in grams) of temperature-corrected maximal rates of whole-organism biomass
production (PeE/kT, measured in grams per individual per year) for a wide variety of organisms, from unicellular eukaryotes
to plants and mammals (from Ernest et al. 2003). Data, which span 20 orders of magnitude in body size, have been
temperature corrected using Eq. 6. The allometric exponent, indicated by the slope, is close to the predicted value of  (95%
CI, 0.75­0.76).
function of body mass, 0.24, is almost identical to
the predicted exponent of  (Savage et al., in press
a).
We offer two complementary, non-mutually exclusive
hypotheses for the body size and temperature dependence
of field mortality rates. First, the cumulative
effects of metabolism with age may affect the ability
of individual organisms to resist ecological causes of
death, whether they be biotic or abiotic in origin. Studies
of aging have led to a theory of senescence that
attributes aging and eventual death to cumulative damage
at the molecular and cellular levels by the free
radicals produced as byproducts of aerobic metabolism
(Gerschman et al. 1954, Hartman 1956, Cadenas and
Packer 1999). Second, the size and temperature dependence
of field mortality rates suggest that Eq. 5
characterizes rates of ecological interactions that lead
to death, including competition, predation, parasitism,
and disease. As we will show, the rates of these interactions
do indeed show the predicted temperature de-
pendence.
Stoichiometry
At the individual level, energy and materials are
linked by the chemical equations of metabolism, by the
composition of organelles and other constituents of
protoplasm, and by fundamental constraints on structure
and function at cellular to whole-organism levels
of organization. Many of these constraints are related
directly to metabolism. The average rate of turnover
of an element (i.e., the inverse of residence time) is
equal to the whole-organism flux divided by the wholeorganism
pool or storage. The fluxes (per individual
rates of uptake and loss) of most elements vary with
body size in direct proportion to whole-organism metabolic
rate, as F M 3/4
(e.g., Peters 1983). Pools of
the commonest constituents of protoplasm, including
carbon, hydrogen, oxygen, and water, usually scale linearly
with body mass, i.e., as S M1
. So, for these
common elements, turnover rate, on average, scales as
F/S M 3/4
/M1
M 1/4
. However, this is not true of all
element pools, especially those that have some special
function in metabolism. Metabolism of eukaryotes
takes place primarily in organelles: chloroplasts, mitochondria,
and ribosomes, which are, respectively, the
sites of photosynthesis, respiration, and protein synthesis.
These organelles are effectively invariant units;
their structure and function are nearly identical across
taxa and environments. The reaction rate per organelle
is independent of body size (but not temperature), so
the rate of whole-organism metabolism depends on the
total numbers of organelles. Consequently, numbers of
these organelles per individual scale as M3/4, and concentrations
or densities of the organelles scale as M 1/4
1778 JAMES H. BROWN ET AL. Ecology, Vol. 85, No. 7
Perspectives
FIG. 3. Temperature (measured in K) and mass (measured in grams) dependence of developmental rates for eggs of
zooplankton in the laboratory (data from Gillooly and Dodson 2000) and fish in the field (data from Pauly and Pullin 1988).
Hatching time data have been converted to rates (1/time) and plotted as functions of temperature (upper panels, where the
rate is measured in g1/4
/day) and mass (lower panels, where the rate is measured as 1/day), as described in the section
Ontogenetic growth. The activation energy and allometric exponent, as indicated by the slopes in the upper and lower panels,
respectively, are similar to the predicted values of 0.60­0.70 eV (95% CIs from left to right, 0.68­0.78 eV and 0.62­0.73)
and  (95% confidence intervals, from left to right, 0.24 to 0.29 and 0.16 to 0.29).
FIG. 4. Temperature (measured in K) and mass (measured in grams) dependence of fish mortality rates in the field (data
from Pauly 1980). (A) Relationship between mass-corrected mortality rate, ln(ZM1/4, measured in grams1/4 per year), and
temperature, 1/kT (measured in K). The activation energy, indicated by the slope, is lower than the predicted range of 0.60­
0.70 eV (95% CI, 0.37 to 0.54). (B) Relationship between temperature-corrected mortality rate, ln(ZeE/kT, measured as
1/year), and body mass, ln(M), measured in grams. The allometric exponent, indicated by the slope, is close to the predicted
value of  (95% CI, 0.20 to 0.27).
July 2004 1779MACARTHUR AWARD LECTURE
Perspectives
FIG. 5. Temperature (in K) and mass (measured in grams) dependence of maximal rates of population growth, rmax, for
a wide variety of organisms (A and B, respectively; data sources are listed in Savage et al., in press a). Data are plotted as
in Figs. 3 and 4; rmax is measured in g1/4
per day in (A) and as 1/day in (B). There are fewer data points in (B) because there
are multiple temperature points for a species of a given mass. The activation energy and allometric exponent, indicated by
the slopes in (A) and (B), respectively, are close to the predicted values of 0.60­0.70 eV (95% CI, 0.56­0.80) and  (95%
CI, 0.21 to 0.25), respectively.
(Niklas and Enquist 2001, West et al. 2002; J. F. Gillooly
and A. P. Allen, unpublished data). This has been
shown to be true for mitochondria (West et al. 2002),
chloroplasts (Niklas and Enquist 2001), and RNA (Foss
and Forbes 1997). Thus, element pools associated with
organelles such as these should scale with body size
as S M 3/4, and turnover rates of these pools should
be independent of body size (F/S M 3/4/M 3/4 M0).
The extent to which whole-body stoichiometry is
determined by these pools, and thus varies with body
size, will depend on their sizes relative to other pools.
For example, whole-body phosphorus concentrations
should decline with increasing body size in growing
unicellular organisms because they contain relatively
high concentrations of phosphorus in RNA relative to
phosphorus in other pools. However, whole-body phosphorus
concentrations in most multicellular organisms
should vary little with body size because most phosphorus
is found in other pools that do not scale with
body size (J. F. Gillooly and A. P. Allen, unpublished
data). Similar reasoning should apply to the concentrations
of nitrogen in plants, because a significant fraction
is found in chloroplasts.
POPULATION AND COMMUNITY DYNAMICS
We can extend this framework to population and
community levels of ecological organization. Many
features of population dynamics and community organization
are due to effects of body size, temperature,
and stoichiometry on the performance of individual
organisms.
Population growth rates and rmax
Population dynamics can be complex and unpredictable,
but the potential for exponential growth that
underlies these fluctuations has been called the one
unequivocal law of population ecology (Turchin 2001).
The maximal rate of exponential increase, rmax, is predicted
to scale according to Eq. 7. This follows from
the fact that reproduction is fueled by metabolism, and
that mass-specific production rates and mortality rates
follow Eq. 7. In fact, metabolic rates of microbes are
often determined by measuring maximal population
production Ptot or maximal population growth rates,
rmax.
The  mass dependence of rmax has been well documented
empirically (Slobodkin 1962, Blueweiss et al.
1978), but what about the temperature dependence?
Fig. 5 shows that Eq. 5 describes tightly constrained
variation in rmax across a wide variety of organisms,
from unicellular eukaryotes to mammals. The commonality
is impressive, especially because these organisms
have very different modes of reproduction and
occur in a wide variety of environments (Savage et al.,
in press a).
This finding suggests that some interpretations of
differences in life history and resulting population processes
should be reexamined. For example, differences
between populations in life history, including the classical
r and K strategies, have often been viewed as
adaptations to particular environmental conditions.
Metabolic theory shows that smaller organisms, and
those operating at higher temperatures, tend to have
higher rmax values than larger, colder organisms, simply
as a consequence of allometric and kinetic constraints.
We hasten to add, however, that this does not necessarily
mean that size- and temperature-related differences
between populations in life histories are not
adaptive. Organisms can respond to selection resulting
from different environments by changing body size.
For example, strong selection, perhaps for high reproductive
rates in the absence of predators, apparently
1780 JAMES H. BROWN ET AL. Ecology, Vol. 85, No. 7
Perspectives
FIG. 6. Mass dependence of population density in terrestrial
mammals (data sources are listed in Ernest et al. [2003],
including data from Damuth [1987]). Density was measured
as no. individuals/km2, and mass was measured in grams. Data
were analyzed without temperature correction because mammals
have very similar body temperatures. The slope of this
relationship gives an allometric exponent close to the predicted
value of  (95% CI, 0.72 to 0.82). There is considerable
variation in the densities of mammals of similar
size, which is not surprising since the data are for all kinds
of mammals from throughout the world. So, for example,
some of the residual variation is related to trophic level: carnivores
with lower rates of resource supply tend to have lower
population densities than herbivores.
causes rapid dwarfing of elephants and other large
mammals on islands (e.g., Lister 1989, Roth 1990,
Brown 1995). Some organisms can also change temperature
adaptively. For example, many terrestrial ectothermic
animals exhibit some kind of behavioral thermoregulation:
they seek out warm microenvironments
to elevate body temperatures and increase rates of production
for growth and reproduction.
Population density
It is straightforward to solve the equation for population
growth rate for the steady state when the number
of individuals, N, is not changing (dN/dt 0) The
equilibrium number of individuals or carrying capacity,
K, is predicted to vary as
3/4 E/kT
K [R]M e (9)
linearly with the supply rate or concentration of the
limiting resource [R], as a power function of body
mass, and exponentially with temperature (Savage et
al., in press a). The qualitative effects of resource supply
and body size are not surprising: more individuals
with increased resource or decreased size. The effect
of temperature, however, may not be so intuitive. Increasing
the temperature actually reduces the carrying
capacity, because the same supply of energy supports
a smaller number of individuals, each fluxing energy
and materials at a higher rate. This prediction of an
inverse Boltzmann relationship between equilibrium
abundance and environmental temperature for ectotherms
is supported by the analysis of Allen et al.
(2002).
If resource supply rate [R] and temperature T are
held constant, then population density should vary inversely
with body size, as M 3/4. This is the basis for
deriving a resource-based thinning law of plant ecology
in which the number of stems, N, is predicted to vary
with plant mass as N M 3/4, or with stem diameter,
D, as N D 2 (Enquist et al. 1998, Belgrano et al.
2002; see also Lonsdale 1990). The theory assumes
that sessile plants grow until limited by competition
for resources, and that individual resource requirements
scale as M 3/4
. The theory accurately predicts thinning
trajectories in even-aged stands, which follow a M 3/4
or D 2
power law. A more complex model that incorporates
growth and mortality predicts size­frequency
distributions of the trees in steady-state forests with
stable age and size distributions (G. B. West, B. J.
Enquist, and J. H. Brown, unpublished data). This model
predicts the same scaling of number of stems of a
given size as a function of plant mass or stem diameter
(N M 3/4
D 2
). Data from forests throughout the
world show size distributions that are very similar to
the predicted scaling (Enquist and Niklas 2001).
Eq. 9 predicts that carrying capacity or equilibrium
population density should also scale as M 3/4
in mobile
animals if one again assumes that the rate of resource
supply is held constant. One potentially confounding
issue is the unit of analysis. The theory predicts how
many individuals of a given size can be supported, but
the data are often compiled by species. For example,
Damuth (1981, 1987; see also Carbone and Gittleman
2002) showed empirically that population densities of
species of terrestrial mammals from all over the world
scaled as M 3/4. There are, however, at least two orders
of magnitude variation in the population densities of
species of any given size (Fig. 6). Most of this variation
can almost certainly be attributed to variation in resource
supply. The data come from a wide variety of
environments that differ considerably in resource availability,
and from mammal species that vary in diet from
herbivores to carnivores. So to test the theory properly,
the densities of all coexisting species within a trophic
group and body size category should be summed, as
is done for trees in forest communities.
The M 3/4
scaling of equilibrium population density
with body size raises interesting theoretical questions.
Because the number of individuals per unit area, N,
scales as M 3/4
and whole-organism metabolic rate
scales as M 3/4
, total energy use per unit area for a size
class is M 3/4
M 3/4
M0
. Within a functional group
sharing a common resource, the rate of energy flux per
unit area of the combined populations of different-sized
organisms is predicted to be independent of size. This
energy equivalence argument can also be turned
around. Whenever total population density scales empirically
as M 3/4;
, the resulting invariance in energy
July 2004 1781MACARTHUR AWARD LECTURE
Perspectives
TABLE 1. Studies in which relevant components of competitive or predator­prey interactions have been studied at different
temperatures so as to allow estimation of the activation energy, E.
Study
Interspecific
interaction Taxon Measure E (eV)
Burnett (1951)
Spitze (1985)
Eggleston (1990)
Luecke and O'Brien (1983)
Verity (1985)
Park (1954)
parasitism
predation
predation
predation
grazing
competition
wasp/sawfly
fly larvae/zooplankton
crab/oyster
zooplankton
zooplankton/phytoplankton
beetle
rate of parasitism
attack rate
attack rate
feeding rate
grazing rate
time to competitive
exclusion
0.81
0.56
0.80
0.81
0.57
0.64
Note: Although the number of measurements is usually small, resulting in wide confidence intervals, note that the values
of E vary around the theoretically predicted range of 0.60­0.70 eV. SI conversion: 1 eV 23.06 kcal/mol 96.49 kJ/mol.
flux implies that resources are available to and are used
by each body size class at equal rates. Why should this
be so? The resource-based thinning theory for plants
reasonably assumes that sessile individuals of different
size compete for the same limiting resources (light,
water, nutrients). So far, however, we have no comparable
theory to explain why the rate of supply of
usable energy should be approximately constant for
differently sized mammals or other mobile animals that
utilize a broad spectrum of resources.
Interspecific interactions
Since the theoretical studies of Lotka (1925) and
Volterra (1926) and the classical experiments of Gause
(1934), Park (1948), and Huffaker (1958), ecologists
have tried to understand how pairs of competing species
or of predators and prey coexist with stability in
the same environment. The experimental studies found
that coexistence was difficult to obtain in simple laboratory
environments: one of the populations almost
invariably went extinct. For example, in Park's (1954)
classic experiments with flour beetles, by varying the
temperature, he was able to reverse the outcome of
competition, changing which species survived and
which went extinct. Less appreciated is the fact that
time to competitive exclusion across three temperatures
was inversely related to temperature with an activation
energy of 0.64 eV (1 eV 96.49 kJ/mol), nearly identical
to the average for individual metabolism. A number
of other interaction rates and times, including rates
of parasitism and predator attack rates, show similar
temperature relations (Table 1; see also Tilman et al.
1981, Dunson and Travis 1991). Metabolic theory predicts
the pace of these interactions, because rates of
consumption and population growth are determined by
rates of individual metabolism and have the same body
size and temperature dependence.
Species diversity
The scaling of rates of ecological interactions has
important implications for coexistence and species diversity.
The qualitative empirical patterns of biodiversity
would suggest that the processes that generate and
maintain species richness scale similarly to other biological
rates, as in Eq. 7. Other things being equal,
there are more species of small organisms than large
ones and more species in warm environments than cold
ones.
The fact that species diversity varies inversely with
body size suggests that metabolism plays a central role
(e.g., Hutchinson and MacArthur 1959, May 1978,
1986, 1988, Brown 1995). As recently as a decade ago,
the available evidence suggested that the highest diversity
occurred in small, but not the smallest, organisms
(i.e., in small insects; see May 1978, 1986). Recent
data, however, reveal enormous microbial diversity
and suggest that species richness may continue to
increase with decreasing body size right on down to
the smallest prokaryotes and perhaps even to viruses
(e.g., Pace 1997).
It has long been known that diversity of most taxonomic
and functional groups is highest in the tropics,
but this has usually been attributed to higher productivity
(resource availability) or reduced seasonality,
rather than to the kinetic effect of higher temperatures
(e.g., Brown and Lomolino 1998; but see Rohde 1992).
We have recently shown, however, that species richness
in many groups of plants and animals has the same
Boltzmann relationship to environmental temperature
that metabolic rate does (Eq. 3; see Allen et al. 2002).
This result holds true not only along latitudinal gradients,
but also along elevational gradients where variables
such as photon flux, seasonal changes in day
length, and biogeographic history are held relatively
constant (Fig. 7). The implication is that much of the
variation in species diversity is directly attributable to
the kinetics of biochemical reactions and ecological
interactions.
The temperature dependence of population growth
and interspecific interactions brings into question explanations
for diversity that invoke long time lags (e.g.,
Hutchinson 1961, Bell 2001, Hubbell 2001). The highest
diversity on earth is found in warm, productive
environments, such as tropical rain forests and coral
reefs, where the kinetics of interactions might be expected
to lead to rapid exclusion. We hypothesize that
diversity is largely a consequence of evolutionary processes
that obey Eqs. 7 and 8: small or warm organisms
1782 JAMES H. BROWN ET AL. Ecology, Vol. 85, No. 7
Perspectives
FIG. 7. Temperature dependence (temperature measured in K) of amphibian species richness in two geographic gradients
(Allen et al. 2002). (A) A latitudinal gradient in North America (data from Currie 1991). (B) An elevational gradient over
2600 m on Volcan Barva in Costa Rica (data from Duellman 1988). The slopes indicate nearly identical effects of temperature
on diversity in the two gradients, with activation energies close to the predicted value of 0.60­0.70 eV (95% confidence
intervals, from left to right, 0.63­0.77 and 0.55­0.87).
having faster ecological dynamics than large or cold
ones should also have faster evolutionary dynamics,
resulting in higher rates of speciation and a higher
standing stock of species. We have shown that Eq. 7
predicts rates of molecular evolution for a variety of
genes and genomes for ectotherms and endotherms (J.
F. Gillooly and A. P. Allen, unpublished data). Van
Valen (1973) attributed the origin and maintenance of
biodiversity largely to the ``Red Queen'' phenomenon,
rates of species interaction and coevolution. We agree,
and conjecture that the Red Queen runs according to
Eq. 7: faster in warmer environments and smaller or-
ganisms.
Although this conjecture is consistent with many
facts about biodiversity, it raises additional questions.
First, how can the kinetic effects of high temperature
be distinguished from the resource supply effects of
high productivity, which also increases with increasing
temperature? Second, how do faster rates of interspecific
interaction and evolution result in higher standing
stocks of species? This conjecture also raises the question
of why ectotherms, whose body temperatures and
metabolic rates vary with environmental temperature,
and endotherms, which have relatively high and constant
body temperatures, show qualitatively similar
geographic patterns of diversity. One hypothesis would
again invoke the Red Queen and suggest that species
diversity of endotherms is due largely to interactions
with ectotherms: food resources, competitors, predators,
parasites, and diseases. Alternatively, biodiversity
gradients may be driven largely by ecosystem productivity
for endotherms, and by temperature effects on
biochemical kinetics for ectotherms. Consistent with
this latter hypothesis, average population densities of
ectotherms, but not endothermic mammals, decline exponentially
with temperature toward the warm tropics
(Allen et al. 2002). Clearly, much additional work on
the relationship between metabolism and biodiversity
is needed, but a metabolic perspective has sharpened
many of the questions and has suggested where to look
for some of the answers.
ECOSYSTEM PROCESSES
Some of these questions can be addressed by probing
more deeply the effects of biological metabolism on
the fates of energy and materials in ecosystems. Biologically
regulated whole-ecosystem stores and fluxes
of elements and compounds, such as phosphorus, nitrogen,
and carbon, are simply the sums of the stores
and fluxes of the constituent organisms. Metabolic theory
therefore makes explicit predictions about the contribution
of biota to biogeochemical cycles. Specifically,
Eq. 7 provides the basis for predicting how size,
temperature, and stoichiometry determine magnitudes
of stores and rates of flux within and between compartments
such as primary producers, herbivores, predators,
and detritivores.
Standing stock of biomass
It is straightforward to derive an expression for
standing stock biomass. Eq. 9 gives the effects of body
mass and temperature on equilibrium population density
(number of individuals per unit area). Multiplying
this expression by the body size per individual, M,
gives the corresponding equation for standing stock or
stored biomass, W, per unit area:
1/4 E/kT
W [R]M e . (10)
The rate of supply of limiting resource, [R], has direct
linear effects on both carrying capacity and biomass.
Total biomass increases nonlinearly with increasing
body size and decreasing temperature. Large and/or
cold organisms retain more resources in their bodies
because they flux them more slowly through their met-
July 2004 1783MACARTHUR AWARD LECTURE
Perspectives
FIG. 8. Relationship of carbon turnover rate (measured as
[day] 1) to average plant size for plant biomass (measured in
grams) in aquatic and terrestrial ecosystems (analysis by A.
P. Allen, J. F. Gillooly, and J. H. Brown, unpublished manuscript;
carbon turnover data from Cebrian [1999] and for
plant size data from Belgrano et al. [2002]). Data have not
been temperature corrected, because environmental temperatures
were not reported. The slope of the relationship (solid
line) gives an allometric exponent close to the predicted value
of  (dashed line; 95% CI, 0.21 to 0.24).
abolic pathways, and vice versa for small and/or hot
organisms.
Energy flux and biomass production
At steady state, the rate of resource uptake by consumers
or ``predators'' is some constant fraction of the
rate of production of producers or ``prey.'' As individuals,
both producers and consumers flux energy with
the whole-organism and mass-specific scalings given
in Eqs. 4 and 7. However, the rate of energy flux for
populations should show a different mass dependence,
but not temperature dependence, because of the scaling
of population density and biomass. Rate of flux per
unit area, Ftot, can be derived by multiplying Eq. 4, for
the whole-organism metabolic rate per individual, by
M 3/4
, the number of individuals per unit area (from
Eq. 9). The result is
0 E/kT
F [R]M e .tot (11)
The rate of biological energy flux or productivity per
unit area of an ecosystem is therefore predicted to be
independent of body size but to increase with increasing
temperature. Enquist et al. (1998; also Niklas and
Enquist 2001) show that across diverse ecosystems,
rates of primary production, measured as rates of
whole-plant xylem flux, are independent of plant size
as predicted by Eq. 11. The data of Enquist et al. (1998:
Fig. 4) show about two orders of magnitude variation
in rates of productivity, which is small in comparison
to the nearly 12 orders of magnitude variation in plant
mass. Most of the variation in productivity is probably
due to both temperature and stoichiometry. The data
set includes ecosystems from around the world with
substantially different temperatures and energy, water,
and nutrient availability. The size invariance explicit
in Eq. 11 means that ecosystems with similar temperature
regimes and rates of resource supply, such as
adjacent forests and grasslands, should have nearly
equal rates of primary production. Clearly, however,
the forests contain much more stored biomass, as predicted
by Eq. 10.
One complication is that plant metabolic rate is the
rate of photosynthesis: the rate of conversion of solar
energy into organic compounds. Photosynthesis consists
of multiple biochemical reactions, some of which
are temperature dependent and have a range of activation
energies (0.35­0.65 eV; Bernacchi et al. 2001),
and some of which are dependent only on light (Farquhar
et al. 1980). Terrestrial plants maximize photosynthesis
in different environments by differentially
partitioning proteins among enzymatic reactions based
on their respective temperature and light dependencies
(Farquhar et al. 1980, Field and Mooney 1986). Less
well understood, however, is how photosynthesis at the
level of individual plants is manifested in global patterns
of plant production. We find that the activation
energy for terrestrial net primary production (gross
plant production minus plant respiration) across the
globe is well described by a Boltzmann relationship
with an activation energy of 0.33 eV (A. P. Allen, J.
F. Gillooly, and J. H. Brown, unpublished manuscript).
This value is approximately half the magnitude of the
activation energy for respiration or secondary production
( 0.63 eV). This has important consequences for
carbon cycles and organic matter storage (e.g., Schlesinger
1991).
Biomass turnover and energy flux
In the ecological literature, especially in applied disciplines
such as fisheries, production is often expressed
as the production/biomass ratio, Ptot/W, of total population
production, Ptot, to standing stock biomass, W.
Given that Ptot PN, and that W NM, this quantity
must scale as
1/4 E/kT
P /W M etot (12)
the same as mass-specific metabolic rate (Eq. 7). Empirical
studies have shown this predicted size dependence
for populations of different species (Peters
1983). For a steady-state population, production reflects
the replacement of individuals lost due to mortality,
so production must scale with body size and
temperature the same as mortality rate, Z, consistent
with Eqs. 7 and 12 and the empirically observed scaling
(Savage et al., in press a; Fig. 4). Furthermore, because
rates of biomass production and consumption must be
equal at steady state, Eqs. 7 and 12 also predict rates
1784 JAMES H. BROWN ET AL. Ecology, Vol. 85, No. 7
Perspectives
FIG. 9. Temperature dependence (temperature in K) of short-term root decay rate (measured as [day] 1
) as characterized
by the rate constant, k (analysis by A. P. Allen, J. F. Gillooly, and J. H. Brown, unpublished manuscript; data from Silver
and Miya [2001]). (A) The observed activation energy, as indicated by the slope, is within the range of values (0.60­0.70
eV) predicted on the basis of metabolic rate (95% CI, 0.43­0.76). (B) Plotting the residuals about the regression line in (A)
as a function of C:N shows that much of the variation is due to stoichiometry (P 0.05).
of biomass turnover. Fig. 8 (from A. P. Allen, J. F.
Gillooly, and J. H. Brown, unpublished manuscript;
data from Cebrian 1999) shows that carbon turnover
rates in a broad assortment of terrestrial and aquatic
ecosystems scale with average plant size as M 0.22. Not
only is this very close to the predicted M 1/4, but also
size varies over 20 orders of magnitude and accounts
for 84% of the variation in these data. Thus retention
times for carbon and nutrients must show the reciprocal
relation, as in Eq. 8. Temperature and nutrient supply
undoubtedly explain much of the remaining variation.
Empirical studies also support the predicted temperature
dependence. Total ecosystem respiration from
a broad assortment of terrestrial ecosystems around the
world, measured by eddy covariance towers as nighttime
CO2 flux, varies with temperature as predicted
based on individual metabolism. The average activation
energy from 19 sites was 0.62 eV, within the predicted
range of 0.60­0.70 eV (Enquist et al. 2003).
Similarly, Fig. 9 shows that temperature alone accounts
for 53% of the variation in short-term rates of decomposition
from sites around the world (A. P. Allen, J. F.
Gillooly, and J. H. Brown, unpublished manuscript;
data from Silver and Miya 2001). The activation energy
is 0.60 eV, not significantly different from the range
0.60­0.70 eV predicted on the basis of aerobic metabolism.
Furthermore, 58% of the residual variation can
be explained by stoichiometry (in this case, the C:N
ratio of the litter; see Fig. 9).
This metabolic framework also could be applied to
address more precisely and quantitatively the questions
raised by Odum (1969) in his classic paper on ``The
Strategy of Ecosystem Development.'' For example, it
should be possible predict the dynamics of succession:
how productivity, biomass, and material turnover rates
change with increasing plant size during transition from
herbaceous-dominated to tree-dominated ecosystems
following either natural disturbances, such as forest
fires, or human perturbations, such as abandonment of
agricultural fields. Metabolic theory also provides a
framework for more explicitly incorporating stoichiometry
and understanding the effects of limited water
and nutrients on variation in productivity and other
processes across biomes and geographic gradients. Regression
models that incorporate these variables are
able to account for much of the observed variation (e.g.,
Lieth 1973), but it should be possible to replace these
with mechanistic analytical models based on first prin-
ciples.
Trophic dynamics
Another major focus of ecosystem science has been
the structure and dynamics of food webs, which depict
the flows of energy and materials through ecosystems
due to trophic interactions. Metabolism has usually
been incorporated into food web theory only to the
extent of showing that the fluxes of energy and materials
obey the laws of thermodynamics and conservation
of energy, mass, and stoichiometry (but see Kerr
and Dickie 2001). It should be possible to do much
more, in particular to use metabolic theory to understand
the abundance, biomass, energy use, and elemental
chemical composition of species populations or
entire functional groups in terms of the effects of body
size, temperature, and stoichiometry on metabolic rate.
We illustrate the possibilities with two examples.
Ecologists have long depicted trophic organization
as pyramids of energy, biomass, or abundance. Each
layer of a pyramid corresponds to a successively higher
trophic level, starting with primary producers and going
up through herbivores, primary carnivores, and so
on. Metabolic theory makes quantitative predictions for
how body size, temperature, and stoichiometry affect
the pools and fluxes of biomass and energy. At steady
state, the Second Law of Thermodynamics demands
that there be less available energy at higher trophic
July 2004 1785MACARTHUR AWARD LECTURE
Perspectives
FIG. 10. A simple graphical model to explain the invariance of biomass as a function of body size of pelagic organisms
in ocean and lake ecosystems (from Brown and Gillooly 2003), where M is body mass, E is activation energy of metabolism,
B is mass-specific rate of metabolism, and N is number of individuals. If the ratio of predator size to prey size is 10 000,
and 10% of energy is transferred between successive trophic levels, Eq. 13 predicts allometric scaling of total abundance,
energy use, and biomass (A) within trophic levels (dashed lines: M 3/4
, M0
, M1/4
, respectively) and (B) across trophic levels
(continuous lines: M 1, M 1/4, M0, respectively) from phytoplankton (P) to zooplankton (Z) to planktivorous fish (F).
levels because, first, energy is lost within a trophic level
due to respiration and heat production, and second,
energy is lost between trophic levels due to inefficiencies
in transferring the biomass produced at one trophic
level, designated 0, to the next higher trophic level,
designated 1. The loss of energy between two adjacent
trophic levels can be characterized by a Lindeman efficiency,
, the ratio of total metabolic energy fluxes
at trophic level 1 to those at level 0. So, from Eq. 4 it
follows that i1N1 e E/kT/i0N0 e E/kT, where i0
3/4 3/4M M1 0
and i1 are the normalization constants for field metabolic
rate, and N0, N1, M0, and M1 are the population
densities and body masses at trophic levels 0 and 1,
respectively. Assuming that the system is in steady
state and that temperatures and normalization constants
do not differ between trophic levels, this simplifies to
N1 /N0 , and must always be 1. Given3/4 3/4M M1 0
these same assumptions, we can also derive comparable
relations for abundance, N1/N0 (M0/M1)3/4
(M1/M0) 3/4
; and for biomass, W1/W0 ,(M0/M1) 1/4
(M1/M0)1/4
. Thus, it is impossible to observe inverted
pyramids of energy flux, but possible to observe inverted
pyramids of abundance if the higher trophic level
is composed of organisms of sufficiently smaller
size; e.g., phytophagus insects feeding on trees. It is
also possible to observe inverted pyramids of biomass
if the higher trophic level is composed of organisms
of sufficiently larger size, e.g., whales feeding on
plankton. Note that the more explicit version incorporating
normalization constants and temperature dependence
can be used to give a more exact prediction,
as when, for example, a trophic level is composed primarily
of endotherms with elevated body temperatures.
Usually, however, the simpler inequalities will be conservative,
because the organisms at higher trophic levels
tend to have somewhat higher normalization constants
for metabolic rate and because some of the energy
goes directly to decomposers rather than to traditional
``consumers'' at higher trophic levels.
A second and related example concerns the relationship
between body size, biomass, and abundance
in pelagic ecosystems. Since the 1970s, ecologists have
noted the empirical pattern that in both freshwater and
marine ecosystems, total standing biomass, W, is invariant
with respect to body size (i.e., W M0) across
all pelagic organisms from unicellular plankton to the
largest animals. Consequently, abundance varies with
body size as N M 1 (e.g., Sheldon and Parsons 1967,
Sheldon et al. 1972, 1977, Peters 1983, Cyr 2000; see
also Kerr and Dickie 2001, Cohen et al. 2003). A simple
model can explain this pattern (Fig. 10; see also Brown
and Gillooly 2003). There are powerful body size constraints
on the flow of energy in pelagic ecosystems.
Primary producers are minute unicellular algae and
prokaryotes, whereas successive trophic levels consist
of organisms of increasing size, zooplankton, planktivorous
fish, and so on. If the size of the unicellular
algae at trophic level 0 is equal to M0 and is the
average ratio of predator body size to prey body size,
then the dependence of trophic level on mass can
be described by the equation log (M/M0)
log(M/M0)/log( ), where 0 is the trophic level for
algae of size M0. If we further assume that the total
rate of metabolism at trophic level 0 is equal to
i0N0 e E/kT, and that and the Lindeman efficiency3/4M0
are constants across trophic levels, then the total rate
of metabolism for organisms of size M is
3/4 E/kTI (i N M e )tot 0 0 0
log( )/log( )
M3/4 E/kT
(i N M e ) .0 0 0
M0
Following Eq. 4, the total number of organisms of a
given size is the following:
1786 JAMES H. BROWN ET AL. Ecology, Vol. 85, No. 7
Perspectives
[log( )/log( )] 3/4
I Mtot
N N . (13)0
I M0
Within a trophic level, where resource supply is relatively
constant, Eq. 13 predicts that abundance should
decrease with size as M 3/4, as has been observed empirically
(e.g., Belgrano et al. 2002, Li 2002). Between
trophic levels, the transfer of energy, characterized by
the Lindeman efficiency , has been estimated empirically
to be 10% (Lindeman 1942). The range of body
sizes within a trophic level, and the difference in average
size between trophic levels, is about four orders
of magnitude. Consequently, (log )/(log ) 
in Eq. 11, and abundance declines with body size as
M 1/4 3/4 M 1 across all trophic levels and the entire
spectrum of body sizes (Brown and Gillooly 2003). It
follows that energy flux, F, declines with body mass
as M(log )/(log ) M 1/4, and that biomass scales as M0
and therefore is invariant (Fig. 10).
We do not yet have a mechanistic theory to explain
why is often 10 1
or why is often 104
. The
fraction of metabolic energy allocated to biomass production
by the lower trophic level sets an upper limit
on , because production at the lower trophic level
fuels metabolism at the next highest trophic level (Kerr
and Dickie 2001). This is only an upper limit, however,
because it does not include energy losses incurred by
the higher trophic level due to foraging and assimilation.
The fact that 104
in size-structured pelagic
ecosystems is intriguing (see also Kerr and Dickie
2001, Cohen et al. 2003). The quarter-power allometry
implies that predator­prey body size ratios potentially
can be explained in terms of metabolic constraints.
CONCLUSIONS AND CAVEATS
We close with a few words about the strengths and
limitations of the theory that we have presented. First,
we should be explicit about what we mean by a metabolic
theory of ecology. We consider it to be a mechanistic,
quantitative, synthetic framework that (1) characterizes
the effects of body size and temperature on
the metabolism of individual organisms, and (2) characterizes
the effects of metabolism of individual organisms
on the pools and flows of energy and matter
in populations, communities, and ecosystems. Many
parts of this framework were established decades ago.
Our work has built upon this foundation, primarily by
developing mechanistic models that explain quarterpower
allometric scaling in biology, combining the effects
of body size and temperature on metabolic rate
in a single expression, and showing how the metabolism
of individual organisms affects the structure and
dynamics of ecological systems. Other parts of the
framework are still incomplete. Many other investigators
are contributing to the emerging theory. Nevertheless,
in its current state metabolic theory appears
to predict the magnitudes and to elucidate the mechanisms
of many empirical phenomena in ecology.
Second, metabolic theory suggests that energy and
materials (or energy and stoichiometry) are not fundamentally
different ecological currencies that operate
independently of each other to affect the structure and
dynamics of ecological systems. They are inextricably
linked. The fluxes, stores, and transformations of energy
and materials are stoichiometrically constrained
by the biochemistry and physiology of metabolism.
Energy is required to perform biological work, including
acquiring and transforming material resources. Materials,
both carbon compounds and elemental nutrients,
are required to synthesize the chemical compounds
that are the basis of all biological structures
and functions. At all levels, from individual organisms
to ecosystems, the processing of energy and materials
is linked due to metabolic constraints.
Third, metabolic processes relate the structure and
function of individual organisms to the roles of organisms
in ecosystems. On the one hand, many of these
linkages are not yet well understood. Both more and
better data and new and better theories are needed. On
the other hand, much progress can be made using existing
data and theories. We have shown how the same
principles of allometry, kinetics, and stoichiometry can
be used to understand quantitatively the fluxes of both
energy and materials in different kinds of organisms
and in different kinds of ecosystems. This is because
the biogeochemical processes in ecosystems are largely
consequences of the collective metabolic processes of
the constituent organisms.
Fourth, we envision a metabolic theory that would
eventually provide a conceptual basis for ecology similar
to that which genetic theory provides for evolution.
Metabolism, like inheritance, is one of the great unifying
processes in biology, making connections between
all levels of organization, from molecules to ecosystems.
Metabolic theory would by no means be the
only ecological theory nor would it account for all
important patterns and processes. It does, however, provide
a conceptual framework for ecological energetics
and stoichiometry. It does account for much of the
variation in ecological rates and times. It is based on
first principles of energy, mass, and stoichiometric balances,
thermodynamics, biochemical energy transformations,
chemical reaction kinetics, and fractal-like biological
designs. It uses the biological processing of
energy and materials to make linkages between individual
organisms and the ecology of populations, communities,
and ecosystems.
Fifth, metabolic theory is emphatically not a ``theory
of everything.'' As presently formulated, its domain is
restricted to effects of allometry, kinetics, and stoichiometry
on the biological processing of energy and
materials. Within this domain, it appears to explain
much of the variation in pools, rates, and times. As our
figures show, however, it cannot explain all of the variation.
The existence of residual variation calls attention
to the importance of other variables and processes
July 2004 1787MACARTHUR AWARD LECTURE
Perspectives
not included in either the specific models or the general
theory. A strength of the theory, however, is that it
makes explicit quantitative predictions based on first
principles. The residual variation can then be measured
as departures from these predictions, and the magnitude
and direction of these deviations may provide clues to
their causes. Additionally, much of ecology lies outside
the domain of metabolic theory. There are many phenomena
for which metabolic processes either do not
apply or play at most a small contributing role. Examples
include species­area and species­time relationships,
distributions of abundances among coexisting
species of similar size, temperature and resource
requirements, and the Taylor power law relationship
between mean and variance of population size over
time or space.
Finally, in this paper we have been concerned only
with basic science, with developing a conceptual
framework for ecology based on first principles of biology,
physics, and chemistry. This is not the place to
apply the theory to practical problems of environmental
policy and management. It should be apparent, however,
that there are many such applications, from wildlife,
fisheries, and forest management to global change
ecology. The theory helps one to understand some of
the changes that have occurred as humans have altered
size distributions of organisms, environmental temperatures,
and chemical stoichiometry of ecosystems.
The theory offers a predictive framework for assessing
and responding to human-induced changes in the abundance,
distribution, and diversity of organisms, and the
fluxes of energy and materials in ecological systems.
ACKNOWLEDGMENTS
This paper is dedicated to the memory of Robert MacArthur
for his contribution to ecological theory and his encouragement
of young ecologists, including J. H. Brown. We thank
the many people who have contributed data and ideas that
have influenced our thinking. The list is long. In addition to
many others, it includes B. Enquist, E. Charnov, W. Woodruff,
H. Olff, and colleagues, students, and visitors at the University
of New Mexico, the Santa Fe Institute, and Los Alamos
National Laboratory. S. Dodson, S. Levin, R. Paine, D. Tilman,
and several anonymous reviewers read the manuscript
and made helpful comments. G. B. West and J. H. Brown
were supported by a Packard Interdisciplinary Science
Award, a NSF Biocomplexity grant (DEB-0083422), and the
Thaw Charitable Trust. G. B. West was also supported by
NSF grant PHY-0202180.
LITERATURE CITED
Allen, A. P., J. H. Brown, and J. F. Gillooly. 2002. Global
biodiversity, biochemical kinetics and the energy equivalence
rule. Science 297:1545­1548.
Arrhenius, S. 1889. Uber die Reaktionsgeschwindigkeit bei
der Inversion von Rohrzucker durcj Sauren. Zeitschrift fur
Physik Chemique 4:226­248.
Bartholomew, G. A. 1981. A matter of size: an examination
of endothermy in insects and terrestrial vertebrates. Pages
45­78 in B. Heinrich, editor. Insect thermoregulation. John
Wiley, New York, New York, USA.
Belgrano, A., A. P. Allen, B. J. Enquist, and J. F. Gillooly.
2002. Allometric scaling of maximum population density:
a common rule for marine phytoplankton and terrestrial
plants. Ecology Letters 5:611­613.
Bell, G. 2001. Ecology: neutral macroecology. Science 293:
2413­2418.
Bernacchi, C. J., E. L. Singsaas, C. Pimentel, A. R. Portis,
and S. P. Long. 2001. Improved temperature response functions
for models of Rubisco-limited photosynthesis. Plant
Cell and Environment 24:253­259.
Blueweiss, L., H. Fox, V. Kudzma, D. Nakashima, R. Peters,
and S. Sams. 1978. Relationships between body size and
some life history parameters. Oecologia 37:257­272.
Boltzmann, L. 1872. Weitere Studien u¨ber das Wa¨rmegleichgewicht
unter Gasmoleku¨len. Sitzungsberichte der mathematisch-naturwissenschlaftlichen
Classe der kaiserlichen
Akademic der Wissenschaften Wien 66:275­370.
Brown, J. H. 1995. Macroecology. University of Chicago
Press, Chicago, Illinois, USA.
Brown, J. H., and J. F. Gillooly. 2003. Ecological food webs:
high-quality data facilitate theoretical unification. Proceedings
of the National Academy of Sciences (USA) 100:
1467­1468.
Brown, J. H., and M. V. Lomolino. 1998. Biogeography.
Sinauer, Sunderland, Massachusetts, USA.
Burnett, T. 1951. Effects of temperature and host density on
the rate of increase of an insect parasite. American Naturalist
85:337­352.
Cadenas, E., and L. Packer, editors. 1999. Understanding the
process of aging. Marcel Dekker, New York, New York,
USA.
Calder, W. A., III. 1984. Size, function and life-history. Harvard
University Press, Cambridge, Massachusetts, USA.
Carbone, C., and J. L. Gittleman. 2002. A common rule for
the scaling of carnivore density. Science 295:2273­2276.
Cebrian, J. 1999. Patterns in the fate of production in plant
communities. American Naturalist 154:449­468.
Chapin, F. S., III., P. A. Matson, and H. A. Mooney. 2002.
Principles of ecosystem ecology. Springer-Verlag, New
York, New York, USA.
Charnov, E. L. 1993. Life history invariants: some explorations
of symmetry in evolutionary ecology. Oxford University
Press, Oxford, UK.
Cohen, J. E., T. Jonsson, and S. R. Carpenter. 2003. Ecological
community description using the food web, species
abundance, and body size. Proceedings of the National
Academy of Sciences (USA) 100:1781­1786.
Currie, D. J. 1991. Energy and large-scale patterns of animaland
plant-species richness. American Naturalist 137:27­
49.
Cyr, H. 2000. Individual energy use and the allometry of
population density. Pages 267­295 in J. H. Brown and G.
B. West, editors. Scaling in biology. Oxford University
Press, New York, New York, USA.
Damuth, J. 1981. Population density and body size in mammals.
Nature 290:699­700.
Damuth, J. 1987. Interspecific allometry of population-density
in mammals and other animals: the independence of
body-mass and population energy-use. Biological Journal
of the Linnean Society 31:193­246.
Duellman, W. E. 1988. Patterns of species-diversity in anuran
amphibians in the American Tropics. Annals of the Missouri
Botanical Garden 75:79­104.
Dunson, W. A., and J. Travis. 1991. The role of abiotic factors
in community organization. American Naturalist 138:
1067­1091.
Eggleston, D. B. 1990. Behavioral mechanisms underlying
variable functional responses of blue crabs, Callinectes sapidus,
feeding on juvenile oysters, Crassostrea virginica.
Journal of Animal Ecology 59:615­630.
Elser, J. J., D. R. Dobberfuhl, N. A. MacKay, and J. H. Schampel.
1996. Organism size, life history, and N:P stoichiometry.
BioScience 46:674­684.
1788 JAMES H. BROWN ET AL. Ecology, Vol. 85, No. 7
Perspectives
Elser, J. J., W. F. Fagan, R. F. Denno, D. R. Dobberfuhl, A.
Folarin, A. Huberty, S. Interlandi, S. S. Kilham, E. McCauley,
K. L. Schulz, E. H. Siemann, and R. W. Sterner.
2000a. Nutritional constraints in terrestrial and freshwater
food webs. Nature 408:578­580.
Elser, J. J., R. W. Sterner, E. Gorokhova, W. F. Fagan, T. A.
Markow, J. B. Cotner, J. F. Harrison, S. E. Hobbie, G. M.
Odell, and L. J. Weider. 2000b. Biological stoichiometry
from genes to ecosystems. Ecology Letters 3:540­550.
Enquist, B. J., J. H. Brown, and G. B. West. 1998. Allometric
scaling of plant energetics and population density. Nature
395:163­165.
Enquist, B. J., E. P. Economo, T. E. Huxman, A. P. Allen, D.
D. Ignace, and J. F. Gillooly. 2003. Scaling metabolism
from organisms to ecosystems. Nature 423:639­642.
Enquist, B. J., and K. J. Niklas. 2001. Invariant scaling relations
across tree-dominated communities. Nature 410:
655­660.
Enquist, B. J., G. B. West, E. L. Charnov, and J. H. Brown.
1999. Allometric scaling of production and life-history
variation in vascular plants. Nature 401:907­911.
Ernest et al. 2003. Thermodynamic and metabolic effects on
the scaling of production and population energy use. Ecology
Letters 6:990­995.
Falkowski, P., et al. 2000. The global carbon cycle: a test of
our knowledge of earth as a system. Science 290:291­296.
Farquhar, G. D., S. von Caemerrer, and J. A. Berry. 1980. A
biochemical model of photosynthetic CO2 assimilation in
leaves of C3 plants. Planta 149:78­90.
Field, C. B., and H. A. Mooney. 1986. The photosynthesisnitrogen
relationship in wild plants. Pages 25­55 in T. J.
Givnish, editor. The economy of plant form and function.
Cambridge University Press, Cambridge, UK.
Foss, H. E., and V. E. Forbes. 1997. Effects of the polycyclic
aromatic hydrocarbon fluoranthene on growth rate and nucleic
acid composition of Capitella sp. I. Marine Biology
129:489­497.
Gause, G. F. 1934. The struggle for existence. Williams and
Wilkins, Baltimore, Maryland, USA.
Gerschman, R., D. L. Gilbert, S. W. Nye, P. Dwyer, and W.
O. Fen. 1954. Oxygen poisoning and x-irradiation: a mechanism
in common. Science 19:623­629.
Gillooly, J. F., J. H. Brown, G. B. West, V. M. Savage, and
E. L. Charnov. 2002. Effects of size and temperature on
metabolic rate. Science 293:2248­2251.
Gillooly, J. F., E. L. Charnov, G. B. West, V. M. Savage, and
J. H. Brown. 2001. Effects of size and temperature on
developmental time. Nature 417:70­73.
Gillooly, J. F., and S. I. Dodson. 2000. The relationship of
neonate mass and incubation temperature to embryonic development
time in a range of animal taxa. Journal of Zoology
251:369­375.
Hartman, D. 1956. Aging: a theory based on free radical and
radiation chemistry. Journal of Gerontology 11:298­300.
Hubbell, S. P. 2001. A unified neutral theory of biodiversity
and biogeography. Princeton University Press, Princeton,
New Jersey, USA.
Huffaker, C. B. 1958. Experimental studies on predation:
dispersion factors and predator­prey oscillations. Hilgardia
27:343­383.
Hutchinson, G. E. 1961. The paradox of the plankton. American
Naturalist 95:137­145.
Hutchinson, G. E., and R. H. MacArthur. 1959. A theoretical
ecological model of size distributions among species of
animals. American Naturalist 93:117­125.
Huxley, J. S. 1932. Problems of relative growth. Methuen,
London, UK.
Ingestad, T. 1979. Mineral nutrient-requirements of Pinus
silvestris and Picea abies seedlings. Physiologia Plantarum
45:373­380.
Kerr, S. R., and L. M. Dickie. 2001. The biomass spectrum.
Columbia University Press, New York, New York, USA.
Kleiber, M. 1932. Body size and metabolism. Hilgardia 6:
315­332.
Kozlowski, J., and J. Weiner. 1997. Interspecific allometries
are by-products of body size optimization. American Naturalist
147:101­114.
Li, W. K. W. 2002. Macroecological patterns of phytoplankton
in the northwestern North Atlantic Ocean. Nature 419:
154­157.
Lieth, H. 1973. Primary production: terrestrial ecosystems.
Human Ecology 1:303­332.
Lindeman, R. 1942. The trophic-dynamic aspect of ecology.
Ecology 23:399­418.
Lister, A. M. 1989. Red deer dwarfing on Jersey in the last
interglacial. Nature 342:539­542.
Lonsdale, W. M. 1990. The self-thinning rule: dead or alive?
Ecology 71:1373­1388.
Lotka, A. J. 1925. Elements of physical biology. Williams
and Wilkins, Baltimore, Maryland, USA.
Luecke, C., and W. J. O'Brien. 1983. The effect of heterocope
predation on zooplankton communities in arctic ponds.
Limnology and Oceanography 28:367­377.
May, R. M. 1978. The dynamics and diversity of insect faunas.
Pages 188­204 in L. A. Mound and N. Waloff, editors.
Diversity of insect faunas. Blackwell, Oxford, UK.
May, R. M. 1986. The search for patterns in the balance of
nature: advances and retreats. Ecology 67:1115­1126.
May, R. M. 1988. How many species are there on earth?
Science 241:1441­1440.
Morowitz, H. J., J. D. Kostelnik, J. Yang, and G. D. Cody.
2000. The origin of intermediary metabolism. Proceedings
of the National Academy of Sciences (USA) 97:7704­
7708.
Nagy, K. A. 2001. Food requirements of wild animals: predictive
equations for free-living mammals, reptiles, and
birds. Nutrition Abstracts and Reviews, Series B 71:21r­
31r.
Niklas, K. J. 1994. Plant allometry: the scaling of form and
process. University of Chicago Press, Chicago, Illinois,
USA.
Niklas, K. J., and B. J. Enquist. 2001. Invariant scaling relationships
for interspecific plant biomass production rates
and body size. Proceedings of the National Academy of
Sciences (USA) 98:2922­2927.
Odum, E. P. 1969. The strategy of ecosystem development.
Science 164:262­270.
Pace, N. R. 1997. A molecular view of microbial diversity
and the biosphere. Science 276:734­740.
Park, T. 1948. Experimental studies of interspecies competition:
I. Competition between populations of the flour beetles,
Tribolium confusum Duvall and Tribolium castaneum
Herbst. Ecological Monographs 18:267­307.
Park, T. 1954. Experimental studies of interspecific competition
II. Temperature, humidity, and competition in two
species of Tribolium. Physiological Zoology 27:177­238.
Pauly, D. 1980. On the interrelationships between natural
mortality, growth parameters, and mean environmental
temperature in 175 fish stocks. Journal du Conseil 39:175­
192.
Pauly, D., and R. S. V. Pullin. 1988. Hatching time in spherical,
pelagic, marine fish eggs in response to temperature
and egg size. Environmental Biology of Fishes 22:261­
271.
Peters, R. H. 1983. The ecological implications of body size.
Cambridge University Press, Cambridge, UK.
Peterson, J., and J. S. Wroblewski. 1984. Mortality rates of
fishes in the pelagic ecosystem. Canadian Journal of Fisheries
and Aquatic Sciences 41:1117­1120.
July 2004 1789MACARTHUR AWARD LECTURE
Perspectives
Redfield, A. C. 1958. The biological control of chemical
factors in the environment. American Scientist 46:205­221.
Reiners, W. A. 1986. Complementary models for ecosystems.
American Naturalist 127:59­73.
Rohde, K. 1992. Latitudinal gradients in species-diversity:
the search for the primary cause. Oikos 65:514­527.
Roth, V. L. 1990. Insular elephants: a case study in body
mass estimation and ecological inference. Pages 151­179
in J. Damuth and B. J. MacFadden, editors. Body size in
paleobiology: estimation and biological implications. Cambridge
University Press, New York, New York, USA.
Savage, V. M., J. F. Gillooly, J. H. Brown, G. B. West, and
E. L. Charnov. In press a. Effects of body size and temperature
on population growth. American Naturalist.
Savage, V. M., J. F. Gillooly, W. H. Woodruff, G. B. West,
A. P. Allen, B. J. Enquist, and J. H. Brown. In press b.
The predominance of quarter-power scaling in biology.
Functional Ecology.
Schlesinger, W. H. 1991. Biogeochemistry: an analysis of
global change. Academic Press, San Diego, California,
USA.
Schmidt-Nielsen, K. 1984. Scaling: why is animal size so
important? Cambridge University Press, Cambridge, UK.
Schmidt-Nielsen, K. 1997. Animal physiology. Cambridge
University Press, Cambridge, UK.
Sheldon, R. W., and T. R. Parsons. 1967. A continuous size
spectrum for particulate matter in the sea. Journal of the
Fisheries Research Board of Canada 24:900­925.
Sheldon, R. W., A. Prakash, and W. H. Sutcliffe. 1972. The
size distribution of particles in the ocean. Limnology and
Oceanography 17:327­340.
Sheldon, R. W., W. H. Sutcliffe, and M. A. Paranjape. 1977.
Structure of pelagic food-chain and relationship between
plankton and fish production. Journal of the Fisheries Research
Board of Canada 34:2344­2353.
Silver, W. L., and R. K. Miya. 2001. Global patterns in root
decomposition: comparisons of climate and litter quality
effects. Oecologia 129:407­419.
Slobodkin, L. B. 1962. Growth and regulation of animal populations.
Holt, Reinhart, and Winston, New York, New
York, USA.
Spitze, K. 1985. Functional response of an ambush predator:
Chaoborus americanus predation on Daphnia pulex. Ecology
66:938­949.
Stearns, S. C., M. Ackerman, M. Doebeli, and M. Kaiser.
2000. Experimental evolution of aging, growth, and reproduction
in fruitflies. Proceedings of the National Academy
of Sciences (USA) 97:3309­3313.
Sterner, R. W. 1990. The ratio of nitrogen to phosphorus
resupplied by herbivores: zooplankton and the algal competitive
arena. American Naturalist 163:209­229.
Sterner, R. W., and J. J. Elser. 2002. Ecological stoichiometry:
the biology of elements from molecules to the biosphere.
Princeton University Press, Princeton, New Jersey,
USA.
Sutcliffe, W. H. J. 1970. Relationship between growth rate
and ribonucleic acid concentration in some invertebrates.
Journal of the Fisheries Research Board of Canada 27:606­
609.
Taylor, C. R., N. C. Heglund, and G. M. O. Maloiy. 1982.
Energetics and mechanics of terrestrial locomotion. I. Metabolic
energy consumption as a function of speed and body
size in birds and mammals. Journal of Experimental Biology
97:1­21.
Thompson, D. W. 1942. On growth and form: a new edition.
Cambridge University Press, Cambridge, UK.
Tilman, D. 1988. Plant strategies and the dynamics and structure
of plant communities. Princeton University Press,
Princeton, New Jersey, USA.
Tilman, D., M. Mattson, and S. Langer. 1981. Competition
and nutrient kinetics along a temperature-gradient: an experimental
test of a mechanistic approach to niche theory.
Limnology and Oceanography 26:1020­1033.
Turchin, P. 2001. Does population ecology have general
laws? Oikos 94:17­26.
Van Valen, L. M. 1973. A new evolutionary law. Evolutionary
Theory 1:1­30.
Verity, P. G. 1985. Grazing, respiration, excretion, and
growth rates of tintinnids. Limnology and Oceanography
30:1268­1282.
Vitousek, P. M. 1982. Nutrient cycling and nutrient use efficiency.
American Naturalist 119:553­572.
Volterra, V. 1926. Fluctuations in the abundance of a species
considered mathematically. Nature 118:558­560.
West, G. B., J. H. Brown, and B. J. Enquist. 1997. A general
model for the origin of allometric scaling laws in biology.
Science 276:122­126.
West, G. B., J. H. Brown, and B. J. Enquist. 1999a. A general
model for the structure and allometry of plant vascular
systems. Nature 400:664­667.
West, G. B., J. H. Brown, and B. J. Enquist. 1999b. The
fourth dimension of life: fractal geometry and allometric
scaling of organisms. Science 284:1677­1679.
West, G. B., J. H. Brown, and B. J. Enquist. 2001. A general
model for ontogenetic growth. Nature 413:628­631.
West, G. B., W. H. Woodruff, and J. H. Brown. 2002. Allometric
scaling of metabolic rate from molecules and mitochondria
to cells and mammals. Proceedings of the National
Academy of Sciences (USA) 99:2473­2478.
Withers, P. C. 1992. Comparative animal physiology. Brooks/
Cole Thompson Learning, Pacific Grove, California, USA.
1790
FORUM
The Metabolic Theory of Ecology1
Scaling in biology has a rich and important history. Typically body mass, or some other
parameter relating to organism size, is related to anatomical, physiological, and ecological parameters
across species. Quite remarkably, diverse organisms, from tiny microbes to the earth's
largest organisms are found to fall along a common slope, with a high degree of variance explained.
The beauty of such scaling ``laws'' has been the generality in biotic organization that they suggest,
and the challenge (for ecologists) has often been interpreting their mechanistic bases and ecological
consequences.
Scaling laws have thus far inspired scientists in at least three major areas. First, scaling laws
may illuminate biology that is otherwise shrouded. For example, if scaling relationships can
account for variation in a parameter of interest, the residual variation may be much more easily
examined because the major influence of some trait, say, body size, is removed. Second, some
scientists have taken an interest in ``the exponent''--essentially the exponential scaling values
that produce the allometric relationship. What are the precise values of these exponents? Are
they all from a family of particular values (quarter powers) for many different biological relationships?
This area seeks to define the generality of patterns in nature and to explore the empirical
robustness of the relationships. Third, from a mechanistic perspective, if scaling laws are mechanistic
and truly general, then this suggests some underlying common biological process that
forms the structure and function of species and ultimately generates biological diversity. The
mechanistics of scaling from metabolism and the currently favored fractal network model of
resource acquisition and allocation may allow scientists to understand the laws of how life
diversified and is constrained. Perhaps more importantly, such a mechanistic understanding should
allow the successful prediction of evolutionary trends, responses of organisms to global change,
and other basic and applied biological problems.
The Ecological Society of America's MacArthur Award winner, James H. Brown, working
together with colleagues for over a decade on scaling in biology, has arrived at an outline for a
metabolic theory of ecology--a proposal for a unifying theory employing one of the most fundamental
aspects of biology, metabolism. This metabolic theory incorporates body size, temperature
(metabolic kinetics described by the Boltzmann factor), and resource ratios of the essential
elements of life (stoichiometry). Indeed, this bold and visionary proposal is likely to
inspire ecologists and provoke much discussion. My goal in assembling this Forum was to work
toward a balanced discussion of the power and logic of the metabolic theory of ecology. I have
asked both junior and senior scientists to evaluate the ideas presented in the metabolic theory
and to go beyond the listing of strong and weak points. As such, this collection of commentaries
should be viewed neither as a celebration of the theory nor as a roast of Jim Brown. It should,
however, serve as a springboard for future research and refinements of the metabolic theory.
Several themes and axes of admiration and agitation emerge from the forum. The focus on
metabolism, and metabolic rate in particular, is an advance that most agree is the fundamental
basis for the processes of acquisition of resources from the environment and, ultimately, survival
and reproduction of organisms. The combination of size, temperature, and nutrients has compelling
predictive power in explaining life-history traits, population parameters, and even broader-scale
ecosystem processes. The key point here is that Brown et al. are making a direct link between
factors that affect the functioning of individuals and the complex role that those individuals play
in communities and ecosystems. Although what we have before us is a proposal for a unified
theory of ``biological processing of energy and materials'' in ecosystems, Brown et al. embrace
the unexplained variation and acknowledge other areas of ecology that may not be subject to
metabolic laws.
1 Reprints of this 51-page Forum (including the MacArthur Lecture) are available for $7.75 each, either
as pdf files or as hard copy. Prepayment is required. Order reprints from the Ecological Society of America,
Attention: Reprint Department, 1707 H Street, N.W., Suite 400, Washington, D.C. 20006.
Forum
The commentaries presented in this Forum are unanimous in their admiration of Brown et al.'s
broad theoretical proposal and its clear predictions. Yet, points of discussion abound and range
widely: What really is the correct exponent? Does the scale at which scaling is applied affect its
explanatory power? Are the laws really based on mechanism or phenomena? How does the
addition of temperature and resource limitation enhance the power of scaling relationships? And,
is scaling up from the metabolic rate and body mass of organisms to population dynamics,
community structure, and ecosystem processes possible? This Forum ends with Brown's response
to the commentaries. Although there will be continued debate over the correct exponent, the data
at hand from the broadest taxonomic groups support quarter powers. There is general agreement
over the issue of scale and the fact that, depending on the scale of interest, metabolic theory may
have more or less to offer. Finally, nutrient stoichiometry is the most recent addition to metabolic
theory, and all agree that further research and refinement will determine the role for such nutrient
ratios in the ecological scaling. The benefits of a metabolic theory of ecology are clear. The
authors of this Forum have outlined some of the future challenges, and tomorrow's questions
will evaluate these theses.
--ANURAG A. AGRAWAL
Special Features Editor
Key words: allometry; biological scaling; body size; Boltzmann factor; ecophysiology; functional
ecology; laws in ecology; MacArthur Award paper; macroecology; nutrient stoichiometry.
2004 by the Ecological Society of America
Forum
1792 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
Ecology, 85(7), 2004, pp. 1792­1794
2004 by the Ecological Society of America
THE VALUE OF NULL THEORIES IN ECOLOGY
JOHN HARTE1
Energy and Resources Group, University of California, 310 Barrows Hall, Berkeley, California 94720 USA
Reactions to the metabolic theory of ecology (MTE)
proposed by Brown et al. (2004, this issue) are likely
to fall into the following categories.
Enthusiastic support.--MTE persuasively demonstrates
how a few simple, well-founded physical principles
concerning energy and temperature can explain
an impressive fraction of the natural variability in organism-level
productivity, developmental rates, mortality,
and other life history traits, and in ecosystemlevel
carbon turnover, population density, and resource
partitioning. This is particularly impressive, given that
the theory assumes nothing about many of the concepts
that most ecologists had probably thought to be essential
input to any comprehensive theory, such as reproductive
strategies, succession, stability, food webs, spatial
distribution of individuals and species, stochastic
and cyclic temporal variability, the influence of disturbance
regimes, and organism behavior (including its
role in determining effective environmental temperature).
MTE will be a major component of a parsimonious
theory of nearly everything in ecology. Here at
last is an agenda for ecology.
Limited admiration.--MTE explains parsimoniously
a very limited subset of ecosystem traits, but it cannot
hope to say anything useful about most of the things
that we care about in ecology, such as reproductive
strategies, succession, stability, food webs, spatial distribution
of individuals and species, stochastic and cyclic
temporal variability, the influence of disturbance
regimes, and organism behavior. A parsimonious theory
of nearly everything in ecology is, at best, far in
the future. In the meantime, there are also critical questions
in applied ecology. What will ecosystems look
like under global warming? What sustains and what
threatens ecosystem services? How can ecosystems be
restored and managed? How can we best design reserves?
We do not have the luxury of waiting indefinitely
for some future comprehensive theory of ecology
to answer these practical questions; unfortunately,
MTE will not help us here.
Skeptical dismissal.--The unexplained variances in
MTE are large and all those ignored aspects of ecology
(listed in Limited admiration) would have to be ingredients
in any theory that would convincingly explain
Manuscript received 14 October 2003. Corresponding Editor:
A. A. Agrawal. For reprints of this Forum (including
the MacArthur Award paper), see footnote 1, p. 1790.
1 E-mail: jharte@socrates.berkeley.edu
even just the limited things that MTE purports to explain.
One needs to consider nearly everything to explain
anything in ecology; parsimony and ecology are
immiscible.
In some fields of science, responses to proposed new
radical advances are more tightly bounded than this.
Nearly all physicists accept the goal of a ``theory of
everything'' (TOE), and they may well achieve that
goal if ``everything'' is understood to mean all of the
physical phenomena that occur at subatomic and cosmological
scales. Less clear, however, is whether any
such theory could also encompass emergent physical
phenomena at intermediate scales, where we live.
Brown et al. (2004), making the case for Enthusiastic
support, suggest that MTE, in combination with population
genetics and evolution, can indeed provide the
basis for an ecological TOE. Although the successes
of the physics-based MTE are unlikely to dispel skepticism
about the possibility of a physics-based TOE for
biological phenomena, could MTE plus evolution and
genetics conceivably do the trick, as Brown et al. suggest?
More generally, what would an ecological TOE
look like? Is it possible in ecology, and if so, how would
we get there from here?
An ecological TOE would provide, at the very least,
an accurate and predictive understanding, across all
ecologically interesting spatial and temporal scales, of
the distribution and abundance of organisms in interaction
with each other and their environment. Unlike
physics, however, ecology has to deal with contingency.
A theory that beautifully describes the distribution
and abundance of organisms at the spatial scale of a
meadow and the temporal scale of an NSF grant would
also have to scale up spatially to deal with the geologic
contingency of continent edges and temporally to encompass
global warming. Because of that, most ecologists
would probably answer our rhetorical question
``Is a TOE possible?'' with a resounding ``no.'' I tend
to agree, although hesitantly, because I think we can
go farther than we have--by embracing, rather than
dismissing, approaches such as MTE.
Progress in science comes from the interplay of enlarging
possibilities (envisioning options for how nature
might work) and narrowing those options (empirical
testing). Clearly stated null hypotheses and null
models help to accomplish the latter because their failures
permit us to identify situations in which a nonnull
alternative is needed. Failure is what drives science
forward.
July 2004 1793METABOLIC THEORY OF ECOLOGY
Forum
MTE also will surely fail if pushed too far. The unexplained
variances in the figures in Brown et al. (2004)
are undoubtedly just a preview of what will arise as
the theory attempts to widen its domain of applicability.
A recently proposed ``neutral theory'' of ecology
(Hubbell 2001) is probably also ``wrong,'' and, indeed,
instances of its failure to accurately describe patterns
in nature have been suggested (Condit et al. 2002, Clark
and McLachlan 2003). If ecology were physics, this
might be considered sufficient evidence to dismiss such
theories entirely, but given the parsimony of both of
these theories, that would not promote progress in ecol-
ogy.
Theories are of most interest when the ratio of the
number of predictions that they make to the number of
assumptions and adjustable parameters in the theory is
large. The MT of Brown et al. (2004) and Hubbell's
neutral theory are examples of theories based on very
few assumptions and very few adjustable parameters,
yet they are potentially capable of predicting a wide
range of phenomena.
Suppose that the interrelationships among many
types of phenomena are reasonably well predicted by
a theory, yet each phenomenon is, separately, better
predicted by some ad hoc explanation or cobbled-together
model than by that theory. If those successful
explanations or models each require a different set of
assumptions or parameters for each comparison, then
it may be premature to reject the theory. In other words,
the insight afforded by the theory into the interconnections
among phenomena previously thought to be
disconnected ought to trump slightly better fits afforded
by ad hoc explanations.
As a natural extension of the idea of null hypotheses
and null models, I suggest that the notion of a ``null
theory'' is of value in ecology. By a null theory, I mean
a set of relatively few and clearly stated assumptions
that can be used to make a comprehensive set of falsifiable
predictions about a wide variety of issues in
ecology. In contrast to null models, which address specific
ecological questions, null theories attempt to provide
a single coherent set of answers to many questions.
Without a null theory, those questions might have been
considered independent of one another; a null theory
would unify them under one framework. Each of those
questions might be addressed with a null model, but
in typical applications of null models, a unique null
model is tailored to each question. Thus, there are many
ways to create models of what nature might be like if
it were random. For example, random models for the
species­area relationship could involve random assignments
of individuals, random assignments of species,
or random shuffling of census quadrats. If a common
set of assumptions about randomness were used
to create an array of null models that together addressed
a comprehensive collection of questions, then the array
of models would fit our notion of a null theory; indeed,
it might be called a random null theory. But surely
there is no reason to restrict null theories to those that
are random.
A decade ago, a null metabolic theory of ecology
could have been constructed around the body-mass-tothe-two-thirds-power
scaling law, because that is a null
expectation based on surface : volume ratios. All of the
equations that Brown et al. (2004) discuss could have
been written then, with  replacing , and an equally
comprehensive theory developed. Although such a theory
was never constructed, falsification of the twothirds-power
metabolic rule paved the way for what
Brown et al. have accomplished.
Just as it is the failures of null hypotheses and null
models that most enlarge our understanding, so it is
the mismatches between collections of data and null
theories that make null theories useful. We should expect
null theories to ``fail,'' just as we expect null hypotheses
and null models to fail under many circumstances.
However, by examining the instances in which
a null theory fails to describe all of the data, and in
particular looking carefully at the patterns in the discrepancies,
we can establish more firmly the existence
of mechanisms in nature that explicitly violate the simple
assumptions underlying the theory, and thereby
learn a great deal about how nature works. Whether
the outcome of this is an improvement of the null theory
or the development of a whole new theoretical
construct may be less important than is the added insight
into the mechanisms at work in ecology.
Eventually, the patterns of success and failure of null
theories may suggest the outlines of an ecological theory
of nearly everything. Such a theory, rising from
the ashes of null theories, might even be considered
just another null theory--it won't really matter what
we call it. The important thing is that it be falsifiable,
and that it parsimoniously predict many more phenomena
than it has parameters to adjust. It would be exciting
if its base were broader than physics.
MTE is certainly parsimonious and its predictions
match observations in nature to a remarkable degree
over many orders of magnitude of variation in biological
parameter space. At the same time, it appears so
far to be able to address only a modest fraction of
questions of concern to ecologists. It is a fine example
of a null theory in that (1) it ties together multiple
phenomena within one set of extremely simple assumptions,
and (2) departures from its predictions can
inform us about other factors besides metabolism and
temperature that are at work in ecology. In the search
for a TOE, or at least a more comprehensive null theory
of ecology--one that would improve, and expand the
scope of, MTE--Brown et al. should look forward to
MTE's failures with enthusiasm.
LITERATURE CITED
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Forum
1794 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
Clark, J. S., and J. S. McLachlan. 2003. Stability of forest
biodiversity. Nature 423:635­638.
Condit, R., et al. 2002. Beta- diversity in tropical forest trees.
Science 295:666­669.
Hubbell, S. P. 2001. The unified neutral theory of biodiversity
and biogeography. Princeton University Press, Princeton,
New Jersey, USA.
Ecology, 85(7), 2004, pp. 1794­1796
2004 by the Ecological Society of America
METABOLIC ECOLOGY: LINKING INDIVIDUALS TO ECOSYSTEMS
PABLO A. MARQUET,1,3
FABIO A. LABRA,1
and BRIAN A. MAURER2
1Center for Advanced Studies in Ecology and Biodiversity and Departamento de Ecologi´a, Pontificia Universidad Cato´lica
de Chile, Alameda 340, Santiago, Chile
2Department of Fisheries and Wildlife, Michigan State University, East Lansing, Michigan 48823 USA
INTRODUCTION
Metabolism sustains life and controls the growth,
reproduction, and longevity of living entities. As
Brown et al. (2003, 2004) show, the ``fire of life'' is
central to our understanding of patterns and dynamics
at all levels of biological organization. However simple,
it took 70 years to substantiate this statement; from
Kleiber's (1932) conclusion that the mass of the organism
raised to the  power was the best predictor
of metabolism to the model of West et al. (1997, 1999)
that explains this relationship as a consequence of fundamental
attributes of biological networks. This work
paved the way to the Metabolic Theory of Ecology
(MTE) outlined by Brown et al. (2004). We think that
the theory outlined by Brown and co-workers represents
a breakthrough that endows ecological sciences
with a fresh perspective and a quantitative theory to
tackle ecological complexity, from individuals to ecosystems.
However, as with any new theory in science,
it can be improved and refined.
THEORETICAL UNDERPINNINGS OF THE
METABOLIC THEORY
The ultimate success of the emerging metabolic theory
of ecology (Brown et al. 2003, 2004) depends to a large
extent on whether it is truly a mechanistic theory based
on first principles, or whether, like so many other theories
in ecology, it is fundamentally phenomenological.
The theory is based on what we call a general metabolic
equation (GME):
P F(M, T, R) (1)
where P is the rate of some metabolic process, which
is some function F of body mass (M), temperature (T),
and the concentration of the materials (R) needed to
Manuscript received 20 October 2003. Corresponding Editor:
A. A. Agrawal. For reprints of this Forum (including
the MacArthur Award paper), see footnote 1, p. 1790.
3 E-mail: pmarquet@genes.bio.puc.cl
fuel and maintain metabolism. Following Gillooly et
al. (2001) and Brown et al. (2003), who argue that the
effects of M and T are multiplicative, and assuming
that the effects of concentration of materials is also
multiplicative, Eq. 1 becomes
3/4P B M exp( E/kT)f(R)0 (2)
where B0 is a constant, E is the ``activation energy of
metabolism,'' k is Boltzmann's constant, and f is a heretofore
unspecified function. In the strictest sense, Eq.
2 is not a mechanistic equation; rather, it is statistical
mechanical. By this we mean that the functions used
in the equation emerge from the properties of the ensemble
of molecules that comprise the physical unit
that is generating metabolic energy (typically, an or-
ganism).
The statistical mechanics of the body size effect has
a strong theoretical justification (West et al. 1997, 1999).
However, the effect of temperature on metabolic rate as
modeled by Gillooly et al. (2001) uses the exponential
form given in Eq. 2 with relatively little theoretical justification.
In statistical mechanics, the term exp( E/kT),
often referred to as the ``Boltzmann factor,'' is proportional
to the fraction of molecules of a gas that attain
an energy state of E (Schrodinger 1941, Pauling 1970)
at an absolute temperature T. To react, the molecules
must possess ``activation energy,'' that is, they must
collide with one another with sufficient energy to change
their state (Pauling 1970). Temperature increases the
proportion of molecules that attain sufficient energy to
react. Hence, the Boltzmann factor can be used to describe
the rate of the reaction. This heuristic approach
for using the Boltzmann factor in describing metabolism
would be extremely difficult to derive in a mechanistic
fashion, considering the very large number of different
biochemical reactions that comprise metabolism. We
should therefore consider the Boltzmann formulation
used by Gillooly et al. (2001) as an approximation of a
much more complicated functional relationship between
metabolism and temperature.
July 2004 1795METABOLIC THEORY OF ECOLOGY
Forum
The concentration of resources (R, or stoichiometry)
is the third component of the GME. However, its relationship
to metabolism lacks an analytical expression,
which prevents the MTE from making explicit
how it interacts with T and M in affecting individual
or population attributes. At first glance, it is not entirely
clear how to include stoichiometric effects in the GME
(the function f in Eq. 2). However, it is reasonable to
expect that f should have a multiplicative effect on
metabolism, and because organisms often show a
``functional response'' in reaction to changes in the
abundance of a limiting resource, f could be modeled
as a Michaelis-Menten function (Real 1978, Maurer
1990). If the ingestion rate is proportional to the metabolic
rate, then one would expect that metabolic processes,
such as biomass production, would show a similar
sort of saturating response and that the MichaelisMenten
equation could be used. There is, in fact, experimental
evidence that such responses do occur
(Giebelhausen and Lampert 2001).
Interestingly, each term in the GME relates to processes
whose primary mechanistic effects occur on different
spatial and temporal scales. Temperature has its
primary effect at the molecular scale, by influencing
the rate of molecular movements through the parts of
the metabolic machinery that depend on passive diffusion.
Body size affects metabolism at a larger scale
via constraints derived from fractal-like distribution
networks. Finally, stoichiometric effects occur at the
scale of the whole organism in interaction with its environment.
This feature of the GME bequeaths the MTE
with a desirable property: cross-scale integration.
We think that the MTE still requires refinement and
further articulation. However, there is sufficient evidence
to suggest that the MTE may provide a fundamental
theoretical link between what we know about
physical systems and what we know about ecological
systems.
THE MTE AND THE STRUCTURE OF LOCAL
ECOLOGICAL SYSTEMS
The MTE rests heavily on individual-level phenomena,
which by aggregation allow one to make predictions
upon whole-system patterns, processes, and rates. It is
striking how strong the fit between predicted and observed
patterns usually is, considering that most data on
individuals and species populations come from different
places around the world, with different biogeographic
histories, disturbance regimes, and productivities. It
might seem striking that a theory that is, for the most
part, free of ecological context (Marquet 2002) can be
so powerful. However, this is to some extent expected,
given that the theory focuses on ``bulk properties'' of
ecological systems that are less affected by local ecological
idiosyncrasies. The MTE is a theory about central
tendencies in ecological phenomena that predicts how
the average individual, population, and ecosystem
should behave and be structured. Although many would
say that the interesting biology is in the scatter and that
such a thing as an average ecological system does not
exist, but just different realizations of the average system,
it is important to recognize that unless we have a
mechanistic theory that provides us with an expected
baseline, we are not able to identify any deviation worth
explaining in the first place. In this sense, both approaches
are interesting and complementary.
We have no doubt that the MTE can provide many
insights on fundamental ecological questions at local,
regional, and global scales. In particular, at a local
scale: (1) it provides an explanation of why, in a local
community, population density should scale as M 3/4
within trophic levels and as M 1 across them, a pattern
that has been empirically observed in aquatic ecosystems
(e.g., Marquet et al. 1990); and (2) it predicts that
population energy use should be independent of body
mass within trophic levels, but should decrease at higher
trophic levels. Further, the amount of energy that
moves from one level to the next should be affected
by the characteristic metabolic scaling of the species
in each trophic level. However, there are other important
patterns within local communities, such as species
abundance and species size distributions, to which the
MTE could be applied, and that, in principle, it should
be able to explain, since they affect and are affected
by energy fluxes.
A close examination of the MTE shows that several
predictions can be made regarding the effects of resource
supply upon equilibrium abundance and how
abundance should vary across resource and temperature
gradients for metabolically different organisms. In
particular, Eq. 9 of Brown et al. (2004) states that the
equilibrium number of individuals or carrying capacity
(K) in a local community should vary as K
RM 3/4
eE/kT
. Further, because metabolic rate (P) is P
M 3/4e E/kT (Brown et al. 2004: Eq. 4), we can express
carrying capacity as
R
K . (3)
P
Eq. 3 implies that, given a fixed amount of resources
R, organisms with lower metabolic demands will
achieve higher equilibrium population numbers or carrying
capacities. For any given temperature, mass-corrected
metabolism is higher in some groups than others
(see Brown et al. 2004: Fig. 1a); thus, everything else
being equal, carrying capacities should follow the inverse
pattern, decreasing from plants to endotherms. In
other words, there should be a negative relationship
between the intercept of the mass-corrected relationship
between metabolic rate and temperature and the
total abundance of metabolically different organisms
in a given community. This relationship would be even
stronger if we were to consider trophic structure and
the fact that energy or resources become more limiting
farther up in a food chain. Because organisms with
Forum
1796 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
FIG. 1. Relationship between area-corrected number of
species expressed as the intercept of the species­area curve
(CS), and mass- and temperature-corrected metabolic rate expressed
as the intercept of the mass-corrected metabolic rate
vs. temperature (CM). Data are for the Channel Islands, Sea
of Cortes, and West Indies, and include plants, reptiles, land
snails, birds, and mammals. Within each system, we only use
islands for which data on all groups were available. The solid
line corresponds to the best-fit exponential equation CS
exp(15.6 0.75CM).
lower metabolic demands are more likely to sustain
higher population numbers, they will, on average, support
more populations of different species above the
minimum size required for persistence. Thus, higher
species richness should be expected for groups with
lower metabolic needs. This argument, similar to the
one traditionally used to explain the effect of energy
availability on species diversity (e.g., Wright 1983,
Currie 1991), predicts that in a local community, species
diversity in any given metabolic group should be
inversely correlated with metabolic demands. Our analysis
shows (Fig. 1) that there is indeed a negative relationship
(F1,12 67.07, P 0.001, r2
0.84) between
the area-corrected number of species (represented by
the intercept of the species­area relationship CS) and
the temperature- and mass-corrected metabolic rate
(represented by the intercept of the mass-corrected metabolic
rate vs. temperature, CM) for metabolically different
groups of organisms in islands. That this relationship
exists indicates the heuristic value and predictive
power of the MTE. It is especially significant
because many other factors besides metabolism affect
the number of species on islands. In addition, resource
supply rate is not the same for all species groups because
of their trophic position, yet the pattern seems
to be robust to this.
The main point that we want to make with this analysis
is that the MTE can provide fruitful insights and
testable predictions to advance our understanding of
the structure of local ecological systems. However, further
development and testing of this approach will require
the collection of more and better data on the
richness, density, biomass, and metabolic activity of
species within local ecosystems. We need standardized
data on biodiversity, which will allow for rigorous tests
of the MTEs predictions at a local scale. This might
be a daunting task, but to advance in our understanding,
we need comprehensive and complete analyses of ecological
systems. The 13 years and millions of dollars
invested in sequencing the human genome can help to
save lives, but to characterize ecological systems in
terms of their total species composition, abundance,
and function, or the ``econome,'' can help to save the
human enterprise on earth.
ACKNOWLEDGMENTS
We appreciate comments and discussion provided by Jeniffer
Dunne, Van Savage, James Gillooly, and David Storch.
We acknowledge the support of the Santa Fe Institute through
an International Fellowship, FONDAP-FONDECYT 1501-
0001 (both to P. A. Marquet) and a CONICYT graduate fellowship
to F. A. Labra.
LITERATURE CITED
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Brown, J. H., J. F. Gillooly, G. B. West, and V. M. Savage.
2003. The next step in macroecology: from general empirical
patterns to universal ecological laws. Pages 408­
423 in T. M. Blackburn and K. J. Gaston, editors. Macroecology:
concepts and consequences. Blackwell, Oxford,
UK.
Currie, D. J. 1991. Energy and large scale patterns of animal
and plant species richness. American Naturalist 137:27­
49.
Giebelhausen, B., and W. Lampert. 2001. Temperature reaction
norms of Daphnia magna: the effect of food concentration.
Freshwater Biology 46:281­289.
Gillooly, J. F., J. H. Brown, G. B. West, V. M. Savage, and
E. L. Charnov. 2001. Effects of size and temperature on
metabolic rate. Science 293:2248­2251.
Kleiber, M. 1932. Body size and metabolism. Hilgardia 6:
315­332.
Marquet, P. A. 2002. Of predators, prey, and power laws.
Science 295:2229­2230.
Marquet, P. A., S. A. Navarrete, and J. C. Castilla. 1990.
Scaling population density to body size in rocky intertidal
communities. Science 250:1125­1127.
Maurer, B. A. 1990. Dipodomys populations as energy processing
systems: regulation, competition, and hierarchical
organization. Ecological Modelling 50:157­176.
Pauling, L. 1970. General chemistry. Dover, New York, New
York, USA.
Real, L. A. 1978. The kinetics of functional response. American
Naturalist 111:289­300.
Schrodinger, E. 1941. Statistical thermodynamics. Dover,
New York, New York, USA.
West, G. B., J. H. Brown, and B. J. Enquist. 1997. A general
model for the origin of allometric scaling laws in biology.
Science 276:122­126.
West, G. B., J. H. Brown, and B. J. Enquist. 1999. The fourth
dimension of life: fractal geometry and the allometric scaling
of organisms. Science 284:1677­1679.
Wright, D. H. 1983. Species­energy theory and extension of
species­area theory. Oikos 41:496­506.
July 2004 1797METABOLIC THEORY OF ECOLOGY
Forum
Ecology, 85(7), 2004, pp. 1797­1799
2004 by the Ecological Society of America
DOES METABOLIC THEORY APPLY TO COMMUNITY ECOLOGY?
IT'S A MATTER OF SCALE
DAVID TILMAN,1
JANNEKE HILLERISLAMBERS, STAN HARPOLE, RAY DYBZINSKI, JOE FARGIONE,
CHRIS CLARK, AND CLARENCE LEHMAN
Department of Ecology, Evolution and Behavior, 1987 Upper Buford Circle, University of Minnesota, St. Paul,
Minnesota 55108 USA
When the seven of us read and discussed Brown et
al. (2004), there were moments of insight, of enthusiastic
consensus, and of strongly divergent opinion.
We agreed that the empirical relations and scaling theory
of Brown et al. (2004) hold great appeal because
of their power to abstract and simplify some of the
complexity of nature. The earth harbors several million
species, each having unique aspects to its morphology,
physiology, and life history. A fundamental goal of
science is to simplify and explain such complexity.
Brown et al. (2004) do just this. They have documented
robust patterns relating the body size and temperature
of species to their basal metabolic rate; plotted on loglog
scales, these empirical functions are well fit by
straight lines. Moreover, they have used these scaling
relations to make numerous predictions about other patterns
and processes, thus greatly extending an approach
that already had been shown to have considerable power
(e.g., Huxley 1932, McMahon and Bonner 1983,
Peters 1983, May 1986).
One question that generated considerable debate
among us was whether metabolic scaling theory represents
a fundamental mechanism that has shaped life
on earth, or whether it is a description of correlated
patterns of as yet poorly known causes. Brown et al.
(2004) hypothesize that scaling relations have a fundamental
basis that comes from the universality of metabolic
activation energy and of the fractal branching
networks that determine resource distribution within
individual organisms. This elegant hypothesis intrigued
us. It brought to the forefront questions raised when
we spent a semester last year reading many of the papers
upon which Brown et al. (2004) is based. Are
slopes really multiples of , or is this just the best
small-whole-number ratio approximation? How might
mechanical constraints, which may scale differently
with body size (e.g., McMahon and Bonner 1983), contribute
to these patterns? Larger organisms must, after
all, have a higher proportion of their mass in woody
stems or bones or other support tissues that have low
metabolic costs but high costs for their construction.
Manuscript received 3 November 2003. Corresponding
Editor: A. A. Agrawal. For reprints of this Forum (including
the MacArthur Award paper), see footnote 1, p. 1790.
1 E-mail: tilman@umn.edu
Might growth rate (McMahon and Bonner 1983) be the
controlling variable, rather than metabolic rate? Or
might body size and metabolism be easily measured
surrogates of the actual traits that determine species
interactions and abundances? After all, within the
framework of community ecology, it is traits such as
competitive ability, dispersal, and predator defenses,
and not metabolism and body size, that directly determine
which species win or lose, which persist and speciate,
or which go extinct.
Of the various predictions that Brown et al. (2004)
derived, perhaps the most surprising to community
ecologists may be that within a trophic level, species
of vastly different body sizes should get equal shares
of their limiting resources. Simply put, all of the herbivorous
arthropods within a 10-fold range of body
sizes should consume roughly the same amount of food
as all of the herbivorous mammals within a 10-fold
range of body sizes. This suggests that, on average,
species should be getting approximately equal-sized
``slices'' of the limiting resources for which they compete.
Does this mean that there are limits to similarity
that lead to relatively even packing of competing species
along gradients? If so, what mechanisms could
cause this, and how would community ecologists test
this prediction in the field?
Another prediction made by Brown et al. (2004) is
that higher temperatures in the tropics may lead to faster
metabolism, shorter generation times, and thus faster
rates of speciation, accounting for the latitudinal biodiversity
gradient. This is an interesting alternative to
other hypotheses for latitudinal diversity gradients,
such as the hypothesis that diversity is lower toward
the poles because of higher rates of extinction from a
less stable climate and glaciation, or that there are fewer
ways to survive and grow in progressively colder
habitats because life is a water-based (not an ice-based)
process. The metabolic approach may also offer insight
into r vs. K selection. Brown et al. (2004) suggest that
species selected for fast population growth rates would
necessarily have higher metabolism, smaller body size,
and higher temperature. K-selected species are not necessarily
selected for slow population growth rates, but
this may be a consequence of selection for predation
resistance or resource use efficiency, which often are
Forum
1798 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
FIG. 1. (A) Predictive power of body size. We used the data in Brown et al. (2004) and simulations to explore the
relationship between the range of organism sizes studied and the explanatory power of size. First, we calculated the unexplained
variance around the regression lines in Figs. 2, 3, 5, and 6 of Brown et al. (2004) using the slope, number of sample points,
and R2
of relationships between size and organismal biomass growth rate, fish mortality, population growth rate, and population
density. Next we calculated R2
for simulated data sets of species covering narrower ranges in body size. To do this, we
randomly sampled 100 ``species'' from a uniform distribution of body sizes between a specified size range. We next generated
response variables for each species (i.e., predicted biomass growth rate, fish mortality, population growth rate, and population
density) using observed slopes and intercepts and estimated variance. Finally, we used simple linear regressions to calculate
the R2
between organism size and the process of interest. We repeated this 200 times for each of 200 equally distributed size
ranges (from 0 to the size range used in Brown et al. [2004]). Lines connect the mean R2
values for each size range. (B)
Size range of studied organisms, based on papers in the journal Ecology. We examined all recent papers in Ecology that
referenced specific organisms or types of organisms (190 papers from issues 1­9, volume 84, 2003). We tabulated the
organisms described in each paper, assigned them to size classes, and then determined the orders of magnitude size range
(difference between the log10 estimated mass in grams of the largest and smallest organisms). The horizontal axis is organism
size range; the vertical axis is the number of papers that studied species in that range.
enhanced by larger body size. These examples again
suggest that the robustness of scaling relations may
come not from their direct mechanistic relevance, but
from the ability of a single variable, body size, to abstract
a suite of correlated traits when making comparisons
across broad scales. Whatever the underlying
mechanisms might be, the predictions in Brown et al.
(2004) demonstrate that scaling relations can be a powerful
way to reduce dimensionality and to abstract some
of the complexity of nature.
We had considerable debate, though, about the
breadth of applicability of metabolic scaling theory. It
is clear that scaling relationships hold best when examining
patterns across a wide spectrum of body sizes
(such as from microbes to megafauna) within an ecosystem,
continent, or the globe (Fig. 1A). Because detailed,
mechanistic treatments of the interactions
among all species in an ecosystem are impossible, abstraction
is essential. Metabolic theory may, for instance,
allow better parameterization and understanding
of ecosystem nutrient and energy fluxes caused by
the large size range of species, such as from bacteria
to sequoias, in ecosystems.
It is less clear, however, if metabolic scaling will
prove useful in addressing many of the central questions
of population and community ecology, such as
population regulation and controls of coexistence, of
species relative abundance patterns, and of diversity
(e.g., Tilman 1999, Hubbell 2001, Sterner and Elser
2002, Chase and Leibold 2003). Much of community
ecology pursues these questions by exploring the mechanisms
of local interactions among often similar-sized
species. An analysis of the relations reported by Brown
et al. (2004) shows that the strength of the correlation
between various ecological processes and body size
diminishes as the range in body sizes decreases (Fig.
1A). The variation in species traits that seems so small
when comparing bacteria to elephants looms large
when comparing beech trees to oaks, or a prairie grass
with a prairie forb.
The data presented in Brown et al. (2004) show that
organisms of similar body size can have 20-fold differences
in their traits. Moreover, these data show that
body size explains only 2­20% of the observed variance
in predicted responses when species fall within a
10-fold range in body sizes (Fig. 1A). Scaling relations
thus have increasingly limited predictive ability in
comparisons of organisms of more similar size. Such
comparisons, however, are a central part of ecology;
roughly half of a sample of papers recently published
in Ecology focused on only one species or on several
July 2004 1799METABOLIC THEORY OF ECOLOGY
Forum
species that were within an order of magnitude in body
mass (Fig. 1B).
Much of our recent work has focused on how the
identity and number of grassland plant species interacting
in a local neighborhood influences processes
such as primary productivity. The species that we study
are herbaceous perennials that differ by less than  of
an order of magnitude in adult body size. In our biodiversity
experiment (Tilman et al. 2001), the number
of plant species explained 37% of the variance in total
biomass in 2002 (linear regression: N 168, P
0.0001). Species number and functional group composition
explained 68% of this variance in total biomass
(multiple regression: F28, 139 10.4, P 0.0001).
The scaling approach, which works so well across large
scales of body size, predicts at most 12% of the variance
in various ecological processes for the range of
body sizes in our study (Fig. 1A). Thus, on our scale,
plant functional traits and plant diversity are much
more important than body size. Conversely, our work
on the local neighborhood effects of diversity gives
little, if any, insight into the potential relationship between
diversity and productivity on geographic scales
where species come from different species pools and
where other factors, such as climate, soil, and plant
traits, are correlated and change simultaneously.
An analogy and an insight into the power and limits
of the scaling approach come from a consideration of
another complex system with which we are familiar:
computers and related digital devices. Like an organism,
a silicon circuit has a metabolism, measured by
how much electricity it consumes. The volume of information
that a digital device can process, the airflow
needed to cool it, its reliability and longevity, and other
properties are all a function of its size and, thus, its
metabolism. Such macroscopic properties of digital devices
are essential for whole-system tasks like designing
power supplies and writing warranties. The relationship
of metabolic scaling to ecology is analogous;
it gives significant insights into macroscopic ecological
patterns and predicts other patterns and processes
across large scales and whole systems. Many different
functions, however, can be performed by digital devices
with identical sizes and energy demands, just as
many different ecological roles can be performed by
organisms of similar size and temperature. It is these
ecological roles, not metabolisms per se, that determine
species coexistence and abundances and ecosystem
functioning.
One of the mysteries of scaling theory is why it has
such great explanatory power at large scales, but not
at small scales. The vast diversity of alternative roles
that can be filled by organisms of equal body size probably
accounts for the 20-fold variation observed
around the mean scaling trend. Perhaps when comparisons
are made across larger body size ranges, the constraints
of body size and its correlates increasingly predominate
over the interspecific trade-offs in resource
use, dispersal, and disease resistance that are the more
proximate determinants of species interactions and
abundance. If, as seems likely, scaling relations do have
their basis in metabolic activation energy, fractal
branching, and structural constraints, then these forces
must be acting at a deeper level, such as by defining
body size and metabolic constraints that shaped the
form and functioning of life as single-celled organisms
evolved into multicellular plants and animals.
In summary, Brown et al. (2004) have provided a
new window through which we can ponder nature. The
simplicity and potential generality of the view that they
provide is welcome; ecology as a discipline cannot afford
to wallow in special cases. Metabolic theory provides
a unique and insightful macroscopic perspective,
one that appears to have great utility for comparisons
of organisms of vastly different sizes. The possible
causes of these patterns, the applicability of the approach
to studies of similar-sized organisms, and the
potential synthesis of mechanistic and macro-ecological
approaches are challenges that are likely to be pursued
for years to come.
LITERATURE CITED
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Chase, J. M., and M. A. Leibold. 2003. Ecological niches:
linking classical and contemporary approaches. University
of Chicago Press, Chicago, Illinois, USA.
Hubbell, S. P. 2001. The unified neutral theory of biodiversity
and biogeography. Monographs in Population Biology,
Princeton University Press, Princeton, New Jersey, USA.
Huxley, J. S. 1932. Problems in relative growth. Methuen,
London, UK.
May, R. M. 1986. The search for patterns in the balance of
nature: advances and retreats. Ecology 67:1115­1126.
McMahon, T. A., and J. T. Bonner. 1983. On size and
life.Scientific American/W. H. Freeman, New York, New
York, USA.
Peters, R. H. 1983. The ecological implications of body size.
Cambridge University Press, New York, New York, USA.
Sterner, R. W., and J. J. Elser. 2002. Ecological stoichiometry.
Princeton University Press, Princeton, New Jersey, USA.
Tilman, D. 1999. The ecological consequences of changes
in biodiversity: a search for general principles. Ecology 80:
1455­1474.
Tilman, D., P. B. Reich, J. Knops, D. Wedin, T. Mielke,
and C. Lehman. 2001. Diversity and productivity in a
long-term grassland experiment. Science 294:843­845.
Forum
1800 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
Ecology, 85(7), 2004, pp. 1800­1802
2004 by the Ecological Society of America
USING THE METABOLIC THEORY OF ECOLOGY TO PREDICT GLOBAL
PATTERNS OF ABUNDANCE
MICHAEL KASPARI1
Department of Zoology, University of Oklahoma, Norman, Oklahoma 73019-0235 USA
INTRODUCTION
Studies of abundance (N)--the number of individuals
of a taxon in a given area and time--have traditionally
focused on the dynamics of local species populations
over generations. The conceptual basis of this
approach has been demographic (i.e., dN/dt birth rate
death rate migration rate). Brown and colleagues
(2004) in introducing the Metabolic Theory of Ecology
focus on a different question: how should abundance
in entire communities at equilibrium vary as we move
about in space and time? Their answer, the Metabolic
Theory of Abundance (henceforth MTA), uses a mass
balance approach (Odum 1971, Kaspari et al. 2000). It
has the potential to guide work on this subject for years
to come.
Brown and colleagues ask us to picture abundance
not as the net arrival of mortal, reproductive units with
legs, but as the number of co-occurring energy transformers.
K is the equilibrial abundance of individual
ectotherms limited by the same resources, of similar
size, and that experience the same environment. This
formulation of K may be strange to ecologists from the
demographic school. But the body size, trophic habits,
and abundance of higher taxa and functional groups
have shown themselves worthy of study (e.g., Siemann
et al. 1996).
In the MTA, K varies with resource availability, access
to those resources, and the way the resources are
divided up among individuals:
3/4 E/kT
K [R]M e . (1)
[R] is the resource supply rate. Brown and colleagues
focus on energy, which places us on the familiar
grounds of metrics like Net Primary Productivity (in
grams of carbon per square meter per year). The MTA
predicts that K should increase linearly with [R], ceteris
paribus, although no data are presented to support this
prediction. The ability of living cells to do metabolic
work, and hence to access available [R], is a negative
decelerating function of environmental temperature T
(in Kelvin), E is the activation energy ( 0.63 eV; 1
eV 96.49 kJ/mol), and k is Boltzmann's factor. This
Manuscript received 14 October 2003. Corresponding Editor:
A. A. Agrawal. For reprints of this Forum (including
the MacArthur Award paper), see footnote 1, p. 1790.
1 E-mail: mkaspari@ou.edu
prediction holds for trees, and more messily, for a collection
of animal ectotherms (Allen et al. 2002). So far
we have described the amount of energy captured by
our taxon or trophic group. To find K, this energy must
be divided up based on the individual's capacity to use
it. Whole-organism metabolism rate scales to M 3/4
, so
K should be a negative decelerating function of M (Damuth
1981, Enquist et al. 1998). In sum, the MTA
focuses on how available energy is harvested and respired.
It is thus explicitly bottom-up (Power 1992);
mortality from predation is assumed to be negligible
or at least invariant with M, T, and [R].
The MTA is a clear offspring of macroecology
(Brown 1995), meant to be tested at broad spatial and
taxonomic scales spanning a broad range of M, T, and
[R]. It does what good theory should do. It builds from
first principles, addresses the shape of long-standing
patterns (Blackburn and Gaston 1997), predicts other
non-intuitive patterns (Damuth 1981), and would even
change the way we plot our data (e.g., by a priori correcting
for mass and temperature). Finally, it pulls together
[R], T, and M, three factors that have often been
treated in isolation. So what challenges and opportunities
do we face as we gear up to test the MTA?
TESTING THE MTA--QUANTIFYING ABUNDANCE
The MTA focuses on how energy is captured and
partitioned by individuals. Because available energy
[R] attenuates each time carbon-rich molecules are harvested,
excreted, and respired, Brown and colleagues
(2004) are careful to specify that abundance ideally
refers to all members of the same trophic group (an
alternative focus on taxon abundance would come with
the assumption that the proportion of [R] harvested by
that taxon is invariant across sites). It is thus not surprising
that much of the early work in MTE (Enquist
et al. 1998, Enquist and Niklas 2001) has mined global
plant data sets. Plants occupy an unambiguous trophic
group. Plants are also easy to count. But where are the
data sets for consumer abundance across global gradients
of [R] and T?
Global abundance data sets should be a basic goal
of ecology. Such data are scarce, however, because mobile
organisms are hard to count and relative abundance
estimators are hard to standardize across habitats
(Southwood 1978). Luckily, terrestrial brown food
webs (detritus, microbes, microbivores, and their pred-
July 2004 1801METABOLIC THEORY OF ECOLOGY
Forum
FIG. 1. Studies of 49 ant communities arrayed along the
productivity gradient ([R] is the resource supply rate) show
that trophic groups accumulate at different rates with net
aboveground productivity (Kaspari 2001). Note the log­log
scale.
ators) address many of these limitations (Copley 2000):
they occur everywhere from the poles to the tropics;
they can be quantified in 1-m2 plots (Coleman and Crossley
1996); and the taxa (the microbivores in a patch
of litter may include ciliates, rhizopods, nematodes,
collembola, oribatids, millipedes, and ants) span a
range of M (Moore et al. 1988). I am confident that the
MTA will foster the collection of new abundance data
in the same way that quantitative biodiversity theory
(Rosenzweig 1995, Hubbell 2001, Allen et al. 2002) is
promoting studies of species richness.
Ecological stoichiometry constitutes a second challenge
to the MTA. Individuals regularly confront elemental
deficits beyond carbon (Mertz 1987). For example,
primary consumers from the green and brown
food webs (herbivores and decomposer microbes, respectively)
appear especially likely to face stoichiometric
imbalances (Kaspari and Yanoviak 2001, Sterner
and Elser 2002, Davidson et al. 2003). How can an
energy-based theory deal with environmental deficits
in elements like N, P, and Mb?
One solution is to quantify the energy costs of those
activities required to meet elemental deficits. The herbivores
that travel to find limiting sodium-rich plants
(Belovsky 1978) or that compensate for defensive compounds
in their food (Berenbaum and Zangerl 1994)
are both doing so by catabolizing sugars. If so, the slope
of the [R]­K curve should be an inverse function of
the group's stoichiometric deficit. For example, soil ant
abundance increases as NPP3/4
(net primary production,
as yet uncorrected for M; personal observation) across
the New World (Kaspari et al. 2000). Different ant
trophic groups, however, accumulate differently (Fig.
1; see Kaspari 2001). Herbivore abundance increases
slowly with NPP, predators and fungivores more quickly.
Omnivores have an intermediate slope. A working
hypothesis is that ant herbivores have low [R]­K slopes
because they must work harder than predators to meet
their stoichiometric deficits.
TWO VARIATIONS ON A THEME OF METABOLISM
AND ABUNDANCE
The MTA characterizes environments by their mean
[R] and T. Both, however, become more seasonal moving
from the equator toward the poles. The MTA may
thus ignore a key reality of ectotherm life: metabolic
costs and productivity vary seasonally. For example,
in all but the most productive biomes (i.e., wet tropical
rain forests), the same NPP can be squeezed into a few
months or spread out over the year (contrast tundra
with mediterranean shrubland). In a seasonally cold
biome where NPP is concentrated in the summer
months, ectotherms can eat when food is plentiful and
respire less of that energy away when winter comes.
In contrast, an ever-warm environment extracts yearlong
respiration costs. Somewhat counterintuitively
then, environments with winters can provide a metabolic
refuge and enhance K compared to aseasonal environments
with the same mean [R] and T (Kaspari et
al. 2000). Seasonality matters. This may be another
reason for the observation of Allen et al. (2002) that
N's for ectotherms, but not endotherms, decline toward
the warm tropics.
Finally, holding [R] and T constant, K is predicted
to decrease as M 3/4. But why should M vary from place
to place? Intriguingly, two of the leading models for
body size gradients have [R] and T as their independent
variables. Where predation risk is high, the optimal
body size should decrease with NPP (Kozlowski 1992).
Ectotherm size at maturity has long been shown to
decrease with T (Atkinson 1995). If community body
size gradients are real, this suggests that where M is a
function of T and [R], the MTA may be overparame-
terized!
PROSPECTS
The MTA challenges community ecologists to look
beyond our traditional focus on species toward the
properties of higher taxa and functional groups. It challenges
us to pursue fundamental natural history--size,
abundance, trophic relationships--for all taxa at a global
scale. As ecologists, we obviously have some distance
to go before we understand even the basic patterns
of abundance. The MTA provides one interesting
and quantitative road map for the journey ahead.
ACKNOWLEDGMENTS
This material is based upon work supported by the National
Science Foundation under Grant No. 0212386.
LITERATURE CITED
Allen, A. P., J. H. Brown, and J. F. Gillooly. 2002. Global
biodiversity, biochemical kinetics, and the energetic-equivalence
rule. Science 297:1545­1548.
Atkinson, D. 1995. Temperature and organism size--a biological
law for ectotherms? Advances in Ecological Research
25:1­58.
Belovsky, G. 1978. Diet optimization in a generalist herbivore:
the moose. Theoretical Population Biology 14:103­
134.
Forum
1802 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
Berenbaum, M. R., and A. R. Zangerl. 1994. Costs of inducible
defense: protein limitation, growth, and detoxification
in parsnip webworms. Ecology 75:2311­2317.
Blackburn, T. M., and K. J. Gaston. 1997. A critical assessment
of the form of the interspecific relationship between
abundance and body size in animals. Journal of Animal
Ecology 66:233­249.
Brown, J. H. 1995. Macroecology. University of Chicago,
Chicago, Illinois, USA.
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Coleman, D. C., and D. A. Crossley. 1996. Fundamentals of
soil ecology. Academic Press, New York, New York, USA.
Copley, J. 2000. Ecology goes underground. Nature 406:
452­454.
Damuth, J. 1981. Interspecific allometry of population density
in mammals and other animals: the independence of
body mass and population energy use. Biological Journal
of the Linnaean Society 31:193­246.
Davidson, D. W., S. C. Cook, R. R. Snelling, and T. H. Chua.
2003. Explaining the abundance of ants in lowland tropical
rainforest canopies. Science 300:969­972.
Enquist, B. J., J. H. Brown, and G. B. West. 1998. Allometric
scaling of plant energetics and population density. Nature
395:163­165.
Enquist, B. J., and K. J. Niklas. 2001. Invariant scaling relations
across tree-dominated communities. Nature 410:
655­660.
Hubbell, S. 2001. The unified neutral theory of biodiversity
and biogeography. Princeton University Press, Princeton,
New Jersey, USA.
Kaspari, M. 2001. Taxonomic level, trophic biology, and the
regulation of local abundance. Global Ecology and Biogeography
10:229­244.
Kaspari, M., L. Alonso, and S. O'Donnell. 2000. Three energy
variables predict ant abundance at a geographic scale.
Proceedings of the Royal Society London B 267:485­490.
Kaspari, M., and S. Yanoviak. 2001. Bait use in tropical litter
and canopy ants--evidence for differences in nutrient limitation.
Biotropica 33:207­211.
Kozlowski, J. 1992. Optimal allocation of resources to
growth and reproduction: implications for age and size at
maturity. Trends in Ecology and Evolution 7:15­19.
Mertz. 1987. Trace elements in human and animal nutrition.
Academic Press, San Diego, California, USA.
Moore, J. C., D. E. Walter, and H. W. Hunt. 1988. Arthropod
regulation of micro- and mesobiota in below-ground detrital
food webs. Annual Review of Entomology 33:419­
439.
Odum, E. P. 1971. Fundamentals of ecology. Third edition.
Saunders, Philadelphia, Pennsylvania, USA.
Power, M. E. 1992. Top-down and bottom-up forces in food
webs: do plants have primacy? Ecology 73:733­746.
Rosenzweig, M. L. 1995. Species diversity in space and time.
Cambridge University Press, Cambridge, UK.
Siemann, E., D. Tilman, and J. Haarstad. 1996. Insect species
diversity, abundance and body size relationships. Nature
380:704­706.
Southwood, T. R. E. 1978. Ecological methods. Second edition.
Chapman and Hall, London, UK.
Sterner, R. W., and J. J. Elser. 2002. Ecological stoichiometry:
the biology of elements from molecules to the biosphere.
Princeton University Press, Princeton, New Jersey,
USA.
Ecology, 85(7), 2004, pp. 1802­1804
2004 by the Ecological Society of America
AN ILLUSION OF MECHANISTIC UNDERSTANDING
HE´ LE` NE CYR1 and STEVE C. WALKER
Department of Zoology, University of Toronto, Toronto, Ontario, Canada M5S 3G5
INTRODUCTION
James Brown and his colleagues (2004) are at the
forefront of a recent resurgence of interest in explaining
the ubiquitous relationships between the body size of
organisms and everything that they do (West et al.
1997, 1999). Here, Brown et al. argue that their general
allometric model for metabolism, expanded to include
temperature effects and stoichiometric constraints, offers
a mechanistic framework to unify ecological thinking.
Body size, temperature, and stoichiometry have
long been recognized to drive many aspects of biology
and ecology; thus, in general terms, the approach is
familiar and reasonable. The claim that a metabolic
theory could link ecology as a whole is interesting and
Manuscript received 20 October 2003. Corresponding Editor:
A. A. Agrawal. For reprints of this Forum including the
MacArthur Award paper, see footnote 1, p. 1790.
1 E-mail: helene@zoo.utoronto.ca
challenging, but surprisingly poorly justified by Brown
et al. (2004). We discuss two main problems with their
argument.
DO WE KNOW THE MECHANISM BEHIND
ALLOMETRIC RELATIONSHIPS? DO WE NEED TO?
The claim of a mechanistic basis to the metabolic
theory of ecology is premature. There is currently no
agreement on the mechanism(s) that generates allometric
relationships. The network model proposed by
West et al. (1997, 1999) focuses on the metabolism of
individuals and assumes optimal distribution of energy
through a fractal network, but this approach has been
strongly criticized (Dodds et al. 2001). Several other
models, based on very different processes and assumptions,
also have been proposed (life history optimization,
Kozlowski and Weiner [1997]; internal metabolite
transportation, Dreyer and Puzio [2001], Ban-
July 2004 1803METABOLIC THEORY OF ECOLOGY
Forum
avar et al. [2002]; resource partitioning, Kooijman
[2000]; chemiosmosis and life history evolution, Demetrius
[2003]; the multiplicity of biochemical pathways,
Hochachka et al. [2003]), but have not yet been
compared critically. We should not be lured by the
illusion of mechanistic understanding.
Moreover, no single allometric exponent is generally
accepted. We disagree with the dogmatic use of a 
exponent by J. Brown and colleagues, to the point of
correcting body mass in their analyses by this exponent.
A unique  exponent for allometric relationships of
metabolic rates is currently undefensible, both on theoretical
and on empirical grounds. In contrast to West
et al. (1999), most of the recent alternative models of
metabolic rate allometry suggest a range of possible
exponents. Allometric exponents are expected to vary
with the mass dependence of survivorship (Kozlowski
and Weiner 1997), thermal regulation (  for endotherms,
1 for ectotherms; Kooijman [2000]), balance
between metabolic supply and demand (although  is
an optimal value; Banavar et al. [2002]), level of activity
(basal vs. maximum metabolic rate; Hochachka
et al. [2003]), and variability in population size ( for
species with rapidly fluctuating population sizes,  for
species with stable population sizes; Demetrius
[2003]). Deviations from a  exponent also have been
found empirically. Recent analyses of very large data
sets for birds and mammals support a  exponent
(Dodds et al. 2001, White and Seymour 2003). Similarly,
the exponents for population density­body size
relationships vary among communities, and the overall
relationship has an exponent significantly steeper than
 (Cyr et al. 1997a, b). The energy equivalence rule
and the suggestion that trophic transfers explain the
steep slopes measured in pelagic systems were specifically
tested with an extensive data set, and discounted
by Cyr (2000). Despite more than a century of work
on this topic, the jury is still out on the magnitude of
the allometric exponents.
This lack of mechanistic understanding does not deter
from the potential importance of a metabolic theory
of ecology. The existence and the strength of allometric
and of temperature relationships are well established.
The question raised by Brown et al. is really whether
these powerful relationships account for ecological interactions
at all other scales of interest, from population
to community to ecosystem ecology.
HOW DO WE CROSS SCALES WITH A METABOLIC
THEORY OF ECOLOGY?
A second, more serious problem arises in extending
this metabolic framework to scales of increasing complexity.
The approach proposed by Brown et al. (2004)
is largely justified by the existence of macroecological
patterns. These general relationships are very useful in
providing a broad context to interpret data, but are not
meant to provide precise predictions under specific
conditions. Unless these models are greatly refined (and
this is not a trivial matter of adjusting coefficients),
they will be of little use to population and community
ecologists. Few population ecologists would be satisfied
with values of rmax or K (sensu Brown et al. (2004),
i.e., mean population density) that span several orders
of magnitude. This is not to say that a metabolic approach
cannot work.
A metabolic framework, if modeled at the right scale,
can be powerful. More refined physiological models
do exist, and have been applied successfully in population
ecology (Kooijman 2000, Nisbet et al. 2000).
These models assume that organisms have clear constraints
on how they can partition resources. The energy
and material available to them (i.e., assimilated from
their food) are divided among metabolism (for maintenance
of tissues and basic functions), somatic production,
and reproduction, and the input of energy and
material must match any change in biomass plus outputs.
The dynamic energy and material budget models
proposed by Kooijman (2000) and Nisbet and colleagues
(2000) account for the effects of body size,
temperature, and stoichiometry, and can be used to
predict various aspects of population dynamics. These
models offer a powerful framework to test theoretical
issues in population ecology, but are much more complex
than the models proposed by Brown et al. (2004)
and require careful parameterization for individual species.
There are no shortcuts, yet.
The extension of these physiological models to more
natural conditions and to communities is less obvious.
Careful tests of the dynamic budget models have shown
that even simple aspects of more natural systems (e.g.,
low food availability, low food quality) can alter the
dynamics of a population in very significant ways (e.g.,
Nelson et al. 2001). It is well recognized that population
dynamics are context dependent, and will change
depending on interactions with other species (competitors,
predators) and with the environment (e.g., Chase
et al. 2002). The dynamics of natural populations are
unlikely to simply follow from constraints on the energy
budget of individual organisms, but must take into
account a suite of external factors. Increasing the complexity
of models beyond a few variables is generally
counterproductive, so a simple extension of these physiological
models to natural populations or to communities
may not be possible. A different modeling framework
may be required.
Community ecology is replete with general patterns
(e.g., species­abundance curves, species­area curves,
diversity­productivity relationships, density­body size
relationships, community size spectra, food web structure,
predator­prey size ratios). The mechanisms generating
these relationships are still uncertain, but there
is no doubt that the availability of energy and material
affects the biomass, productivity, and diversity of organisms
in communities. However, measuring how
much resource is really available to organisms is a
difficult task, and there is no reason to believe that
Forum
1804 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
species of all sizes have equal access to resources (as
suggested by the energy equivalence rule). Even apparently
simple questions have baffled ecologists for
decades. For example, how is energy divided among
species in a community and how efficiently is it transferred
through food webs? Models of energy and material
transfer need to be tested on communities of organisms
that actually live in the same environment.
Global allometric relationships built from data collected
in many different communities, such as those
used by Brown et al., include too many other sources
of variability (Cyr 2000) and are useless for this task.
A metabolic framework that would integrate community
ecology is promising, but remains to be tested in
a convincing manner.
The approach proposed by Brown et al. (2004) is
most easily justified for ecosystem ecology, and has
indeed been applied successfully in this context. There
are two reasons for this. First, the currencies of interest
(energy, nutrients, and other chemical elements) are the
same. Second, the error associated with predictions
from general allometric models is not unrealistically
large compared to errors associated with many ecosystem
variables. Ecosystem ecologists commonly
have to use low-precision measurements and estimates
when dealing with large spatial and temporal scales.
When more precise predictions are necessary, the use
of more detailed models (e.g., Kooijman 2000) is possible.
There are many good examples of the effectiveness
of an allometric/metabolic approach in ecosystem
ecology (e.g., Vanni 2002).
Ecologists have long recognized the strength of allometric
relationships and the ubiquitous role that temperature
plays in biology. By proposing a metabolic
theory of ecology, Brown et al. challenge us to explore
the implications of these well-known relationships at
all scales. This approach has already shown promising
results in theoretical population ecology and in ecosystem
ecology, but the case remains to be made convincingly
for populations under more natural settings
and for communities. The mechanisms proposed by
Brown et al. (2004) are interesting. However, the conceptual
unification of ecology is more likely to depend
on our ability to relate variables and processes across
scales of increasing complexity than on a mechanistic
interpretation of patterns.
LITERATURE CITED
Banavar, J. R., J. Damuth, A. Maritan, and A. Rinaldo. 2002.
Supply­demand balance and metabolic scaling. Proceedings
of the National Academy of Sciences (USA) 99:
10506­10509.
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Chase, J. M., P. A. Abrams, J. P. Grover, S. Diehl, P. Chesson,
R. D. Holt, S. A. Richards, R. M. Nisbet, and T. J. Case.
2002. The interaction between predation and competition:
a review and synthesis. Ecology Letters 5:302­315.
Cyr, H. 2000. The allometry of population density and interannual
variability. Pages 267­295 in J. H. Brown and G.
B. West, editors. Scaling in biology. Oxford University
Press, Oxford, UK.
Cyr, H., J. A. Downing, and R. H. Peters. 1997a. Densitybody
size relationships in local aquatic communities. Oikos
79:333­346.
Cyr, H., R. H. Peters, and J. A. Downing. 1997b. Population
density and community size structure: comparison of aquatic
and terrestrial systems. Oikos 80:139­149.
Demetrius, L. 2003. Quantum statistics and allometric scaling
of organisms. Physica A 322:477­490.
Dodds, P. S., D. H. Rothman, and J. S. Weitz. 2001. Reexamination
of the ``-law'' of metabolism. Journal of Theoretical
Biology 209:9­27.
Dreyer, O., and R. Puzio. 2001. Allometric scaling in animals
and plants. Journal of Mathematical Biology 43:144­156.
Hochachka, P. W., C. A. Darveau, R. D. Andrews, and R. K.
Suarez. 2003. Allometric cascade: a model for resolving
body mass effects on metabolism. Comparative Biochemistry
and Physiology, Part A 134:675­691.
Kooijman, S. A. L. M. 2000. Dynamic energy and mass budgets
in biological systems. Cambridge University Press,
Cambridge, UK.
Kozlowski, J., and J. Weiner. 1997. Interspecific allometries
are by-products of body size optimization. American Naturalist
149:352­380.
Nelson, W. A., E. McCauley, and F. J. Wrona. 2001. Multiple
dynamics in a single predator­prey system: experimental
effects of food quality. Proceedings of the Royal Society
of London B 268:1223­1230.
Nisbet, R. M., E. B. Muller, K. Lika, and S. A. L. M. Kooijman.
2000. From molecules to ecosystems through dynamic
energy budget models. Journal of Animal Ecology
69:913­926.
Vanni, M. J. 2002. Nutrient cycling by animals in freshwater
ecosystems. Annual Review of Ecology and Systematics
33:341­370.
West, G. B., J. H. Brown, and B. J. Enquist. 1997. A general
model for the origin of allometric scaling laws in biology.
Science 276:122­126.
West, G. B., J. H. Brown, and B. J. Enquist. 1999. The fourth
dimension of life: fractal geometry and allometric scaling
of organisms. Science 284:1677­1679.
White, C. R., and R. S. Seymour. 2003. Mammalian basal
metabolic rate is proportional to body mass2/3. Proceedings
of the National Academy of Sciences (USA) 100:4046­
4049.
July 2004 1805METABOLIC THEORY OF ECOLOGY
Forum
Ecology, 85(7), 2004, pp. 1805­1807
2004 by the Ecological Society of America
METABOLIC RATE OPENS A GRAND VISTA ON ECOLOGY
KATHRYN L. COTTINGHAM1
AND M. SCOT ZENS
Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755 USA
INTRODUCTION
Wouldn't it be nice if ecologists could use a few
simple parameters, such as the size of an organism and
the temperature at which it operates, to predict individual
mortality, population growth rate, species diversity,
or ecosystem production? Boldly going where
few ecologists tread, Jim Brown seeks a grand synthesis
in ecology that transcends specific organisms and environments.
For much of the past decade, he and his
colleagues have worked to develop unifying ecological
principles from basic physical and chemical constraints
on organisms.
In this new paper, Brown et al. (2004) open a new
vista on ecology by (1) nominating metabolic rate as
the essential integrator of organismal biology, (2) providing
a bold new synthesis of the effects of mass and
temperature on metabolic rate, and (3) proposing a
number of hypotheses about the influences of mass and
temperature on aggregate ecological phenomena ranging
from whole organisms to community structure to
ecosystem processes. In this commentary, we address
each of these contributions, emphasizing the second.
METABOLIC RATE AS THE INTEGRATOR AND
ORGANIZER OF DISPARATE THEORY
Brown et al. (2004) begin by defining metabolism
as the biological processing of energy and materials.
Although it is difficult to measure field metabolic rates,
much evidence suggests that basal metabolic rate is
governed by resource uptake, chemical transformation,
and the distribution of transformed resources throughout
the body. Metabolic rate is therefore both a simple
and valuable integrating concept and a key linkage between
physical and chemical processes and the individual,
community, and ecosystem. If we can measure
it, metabolic rate gives us a holistic measure of individual
performance unconfounded by issues of allocation
to growth and reproduction.
A particularly novel component of this paper by
Brown and colleagues is their deliberate challenge to
the long-standing tradition of considering energy and
materials as separate currencies for examining ecological
questions (e.g., Reiners 1986). Instead, Brown et
al. argue that energy and materials ``are inextricably
Manuscript received 16 October 2003. Corresponding Editor:
A. A. Agrawal. For reprints of this Forum including the
MacArthur Award paper, see footnote 1, p. 1790.
1 E-mail: cottingham@dartmouth.edu
linked by the chemical equations of metabolism'' (p.
1774). This alternative viewpoint will definitely provoke
spirited discussions among ecosystem ecologists
and may spark a careful reconsideration of the heretofore
independent research on energy and materials.
THE COMBINED EFFECTS OF MASS AND
TEMPERATURE ON METABOLISM
After making their argument for the primacy of metabolic
rate, Brown et al. (2004) provide an equation
for metabolic rate as a function of body size (as indexed
by mass; West et al. [1997], Enquist et al. [1998]) and
temperature (as summarized by the Bolzmann factor;
Gillooly et al. [2001]). Their equation predicts individual
metabolic rate (MR) from the average mass (M,
in grams) and the average operating temperature (T, in
Kelvin):
3/4 E/(kT)MR aM e (1)
where a is a scaling constant, E is the activation energy,
and k is Boltzmann's constant.
We believe that Eq. 1 has the potential to revolutionize
the field of ecology. However, we consider it
to be a working hypothesis for two reasons. First, the
equation needs to be more explicitly rooted in quantitative
derivations from axiomatic properties of physical
and chemical systems. Second, the fundamental
hypotheses generated by this theory must face stronger
and more appropriate empirical tests. We will detail
each of these concerns.
Concerns about the derivation
Eq. 1 is the cornerstone of Brown et al. (2004), but
a full derivation of the form of the equation has not
yet been provided. The partial derivation provided by
Gillooly et al. (2001) suggests that the equation rests
on the following logical steps.
1) Whole-organism metabolic rate (MR) is defined
as the sum of the rates of energy produced by individual
biochemical reactions Ri:
MR R . (2)i
i
We believe that this link between MR and its mechanistic
underpinnings requires explicit support from the
biochemical literature, especially because the behavior
of a chain of reactions is usually better described by
the behavior of the limiting reaction than by the sum
of the reactions in the chain (e.g., Voet and Voet 1995).
Forum
1806 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
2) Each individual reaction depends on the product
of three components: the concentration of reactants (ci),
the fluxes of reactants (fi), and the kinetic energy of
the system (ki):
R c f k .i i i i (3)
This unsupported assertion is logically necessary to
allow the simple form of Eq. 1, but can kinetic energy
really be isolated from the fluxes of reactants in a chain
of reactions? We would appreciate references to confirm
this claim.
3) To justify the independence of mass and temperature
in Eq. 1, Gillooly et al. (2001:2249) state that
the concentrations and fluxes ``contain the majority of
the body mass dependence,'' (an apparent empirical
result, not shown in the paper), such that their product
scales with body mass as M 3/4 for each reaction:
3/4R (M )k .i i (4)
This substitution rests on the work of West et al. (West
et al. 1997, Enquist et al. 1998), who predicted that
whole-organism metabolism is constrained by the effective
surface areas across which resources are exchanged
with the environment. We would like to see
the substitution of M 3/4 for (cifi) for each reaction explained
more carefully, because different reactions do
have different mass dependencies (e.g., Hochachka et
al. 2003) and the assumption of equal mass dependencies
is what makes it possible to separate the mass and
temperature effects on metabolic rate (see [5]).
4) Assuming that ki ``contains the dominant temperature
dependence'' (Gillooly et al. 2001:2249; an apparent
empirical result not shown) and is therefore proportional
to the Boltzmann factor for each reaction, we
obtain:
3/4 E /(kT)iR (M )(e ).i (5)
5) Finally, by assuming that the activation energies
Ei are identical for all reactions in the summation, Gillooly
et al. (2001) factored out the mass and temperature
terms to obtain:
3/4 E/(kT)
MR R [(M )(e )]i
i i
3/4 E/(kT)
(M )(e ). (6)
That activation energies differ among the component
reactions of metabolism is supported by data provided
in Gillooly et al. (2001) and Brown et al. (2004) indicating
a range of Ei's for different organisms and
properties.
Thus, we believe that the available literature does
not yet provide the links to physical and chemical first
principles to support the independence of mass and
temperature effects on metabolic rate implied by
Eq. 1.
Concerns about the empirical analyses
At some point in its development, new theory needs
to be confronted with real-world measurements (Hilborn
and Mangel 1997). We have some concerns about
the data and statistical methods used by Brown et al.
(2004). First, field metabolic rates (FMR) for whole
organisms are difficult, if not impossible, to measure
in most organisms, so most tests of the metabolic theory
have used laboratory estimates of basal metabolic
rates (BMR). This is justified by Brown et al. (2004)
by the curious biological phenomenon in which the
average FMR is some ``fairly constant multiple, typically
about two to three, of the basal metabolic rate''
(p. 1773). The assumed proportionality of FMR and
BMR permits inference to organisms in the field, but
we see this assumption as an inferential chasm that
only a strong theory of measurements (sensu Ford
2000) could bridge. Second, the analyses of Brown et
al. use a single value of metabolic rate, mass, and operating
temperature for each species, and we are told
little about how the single values per species were derived
(even in species with sexual dimorphism or indeterminate
growth, for which choosing a single value
is not a trivial issue). Is it really appropriate to use a
mean or median to summarize the distribution of values
exhibited by real organisms?
Third, the analyses in Brown et al. do not comply
with current statistical standards for comparative studies,
as they fail to correct for the complications introduced
by errors-in-variables (Model II regression; Sokal
and Rohlf 1995, McArdle 2003) and the lack of
phylogenetic independence within taxa (Harvey and
Pagel 1991). Moreover, lack-of-fit tests (Draper and
Smith 1981) indicate that a line is not the best fit
through the observed data, at least for the analyses
depicted in Fig. 1 of Brown et al. (2004). In short, it
is premature to draw conclusions about the similarity
of mass and temperature effects estimated from data
to the values predicted by metabolic theory, based on
the analyses provided by Brown et al. (2004).
The exciting prospects raised by Eq. 1
Despite our concerns, we strongly believe that the
synthesis by Brown et al. of mass and temperature effects
on metabolism lays the groundwork for a valuable
and unique filter for studying the complexity of natural
systems. For example, Eq. 1 of Brown et al. (2004)
provides a way to disentangle the confounding effects
of mass and temperature and then to look for patterns
in the residuals. Consider an example with the increased
environmental temperatures expected under
climate change. Eq. 1 predicts the effects of increased
operating temperature on the metabolic rate of organisms
of a given mass. Consequent predictions of ontogenetic
growth rate, standing biomass, and biomass
turnover guide us to both what variables to monitor
and their interpretation. Strong deviations from predicted
ontogenetic growth (e.g., Brown et al. 2004: Fig.
3) or biomass turnover (e.g., Brown et al. 2004: Fig.
9) would clearly indicate systems needing further in-
vestigation.
July 2004 1807METABOLIC THEORY OF ECOLOGY
Forum
Alternatively, consider the genetically modified organisms
(GMOs) with modifications to growth rates
(e.g., Atlantic salmon; Hew et al. [1995], Abrahams
and Sutterlin [1999]) and abiotic tolerances (e.g., many
food crops; Sharma et al. [2002]) which are rapidly
being incorporated into our environment. A metabolic
theory of ecology could provide a baseline prediction
for how GMOs with altered growth rate or temperature
responses should be different from their parent populations.
In fast-growing GMO salmon, for instance,
metabolic rate should be elevated and the strengths of
interactions with both competitors and prey should be
predictable.
EXTENSIONS OF THE METABOLIC THEORY BEYOND
INDIVIDUALS
The third major component of the Brown et al.
(2004) paper extends the metabolic theory to population,
community, and ecosystem metrics. Although
space prevents us from making a full comment on this
aspect of the paper, we would like to point out that in
deriving the equations for these metrics, Brown and
colleagues generally assume that the combined dynamics
of multiple organisms are at steady state. For example,
the equation to predict population-level survival
and mortality rates from the average individual mass
and operating temperature relies on a ``population balance''
in which organisms that die are replaced by new
individuals (i.e., the net population growth rate is 0).
This assumption allows Brown et al. to bypass the complexity
of temporal dynamics within particular organisms
or ecosystems, which matches the static, crosssystem
comparisons used in their paper. However, it is
much less likely to apply when the focus is on the
dynamics of specific real-world populations. We believe
that the same physical and chemical principles
will almost certainly constrain individuals whether or
not they are at a population or community equilibrium,
and we urge ecologists to work toward relaxing the
equilibrium assumption in further extensions of the
metabolic theory to higher level ecological processes.
ACKNOWLEDGMENTS
We thank Mark McPeek, Eric Schaller, Roger Sloboda, and
Megan Donahue for their advice on some of the issues raised
in this commentary. Drew Allen, Jamie Gillooly, and Brian
Enquist fielded our esoteric inquiries while Jim Brown was
unreachable in the Australian Outback.
LITERATURE CITED
Abrahams, M. V., and A. Sutterlin. 1999. The foraging and
antipredator behaviour of growth-enhanced transgenic Atlantic
salmon. Animal Behaviour 58:933­942.
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Draper, N. R., and H. Smith. 1981. Applied regression analysis.
Second edition. John Wiley, New York, New York,
USA.
Enquist, B. J., J. H. Brown, and G. B. West. 1998. Allometric
scaling of plant energetics and population density. Nature
395:163­165.
Ford, E. D. 2000. Scientific method for ecological research.
Cambridge University Press, New York, New York, USA.
Gillooly, J. F., J. H. Brown, G. B. West, V. M. Savage, and
E. L. Charnov. 2001. Effects of size and temperature on
metabolic rate. Science 293:2248­2251.
Harvey, P. H., and M. D. Pagel. 1991. The comparative method
in evolutionary biology. Oxford University Press, New
York, New York, USA.
Hew, C. L., G. L. Fletcher, and P. L. Davies. 1995. Transgenic
salmon: tailoring the genome for food production. Journal
of Fish Biology 47:1­19.
Hilborn, R., and M. Mangel. 1997. The ecological detective:
confronting models with data. Cambridge University Press,
New York, New York, USA.
Hochachka, P. W., C. A. Darveau, R. D. Andrews, and R. K.
Suarez. 2003. Allometric cascade: a model for resolving
body mass effects on metabolism. Comparative Biochemistry
and Physiology A--Molecular and Integrative Physiology
134:675­691.
McArdle, B. H. 2003. Lines, models, and errors: regression
in the field. Limnology and Oceanography 48:1363­1366.
Reiners, W. A. 1986. Complementary models for ecosystems.
American Naturalist 127:59­73.
Sharma, H. C., J. H. Crouch, K. K. Sharma, N. Seetharama,
and C. T. Hash. 2002. Applications of biotechnology for
crop improvement: prospects and constraints. Plant Science
163:381­395.
Sokal, R. R. and F. J. Rohlf. 1995. Biometry, Third edition.
W. H. Freeman, New York, New York, USA.
Voet, D., and J. G. Voet. 1995. Biochemistry. Second edition.
John Wiley, New York, New York, USA.
West, G. B., J. H. Brown, and B. J. Enquist. 1997. A general
model for the origin of allometric scaling laws in biology.
Science 276:122­126.
Forum
1808 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
Ecology, 85(7), 2004, pp. 1808­1810
2004 by the Ecological Society of America
CAN FUNCTION AT THE ORGANISMAL LEVEL EXPLAIN
ECOLOGICAL PATTERNS?
M. A. R. KOEHL1
AND BRYCE D. WOLCOTT
Department of Integrative Biology, University of California, Berkeley, California 94720-3140 USA
INTRODUCTION
Brown et al. (2004) propose that ``first principles of
chemistry, physics, and biology'' can be used to link
the function of individual organisms to ecological processes.
By arguing that metabolic rate controls ecological
processes at all levels of organization, from the
individual to the biosphere, they propose that a metabolic
theory of ecology can be a powerful unifying
principle. Because the scope of their vision is so broad,
and because the models on which these ideas are based
are controversial, the papers by Brown, West, and their
collaborators (cited in Brown et al. 2004) have stimulated
lively intellectual debate within and between
disciplines, and have spawned new research in a number
of different fields. By stirring the pot with their
broad-reaching ideas, Brown and his colleagues are
making a significant contribution to the advancement
of both physiology and ecology, whether or not their
theories turn out to be correct or general in their ap-
plicability.
MECHANISTIC VS. PHENOMENOLOGICAL MODELS
Mathematical models in ecology and organismal biology
can be mechanistic or phenomenological. The
strengths and limitations of these two approaches have
been debated (reviewed by Schoener 1986, Koehl
1989). Mechanistic models assume that particular processes
determine the behavior of a system, and build
a quantitative description of how the system works
based on these underlying mechanisms. An example of
such an approach is the modeling cited by Brown et
al. (2004) of how materials are distributed within organisms
by branching transport systems. This mechanistic
approach shows how uptake and transport rates
of resources within an organism can limit its metabolic
rate, and predicts that whole-organism basal metabolic
rate should scale as body mass raised to the  power.
In contrast, other models are phenomenological descriptions
of a system. For example, the regression
equations describing the data in Figs. 1­5 in Brown et
al. (2004) provide quantitative expressions of how the
systems being plotted behave, showing that processes
Manuscript received 13 November 2003. Corresponding
Editor: A. A. Agrawal. For reprints of this Forum (including
the MacArthur Award paper), see footnote 1, p. 1790.
1 E-mail: cnidaria@socrates.berkeley.edu
occur at particular rates, rather than how those rates
are produced. Although phenomenological models provide
an effective way of organizing observations to
reveal patterns and of making predictions about the
performance of systems for which we have data, mechanistic
models can be powerful tools for developing
our understanding of how a system works.
STUDYING ORGANISM-LEVEL FUNCTION TO
UNDERSTAND ECOLOGICAL PROCESSES
Brown et al. (2004) argue that metabolic theory can
help to explain the patterns observed in many ecological
processes. This approach is part of a long, although
sometimes ignored, tradition of studying how processes
operating at the level of individual organisms can determine
the properties of populations, communities,
and ecosystems (reviewed in Koehl 1989). The philosophical
underpinnings of using such a reductionist
approach in ecology were discussed by Schoener
(1986). To put the metabolic theory of Brown et al.
(2004) in perspective, we will mention a few examples
of earlier attempts to use basic laws of physics and
chemistry to explain defined aspects of organismallevel
function and the ecological consequences of those
functions.
Theories of heat and mass transport have been coupled
with analyses of physical aspects of the environment
to reveal constraints on distributions and interactions
of organisms. This approach has been used to
explain ecological phenomena ranging from predatorprey
interactions (Porter et al. 1975) to reproductive
strategies (Kingsolver 1983). More recently, this biophysical
approach has been used to explore some of
the ecological consequences of global climate change
(e.g., Grant and Porter 1992, Helmuth et al. 2002). A
different reductionist approach, focusing on the function
of heat-shock proteins, is also being used to explore
how thermal tolerance relates to biogeographic
patterns of species distributions (e.g., Tomanek and Somero
1999).
Foraging ecology provides some other examples of
using basic principles of chemistry and physics to relate
the function of organisms to ecological processes.
Chemical reactor theory has been used to understand
the kinetics of digestion by guts of different designs,
and the functional insights emerging from such analyses
have been used to explain ecological patterns in
July 2004 1809METABOLIC THEORY OF ECOLOGY
Forum
foraging strategies (e.g., Penry and Jumars 1987). Similarly,
basic rules of aerodynamics have been used to
explain the mechanical and energetic constrains on foraging
by flying animals, providing functional explanations
of ecological patterns, such as the absence of
folivory among flying animals (Dudley and Vermeij
1992), or the different foraging strategies used by hummingbirds
living at low vs. high altitudes (Feinsinger
et al. 1979).
Basic principles of fluid and solid mechanics have
also been used to analyze the susceptibility of benthic
and intertidal marine organisms to physical disturbance
(e.g., Denny 1999, Koehl 1999), an important process
in structuring many communities. A scaling rule that
emerged from the physics was hypothesized to explain
the observation that organisms on wave-swept shores
are small, but subsequent research showed that this
physical constraint is usually not what limits the size
of those organisms (Denny 1999). However, investigation
of the hypothesis led to many discoveries about
the mechanical design of marine organisms, the spatial
and temporal patterns of physical stresses in waveswept
habitats, and the interplay of mechanical design
and life history strategy in variable environments (reviewed
in Denny 1999, Koehl 1999).
The metabolic theory of ecology of Brown et al.
(2004) is much more ambitious than any of the examples
just cited. Earlier applications of organismal
functional biology to address ecological problems have
focused on specific processes, such as foraging or disturbance.
In contrast, Brown et al. (2004) point out the
applicability of the metabolic theory to a wide range
of ecological issues, from life history to population
interactions and ecosystem processes. Therefore, as organismal
biologists and ecologists debate and test the
assumptions and predictions of the metabolic theory,
its impact no doubt will be far greater than that of the
earlier, more narrowly focused links between basic
chemistry and physics with ecology.
THE MODEL HAS STIMULATED NEW SYNTHESIS
AND RESEARCH IN ORGANISMAL BIOLOGY
An earlier attempt to provide a mechanistic explanation
for the scaling of metabolic rate with body size,
the elastic similarity model of McMahon (1973), was
controversial and spawned a flurry of research activity
and new discoveries about the biomechanics of skeletal
design in animals and plants, and of locomotion. The
controversies swirling around the models proposed by
Brown and collaborators seem to be having a similar
effect on the field of physiology. For example, debate
about one of the underlying assumptions of the model,
that the terminal branches of a biological transport network
(such as capillaries, or mitochondria) are invariant
in size, has led to re-examination of experimental
data about the morphology and performance of cardiovascular
systems (Dawson 2001) and about mitochondrial
structure and function (Porter 2001) in animals
of different sizes.
Physiologists studying metabolic pathways have objected
to the idea that a single process, transport of
materials through hierarchical, fractal-like networks,
limits metabolic rate (e.g., Darveau et al. 2002). Although
the alternative model proposed by Darveau et
al. (2003) is seriously flawed (e.g., Banavar et al. 2003),
we should not ignore the body of experimental work
showing that a variety of interrelated physiological and
biochemical processes all contribute to limiting the
rates of ATP synthesis and use in cells. These processes,
some of which are important in controlling the
overall metabolic rate of an animal when it is at rest
while others play a larger control role when the animal
is active, scale differently with body size.
Another assumption of the metabolic theory of
Brown et al. (2004) is that natural selection has acted
to minimize energy expenditure within a biological
transport system. This assumption flies in the face of
long-standing arguments that complex physiological or
morphological systems that perform a variety of different
functions that affect fitness, and that evolve in
changing environments, are not likely to show optimization
of a single criterion (reviewed in Dudley and
Gans 1991). Nonetheless, optimization models have
proven to be powerful tools in guiding empirical research
(reviewed in, e.g., Koehl 1989), and the models
of Brown and colleagues are clearly serving as a catalyst
for interesting new discussions and experiments
in physiology.
IF THE MODEL IS PHENOMENOLOGICAL, WILL IT
STILL BE USEFUL TO ECOLOGISTS?
Even if the mechanisms responsible for the size dependence
of metabolic rate that have been hypothesized
by Brown et al. (2004) turn out to be inconsistent with
future experimental evidence, the allometric equations
produced by their model may still prove to be useful
descriptions of how the rates of various ecologically
important processes vary with body size and temperature.
However, several cautionary notes should be
mentioned about their central theme that metabolic rate
varies with body mass raised to the  power. Whether
an exponent of  can be statistically distinguished from
one of , given the scatter in the data, has been examined
by a number of investigators (e.g., Dodds et
al. 2001). Furthermore, although the universal model
describing the metabolic rate data spanning 20 orders
of magnitude in body mass (from tiny microbes to large
mammals) has an exponent of , the exponents for
specific clades of organisms within the composite data
set can be higher or lower (e.g., Riisga°rd 1998, Dawson
2001, Dodds et al. 2001). Perhaps more worrying is
the observation, for a variety of invertebrates, that the
metabolic rates of young, rapidly growing individuals
scale with body mass raised to higher exponents than
do those of slowly growing older stages and adults
Forum
1810 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
(Riisga°rd 1998). Because of ontogenetic changes and
species differences in temperature sensitivity, Rombough
(2003) also cautions against using models that
are based on comparisons across different life stages
and types of organisms to make predictions about responses
of particular species.
Brown et al. (2004) are the first to point out that
variation of the data not explained by their metabolic
theory provides clues to factors other than body size
and temperature that can affect metabolic and ecological
processes, and they list some ecological patterns
that probably do not have a metabolic explanation.
Nonetheless, the simple expression that they have developed
to predict the combined effect of size and temperature
on whole-organism metabolic or production
rate (Brown et al. 2004: Eq. 4) is a useful way of
summarizing observations spanning a vast range of organism
size, thereby providing a powerful tool for making
predictions about various ways in which the metabolism
of individual organisms might determine important
ecological processes. Whether or not all of the
aspects of the metabolic theory of Brown et al. (2004)
turn out to be right, this theory will make significant
contributions to our understanding of how organisms
and ecosystems work because it is focusing attention
on the importance of metabolism to ecological processes,
is inspiring so much new research, and is serving
as a catalyst for communication between organismal
biologists and ecologists.
LITERATURE CITED
Banavar, J. R., J. Damuth, A. Maritan, and A. Rinaldo. 2003.
Allometric cascades. Nature 421:713­714.
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Darveau, C. A., R. K. Suarez, R. D. Andrews, and P. W.
Hochachka. 2002. Allometric cascade as a unifying principle
of body mass effects on metabolism. Nature 417:166­
170.
Dawson, T. H. 2001. Similitude in the cardiovascular system
of mammals. Journal of Experimental Biology 204:395­
407.
Denny, M. 1999. Are there mechanical limits to size in waveswept
organisms? Journal of Experimental Biology 202:
3463­3467.
Dodds, P. S., D. H. Rothman, and J. S. Weitz. 2001. Reexamination
of the ```-law'' of metabolism. Journal of
Theoretical Biology 209:9­27.
Dudley, R., and C. Gans. 1991. A critique of symmorphosis
and optimality models in physiology. Physiological Zoology
64:627­637.
Dudley, R., and G. J. Vermeij. 1992. Do the power requirements
of flapping flight constrain folivory in flying animals?
Functional Ecology 6:101­104.
Feinsinger, P., R. K. Colwell, J. Terborgh, and S. B. Chaplin.
1979. Elevation and the morphology, flight energetics, and
foraging ecology of tropical hummingbirds. American Naturalist
113:481­497.
Grant, B. W., and W. P. Porter. 1992. Modeling global macroclimatic
constraints on ectotherm energy budgets. American
Zoologist 32:154­178.
Helmuth, B., C. D. G. Harley, P. M. Halpin, M. O'Donnell,
G. E. Hofmann, and C. A. Blanchette. 2002. Climate
change and latitudinal patterns of intertidal thermal stress.
Science 298:1015­1017.
Kingsolver, J. G. 1983. Ecological significance of flight activity
in Colias butterflies: implications for reproductive
strategy and population structure. Ecology 64:546­551.
Koehl, M. A. R. 1989. From individuals to populations. Pages
39­53 in J. Roughgarden, R. M. May, and S. A. Levin,
editors. Perspectives in ecological theory. Princeton University
Press, Princeton, New Jersey, USA.
Koehl, M. A. R. 1999. Ecological biomechanics: life history,
mechanical design, and temporal patterns of mechanical
stress. Journal of Experimental Biology 202:3469­3476.
McMahon, T. A. 1973. Size and shape in biology. Science
179:349­351.
Penry, D. L., and P. A. Jumars. 1987. Modeling animal guts
as chemical reactors. American Naturalist 129:69­96.
Porter, R. K. 2001. Allometry of mammalian cellular oxygen
consumption. Cellular and Molecular Life Sciences 58:
815­822.
Porter, W. P., J. W. Mitchell, W. A. Beckman, and C. R. Tracy.
1975. Environmental constraints on some predator­prey
interactions. Pages 347­364 in D. M. Gates and R. B.
Schmerl, editors. Perspectives of biophysical ecology.
Springer-Verlag, New York, New York, USA.
Riisga°rd, H. U. 1998. No foundation of a `` power scaling
law'' for respiration in biology. Ecology Letters 1:71­73.
Rombough, P. 2003. Modelling developmental time and temperature.
Nature 424:268­269.
Schoener, T. W. 1986. Mechanistic approaches to community
ecology: a new reductionism. American Zoologist 26:81­106.
Tomanek, L., and G. N. Somero. 1999. Evolutionary and
acclimation-induced variation in the heat-shock responses
of congeneric marine snails (genus Tegula) from different
thermal habitats: implications for limits of thermo tolerance
and biogeography. Journal of Experimental Biology 202:
2925­2936.
July 2004 1811METABOLIC THEORY OF ECOLOGY
Forum
Ecology, 85(7), 2004, pp. 1811­1813
2004 by the Ecological Society of America
ENERGY PARTITIONING BETWEEN DIFFERENT-SIZED ORGANISMS AND
ECOSYSTEM STABILITY
BAI-LIAN LI,1,3
VICTOR G. GORSHKOV,2
AND ANASTASSIA M. MAKARIEVA2
1Department of Botany and Plant Sciences, University of California, Riverside, California 92521 USA
2Theoretical Physics Division, Petersburg Nuclear Physics Institute, 188300, Gatchina, St. Petersburg, Russia
INTRODUCTION
The metabolic approach to ecology presented by
Brown et al. (2004) stems from the seminal work of
West et al. (1997). They hypothesized that material
transport within living beings is organized such as to
minimize the scaling of total hydrodynamic resistance
through vascular networks. Based on this assumption,
the organismal metabolic power P was theoretically
predicted to scale with body mass M as P M 3/4. By
additionally assuming that organismal metabolic processes
accelerate with temperature in the same manner
as individual biochemical reactions, a temperature correction
factor was added to this scaling:
3/4 E/kTP M e . (1)
At the organismal level, these results were criticized
on both theoretical and empirical grounds (e.g., Dodds
et al. 2001, Chen and Li 2003, Makarieva et al. 2003,
2004a). In particular, Makarieva et al. (2004a) showed
how the application of the metabolic approach to the
ontogenetic growth problem (West et al. 2001) resulted
in violation of the energy conservation law. In this short
commentary, however, we will focus on the potential
of the metabolic approach to explain patterns in population
and ecosystem dynamics.
LINKING INDIVIDUAL AND ECOSYSTEM ENERGETICS:
THE LOGIC
The relationship linking individual to population energetics
is:
NP R (2)
where N (number of individuals per square meter) is
the population density of individuals of a given body
size, P is the rate of individual energy use (Watts per
individual), and R (Watts per square meter) is the areaspecific
rate at which the population consumes energy
resources from the environment. Eq. 2 is obvious and
essentially identical to Eq. 9 of Brown et al. (2004), if
the latter is related to unit area and Eq. 1 is taken into
account.
Manuscript received 20 October 2003. Corresponding Editor:
A. A. Agrawal. For reprints of this Forum (including
the MacArthur Award paper), see footnote 1, p. 1790.
3 E-mail: bai-lian.li@ucr.edu
A variable of critical importance in both ecology and
organismal biology is body size. A successful biological
theory is expected to be able to predict the dependence
of individual metabolic power on body size
on the basis of some fundamental assumptions pertaining
to organismal morphology and biochemistry.
For example, the assumptions that underlie Eq. 1 can
be classified as being of this kind.
Similarly, an ecological theory will be able to successfully
predict the scaling of population energy use,
R, with body size only if it identifies and takes into
account some fundamental principles of an ecological
community's organization. As long as the basic principles
of the metabolic approach are restricted to the
organismal level, none of them is relevant to the ecosystem-level
question of whether larger organisms
should claim larger, smaller, or equal shares of an ecosystem's
productivity than smaller organisms. The metabolic
approach stretches to the ecosystem scale by
making a simplifying assumption that if R is independent
of body size, then the scaling of population density
N with body size will be determined by the scaling of
individual metabolic power.
However, it is unclear whether there is a dependence
of R on body size. If there is such a dependence, what
are the fundamental causes and consequences? Although
the metabolic approach refrains from answering
this question, a growing body of evidence suggests that
the scaling of R with body size varies predictably with
the degree of ecosystem stability, thus providing clues
to this central problem of modern ecology (McCann
2000).
ENERGETIC DOMINANCE OF SMALLER ORGANISMS
IN STABLE ECOSYSTEMS
There is some evidence showing that the smaller
organisms claim larger shares of an ecosystem's productivity
in relatively stable ecosystems. For example,
Sprules and Munawar (1986) studied the scaling of
phytoplankton population density N M in 67 sites
forming a stability gradient: from self-sustainable,
oligotrophic ecosystems of open ocean and large lakes
to highly unstable, ``flushing'' eutrophic ecosystems
of shallow lakes and coastal zones that receive major
discharges of nutrients and contaminants. They found
that the scaling exponent consistently increases from
Forum
1812 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
1.16 in stable ecosystems to 0.76 in
unstable ones. These results indicate that in stable
ecosystems smaller organisms consume a larger proportion
of the ecosystem's energy flux than larger
ones, whereas in unstable ecosystems the energy partitioning
among different-sized organisms becomes
more equitable. Biddanda et al. (2001) confirmed the
emerging pattern and showed that in the most stable
aquatic ecosystems, bacteria (the smallest organisms)
fully control the energy use, accounting for 91­98%
of total ecosystem's respiration. In highly eutrophic
waters, the share of bacterial respiration decreases to
9%, indicating the growing role of larger heterotrophs
in less stable ecosystems.
In an extensive survey of phytoplankton (6339 seawater
samples), Li (2002) grouped the phytoplankton
community into three size classes; the difference in cell
mass between the smallest and the largest classes is
about three orders of magnitude (Msmall/Mlarge 10 3).
The pattern characterized by Li (2002) was that the
ratio between population densities of the smallest and
the largest cells grows with increasing degrees of the
ecosystem's stability, the latter being estimated by the
degree of eutrophy and intensity of water mixing (Li
2002: Figs. 2a and 3a, respectively). In stable ecosystems,
the smallest cells outnumber the largest ones by
about four orders of magnitude, Nsmall/Nlarge 104. This
allows the estimation of the scaling exponent as
log10(Nsmall/Nlarge)/log10(Msmall/Mlarge) 4/3. Again,
we are faced with energetic dominance of the smallest
organisms in stable ecosystems. In unstable ecosystems,
the difference between Nsmall and Nlarge is about
one order of magnitude only, producing an approximate
slope of 1/3.
When the differences in the degree of stability of
studied ecosystems are ignored and all phytoplankton
data are pooled in one plot (Li 2002: Fig. 2b), one
obtains 0.78. The ecological meaningfulness of
this result (interpreted by Brown et al. [2004] as supportive
of their approach) is questionable. Depending
on the degree to which stable and unstable ecosystems
are represented in the cumulative data set, the scaling
exponent can vary within broad margins, being more
a function of data assortment procedure than reflecting
properties of real ecosystems.
Turning to terrestrial ecosystems, Damuth (1993) reported
39 values of scaling exponent for a total of
557 mammalian species grouped according to habitat
types, which he classified into closed (forests, woods)
and open (savannahs, grasslands). Thus defined, open
ecosystems appear to be more unstable both in terms
of biomass fluctuations (e.g., Van de Koppel and Prins
1998) and environmental degradation processes like
soil erosion (Lal 1990). The 39 scaling exponents listed
by Damuth (1993) vary from 1.4 to 0.42, with a
mean of 0.71. However, if one analyzes the scaling
exponents separately in closed vs. open ecosystems, it
is observed that the closed (more stable) ecosystems
are, on average, characterized by a significantly more
negative scaling exponent than are open (less stable)
ecosystems, ( 0.88 0.31 vs. 0.50 0.40, mean
1 SD; P 0.01), consistent with the results for aquatic
ecosystems.
PERSPECTIVES FOR THEORETICAL RESEARCH OF THE
ALLOMETRIC R--M SCALING
These analyses suggest that the potential of the R--
M scaling as an informative indicator of ecosystem
stability is tangible and calls for a serious scrutiny
(Makarieva et al. 2004b). There are straightforward
arguments justifying the direct relevance of the energy
use patterns to ecosystem stability and opening the way
for theoretical research (Gorshkov et al. 2000). In accordance
with the statistical law of large numbers, several
small organisms consume the same energy flux in
a more balanced manner than does one large organism,
thus lowering the risk of both underexploitation or
overexploitation of the available resources and reducing
fluctuations of a community's biomass and nutrientcycling
processes. This is like dividing your money
among several investments; return will be stabilized
and loss minimized. Ecosystems where energy use is
dominated by smaller organisms (but not for terrestrial
plants, as we will discuss) are therefore expected to be
more stable than ecosystems where large organisms
consume considerable portions of a community's energy
flux.
The large apparent size of many plants (e.g., trees)
is due to a large amount of metabolically inactive tissues
(wood) that do not participate in energy conversion
processes (Makarieva et al. 2003). Instead, the
photosynthetic power in terrestrial plants is exerted by
units of relatively small size: leaves and needles. In
contrast to rigidly correlated organs within an animal
body, different photosynthesizing units of the same
plant are correlated only very weakly. This allows
plants to make use of the law of large numbers and to
stabilize the flux of primary productivity, in the same
manner as numerous small heterotrophs are able to stabilize
the flux of decomposition. Our prediction is
therefore that, similar to the way in which the smallest
phytoplankton (unicellular photosynthesizing units)
dominate energy flux in stable aquatic ecosystems (Li
2002), the major flux of solar energy in stable terrestrial
ecosystems should also be claimed by plants having
the smallest photosynthesizing units. For example, stable
late-successional stages in boreal forests are dominated
by conifers that have much smaller photosynthesizing
units (needles) than grasses and deciduous
trees of early-successional stages (Whittaker 1975). We
believe that studying the nature and size of photosynthesizing
units (rather than the currently emphasized
apparent plant size) will yield important insights into
how terrestrial ecosystems are organized.
The increasing anthropogenic pressure imposed on
natural life-support systems makes the problem of eco-
July 2004 1813METABOLIC THEORY OF ECOLOGY
Forum
system stability a major challenge for ecological research
(McCann 2000). This challenge is unlikely to
be met by the ecological theory if it confines itself to
theoretically unjustified, axiomatic assumptions, like
the assumption of R M0
within the metabolic approach
of Brown et al. (2004), which, as we have argued,
is empirically unsupported.
LITERATURE CITED
Biddanda, B., M. Ogdahl, and J. Cotner. 2001. Dominance
of bacterial metabolism in oligotrophic relative to eutrophic
waters. Limnology and Oceanography 46:730­739.
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Chen, X., and B.-L. Li. 2003. Testing the allometric scaling
relationships with seedlings of two tree species. Acta Oecologica
24:125­129.
Damuth, J. 1993. Cope's rule, the island rule and the scaling
of mammalian population density. Nature 365:748­750.
Dodds, P. S., D. H. Rothman, and J. S. Weitz. 2001. Reexamination
of the ``3/4-law'' of metabolism. Journal of
Theoretical Biology 209:9­27.
Gorshkov, V. G., V. V. Gorshkov, and A. M. Makarieva. 2000.
Biotic regulation of the environment: key issue of global
change. Springer-Verlag, London, UK.
Lal, R. 1990. Soil erosion and land degradation: the global
risks. Pages 129­172 in R. Lal and B. A. Stewart, editors.
Advances in soil science. Volume 11. Soil degradation.
Springer-Verlag, New York, New York.
Li, W. K. W. 2002. Macroecological patterns of phytoplankton
in the northwestern North Atlantic Ocean. Nature 419:
154­157.
Makarieva, A. M., V. G. Gorshkov, and B.-L. Li. 2003. A
note on metabolic rate dependence on body size in plants
and animals. Journal of Theoretical Biology 221:301­307.
Makarieva, A. M., V. G. Gorshkov, and B.-L. Li. 2004a.
Ontogenetic growth: models and theory. Ecological Modelling,
in press.
Makarieva, A. M., V. G. Gorshkov, and B.-L. Li. 2004b. Body
size, energy consumption and allometric scaling: a new
dimension in the diversity-stability debate. Ecological
Complexity, in press.
McCann, K. S. 2000. The diversity­stability debate. Nature
405:228­233.
Sprules, W. G., and M. Munawar. 1986. Plankton size spectra
in relation to ecosystem productivity, size, and perturbation.
Canadian Journal of Fisheries and Aquatic Science
43:1789­1794.
Van de Koppel, J., and H. H. T. Prins. 1998. The importance
of herbivore interactions for the dynamics of African savanna
woodlands: an hypothesis. Journal of Tropical Ecology
14:565­576.
West, G. B., J. H. Brown, and B. J. Enquist. 2001. A general
model for ontogenetic growth. Nature 413:628­631.
West, G. B., B. J. Enquist, and J. H. Brown. 1997. A general
model for the origin of allometric scaling laws in biology.
Science 276:122­126.
Whittaker, R. H. 1975. Communities and ecosystems. MacMillan,
New York, New York, USA.
Ecology, 85(7), 2004, pp. 1813­1816
2004 by the Ecological Society of America
A ONE-RESOURCE ``STOICHIOMETRY''?
ROBERT W. STERNER1
Ecology, Evolution and Behavior, University of Minnesota, St. Paul, Minnesota 55108 USA
The approach of Brown et al. (2004) might succeed
or fail on two levels. On one level, it can be used as
a purely statistical, predictive tool. Examples given by
Brown and colleagues leave no doubt that temperature
and body size ``explain'' (in the statistical sense) a great
deal. We do need good predictive models for many
reasons, one of them for incorporating more ecology
and thus improving models of global change. The second,
more difficult, level has to do with the reasons
why those statistical predictor variables work the way
they do, and why they are good predictors in the first
place. The processes that Brown et al. propose--fractal
scaling of distribution networks and thermodynamic
kinetics of ``metabolism''--may truly be the mechanistic
basis for the observed patterns, but that, of
Manuscript received 3 November 2003. Corresponding
Editor: A. A. Agrawal. For reprints of this Forum (including
the MacArthur Award paper), see footnote 1, p. 1790.
1 E-mail: stern007@umn.edu
course, is less certain than is the existence of good
statistical correlations.
Brown et al. view the ``big three'' variables to be
temperature, body size, and stoichiometry. Temperature
turns out to be approachable using decades-old
formulations of Arrhenius, Boltzmann, and others. It
is a shock that these models, which have been shown
to work for ``simple'' biological functions such as oxygen
consumption or even bacterial growth (Johnson
et al. 1974), also do a splendid job with the more complex
variables of standing stock and even diversity
(which are not even rates). The critical and surprising
result here is that so much ecological temperature dependence
is described by the Arrhenius-Boltzmann
equation, with near-constant activation energy. What
that success itself means is a fascinating question, perhaps
related to just what is ``metabolism.'' In spite of
their complexity, do one or a small number of core
metabolic pathways regulate organism growth, so that
Forum
1814 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
those kinetics dominate the signals at these higher levels
of observation? Body size relationships also have
had a long history of study, and a family of power laws
has been explored very thoroughly; this literature has
been reenergized by the fractal distribution theory.
Given the success of models with just these two variables
(e.g., Brown et al. 2004: Figs. 1­8), why might
the third--stoichiometry--even be needed? At least in
the statistical sense, not much is left to explain. But
here the mechanistic sense must be considered. Rate
limitation of growth (and therefore metabolism, as defined
by Brown et al.) usually involves scarcity of some
material(s) or resource(s). Therefore, although it might
be that models without explicit mention of material
resources can be good statistical tools (level one), to
understand how these systems work and why they have
the structure they do, we must explicity include the
rate-limiting steps and processes (level two). The fractal
scaling of distribution networks might relate to
movement of many kinds of materials, but it is very
hard to reconcile a temperature­kinetic control of one
step of metabolism with the fact that ecologists know
that, in nature, organisms face multiple limiting constaints.
Either many key biochemical steps have nearly
identical temperature dependence, or the Bolzmanntemperature
interpretation collides with current understandings
about the multiplicity of limiting factors in
nature.
What is the best way to incorporate material limitations
with temperature and body size models into
broad-scale, macroecology models? Or, stated more
generally, what does a combination of metabolic control
theory (see Fell 1997) and ecology look like?
Brown et al. (2004) suggest one possibility. They incorporate
a single term, linear with organism nutrient
content, and generate a comprehensive model including
stoichiometry (see also Brown et al. 2004: Fig. 9). Is
this then the cardinal equation of macroecology,
3/4 E/kTX M e R error
where M, E, k, and T are as in Brown et al. (2004),
and X stands for some ecological parameter of interest,
and R stands for ``resource''? Might such an equation
really ``explain'' (in both senses, statistical and mechanistic)
so much?
We can ask if a single linear term in R is enough to
do the job. If we correct for M and T, or let them be
subsumed into the error term, and just explore how X
varies with R, we now are simply asking how some
parameter of interest varies with the amount of a limiting
resource. Stoichiometrically, if there is but one
potentially limiting reagent and all else remains equal,
product yield will indeed be a simple linear function
of the limiting reagent's amount. However, when more
than one reagent may limit a reaction, the expectation
is more complicated. Over broad ranges of productivity
and, hence, resource abundance, many ecological phenomena
are nonlinear with productivity. Over broad
ranges, biomass often increases with the limiting nutrient
via a saturating, not linear, function (Sterner and
Elser 2002). Work with even- and odd-link trophic
models (Oksanen et al. 1981, DeAngelis 1992) suggests
that responses to nutrient enrichment are dependent on
trophic structure. Diversity may increase, decrease, or
have some hump shape with respect to productivity
(Rosenzweig 1995). There are many other examples of
nonlinear resource effects, and these cast considerable
doubt as to whether there is a Boltzmann-equivalent
term with a single functional form when dealing with
limiting substances.
Resources are a more heterogenous lot than is temperature.
They range from light and chemical energy
to water and a handful of nutrient elements. In some
contexts, space itself, or hiding or nesting sites are
limiting. Often, more than one of these resources plays
some role in controlling rates at any one time, and
sometimes having a lot of one resource means that you
can do with less of another. Also, do we mean resources
within or external to the organism? Finally, in many
contexts, these substances exist in a plethora of forms
and the simple act of determining what pool of resources
is involved provides some real limitation to
universality of these measures.
Brown et al. (2004) sidestep all of this complexity
when they assert: ``Far from being distinct ecological
currencies, as some authors have implied (Reiners
1986, Sterner and Elser 2002), the currencies of energy
and materials are inextricably linked by the chemical
equations of metabolism.'' First, a clarification: what
is ecological stoichiometry about, if it is not about these
inextricable linkages? Elser and I agree that resources
are linked! The critical point is the nature of the linkage.
The context in which the statement of Brown et
al. is true is under fixed stoichiometric coefficients.
With fixed stoichiometric coefficients (i.e., constant nutrient
ratios), knowing one substance tells you everything
about all substances, because they are all simple
proportions of one another. At a sufficiently broad
scale, such an assumption might be fine, in that the
chemistries of different living systems are more alike
than they are different: they all are based on C, N, P,
etc., and all living things need proteins, phospholipid
membranes, nucleic acids, etc. At some highly approximate
level, living things do have a uniform stoichiometry.
However, I say ``might'' because even with
fixed coefficients, strategies for winning in a world of
scarce ``resource one'' might not work for other resources.
One need only think of the different strategies
that plants need for obtaining light compared to soil
resources. In lakes, systems under strong N limitation
often become dominated by large, inedible species of
cyanobacteria, whereas P or Fe limitation produces systems
of very different structure and dominance by very
much smaller cells; other trophic-level effects follow
from these. Community and ecosystem structure and
function are strongly controlled by the identity of the
July 2004 1815METABOLIC THEORY OF ECOLOGY
Forum
limiting resources. The saturating functions of biomass
and productivity alluded to in the previous paragraph
are probably caused by shifts in the identity of limiting
substances when one of them becomes very abundant.
Lessons can be learned from dynamic consumer­resource
models. A larger number of potentially limiting
substances opens up opportunities for coexistence (Tilman
1982), a theoretical prediction recently elegantly
shown empirically by Interlandi and Kilham (2001).
When the number of resources increases from one to
only three, entirely new, complex dynamics are possible
(Huisman and Weissing 2001). For another example,
several of my co-workers and I have done work
at a variety of time and space scales on light gradients
where the fixed stoichiometry of a simple, single-species
population of herbivores creates positive relationships
between primary and secondary productivity in
one range of the experiment, but negative relationships
in the other range (Urabe and Sterner 1996, Sterner et
al. 1998, Urabe et al. 2002). At low light levels, both
primary and secondary production are energy limited,
whereas at high light levels, herbivores switch to material
(phosphorus, we believe) limitation. These kinds
of shifts--driven by element linkage, not in spite of
element linkage, as a casual reading of Brown et al.
might imply--are a signal that the identity of resources
does matter a great deal; it will not generally work to
boil them all down to a single, univariate measure. I
hypothesize that for most ``X,'' it does matter whether
the limiting resource is light, or nitrogen, or iron, or
some combination of all of these.
Furthermore, for many important ecological questions,
assumptions of fixed stoichiometry simply break
down. Plants have different composition than animals,
for example, and even within species, differing growth
rates are associated with different chemical contents
(Elser et al. 2003). Organisms do link the rates of uptake
and use of separate resources, but in an adaptive,
flexible way that responds to shifting stoichiometric
ratios. Note, for example, the very different fluxes of
C, N, and P in metabolic networks under different limiting
factors in the study of Dauner et al. (2001). To
what extent does the set of all possible resources contain
redundant information, so that the set can be collapsed
to a univariate measure? The claim by Brown
et al. (2004) that one can overlook the multiplicity of
limiting resources because they are all linked together,
and are all linked to a single universal currency of
energy is an echo of a previous era in ecology, where
bioenergetics was the hoped-for organizing concept
(Slobodkin 1972, Morowitz 1992, Hairston and Hairston
1993). It was not, and we are beyond that.
Incorporation of materials into broad-scale macroecology
models need not be distastefully complex, or
so idiosyncratic as to resist all generality. I think that
there is quite a bit more work to do and that ultimately,
even at broad scale, we will almost always need a multivariate,
not a univariate, perspective on resources.
Biology has evolved fascinating responses to the optimization
problems that the shifting availability of
these resources creates.
Again, so that this message is not lost: I'm a fan of
the Brown et al. (2004) approach. Macroecology has
produced a set of amazing, inspiring, and, I believe,
also extremely useful microbes-to-monsters plots. But
much of the important work ahead of us in ecology is
at finer spatial and temporal scale. I also believe it to
be the case that the utility of macroecology models will
be proportional to the scale of interest. Tools are most
useful when applied to the right job.
ACKNOWLEDGMENTS
Among my colleagues who read and commented on this
commentary, I want especially to thank Adam Kay, Bob Megard,
and Dave Tilman, and, as usual, Jim Elser, for their
insightful reading.
LITERATURE CITED
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Dauner, M., T. Storni, and U. Sauer. 2001. Bacillus subtilis
metabolism and energetics in carbon-limited and excesscarbon
chemostat culture. Journal of Bacteriology 183:
7308­7317.
DeAngelis, D. L. 1992. Dynamics of nutrient cycling and
food webs. Chapman and Hall, New York, New York, USA.
Elser, J. J., K. Acharya, M. Kyle, J. Cotner, W. Makino, T.
Markow, T. Watts, S. Hobbie, W. Fagan, J. Schade, J. Hood,
and R. W. Sterner. 2003. Growth rate: stoichiometry couplings
in diverse biota. Ecology Letters 6:936­943.
Fell, D. 1997. Understanding the control of metabolism. Portland
Press, London, UK.
Hairston, N. G., Jr., and N. G. Hairston, Sr. 1993. Causeeffect
relationships in energy flow, trophic structure, and
interspecific interactions. American Naturalist 142:379­
411.
Huisman, J., and F. J. Weissing. 2001. Fundamental unpredictability
in multispecies competition. American Naturalist
157:488­494.
Interlandi, S., and S. S. Kilham. 2001. Limiting resources
and the regulation of diversity in phytoplankton communities.
Ecology 82:1270­1282.
Johnson, F. H., H. Eyring, and B. J. Stover. 1974. The theory
of rate processes in biology and medicine. John Wiley, New
York, New York, USA.
Morowitz, H. J. 1992. Beginnings of cellular life: metabolism
recapitulates biogenesis. Yale University Press, New Haven,
Connecticut, USA.
Oksanen, L., S. D. Fretwell, J. Arruda, and P. Niemala¨. 1981.
Exploitation ecosystems in gradients of primary productivity.
American Naturalist 118:240­261.
Reiners, W. A. 1986. Complementary models for ecosystems.
American Naturalist 127:59­73.
Rosenzweig, M. L. 1995. Species diversity in space and time.
Cambridge University Press, Cambridge, UK.
Slobodkin, L. R. 1972. On the inconstancy of ecological
efficiency and the form of ecological theories. Pages 293­
305 in E. S. Deevey, editor. Growth by intussesception:
ecological essays in honor of G. Evelyn Hutchinson. Transactions
of the Connecticut Academy of Sciences, New Haven,
Connecticut, USA.
Sterner, R. W., J. Clasen, W. Lampert, and T. Weisse. 1998.
Carbon : phosphorus stoichiometry and food chain production.
Ecology Letters 1:146­150.
Forum
1816 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
Sterner, R. W., and J. J. Elser. 2002. Ecological stoichiometry:
the biology of elements from molecules to the biosphere.
Princeton University Press, Princeton, New Jersey,
USA.
Tilman, D. 1982. Resource competition and community
structure. Princeton University Press, Princeton, New Jersey,
USA.
Urabe, J., M. Kyle, W. Makino, T. Yoshida, T. Andersen, and
J. J. Elser. 2002. Reduced light increases herbivore production
due to stoichiometric effects of light : nutrient balance.
Ecology 83:619­627.
Urabe, J., and R. W. Sterner. 1996. Regulation of herbivore
growth by the balance of light and nutrients. Proceedings of
the National Academy of Sciences (USA) 93:8465­8469.
Ecology, 85(7), 2004, pp. 1816­1818
2004 by the Ecological Society of America
COMMENTARY ON BROWN ET AL.'S ``TOWARD A METABOLIC
THEORY OF ECOLOGY''
HENRY S. HORN1
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544-1003 USA
What Brown has called ``a metabolic theory of ecology''
is powerful and exciting in scope, accomplishments,
and promise, . . . and controversial in some of
its details. Let me confess that I am a spectator on the
sidelines of the field, rather than an active player. Indeed,
I am uncomfortable about commenting because
most of my information comes from personal friendships
with players on both sides of the controversial
part, and from privileged information in manuscripts
that journal editors send me from a misinformed sense
of my expertise. Accordingly, I shall take the easy path
that commentary offers, and make this a public statement
of tentative thoughts rather than making any attempt
at a scholarly piece. In particular, I shall cite a
small selection of papers deliberately construed to support
my points, rather than giving the literature the
review that it deserves. I hope that friends will remain
friends, and that editors will revise their impression of
my wisdom.
It is hard to say enough about the excitement and
interpretive potential of a theory that unites the explanation
of patterns of scaling from intracellular physiology
to community dynamics, and that allows measurements
throughout those scales to give useful approximations
of numbers needed to address global issues
and to pose interesting evolutionary questions.
Fortunately, the canonical proponents have done an
excellent job of advertisement, mostly in the pages of
Science and Nature, . . . and they have responded to
those of their critics who have also reached the same
venues. I cheerfully endorse most of what I have read
there. But there are still some important points that
leave me uneasy, along with students and colleagues
at home and abroad.
Manuscript received 13 November 2003. Corresponding
Editor: A. A. Agrawal. For reprints of this Forum (including
the MacArthur Award paper), see footnote 1, p. 1790.
1 E-mail: hshorn@princeton.edu
The first point is the empirical question of whether
the primary scaling factor is  or , when for example,
Fig. 1B of Brown et al. (2004), a log­log plot of normalized
temperature-corrected metabolic rate against
body mass, has a best-fit value of 0.71, . . . exactly
midway between  and . This same point is made
more carefully and more forcefully by Dodds et al.
(2001). The variety of contexts in which scaling factors
are modulo  rather than modulo  is encouraging
(Brown et al. 2004 and references therein), but it would
be worthwhile to review this literature to separate definitive
tests from instances in which the  scaling of
metabolism with size entered as an assumption at the
outset.
There is also the semi-theoretical question of whether
there need be an ``either­or'' choice. The nai¨ve version
of the theoretical argument for exactly  assumes
that the fundamental organizing geometry of organisms
is Euclidean and spherical; resources are acquired by
surfaces and used by volumes, but the distribution of
these resources can complicate the analysis. The original
argument for exactly  assumes that the fundamental
geometry of organisms is fractal (West et al.
1997). In the  theory, resources are also acquired by
surfaces, but the theory explicitly and exactly optimizes
a fractal network for distribution of these resources.
Here I go into hazy analogical thinking, but
it strikes me that different modalities of distribution
and different shapes of organisms could favor the applicability
of different balances of the theories . . . and
a scaling rule with power , , or something in be-
tween.
The third point is the paradox that the -power scaling
rule works so well over a range of sizes and shapes
of organisms whose explicit resource-distributing networks
are variously fractal, tree-like but not fractal,
and not even tree-like. This strongly suggests that the
fractal assumption that lies at the heart of the devel-
July 2004 1817METABOLIC THEORY OF ECOLOGY
Forum
opment of the original version of the theory needs to
be replaced by a more general network. Such an approach
should explore explicitly how the cost and efficiency
of that network change with departures from
the optimized fractal structure. Starts in this direction
have been made by the authors of the original theory
in its biological context (West et al. 1999, 2001), and
by others (Banavar et al. 1999, 2002, Dodds et al. 2001,
Gutierrez 2002), some of whom derive scaling rules
that vary between  power and  power. Particular
exponents can also arise from mechanisms of competitive
space-filling at the community level (e.g., Kinzig
et al. 1999), and it would be worthwhile to look for
them anywhere where resources flow through an array
of tiny consumers that remove a fraction of what they
encounter (e.g., small leaves scattered through a big
tree [Horn 1971]; to pick an example only because I
know the author). It is too early to make a generalization
from this variety of ideas, but perhaps the network
of distribution need only be efficient and hierarchical,
not just near-fractal, for exponents to be modulo 
(West et al. 1999), or very near it (others cited previously).
Other modifications may come from biological
variations in the dimensionality of the surface over
which resources are acquired, and details of the metric
of the volume over which they are distributed and used,
. . . but I expect these to be small enough to contribute
more to explaining residuals than to changing the average
scaling of attributes to body size.
The initial assumption of size-independent metabolic
units (West et al. 1997) has received little published
criticism, perhaps because most biologists can cite so
many examples from their own specialties. Accordingly,
Brown et al.'s (2004) extension of the consequences
of this assumption to organism, population, and ecosystem
is novel, interesting, and powerful, independent
of any arguable details.
Some would quibble about the possible role of multiple
normalization factors in fitting varied organisms
to a common line on a graph, but it doesn't bother me.
As Brown et al. (2004) point out, the normalization
factors are appropriate subjects for interpretation in
terms of specific biological attributes. Indeed, one of
the great strengths of this metabolic theory is that a
demonstrated allometry allows the all-pervasive effect
of body size to be accounted for, so that residuals from
the allometry may call for detailed biological interpretation.
Alternatively, the residuals may provide data
from organisms of different sizes to test theoretical
predictions about such biological details. Brown et al.
(2004) also point out that even after normalization the
residuals from some of their regressions span a 20-fold
range (and I read some of their figures as providing a
50-fold range between extremes). That offers plenty of
opportunity for structural idiosyncracies and biologically
interesting details to ``fine-tune'' an average relationship
that spans as much as 20 orders of magnitude
in size. Brown et al. (2004) make this point over and
over again in a wide range of contexts, from physiology
to evolution and from cell to ecosystem.
Indeed this is what makes the whole enterprise of
``A Metabolic Theory of Ecology'' so exciting and
worthwhile. Brown et al. (2004) have derived an extraordinary
range of interpretation and prediction from
``first principles.'' The original framing of the first principles
(West et al. 1997) engendered criticisms and subsequent
modifications that made them less confining
(West et al. 1999, 2001), and such improvements continue.
The extensions of the original theory to the population
and community levels have an internal biophysical
consistency, and strong empirical support that
still allows enough variation to demand biological explanation.
Furthermore, the theory may help in the
search for that explanation.
Robert MacArthur would have been very pleased
with Brown et al. (2004). He was always interested in
patterns at any scale from organism to community to
biogeography, and from ecology to evolution. He had
a particular interest in how body size affected those
patterns. He was a theoretician and a naturalist, with
a conceptual brilliance when he combined the two.
Here is how he might have viewed the controversy over
details:
Ecological patterns, about which we construct theories,
are only interesting if they are repeated. They
may be repeated in space or in time, and they may
be repeated from species to species. A pattern which
has all of these kinds of repetition is of special interest
because of its generality, and yet these very
general events are only seen by ecologists with rather
blurred vision. The very sharp-sighted always find
discrepancies and are able to say that there is no
generality, only a spectrum of special cases. This
diversity of outlook has proved useful in every science,
but it is nowhere more marked than in ecology.
--MacArthur 1968:159.
LITERATURE CITED
Banavar, J. R., J. Damuth, A. Maritan, and A. Rinaldo. 2002.
Supply­demand balance and metabolic scaling. Proceedings
of the National Academy of Sciences (USA) 99:
10506­10509.
Banavar, J. R., A. Maritan, and A. Rinaldo. 1999. Size and
form in efficient transportation networks. Nature 399:130­
132.
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Dodds, P. S., D. H. Rothman, and J. S. Weitz. 2001. Reexamination
of the ``-law'' of metabolism. Journal of Theoretical
Biology 209:9­27.
Gutierrez, W. R. 2002. Volume integration of fractal distribution
networks. Physical Review E 66:041906.
Horn, H. S. 1971. The adaptive geometry of trees. Princeton
University Press, Princeton, New Jersey, USA.
Kinzig, A. P., S. A. Levin, J. Dushoff, and S. Pacala. 1999.
Limiting similarity, species packing, and system stability
for hierarchical competition­colonization models. American
Naturalist 153:371­383.
Forum
1818 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
MacArthur, R. H. 1968. The theory of the niche. Pages 159­
176 in R. C. Lewontin, editor. Population biology and evolution.
Syracuse University Press, Syracuse, New York, USA.
West, G. B., J. H. Brown, and B. J. Enquist. 1997. A general
model for the origin of allometric scaling laws in biology.
Science 276:122­126.
West, G. B., J. H. Brown, and B. J. Enquist. 1999. The fourth
dimension of life: fractal geometry and allometric scaling
of organisms. Science 284:1677­1679.
West, G. B., J. H. Brown, and B. J. Enquist. 2001. A
general model for ontogenetic growth. Nature 413:628­
631.
Ecology, 85(7), 2004, pp. 1818­1821
2004 by the Ecological Society of America
RESPONSE TO FORUM COMMENTARY ON
``TOWARD A METABOLIC THEORY OF ECOLOGY''
JAMES H. BROWN,1,2
JAMES F. GILLOOLY,1
ANDREW P. ALLEN,1
VAN M. SAVAGE,2,3
AND GEOFFREY B. WEST2,3
1
Department 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
We welcome the opportunity to respond to the commentaries
in this Special Feature. We are well aware
that this is not the last word. A full evaluation of the
metabolic theory of ecology (MTE) will be rendered
over time by the wider ecological community and will
probably take years. Here we address some general and
specific issues raised by the commentaries. The MTE
is very much a work in progress--hence the ``toward''
in the title of Brown et al. (2004). To facilitate progress,
we try to clarify some of the controversial or at least
still unresolved issues, rather than simply defend our
paper.
We begin with some general points that emerged
from several commentaries.
Is the exponent  or ?--The values of the allometric
exponents for whole-organism metabolic rate
and other biological rates and times are ultimately empirical
questions. These questions have intrigued biologists
for about 70 years, ever since Kleiber (1932)
measured the basal metabolic rates of mammals and
birds spanning a wide range of body masses, and found
that the slope of his log­log plot was almost exactly
. Extensive studies, culminating in several synthetic
books on allometry in the 1980s, appeared to have
resolved the issue. These books unanimously concluded
that most allometric exponents were quarter powers
rather than the third powers expected on the basis of
Euclidean geometric scaling (McMahon and Bonner
1983, Peters 1983, Calder 1984, Schmidt-Nielsen
1984).
The issue was reopened recently, in particular when
Dodds et al. (2001) and White and Seymour (2003)
analyzed data on basal metabolic rates of mammals and
Manuscript received 1 December 2003. Corresponding
Editor: A. A. Agrawal. For reprints of this Forum (including
the MacArthur Award paper), see footnote 1, p. 1790.
birds and obtained exponents closer to  than . Savage
et al. (2004) have commented on these studies. We
summarize only the two key points:
1) It is problematic to claim a definitive value based
on analyses of existing data on mammalian and avian
basal metabolic rates. The estimated exponent varies
from 0.65 to 0.85, depending on which measurements
and taxa are included, and which statistical procedures
are used.
2) Dodds et al. (2001) and White and Seymour (2003)
compiled and analyzed data only on basal metabolic
rates of mammals and birds. Savage et al. (2004) performed
analyses of many additional data sets, including
basal, field, and maximal whole-organism metabolic
rates, and many other biological rates and times. The
data included not just mammals and birds, but many
other taxa from both terrestrial and aquatic environments.
The variables ranged from cellular and molecular
to whole-organism and population levels. The exponents
varied, but showed distinct peaks and mean values at
almost exactly  for whole-organism basal and field
metabolic rates,  for mass-specific metabolic rates
and many other biological rates (e.g., heart rates and
population growth rates), and  for biological times
(e.g., blood circulation times and gestation periods).
Based on this evidence, Savage et al. (2004) concluded
that there is little justification for reopening the
argument that biological allometries in general have
third-power exponents. Important additional evidence
for the pervasiveness of quarter-power exponents
comes from our recent research, which is based on new
compilations and analyses of published data. For example,
refer to Figs. 2, 5, and 8 in Brown et al. (2004),
which plot data for rates of whole-organism biomass
production, maximal population growth (rmax), and ecosystem
carbon turnover across a wide range of body
July 2004 1819METABOLIC THEORY OF ECOLOGY
Forum
sizes, taxa, and environments. The exponents, 0.76,
0.23, and 0.22, respectively, are very close to the
predicted values of , , and , and the 95% confidence
intervals do not include the Euclidean alternatives
of , , and .
What is the mechanistic basis for quarter-power exponents?--The
data on biological allometries are well
described by power laws, implying that they are the
result of self-similar or fractal-like processes. West et
al. (1997, 1999a, b) developed general mechanistic
models based on geometric and biophysical principles
that explain the quarter-power exponents. These models
address the general problem of distributing metabolic
resources within an organism and, more specifically,
describe the structure and function of mammal
and plant vascular systems. The models of West et al.
hypothesize that the quarter-power scaling exponents
reflect the optimization of these transport networks due
to natural selection. Although the organisms themselves
are three-dimensional, an additional length variable
is required to describe the branching networks,
resulting in scaling exponents with 4, rather than the
Euclidean 3, in the denominator. The structures and
dynamics of resource distribution networks are hypothesized
to be dominated by self-similar fractal-like
branching, although it is likely that some networks may
be ``virtual'' (e.g., within cells of prokaryotes) rather
than ``hard wired'' (e.g., vascular systems of vertebrates
and higher plants).
These models of West et al. have been criticized by
several authors. Cyr and Walter (2004) cite most of the
published critiques. West and collaborators are trying
to respond to the most serious criticisms, but this takes
considerable effort and introduces inevitable time lags
(see Brown et al. 1997, Enquist et al. 1999, West et al.
2002; 2003a, b, in press, Allen et al. 2003, Brown et
al. 2003, Gillooly et al. 2003). Several other responses
are still in press or unpublished. We will not address
the criticisms here, except to state that we have yet to
see compelling theoretical or empirical evidence that
would cause us to retract or substantially change the
models of West et al. Like the content and implications
of the broader MTE, the rigor and realism of the models
for quarter-power scaling will be decided not by the
participants in the immediate debates, but by the broader
scientific community in the fullness of time.
What is a mechanism, and a mechanistic theory?--
Several commentaries question the extent to which
MTE, as we have presented it, is truly mechanistic. We
have three responses.
The first is that there is considerable variation in what
scientists consider to constitute a mechanism; one person's
mechanism is another's empirical phenomenology.
This is a long-standing problem. For example,
physicists still don't completely understand the mechanistic
basis of gravity, even though the force of gravity
can be characterized by analytical equations and used
as a first principle to make useful, accurate predictions
about everything from satellite orbits to biomechanical
properties of bones. We freely admit that there is abundant
room for additional research on mechanisms: from
(1) how the kinetics of the multiple biochemical reactions
of metabolism determine the observed activation
energies at whole-organism and ecological levels
of organization; to (2) how the kinetics of species interaction,
evolution, coevolution, speciation, and extinction
cause the observed temperature dependence in
biogeographic gradients of species diversity. We hope
other research groups will investigate some of the
mechanisms and we welcome all contributions to producing
a more complete and mechanistic conceptual
framework for MTE.
The second response is that mechanisms are described
in much more detail in our other publications.
Most equations in Brown et al. (2004) are the result of
mathematical models described in separate publications.
These models make explicit mechanistic connections
between the metabolic processes of individual
organisms and their ecological and evolutionary con-
sequences.
The third response is that empirical support for these
models and, in particular, for the predicted scalings
with size and temperature, suggests that metabolic rate
is indeed the most fundamental biological rate, and that
its manifestations ramify to affect all levels of biological
organization, from molecules to ecosystems. Data
sources and statistical procedures are not described in
Brown et al. (2004), but are documented in the original
papers. It is important to recognize that the figures in
Brown et al. (2004) are not just descriptive statistical
regression equations. Two points should be emphasized:
(1) theoretically predicted values for allometric
exponents and activation energies, based on metabolic
processes within individual organisms, are incorporated
directly into the analyses and into the plots of the
data; and (2) support for model predictions comes not
only from the high proportions of variation explained
by the regression equations (high values of r2
), but
more importantly from the fact that 95% confidence
intervals for the slopes almost always include the predicted
allometric exponents and activation energies.
What about all the variation?--The authors of the
commentaries represent a wide spectrum of biologists
and ecologists, from those who seek unifying principles,
to those who emphasize diversity and complexity.
Both approaches are valid--indeed both are required
to keep the science focused, balanced, realistic, and
progressing. We are at one end of the spectrum, unabashedly
seeking unifying theory. For those who are
more concerned about the variation, we have three
comments.
First, the influence of metabolism on ecology is most
apparent when comparisons can be made across wide
ranges of body size and temperature, where the pervasive
influences of allometry and kinetics are strong.
When body mass differs by only two- or threefold, or
Forum
1820 METABOLIC THEORY OF ECOLOGY Ecology, Vol. 85, No. 7
temperature varies by only a degree or two, other factors
can assume equal or greater importance. Many of these
factors are outside the domain of metabolic theory. For
example, allometry and kinetics are of little value in
explaining coexistence and species diversity of herbs in
an old field or warblers in a forest, because there is little
variation in both body size and temperature. In effect,
these variables are ``controlled'' by the design of the
study, thereby allowing other factors to be evaluated.
Nevertheless, many systems studied by population and
community ecologists have sufficient variation in body
size and temperature for metabolic theory to be directly
applicable. For example, our model can explain 90%
of the variation in growth rates of zooplankton (Gillooly
et al. [2002]; see also egg-hatching rates in Brown et
al. 2004: Fig. 3). The magnitudes of intra- and interspecific
variation in body mass and seasonal variation
in environmental temperature make these results directly
relevant to population and community dynamics of zooplankton
in temperate lakes.
The second comment is that effects of allometry and
kinetics on individual organisms and ecological systems
are powerful and pervasive. The very fact that
body size and temperature account for most of the variation
in log-scaled ``microbe to monster'' and ``oceans
to forests'' plots is evidence that the allometry and
kinetics of metabolic rate are fundamental to biology
and ecology. These processes are still operating even
when their influences may be obscured by variation
due to other processes. Suppose that we want to understand
the processes involved in secondary succession
from an old field to a forest. Then, the influence
of plant size on species interactions and ecosystem processes
assumes major importance. Or suppose that we
want to predict the ecological consequences of a rise
in average environmental temperature by 2 C. The actual
responses will undoubtedly be complicated by time
lags, transient dynamics, initial species composition,
effects of limiting material resources, and other variables.
Despite these sources of variation, however, metabolic
theory provides a good starting point: it predicts
that rates of individual-, population-, community-, and
ecosystem-level processes will increase as described
by the Boltzmann factor with an activation energy of
0.6­0.7 eV (1 eV 96.49 kJ/mol).
The third point, also made in several commentaries,
is that a theory soundly based on first principles, provides
a baseline--a point of departure--from which to
understand the residual variation. Deviations from predictions
can be grouped loosely into four categories:
(1) measurement errors or other biases in the data; (2)
effects of factors not included in the model or theory;
(3) exceptions that ``prove the rule'' by showing how
violating specific model assumptions leads to predictable
deviations; and (4) discrepancies that expose serious
flaws in the assumptions or operations of the model.
Having a theoretically predicted baseline helps one
to evaluate these possibilities.
Specifics.--Most commentaries raise specific issues
that warrant attention, but we address only two here.
First, Cyr and Walker (2004) extol the virtues of the
dynamic energy budget (DEB) approach of Kooijman,
Nisbet, and collaborators (e.g., Kooijman 2000, Nisbet
et al. 2000). DEB models do indeed describe growth
and reproduction of individuals in terms of metabolic
processes and first principles of energy and material
balance. And they do indeed incorporate more detail--
many more variables and functions--than our deliberately
simple MTE. How much complexity in a model
is desirable or necessary is in part a matter of taste,
and in part a matter of the purpose for which the model
is used. We view the DEB and MTE approaches as
complementary. They make different trade-offs between
specificity and generality, and consequently have
different strengths, weaknesses, and applications.
Second, Sterner (2004) asks whether ``one cardinal
equation of macroecology, X M 3/4e E/kTR error
. . . '' with a ``. . . single linear term in R is enough to
do the job'' (where R is the ``amount'' of some limiting
material resource). This is a straw man. We never
claimed that this is the ``one cardinal equation of macroecology.''
We explicitly stated that many ecological
phenomena, including macroecological species­area
and species­abundance relationships, are outside the
purview of MTE. We did not suggest that the unexplained
variation should be regarded as ``error.'' We
explicitly noted that residual variation may be due to
deterministic influences of stoichiometry, phylogenetic
or functional group affinity, environment, and other
factors that are not included in our models. We did not
say that resource limitation is due to a single reagent
and is linear with respect to R and ``organism nutrient
content.'' We do agree with Sterner that ``there is quite
a bit more work to do'' on ecological stoichiometry
and its relationship to energetics, and for this reason
we deliberately omitted a term for resource abundance
from our models (our Eqs. 4­8) for rates and times at
the individual organism level. We did include a linear
term, R, in our Eqs. 9­11 for abundance, biomass, and
productivity at the population to ecosystem levels.
These models can be taken as testable hypotheses for
the effects of limiting material resources, together with
body size and temperature, on these ecological variables.
The chemical compositions of the fluxes and
pools of material resources are central to organismal
metabolism and must be an essential ingredient of any
complete MTE. Our earlier work has concentrated on
allometry and kinetics. As indicated in Brown et al.
(2004), we have begun to address many of the interrelationships
between energy and materials in both organisms
and ecosystems. A major research program of
Sterner, Elser, and others has concentrated on ecological
stoichiometry, and represents a major contribution
(e.g., Elser et al. 2000, Sterner and Elser 2002). However,
we strongly disagree with Sterner that ``we are
beyond that . . . previous era in ecology, where bio-
July 2004 1821METABOLIC THEORY OF ECOLOGY
Forum
energetics was the hoped for organizing concept.'' Just
change the (our italics) to a. Energetics, updated, based
more firmly on first principles, and interrelated to stoichiometry,
is a powerful organizing concept for ecol-
ogy.
We end by emphasizing that MTE is not intended to
be the theory of everything that is interesting and important
in ecology. Nor is it intended to account for all
of the variation among living things and ecological
systems. Within its domain, however, MTE offers
mechanistic explanations for linking many ecological
patterns and processes to biological, physical, and
chemical constraints on individual organisms. MTE
suggests that underlying the diversity of living things
and the complexity of ecological systems are fundamental
unities, some of which reflect how first principles
of biology, physics, and chemistry govern the
fluxes and pools of energy and materials within organisms
and between organisms and their environments.
LITERATURE CITED
Allen, A. P., J. H. Brown, and J. F. Gillooly. 2003. Response
to Comment on ``Global biodiversity, biochemical kinetics,
and the energetic-equivalence rule.'' Science 299:346.
Brown, J. H., A. P. Allen, and J. F. Gillooly. 2003. Heat and
biodiversity--Response. Science 299:512­513.
Brown, J. H., B. J. Enquist, and G. B. West. 1997. Allometric
scaling laws in biology--Response. Science 278:372­373.
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and
G. B. West. 2004. Toward a metabolic theory of ecology.
Ecology 85:1771­1789.
Calder, W. A. III. 1984. Size, function and life history. Harvard
University Press, Cambridge, Massachusetts, USA.
Cyr, H., and S. C. Walker. 2004. An illusion of mechanistic
understanding. Ecology 85:1803­1805.
Dodds, P. S., D. H. Rothman, and J. S. Weitz. 2001. Reexamination
of the ``-law'' of metabolism. Journal of Theoretical
Biology 209:9­27.
Elser, J. J., R. W. Sterner, E. Gorokhova, W. F. Fagan, T. A.
Markow, J. B. Cotner, J. F. Harrison, S. E. Hobbie, G. M.
Odell, and L. J. Weider. 2000. Biological stoichiometry
from genes to ecosystems. Ecology Letters 3:540­550.
Enquist, B. J., J. H. Brown, and G. B. West. 1999. Plant
energetics and population density--Reply. Nature 15:573­
573.
Gillooly, J. F., E. L. Charnov, J. H. Brown, V. M. Savage,
and G. B. West. 2002. Allometry: how reliable is the biological
time clock? Reply. Nature 424:270­270.
Kleiber, M. 1932. Body size and metabolism. Hilgardia 6:
315­332.
Kooijman, S. A. L. M. 2000. Dynamic energy and mass budgets
in biological systems. Cambridge University Press,
Cambridge, UK.
McMahon, T. A., and J. T. Bonner. 1983. On size and life.
Freeman Press, New York, New York, USA.
Nisbet, R. M., E. B. Muller, K. Lika, and S. A. L. M. Kooijman.
2000. From molecules to ecosystems through dynamic
energy budget models. Journal of Animal Ecology
69:913­926.
Peters, R. H. 1983. The ecological implications of body size.
Cambridge University Press, Cambridge, UK.
Savage, V. M., J. F. Gillooly, W. H. Woodruff, G. B. West,
A. P. Allen, B. J. Enquist, and J. H. Brown. 2004. The
predominance of quarter-power scaling in biology. Functional
Ecology, in press.
Schmidt-Nielsen, K. 1984. Scaling: why is animal size so
important? Cambridge University Press, Cambridge, UK.
Sterner, R. W. 2004. A one-resource ``stoichiometry''? Ecology
85:1813­1816.
Sterner, R. W., and J. J. Elser. 2002. Ecological stoichiometry.
Princeton University Press, Princeton, New Jersey, USA.
West, G. B., J. H. Brown, and B. J. Enquist. 1997. A general
model for the origin of allometric scaling laws in biology.
Science 276:122­126.
West, G. B., J. H. Brown, and B. J. Enquist. 1999a. A general
model for the structure and allometry of plant vascular
systems. Nature 400:664­667.
West, G. B., J. H. Brown, and B. J. Enquist. 1999b. The
fourth dimension of life: fractal geometry and allometric
scaling of organisms. Science 284:1677­1679.
West, G. B., J. H. Brown, and B. J. Enquist. In press. Growth
models based on first principles or phenomenology? Functional
Ecology.
West, G. B., B. J. Enquist, and J. H. Brown. 2002. Ontogenetic
growth: modelling universality and scaling--reply.
Nature 420:626­627.
West, G. B., V. M. Savage, J. F. Gillooly, B. J. Enquist, W.
H. Woodruff, and J. H. Brown. 2003a. Why does metabolic
rate scale with body size? Nature 421:713­713.
West, G. B., V. M. Savage, J. F. Gillooly, B. J. Enquist, W.
H. Woodruff, and J. H. Brown. 2003b. Red herrings and
rotten fish. arXiv. http://arXiv.org/abs/physics/0211058 .
White, C. R., and R. S. Seymour. 2003. Mammalian basal
metabolic rate is proportional to body mass(). Proceedings
of the National Academy of Sciences (USA) 100:
4046­4049.