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vol. 168, supplement
the american naturalist
december 2006
Biological Stoichiometry: A Chemical Bridge between
Ecosystem Ecology and Evolutionary Biology
James Elser*
School of Life Sciences, Arizona State University, Tempe, Arizona
85287
abstract: The mission of the American Society of Naturalists is
“to advance and diffuse knowledge of organic evolution and other
broad biological principles so as to enhance the conceptual unification of the biological sciences.” In this article, I argue that the area
of biology least integrated with knowledge of organic evolution is
the field of ecosystem ecology, as evidenced by a semiquantitative
literature survey of use of terms in the scientific literature. I present
an overview of recent theoretical developments and empirical findings in the emerging field of biological stoichiometry (the study of
the balance of energy and multiple chemical elements in living systems). These developments hold some promise as a means to conceptually integrate ecosystem ecology, with its emphasis on flows and
pools of energy and chemical elements, with evolutionary biology,
with its emphasis on genetic fitness and the biochemical products
of the genome. For example, recent evidence indicates that organismal C : P and N : P ratios have a major impact on biologically
mediated flows of energy and phosphorus; in turn, variations among
taxa in these ratios are connected to evolved differences in organismal
growth rate because of the connection between growth rate and the
need for increased allocation to P-rich ribosomal RNA. In this way,
evolutionary change in growth-related traits, by altering organismal
P requirements, has direct biogeochemical implications, while ecosystem conditions can constrain evolutionary acceleration of growth
rates by imposing a direct P limitation on production of the needed
biochemical machinery of growth. Thus, stoichiometric theory provides a broad biological principle that can interconvert the currencies
and concerns of ecosystem ecology and evolutionary biology, facilitating integration of diverse fields of study and contributing to conceptual unification of the biological sciences.
Keywords: biological stoichiometry, growth rate, phosphorus, ecosystem, evolution.
The mission of the American Society of Naturalists (ASN)
is essentially unchanged since the society’s inception in
1883: “to advance and diffuse knowledge of organic evo-
lution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.” This admirable goal is as simultaneously daunting
and thrilling today as it was more than a century ago.
Perhaps one of the greatest challenges of such an ambitious
agenda is the tremendous increase in subject matter added
to the domain of the “biological sciences” since 1883. What
comes most readily to mind in this respect is the explosion
of knowledge regarding the molecular basis of genetic inheritance and its connection to cellular and organismal
phenotypes. While I will have more to say about this aspect
toward the end of this article, my main emphasis here will
be on the expansion of biology’s realm at the other end
of the biological spectrum, in the development of explicit
scientific research on the flows of energy and materials
between living and nonliving forms in natural systems.
This is what is now known as ecosystem ecology. Given a
long history of major interactions of genetics and evolutionary biology with physiological, population, and community ecology (Collins 1986), my thesis, one that has
also been put forth by others (Holt 1995), is that ecosystem
ecology is the area of biology least connected to other areas
of biology, and especially to “knowledge of organic evolution.” Conceptually unifying ecosystem ecology with the
rest of biology, and especially with evolutionary thinking,
is the most important frontier for biological integration
in the current day. This article will discuss the possible
role of biological stoichiometry, the study of balance of
energy and multiple chemical elements in living systems
(Sterner and Elser 2002), in contributing to this integration. In the context of the symposium for which this article
was prepared, these materials contain my reflections on
my own involvement in this area of work, and thus the
article is not meant to be a comprehensive review of the
entire field.
Evolutionary Biology and Ecosystem Ecology:
Warring Parties No More?
* E-mail: [email protected].
Am. Nat. 2006. Vol. 168, pp. S25–S35. 䉷 2006 by The University of Chicago.
0003-0147/2006/1680S6-41371$15.00. All rights reserved.
Consistent with the claim that ecosystems have not been
on the agenda of the ASN or of evolutionary ecologists,
S26 The American Naturalist
Figure 1: a, Temporal trends in citation frequencies of articles identified in Web of Science (WOS) using the search word “ecosystem” relative to
those found using the word “evolution” (left) and also of “ecosystem” relative to “natural selection” (right). Data for the general scientific literature
are shown with circles; data for articles published in the American Naturalist are shown with triangles. b, Temporal trends in the total number of
citations in the general scientific literature identified using the combined search of “ecosystem” and “evolution” (left) or “ecosystem” and “natural
selection” (right). Of articles found in this way, the total number of articles published in the American Naturalist during each period is indicated
on the figure panels. The article labeled “Dunbar (1960)” is discussed in the text. In all panels, different Y-axes apply to the periods before and
after 1990, when WOS added abstracts to its data records. Lines are fit to temporal trends in citation frequencies in the general literature after 1990.
(No significant trends were seen in articles published in the American Naturalist during this period.)
even though the word “ecosystem” was coined by A. G.
Tansley 70 years ago (Tansley 1935), Web of Science (WOS;
http://isiknowledge.com) associates this term with only a
single article in the American Naturalist between 1955 (the
start of the WOS database) and 1970. This is despite the
fact that ecosystem ecology was developing rapidly in western science during the post–World War II years (Hagen
1992), expanding the domain of biology to include energy
flows in food webs and the cycling of water and chemical
elements in various habitats. To evaluate how the ecosystem concept has entered the general scientific literature
relative to its entry into the work published in the American Naturalist, I analyzed the frequency of scientific articles using the word “ecosystem” relative to those using
“evolution” or “natural selection” in their titles, keywords,
or abstracts (and therefore identifiable using WOS; note
that abstracts were included in the WOS database begin-
ning in 1991). Indeed, the analysis indicates that the
general scientific literature saw a steady increase in the
“ecosystem” : “evolution” ratio (E : Ev hereafter) and,
especially, the “ecosystem” : “natural selection” ratio
(E : NS hereafter) beginning in the mid- to late 1960s (fig.
1). During the past 15 years, there has been a highly significant (P ! .001) increase in E : Ev and E : NS in the
general scientific literature. In contrast to patterns in the
general literature, increases in E : Ev and E : NS are not
apparent in volumes of the American Naturalist until the
late 1970s (fig. 1), and there has been no increase in
E : Ev (P 1 .06) or E : NS (P 1 .8) since 1990. Perhaps
more relevant to the issue of whether knowledge of organic
evolution has been extended to include connections to
ecosystem ecology is whether publications that combine
evolutionary and ecosystem perspectives are increasing in
total and relative frequency, especially in the pages of the
Biological Stoichiometry
American Naturalist. To examine this, I located all articles
including both “ecosystem” and “evolution” (E ⫹ Ev hereafter) or “ecosystem” and “natural selection” (E ⫹ NS
hereafter) in the overall WOS database, as well as in articles
published in the American Naturalist. Before 1991 (when
only titles were included in Science Citation Index), cooccurrences of “ecosystem” with “evolution” were sporadic but tended to increase after 1970, and only one article
was identified with the combination of “ecosystem” with
“natural selection” in the overall literature. Interestingly,
this article was published in the American Naturalist
(Dunbar 1960) and is also the first article identified with
the “ecosystem” and “evolution” combination in the general scientific literature (more on this article shortly). After
1991, co-occurrences of “ecosystem” with “evolution” and
with “natural selection” were considerably more frequent
(reflecting the addition of abstracts to the WOS database)
and, importantly, increased very strongly during the ensuing 15 years. However, there is no similar trend in
E ⫹ Ev or E ⫹ NS apparent in articles published in the
American Naturalist during this recent period.
While there are a variety of shortcomings in semiquantitative literature analyses such as these, they are consistent
with the idea that there was an intellectual disjunction
between the fields of evolutionary biology and ecosystem
ecology throughout much of the second half of the twentieth century. The causes of this divergence are interesting
to contemplate; Collins (1986) suggests that many of these
difficulties may reflect disagreements among scientists in
each discipline regarding the levels of selection that should
be considered in investigating the relationship between
evolution and ecosystems. In fact, the difficulty is highlighted quite clearly in the title of the first article in the
American Naturalist that used the word “ecosystem” in its
title (Dunbar 1960): “The Evolution of Stability in Marine
Environments: Natural Selection at the Level of the Ecosystem.” That is, ecosystem ecologists may have been perceived by evolutionary biologists as promoting an untenable group selection argument (Collins 1986; Ricklefs
2003), leading many evolutionary biologists to dismiss the
relevance and validity of ecosystem-level investigations.
For example, evolutionary ecologist J. P. Collins reports
that, in his experiences as a graduate student in the late
1960s and early 1970s, the general ethos was that one
didn’t think much about evolution and ecosystems (J. P.
Collins, personal communication), as doing so led to
“group selection” arguments, a concept criticized heavily
by leading evolutionists such as G. C. Williams (see Williams 1966) but nevertheless postulated by leading ecosystem ecologists (e.g., Odum 1969). Meanwhile, because
of the emergence of a variety of revolutionary techniques,
evolutionary biologists during the later part of the twentieth century were becoming increasingly focused on es-
S27
tablishing the genetic basis of traits and their long-term
patterns of evolutionary change as the field of evolutionary
ecology emerged (Collins 1986). This focus may have convinced many ecosystem ecologists that their colleagues in
evolutionary ecology were excessively focused on reductionistic analysis of genetic data and had lost touch with
the broader context of the ecological systems within which
organisms and their genes are embedded.
While interest in multilevel selection theory persists,
most recently in the form of certain approaches within the
field of “community genetics” (Whitham et al. 2003; Wilson and Swennson 2003), I suggest that the intellectual
landscape is now shifting away from a tense stand-off between ecosystem and evolutionary perspectives. Ecosystems are no longer seen as distinct “quasi-organismal”
entities but instead are viewed more as complex adaptive
systems composed of a multitude of independent but interacting entities, both living and nonliving, in which Darwinian selection at the level of individual reproductive
success is the dominant mechanism of evolution within
the living domain (O’Neill 2001; Collins 2003). In this
view, complex direct and indirect feedbacks mediated by
biological alterations of physical-chemical habitat conditions are an explicit part of a dynamic selection regime
operating on individual reproductive success. (It is interesting to note that some investigators, e.g., Neuhauser et
al. [2003], who identify themselves as working in “community genetics” also adopt this view and do not invoke
higher-level selection). In any case, understanding complex evolving systems such as these is daunting to contemplate but no more so than the emerging genome and
its metabolic products. The challenge of biological integration today is to merge ecosystem and evolutionary perspectives using theoretical frameworks that operate on a
rigorous mechanistic foundation. In the rest of this article
I will try to illustrate how one such framework, biological
stoichiometry (Elser et al. 2000a; Sterner and Elser 2002),
might contribute to this integration. Biological stoichiometry is the study of balance of energy and multiple
chemical elements in biological systems ranging from molecules to ecosystems. It focuses on key cellular and physiological structures and functions and their associated biochemical demands while considering evolutionary change
primarily from the perspective of individual fitness
(Sterner and Elser 2002; Kay et al. 2005). In doing so, it
simultaneously accounts for the inexorable reciprocal feedbacks that arise from the core chemical construction that
living things share. Thus, I argue that it offers a promising
framework for accomplishing extensive integration across
diverse areas of biology.
S28 The American Naturalist
The Motivation: Ecosystem Nutrient Cycling and
Energy Flows Are Related to the Elemental
Composition of Living Biomass
In one of the most influential articles in the field of biogeochemistry, the oceanographer A. C. Redfield noted the
striking similarity in the ratios of key chemical elements
(C, N, and P) present in seawater and in the biomass of
phytoplankton (Redfield 1958), the canonical ratio being
106C : 16N : 1P. This article is a touchstone of what has
now become known as “ecological stoichiometry,” the
study of the balance of energy and multiple chemical elements in ecological interactions (Sterner and Elser 2002).
In more recent years, application of this type of analysis
to higher trophic levels has produced a suite of new insights. (1) Different zooplankton species and life stages
differ considerably in their C : N : P stoichiometry (Andersen and Hessen 1991; Hessen and Lyche 1991; Elser et
al. 2000c), varying as much as fivefold in body P content
(P as a function of dry weight). (2) Shifts in the relative
dominance of these zooplankton species can alter internal
nutrient cycling in pelagic food webs (Elser and Urabe
1999; Vanni 2002), and these impacts are strong enough
to affect the nature of phytoplankton nutrient limitation
(e.g., shifting from N to P limitation when a P-rich species
like Daphnia dominates) as well as ecosystem-level N fixation (Elser et al. 1988, 2000d; MacKay and Elser 1998)
and sedimentation fluxes (Elser and Foster 1998; Darchambeau et al. 2005). (3) Strong imbalance between autotroph (algae, vascular plant) and animal elemental composition greatly reduces food quality, impairing growth
and reproduction (Hessen 1992; Urabe and Watanabe
1992; Sterner et al. 1993; DeMott et al. 1998; Boersma
2000; Elser et al. 2001; Hood et al. 2005) and potentially
influencing the strength of trophic cascades (Elser et al.
1998). (4) Imposing stoichiometric constraints and feedbacks on models of predator-prey interactions introduces
qualitatively new dynamics, including multiple stable
states, deterministic extinction of the predator, and violations of the competitive exclusion principle (Andersen
1997; Loladze et al. 2000, 2004; Andersen et al. 2004). (5)
Shifts in environmental conditions, such as alterations in
light intensity or CO2 relative to nutrient supply, alter
stoichiometric imbalance and affect zooplankton dynamics
and production in predictable ways (Urabe and Sterner
1996; Sterner et al. 1997, 1998; Diehl et al. 2002; Hessen
et al. 2002; Urabe et al. 2002a, 2002b, 2003; but see Hall
et al. 2004).
A key insight that emerges from this body of work is
that an organismal trait (biomass elemental composition)
and its physiological regulation mediate major patterns
and processes at the ecosystem level, thus providing explicit mechanisms by which environmental alterations can
feed back to alter the selective regime. The work just reviewed has occurred mainly in the field of freshwater
plankton ecology but has also seen increasing application
in freshwater benthic ecology (Frost et al. 2002) and, as
will be discussed below, is expanding into terrestrial ecology as well.
The Mechanisms: Proximate and Evolutionary
Determinants of the Elemental Composition
of Living Biomass
Why do species differ in elemental composition? This relatively simple question, it turns out, has some relatively
simple answers, but the simplicity of this connection underlies a great complexity of biological and evolutionary
mechanisms and ramifications. In an underappreciated article published in the American Naturalist, Reiners (1986)
was among the first to propose a broadly synthetic view
of the mechanistic connections among organismal elemental composition, proximate chemical composition,
and macroevolutionary trends and their implications for
ecosystem dynamics. He argued that the elemental composition of the core biological functions of living things
was essentially the same, yielding a common chemical
composition for “protoplasmic life.” Further, Reiners proposed that major variations in elemental composition were
driven by differences among major life-forms in strategies
related to mechanical support. He contrasted, for example,
the reliance of higher plants on C-rich cellulose for support
with the reliance of vertebrates on Ca- and P-rich apatite
in bone. Indeed, allocation to structural carbohydrates in
vascular plants underlies the strong difference in biomass
C : nutrient ratios in terrestrial and planktonic autotrophs
(Elser et al. 2000c), while variations in allocation to bony
structures has been shown to underpin significant variation in body P content in fishes (Vanni et al. 2002).
However, it now appears that there is biologically significant variation in the elemental composition of organisms that relates not only to structural features but also
to the very core of biological function, the molecular biology of growth via production of ribosomal RNA. The
idea is captured in the “growth rate hypothesis” (GRH),
which states that variation in the P content (and thus
C : P and N : P ratio) of living things is driven by variation
in allocation to P-rich ribosomal RNA that accompanies
differences in growth rate, as elevated ribosome allocation
is generally needed to meet the protein synthesis demands
of rapid growth (Elser et al. 1996, 2000a). Thus, any evolutionary process that results in changes in organismal
growth or development rate may be manifested in changes
in organismal C : N : P ratios, with potential consequences
for that organism’s sensitivity to stoichiometric food quality constraints and its impacts on nutrient cycling. A ge-
Biological Stoichiometry
netic basis for such growth-related variations in RNArelated P demand has also been proposed (Elser et al.
2000a): increased growth rate and associated increases in
transcriptional capacity for rRNA production are associated with changes in the rDNA, particularly in the length
and content of the rDNA intergenic spacer (IGS) and/or
in overall rDNA copy number (for a detailed exposition,
see Weider et al. 2005a). Thus, a mechanistic thread has
been proposed that extends from the organization of a
major gene family (rDNA) through cellular allocation, to
physiological nutritional demands, to trophic interactions
and nutrient cycling in food webs. This provides an explicit
mechanism by which changes in gene frequencies can affect ecosystem processes.
What evidence is there for associations among organismal P and RNA contents, growth rate, and rDNA variation? A variety of recent findings from work on crustacean zooplankton have lent validity to the GRH. This
evidence includes the following. (1) A variety of studies
have shown significant positive correlations among various
combinations of the proposed growth-RNA-P coupling
system, including interspecific or ontogenetic comparisons
of animals growing at their maximal rates (Main et al.
1997; Vrede et al. 1998; Dobberfuhl 1999; Gorokhova and
Kyle 2002), physiological data in which members of a
single species were grown at different rates driven by variations in food quantity and quality (Vrede et al. 2002;
DeMott 2003; Acharya et al. 2004a, 2004b), and field observations (Elser et al. 2000b; Carrillo et al. 2001; DeMott
et al. 2001; but see Arnold et al. 2004 and Ferrao-Filho et
al. 2005). (2) Positive associations among growth rate,
body RNA and P contents, and the presence of long rDNA
intergenic spacer variants were observed in studies of various Daphnia species (Gorokhova et al. 2002; Weider et
al. 2004). (3) A cross-latitude study documented increased
growth rate and P requirements in Arctic Daphnia pulex,
a pattern that is consistent with natural selection operating
to increase growth rate to compensate for short growing
season duration (Elser et al. 2000b). (4) A lab experiment
demonstrated context-dependent success of different
rDNA variants in response to conditions of environmental
and dietary P supply (Weider et al. 2005b).
Because not all studies have shown the predicted positive associations among growth rate and P and RNA contents, more work is needed to address several important
questions, such as the degree of intra- versus interspecific
variation in body P content (see, e.g., DeMott et al. 2004;
DeMott and Pape 2005) along with the effect of the nature
of the growth-limiting factor for the animal (Elser et al.
2003b). However, the overall concordance of data across
multiple types of comparisons and studies indicates that
there are inherent associations among animal growth rate,
rRNA allocation and genetics, and P requirements and that
S29
these associations have important implications for the
ecology and evolution of these species. But does this set
of mechanisms apply to groups of organisms other than
crustacean plankton?
The Ramifications: Horizontal Integration and New
Applications Follow from Identifying
Underlying Mechanisms
Ribosome biogenesis is one of the core functions of cellular
physiology, intimately connected to the processes of
growth and development, themselves key components of
fitness (Arendt 1997). This biological core strongly suggests that the connections identified for crustacean zooplankton should apply well beyond the world of plankton.
Indeed this appears to be the case. First, the close association between RNA content and cellular proliferation
rate is well-known across diverse biota from microbes to
metazoans (Sutcliffe 1970; Elser et al. 2000a). Receiving
much less attention are the consequences of this growthRNA association for organismal P demand. However, recent studies with other groups of organisms show that, as
for crustacean zooplankton, not only is there wide variation in biomass P content across species (e.g., in terrestrial
herbivorous insects; Elser et al. 2000c), but there is also a
positive coupling among growth, RNA, and biomass P
contents (bacteria growing on substrates of contrasting P
content [Makino et al. 2003; Makino and Cotner 2004],
benthic aquatic insects and snails [Frost and Elser 2002;
Elser et al. 2005], fruitflies during ontogenetic development [Watts et al. 2006], and mesquite-feeding desert weevils [Schade et al. 2003]). These observations imply that,
just as for zooplankton, the availability of P in the diet
might also be an important ecological constraint in terrestrial food webs, for which plant secondary chemicals
and nitrogen content have largely been emphasized as potential limiting factors. In fact, the first direct evidence for
dietary P limitation for a terrestrial insect (Manduca sexta
caterpillars feeding on their host plant, Datura wrightii)
has recently appeared (Perkins et al. 2004). Furthermore,
macro- and microevolutionary patterns in insect stoichiometry are now being elucidated. For example, differences
in body P content in major clades of insects have been
identified (Woods et al. 2004), while Jaenike and Markow
(2002) have demonstrated a significant correlation between body P content of various trophically specialized
Drosophila species and that of their host resource.
Thus, common biological mechanisms appear to be operating to affect the biological stoichiometry of species in
both aquatic and terrestrial systems, allowing an explicit
integration of generally divergent fields of ecology to be
accomplished, all within a clear evolutionary framework.
This highlights a key avenue of integration: once a core
S30 The American Naturalist
mechanism is identified by reductionistic digging, it is possible to “come back to the surface” in an integrative, predictive mode of science in which the generality of hypothesized underlying mechanisms is tested at higher levels
of organization in new contexts. The best example of this
in the work I have conducted with my colleagues is the
sequence of events in which Daphnia’s P limitation and
differential N and P recycling was traced to its basis in
Daphnia’s high biomass RNA allocation and thus high P
demands. Similar connections were then uncovered in various insect taxa, culminating in the first experimental demonstration of dietary P limitation in an insect (Perkins et
al. 2004). We suspect that P limitation of terrestrial insects
is widespread but currently unappreciated. This strategy
of digging and resurfacing is possible because living things
share a fundamental core of cellular-genetic functioning
by virtue of their shared ancestry, and it suggests that the
breadth of the integration will often be a function of the
evolutionary depth of the shared function. In this case,
there is little more fundamental than RNA biology, and
thus the ramifications of the growth rate hypothesis are
extremely broad. Indeed, given the identification of a core
biological mechanism, such as the connection between
growth rate, ribosome biogenesis, and cellular P demand,
there is no predicting where its next application may come.
For example, my colleagues and I have recently begun to
apply stoichiometric theory in analysis of cancer dynamics
(Elser et al. 2003a; Kuang et al. 2004) and of the Cambrian
explosion (Elser et al. 2006), outcomes that would have
been difficult to predict when this work began in the realm
of plankton ecology. It is also important to note that ribosome biogenesis is just one component, albeit a very
important one, of organismal metabolism, and it is likely
that greater insights will be gained by taking a broader
view of the shared core of biological metabolism using the
emerging tools of systems biology (e.g., “metabolomics”;
Fiehn 2002). In fact, incorporation of stoichiometric
thinking is already embedded in this rapidly emerging
field, as systems biologists take advantage of the constraints
imposed by the laws of mass balance and stoichiometric
combination to gain detailed pictures of multiple metabolic fluxes using techniques such as isotopomer flux balancing (Sauer 2004). These approaches appear to be ready
for adaptation to important questions in ecosystem ecology, especially with respect to how functionally important
organisms process energy and materials under different
growth conditions. Adaptation of these approaches seems
to be well under way already in biological oceanography
(DeLong and Karl 2005).
This discussion has focused largely on factors affecting
P allocation in organisms, but the stoichiometric approach,
of course, need not be confined to a consideration of P.
Indeed, a variety of studies are using stoichiometric rea-
soning to understand the biological basis and ecological
and evolutionary implications of variation in animal N
content (Ayres et al. 2000; Fagan et al. 2002; Denno and
Fagan 2003; Fagan and Denno 2004; Kay et al. 2004; Davidson 2005), while others are extending the stoichiometric
approach to include trace metals (Quigg et al. 2003; Baines
et al. 2004; Sterner et al. 2004; Twining et al. 2004). Indeed,
the concept of a “metallome” (the entire suite of metals
used by an organism) has been proposed by the biological
chemist R. J. P. Williams (see Williams 2001), while recent
progress has been made in developing high-throughput
systems for screening of organisms for genetic variations
in multielement profiles (Lahner et al. 2003). Connecting
these approaches to their evolutionary ecology context represents an important new frontier.
This article has also emphasized the application of stoichiometric perspectives to animal ecology and evolution,
but it is important to note that stoichiometric analysis has
long been at least an implicit part of algal and plant ecology
(Chapin 1980; Rhee and Gotham 1980; Vitousek 1982),
and this work with plants and algae is increasingly being
applied within an evolutionary framework (Quigg et al.
2003; Reich et al. 2003; Klausmeier et al. 2004; McGroddy
et al. 2004; Niklas 2006). Space precludes a discussion of
these important studies, which the reader should consult
to see how stoichiometric reasoning is generalized to other
elements and diverse biota.
The Future of Biological Integration: Finding Needles
in an Age of Haystack Building
Making a fundamental biological discovery can be likened
to finding a needle in a haystack, given the bewildering
array of species and species interactions that confront ecologists and evolutionary biologists and the challenge of
connecting those interactions to their functional genetic
and biochemical underpinnings. Thus, it is somewhat
alarming as a biologist to realize that, during the past
decade or so, the haystack (e.g., the contents of GenBank)
has been growing at an exponential rate following the
advent of high-throughput sequencing technologies and
other tools of the expanding “omics” industries. Thus, it
is reasonable to wonder whether the challenge of biological
integration can ever be met in the face of the exploding
empirical base, since no one has yet invented a highthroughput machine for production and testing of fundamental concepts and hypotheses. Whether or not such
a machine might be devised, perhaps a more reasonable
hope is that the development of theory, in the form of
both clear conceptual frameworks and quantitative mathematical formulations, may at least provide some tools to
cope with the exponential haystack. However, biologists
of all types have a long history of healthy skepticism about
Biological Stoichiometry
whether comprehensive theoretical frameworks are possible for biology, and often the application of formal mathematical analyses has been beyond the scope of most biologists’ normal working routine. This may also be
changing. For example, Gatenby and Maini (2003) have
recently argued that there is an increasing need for the
development and application of mathematical tools in cancer biology, while Cohen (2004) has gone as far as to say
that “mathematics is biology’s next microscope, only better; biology is mathematics’ next physics, only better.”
Is there any evidence that theoretical advances will be
able to help biologists cope with the rapidly expanding
empirical base emerging from the “omics” industries? In
particular, is there any sign that explicit integration of
different types of biological knowledge is being sought by
life science researchers? To address these questions, I queried WOS for the relative frequency of articles referring
to theory and integration in a biological context. Specifically, I quantified the annual number of citations derived
from a search for “biology” and “theory” (B ⫹ T) relative
to the total number of “biology” citations (to correct for
the overall growth of the literature). Thus, an annual theory index (TI) was calculated as (B ⫹ T)/B. I estimated a
similar integration index (II) by comparing the number
of citations yielded from “biology” and “integration” relative to the “biology” total. These indices show some interesting temporal trends (fig. 2) that need to be considered separately for the periods before and after 1991 (when
WOS added abstracts to their records). First, TI values
were low and erratic before 1975 (fig. 2a) but showed a
strong decline from 1975 to 1989 (P ! .001), suggesting a
declining interest in theoretical biology during this period;
meanwhile, II was low, often 0, and with no obvious trend
(fig. 2b). However, both TI and II increased dramatically
after 1990 (a reflection of the fact that abstracts were added
after 1990, thus yielding a greater likelihood of finding the
sought-after combination). More importantly, both TI and
II increased strongly from 1991 to the present (P ! .02 and
P ! .001, respectively). Thus, the previous trend of low
and declining intersection of biology and theory during
the 1970s–1990s has apparently reversed, and biologists
seem to be becoming more interested in theory in recent
years. Furthermore, they may also be more interested in
a type of theory that is capable of achieving biological
integration of various sorts. This growing interest is timely,
given the magnitude of the challenges facing biology in
connecting the expanding repository of genomic and
genome-driven information to the increasingly important
discipline of ecosystem ecology as human society seeks to
cope with the large-scale impacts of its activities on the
global environment.
In this article, I have suggested that biological stoichiometry, by providing an explicit conceptual framework to
S31
Figure 2: a, Temporal trends in the theory index (TI; the relative citation
frequencies of articles in the general scientific literature identified in WOS
using the combined search “biology” and “theory,” relative to the number
found using “biology” alone). b, As for a, but for the integration index
(II; the relative citation frequencies of articles in the general scientific
literature identified in WOS using the combined search “biology” and
“integration,” relative to the number found using “biology” alone). In
both a and b, different Y-axes apply to the periods before and after 1990,
when WOS added abstracts to its data records. Lines were fit to temporal
trends in the two indices after 1990 and to TI for the period 1973–1989.
translate major evolutionary phenomena into currencies
of interest to ecosystem ecologists (and vice versa), provides a clear means of integrating evolutionary and ecosystem perspectives. Furthermore, the processes of stoichiometric mass balance lend themselves easily to
mathematical formulations, and thus the concepts of biological stoichiometry are readily formalized into tractable
mathematical formulations (see, e.g., Grover 1997; Loladze
et al. 2000; Klausmeier et al. 2004). Thus, stoichiometric
approaches seem well suited to be part of the twenty-first
century theoretical tool kit needed to achieve an integrated
understanding of living systems that extends from the genome to the biosphere. This quantitative integration is
possible because chemical elements are incorporated into
organisms by mechanisms operating at the molecular level
but are supplied to organisms via processes that operate
S32 The American Naturalist
at the ecosystem level. Thus, a stoichiometric thread provides vertical integration across levels of organization in
biology. Furthermore, because of their shared evolutionary
history, all living things rely on the same set of major
chemical elements to build their biomass and execute core
metabolic processes. Thus, a stoichiometric perspective
provides horizontal integration, making it easier to make
comparisons across diverse taxonomic groups and breaking down barriers often set by one’s choice of model organism. Finally, the physiological and ecological processing
of this shared set of chemical elements takes place in a
fundamentally similar manner no matter what particular
type of habitat is of interest (ocean, river, lake, desert,
rainforest, etc.), thus providing an additional means of
horizontal integration in which another set of intellectual
“silos” can be breached. In this way, biological stoichiometry represents “[an]other broad biological principle”
that can contribute to the conceptual unification of the
biological sciences, the long-sought goal of the American
Society of Naturalists.
Acknowledgments
I thank M. McPeek for the opportunity to share these
ideas via the ASN Vice-President’s symposium and via this
article. Work from my laboratory reviewed in this article
was supported by various grants from the National Science
Foundation, the National Institutes of Health, and the
National Aeronautics and Space Administration. I am
grateful to J. P. Collins, M. Kyle, and two anonymous
reviewers for helpful comments on the manuscript.
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Symposium Editor: Mark A. McPeek