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AMER. ZOOL., 26:5-22 (1986)
A Consumer-Resource Approach to Community Structure1
DAVID TILMAN
Department of Ecology and Behavioral Biology, 318 Church St. S.E., University of Minnesota,
Minneapolis, Minnesota 55455
SYNOPSIS. Because all species are consumers and all, eventually, are consumed by other
species, consumer-resource interaction is one of the most fundamental processes of ecology. Simple models that include the direct mechanisms of consumer-resource interactions
may thus be the fundamental building-block for models of community structure. These
models are easily extended to include such complexity as the effects of physical limiting
factors, spatial heterogeneity in resource supply, fluctuating resource supply, and multiple
trophic levels. Each such modification places constraints on the traits of species that can
persist. Consumer-resource models make predictions about many aspects of community
structure, including species richness, species composition, species dominance, population
dynamics, morphological or physiological traits of species, and patterns of phenotypic
variation within species. Thus, each model affords numerous opportunities to test and
modify or reject it. A review of a variety of communities suggests that much of the structure
of each community can be explained by a relatively simple consumer-resource model, but
that different elements of complexity may be important in different communities.
many of the details of the biology of particular
species in particular habitats are
The biosphere contains over a million
described species, and possibly another probably peculiar to those species. Howmillion species yet to be described. Any ever, the similar patterns observed among
given community may contain hundreds of communities suggest that there may be a
species, each interacting with at least sev- few major underlying factors or processes
eral other species and an often variable that constrain many communities (Macabiotic environment. Amid this complex- Arthur, 1972; Lawton, 1984). Such patity, ecologists have found what seem to be terns in the species composition, species
repeatable patterns in species diversity (e.g., dominance and diversity of communities,
Pianka, 1966; MacArthur and Wilson, and in the morphology of dominant species
1967; Connell, 1978; Grime, 1979; Hus- in communities are often called, simply,
ton, 1979; Tilman, 1982; Abramsky and community structure. There has been conRosenzweig, 1984; Shmida etal, 1984), in siderable debate as to how strong such patspecies dominance (Preston, 1948; Whit- terns in community structure are and
taker, 1977; Sugihara, 1980), in species whether there are a few major constraincomposition on gradients (e.g., Pigott and ing factors or processes (e.g., Connor and
Taylor, 1964; Zedler and Zedler, 1969; Simberloff, 1979; SimberlofF and Connor,
MacArthur, 1972; Whittaker and Niering, 1979, 1981; Strong, 1980; and numerous
1975; Tilman, 1982, 1986), in life histories papers in Strong et al., 1984). I do not wish
(Grime, 1979), and in the functional roles to enter this debate. Rather, I would like
and morphology of unrelated species living to explore a theoretical, mechanistic
in physically similar but geographically approach that may provide some insights
separated habitats (Mooney, 1977; Cody in explaining those patterns that are found
and Mooney, 1978; Orians and Paine, to be robust.
1983). Because of the complexity of natThere are two main types of constraints
ural communities and the uniqueness of placed on organisms: those from their
the evolutionary history of each species, physical environment and those from their
biotic environment. The reproductive and
mortality rates of a population are influenced by many aspects of the physical envi1
From the Symposium on Mechanistic Approaches to ronment, such as temperature, humidity
the Study ofNatural Communities presented at the Annual
Meeting of the American Society of Zoologists, 2 7 - and topography. Such physical factors can
be thought of as limiting factors for each
30 December 1983, at Philadelphia, Pennsylvania.
INTRODUCTION
DAVID TILMAN
species (Levin, 1970; Levins, 1979). Additionally, each population exists in a network of other species. Within this network,
all species are consumers and all, eventually, are consumed. The items which a
species consumes are called its resources.
That the consumer-resource interaction is
the central biotic interaction is illustrated
by any diagram of a food web. In a food
web, there are two distinct types of links:
consumer-resource interactions and the
various processes that supply the abiotic
resources required by plants. Thus, each
species is constrained by the availability of
its resources, by the dependence of its
growth rate on resource availability, by the
rate at which it is consumed by other
species, and by various physical limiting
factors. The effects of physical limiting factors can often be incorporated by considering how they influence consumerresource interactions and resource supply.
There is no a priori reason to believe that
any one of these constraints is more or less
important than another. However, for a
given community, one or a few constraints
may be of overriding importance in determining particular characteristics of that
community. If this were so, we would be
able to simplify our initial approach by
ignoring all but these constraints. Thus, we
might have reason to believe that the
species richness and species composition of
a desert plant community is most greatly
influenced by water availability, and choose,
initially, to ignore plant-herbivore interactions. Or, we may believe that the species
composition of a foliage-feeding insect
community is most influenced by predation, and ignore the interactions among
herbivores and plants.
As recent work on "indirect effects" has
illustrated, all such simplifications are
potentially dangerous (Levine, 1976; Holt,
1977; Lynch, 1978; Lawlor, 1979; Vandermeer, 1980; Tilman, 1983). What we
need to do, for any given community, is
find a minimum subset of explanatory factors. One way to find such a minimum subset, given the complexity of nature, would
be to use a stepwise criterion for inclusion.
Starting with a simple mechanisticallybased theory, it would be possible to build
a more complete theory by adding only
those factors that explained a significant
additional portion of the patterns observed.
If the initial theory were based on consumer-resource interactions, this would
yield a minimum subset of the food web
interactions, and would include the important direct and indirect interactions.
In that spirit, I will outline a theoretical
approach to community structure by starting with a highly idealized consumerresource interaction and adding other elements to it one at a time. The most basic
element of the food web is the consumerresource interaction. I will start by considering a two-trophic level system (i.e., a
resource level and a consumer level) that
goes to equilibrium in a spatially and temporally uniform environment. Next I will
discuss how this system is altered by adding
spatially variable resource supply rates, or
a physical factor, or another trophic level,
or temporally varying resources. For each
of these alternatives, I will suggest some
communities that may be adequately
described by it and will discuss the constraints placed on community structure by
each form of the model.
If a particular model successfully explains
one aspect of community structure, such
as patterns in species diversity, but does not
explain another aspect, such as patterns in
life histories, I would suspect that the model
is incomplete or wrong. There are numerous elements in the patterns we observe in
nature. A robust ecological theory should
be able to explain many different types of
patterns simultaneously. At this stage in
our efforts, it may be more productive to
try to test our theories not by seeing how
much more of one particular type of pattern each theory can explain, but by applying each theory to a host of different types
of patterns. Thus, once the ability of a theory to predict species diversity patterns has
been tested, for instance, it may be best to
test it next against its predictions as to which
species should be dominant, or against its
predictions about life history and morphological variations both within and among
species. Although I focus this paper mostly
on patterns in species diversity, actual tests
of the applicability of the consumer-
COMMUNITY STRUCTURE: CONSUMER-RESOURCE APPROACH
resource approach, or any other approach,
should test theory against all aspects of
community structure.
The viewpoint presented in this paper
differs from what I perceive to be the frequent tendency for ecologists to believe that
only one type of interaction will be important in a given situation. For instance, there
have been many debates over whether it is
competition or predation that is important
in a given system. Although simplification
is a necessary starting point for research,
dichotomous logic should not be applied
to what are, in reality, continuous processes. The presence of a predator, for
instance, can modify the outcome of the
interactions between two competitors, but
it does not eliminate their competitive
interaction. It is very possible for the structure of a community to be determined by
the interplay of competition and predation.
There are, though, some regions in which
a single species comprises the vast majority
of the biomass on a trophic level. As a first
approximation, might these tend to meet
the criteria given above for monocultures?
Highly productive marine estuaries often
have large expanses dominated by a single
species of salt grass, such as Spartina alterniflora. In such monospecific stands, physical disturbances, which uproot sections of
salt grass, are rare. For a Georgia salt marsh
(Teal, 1962), the major species feeding on
Spartina were a grasshopper and a plant
hopper, which, in total, consumed about
7% of the annual production, a rather
insignificant amount. Nitrogen may be the
main limiting resource for the Spartina
(Gallagher, 1975; Chalmers, 1979; Hopkinson and Schubauer, 1984). All other
species, which are shorter than the dominant Spartina, are probably light limited
because of the dense shade cast by Spartina.
Thus, as a first approximation, the monoTwo TROPHIC LEVELS: SPATIAL AND
specific portions of some salt marshes may
TEMPORAL HOMOGENEITY
be considered to be equilibrium stands limited by a single resource with an insignifiOne limiting resource
'
For an equilibrium community with two cant third trophic level. In order to explain
trophic levels and a single limiting resource the coexistence of other plant species with
in a physically uniform habitat, theory pre- the dominant, or the observed zonation in
dicts that the one species with the lowest salt marshes, it would be necessary to relax
equilibrial requirement for the limiting at least one of these assumptions.
resource, termed R*, should competitively
Fresh water marshes are another highly
displace all other species (Fig. 1; O'Brien, productive habitat in which all species, with
1974; Hsu et ai, 1977;Tilman, 1977, 1982; the possible exception of the dominant
Armstrong and McGehee, 1980). The species, are likely to be limited by the same
mechanism of this displacement is resource resource, light. In many marshes in which
consumption. There will be increases in herbivory is of minor importance and
the population density of the species with physical disturbances are rare, there are
the lowest equilibrial requirement for the large expanses dominated by a single
limiting resource, such as species A in Fig- species of cattail, Typha latifolia. Many other
ure 1A and B, until it reduces the single areas in which there are almost monospelimiting resource down to RA*. At RA*, the cific stands of plants tend to be highly proreproductive rate of species B is less than ductive, such as the coastal stands of redits mortality rate. Thus, if a community has woods in California, the coastal douglas fir
one limiting resource, two trophic levels stands of Washington, marine kelp forests
{i.e., lacks a significant trophic level preying (Mann, 1973; Reed and Foster, 1984), and
on the consumer species), a physically uni- sedge meadows (Bernard, 1974). Even in
form habitat and goes to equilibrium, we the diverse tropics, some of the least diverse
would expect there to be but a single con- forests occur on the most productive soils
sumer species, i.e., to be a monoculture.
(Huston, 1980). Even when there is only a
I know of no natural communities which single limiting resource, monocultures are
meet all these assumptions and thus should predicted by theory only if herbivores are
have a single species on the consumer level. absent and the systems are undisturbed.
DAVID TILMAN
A. Resource Growth Curves
B. Dynamics
100
1.2-
C. Competition: Temperature Gradient
\
1 /
1/
\
a:
\
\
A
A
/ \/
B
D. Competition: pH Gradient
100'
( I - Holcus)
(2-Alopecurus)
( 3 " Arrhenatherum)
V
50/
\
C
Low
/
D
OC
\
E
High
Temperature
4.0
5.0
6.0
Soil pH
7.0
FIG. 1. A. The solid curves labeled A and B are resource dependent growth (reproduction) curves for species
A and species B. The broken line labeled m is the mortality rate, that both species experience. R* is the
environmental concentration of the resource at which reproduction equals death. RA* is the amount of the
resource required for the survival of species A in this habitat. RB* is the resource level required for survival
of species B. Figure from Tilman (1982). B. When the two species of part A compete for this single limiting
resource, the species with the lower R*, species A, competitively displaces species B. The mechanism of
displacement is resource consumption. The population density of species A can increase until the resource
level is reduced to RA*. At RA*, there is insufficient resource for the survival of species B. The thick lines show
the population densities of species A and B, and the thin line the environmental concentration of the resource
predicted by numerical solution of a Monod model of competition (Tilman, 1982). Figure from Tilman (1982).
C. The equilibrium resource requirement, R*, of 5 different species, labeled A to E, is shown to depend on
temperature. Note that each species is shown to have the lowest R* for a particular range of temperatures.
Theory predicts that species with the lowest R* within a given temperature range should competitively displace
all other species from that range. The temperature ranges in which species A to E are predicted to be dominant
are indicated with broken lines. D. Under experimental conditions in which all species should have been
limited by light availability, the long-term Park Grass fertilization experiments at Rothamsted, England, have
shown that the three dominant species are separated along an experimentally-imposed pH gradient. See
Tilman (1982, p. 170) for more details. This suggests that the competitive ability of these species for light
depends on pH, much as illustrated in part C of this figure. Figure from Tilman (1982).
Reed and Foster (1984) found that marine
kelp forests subject to frequent disturbances and herbivory by sea urchins had a
diverse assemblage of annual algal species
whereas nearby areas with low disturbance
rates and low densities of herbivores were
much less diverse. It would be interesting
to know the extent to which light is the
COMMUNITY STRUCTURE: CONSUMER-RESOURCE APPROACH
major limiting resource in such productive
habitats, in general, and if disturbance and
herbivory are of lesser intensity in monospecific stands than in nearby stands that
are more diverse.
It may be that natural monocultures tend
to have a single limiting resource, have low
densities of herbivores and low disturbance
rates, as the simple theory presented here
suggests. This hypothesis can be tested only
through experimental manipulations.
Grassland communities that have been
experimentally fertilized have dramatic
decreases in species richness (Tilman,
1982). Those provided with all nutrients
in excess, such as some regularly mowed
plots from which herbivorous mammals
were excluded in the Rothamsted Park
Grass Experiments in England, have almost
become monocultures after 100 years of
fertilization (Tilman, 1982). In these communities, light likely became the only limiting resource. Theory and such observations suggest that, to the extent to which
a trophic level is not a monoculture, it is
necessary to consider a model more complex than one with a single limiting
resource, two trophic levels, spatial and
temporal homogeneity, and equilibrium.
Two limiting resources
If there were several limiting resources,
but a two-trophic level community was at
equilibrium in a physically-uniform habitat, there could be no more consumer
species than there were limiting resources
(Armstrong and McGehee, 1980; Tilman
1980, 1982). For many animal communities, such an approach may seem able to
explain the coexistence of as many animal
species as are observed. The resources consumed by herbivorous animals are plants.
Several authors (e.g., Grubb, 1977) have
argued that various parts of a plant species
(such as roots, leaves, flowers, fruits, seeds,
and stems) function as distinct resources.
Thus, there would be no conceptual problem with saying that the simple assumptions above could allow several times more
herbivore species than plant species, and
as many predator species as herbivore
species. For many communities, the
observed diversity of herbivorous and predaceous animals may be less than the num-
ber of their resources. Thus, these simple
assumptions could, potentially, explain the
diversity of these trophic levels. Indeed, it
could be asked why there are not more
animal species (Tilman, 1982).
A problem occurs, though, for most plant
communities. Experimental manipulations
of plant resources have shown that there
are from one to at most four or five limiting
plant resources in a given habitat (Tilman,
1982). And yet, these habitats often contain hundreds of plant species. Clearly, to
explain the structure of these plant communities, it will be necessary to invoke one
or more additional factors, such as spatial
heterogeneity, temporal variability or
another trophic level.
Two
TROPHIC LEVELS: SPATIAL
STRUCTURE
Spatial heterogeneity in a physical factor
More complex patterns can occur if there
is a spatially-structured habitat. The spatial
structure can be in either the intensity of
physical limiting factors or in the supply
rates of limiting resources, or both. At
equilibrium, in a physically-structured habitat with one limiting resource and two
trophic levels, it is possible for a potentially
unlimited number of species to coexist if
each species is a superior competitor for
the limiting resource under a particular
physical regime. For instance, if the physical variable is temperature, a species will
be able to exist in a habitat if there is a
microhabitat with a temperature range for
which it has the lowest R* for the limiting
resource of all the competitors. A hypothetical case is illustrated in Figure 1C. An
experimental study of algal competition for
a single limiting resource at various temperatures showed that this simple approach
had reasonably good predictive power (Tilman et al., 1981). Similar diagrams could
be drawn for the dependence of each
species' R* on any other physical limiting
factor.
Consider, for instance, the patterns
shown by three species of parasitic wasps
introduced into commercial orange
orchards in southern California to control
an insect pest, the red scale, Aonidiella
aurantii (DeBach and Sundby, 1963). These
three species of wasps, Aphytis chrysomphali,
10
DAVID TILMAN
A. lingnanensis, and A. melinus, all of which
apparently compete for a common resource, the red scale, were introduced sequentially to southern California. Each
introduction led to a period of rapid competitive displacement. All three wasps still
exist in California, but each occupies a climatically different region. Although other
factors are surely involved, the current distributional patterns of these species suggest that each may be a superior competitor for red scale for a particular range of
physical conditions (perhaps temperature),
much as illustrated in Figure 1C. Consider,
also, the various plots which received complete mineral fertilizer in the Park Grass
Experiments. Because of the great plant
biomass produced in these plots by the high
availability of all mineral nutrients, light is
the most likely limiting resource. The soil
pH of these plots varied depending on
whether or not the plots were limed and
whether they received nitrogen as ammonium or nitrate. Figure 1D shows that the
three most abundant plants in these plots,
Holcus lanatus, Alopecurus pratensis and
Arrhenatherum avenaceum, were each dominant at a different pH. These differences
would be explained if their light requirements {i.e., the R* for light of each species)
depended on pH, with Holcus having the
lowest R* for light at low pH, Alopecurus
having the lowest R* at intermediate pH,
and Arrhenatherum having the lowest R*
for light at highest pH, much as illustrated
in Figure 1C. Thus, if the resource requirements of consumer species depend on the
level of one or more spatially-variable
physical factors, many species can potentially coexist at equilibrium on one limiting
resource. Similarly, seasonal or other regular temporal changes in physical factors
could allow many such species to coexist
stably.
Spatial heterogeneity in resource supply
If there is just one limiting resource, only
one species will be able to exist at equilibrium in a community of immobile consumers with two trophic levels, no matter
how spatially heterogeneous the supply rate
of the resource might be (Tilman, 1982).
This is predicted because, in each micro-
habitat, the population density of the consumer will, at equilibrium, be great enough
to reduce resource levels down to its R*.
The one species with the lowest R* will be
able to displace all competitors from these
microhabitats. As soon as there are two or
more limiting resources, the number of
species that can coexist depends on the
types of resources. Figure 2 shows the various ways that the reproductive rate of a
species may depend on the joint availabilities of two resources (Tilman, 1980). The
curves drawn are resource-dependent
growth isoclines. All environmental availabilities of R, and R2 which fall on one of
these isoclines lead to the same reproductive rate. This rate is the reproductive rate
which exactly balances the mortality rate
experienced by the species in that habitat.
Thus, all availabilities of R, and R2 along
each of these isoclines lead to no net change
in the population density of the consumer.
If resource availabilities were in the shaded
region outside an isocline, the population
size of the species would increase. If resource availabilities were in the unshaded
region inside an isocline, the population
size would decrease because reproductive
rate would be less than mortality rate.
Most of the resources consumed by plants
are essential. Plants require 20 or so different mineral elements (N, P, K, Ca, Mg,
etc.), water and light. A plant cannot
decrease its need for one of these essential
resources by having more of another. Thus,
the long-term reproductive rate of a plant
(sensu Hubbell and Werner, 1979) is determined by the one resource in lowest availability relative to need, and is independent
of the availability of all other non-limiting
resources. Essential resources give isoclines with right-angle corners (Fig. 2A).
Some resources, such as the pollen collected by pollinators, are complete foods
nutritionally, but the need for pollen as a
food source can be decreased by such
energy-rich but protein-poor foods as nectar. Such resources are called hemi-essential (Fig. 2B). Most of the foods eaten by
animals, because they are parts of other
living organisms, are nutritionally complete, and thus can be substituted for each
other. They may be perfectly substitutable
COMMUNITY STRUCTURE: CONSUMER-RESOURCE APPROACH
11
for each other, giving straight-line isoA. Essential
B. Hemi-essential
clines (Fig. 2C), or complementary, giving
isoclines which bow inward (Fig. 2D), or
antagonistic, giving outward-bowing isoclines (Fig. 2E), or switching, giving outward-facing right-angle-corner isoclines
(Fig. 2F). Many herbivores are specialized
on one or a few host plant species, and tend
to switch from one resource to another,
consuming the one resource that leads to
1 °
1
the greatest reproductive rate. I call
D. Complementary
C.
Substitutable
resources that are consumed in a switching
manner "switching resources." Indeed,
optimal foraging theory (Rapport, 1971;
Covich, 1972) predicts that for nutritionally substitutable resources, consumers
should show switching behavior in two of
the three general cases (Tilman, 1982).
The isoclines of Figure 2 can be used to
predict the outcome of competition for
various types of limiting resources. Let us
E. Antagonistic
F. Switching
first consider two plant species competing
for two essential resources. If the isoclines
cross, as shown in Figure 3A, the point at
which they cross is the environmental concentration (or availability) of the two
resources for which both species could exist
in a habitat. At this point, species A of
Figure 3A is limited by R2 and species B is
limited by R,. The coexistence would be
R« or S
r S.
stable if each species consumed relatively
more of the resource that limited it at equi- FIG. 2. The solid curves show the environmental
librium. Optimal foraging theory (Tilman, concentrations of resources 1 and 2 for which the
1982) predicts that a plant should consume reproductive rate of a population just balances its
rate, for various types of resources. R, and
two essential resources in the proportion mortality
R, are environmental availabilities of resources 1 and
in which the plant is equally limited by the 2. S, and S2 are supply points for the resources. If a
resources. Such optimal foraging, assumed habitat has resource availabilities that fall in the shaded
in Figure 3A and B, causes the two-species region outside this isocline, population size of the
equilibrium points to be locally stable (Til- consumer species should increase. In the unshaded
region inside the isocline, population size should
man, 1980). These consumption rates decrease.
The shapes of the isoclines shown define 6
define the types of habitats in which both different types of resources.
species can coexist or one species competitively displaces the other (Fig. 3A).
In Figure 3, R, and R2 are the environ- should be used. Every possible resource
mental availabilities of resources 1 and 2. supply point can be associated with (mapped
Si and S2 are the maximal amounts of all into) a particular equilibrium outcome of
forms of resources 1 and 2 in the habitat, competition. Assuming that mortality rates
and are used to define the rate of supply are constant from one habitat to the next,
of each resource (Tilman, 1982). The point each habitat is characterized by its resource
(Si, S2) is called the resource supply point. supply point. For Figure 3A, habitats with
It is an idealization of resource supply that a low rate of supply of R, (i.e., a small value
is useful in graphical theory. For actual for S,) and a high rate of supply of R2 (i.e.,
cases, realistic resource supply functions a large S2) will be dominated by species A,
R
r
S
12
DAVID TILMAN
A.
I
A
c.
B
wins
A wins
A & B Coexist
CM
CO
A & B coexist
CM
CO
L-
o
CM
CM
CE
i
or
u
A
wins
or
D.
A & B Coexist
A
wins
or S-|
R1 or
FIG. 3. A. The thin, solid lines with right-angle corners are resource-dependent growth isoclines for species
A and B (see Fig. 2). The point at which these isoclines cross, indicated by a dot, is a two-species equilibrium
point. The thick, solid lines coming out from this two-species equilibrium point have slopes equal to the ratio
of RS:R, in the diets of species A and B. These lines indicate the resource supply points (S,, S2), for which
these two species can stably coexist. Any habitats with resource supply points in the region of coexistence will
have their environmental availabilities, R, and R,, reduced down to those of the two-species equilibrium point.
B. When four species compete for two essential resources, and have resource isoclines as illustrated, there
are habitats in which various pairs of these species can coexist. If there is point-to-point spatial heterogeneity
in resource supply rates within a habitat, as illustrated by the circle, all four could coexist in this habitat. C.
The solid lines show the resouce-dependent isoclines of species A and B, which are competing for two switching
resources. The two species equilibrium point, shown with a dot, is stable. Species A and B will coexist in
habitats with resource supply points (S,, Ss), in the region indicated. D. However, no more than two species
can coexist when limited by two switching resources, no matter what the traits of the species and no matter
how spatially heterogeneous the habitat may be, as illustrated above. As shown, species A and/or B will
displace all other species, at equilibrium, from all habitats in which R, and R» are limiting.
COMMUNITY STRUCTURE: CONSUMER-RESOURCE APPROACH
with species B driven to extinction. This
occurs because species A and B are both
limited by R1; and species A can reduce Rt
to a level below that required for the survival of species B. In habitats with high
rates of supply of Rt but low rates of supply
of R2, both species will be limited by R2,
and species B will displace species A (Fig.
3A). Species A and B should stably coexist
in habitats which have resource supply
points (Si, S2), in the intermediate region
shown (Fig. 3A). In this region, each species
is limited by a different resource.
For two species to stably coexist when
competing for the same limiting resources,
each species must be a superior competitor
for one resource and an inferior competitor for the other resource, and each species
must consume relatively more of the
resource that limits it at equilibrium. These
requirements can be used to explore the
plausibility of coexistence in various cases.
Consider, for instance, the observed
coexistence of soil bacteria and vascular
plants, both of which require and may be
limited by inorganic nitrogen. The available evidence suggests that bacteria have
much lower requirements (R*) for nitrogen than do any vascular plants (e.g., Goring and Clark, 1948; Paul, 1976; Anderson
etai, 1981; Elliot etai, 1983). How could
vascular plants coexist with bacteria? Bacteria also require reduced carbon (organic
matter) as an essential resource. If bacteria
are relatively more limited by organic matter and vascular plants by nitrogen or some
other resource, their coexistence could be
explained. Indeed, consistent with this
view, the addition to soils of non-nitrogenous organic matter or organic matter with
very high carbon:nitrogen ratios, such as
straw, greatly increases bacterial biomass
(Behera and Wagner, 1974; Elliot et al,
1983) and reduces vascular plant growth
(Biederbeck, 1980; Persson, 1980; Parton
etai., 1983), presumably because bacteria,
no longer limited by organic matter, reduce
available nitrogen to levels below that
required by the vascular plants. A similar
pattern may explain the coexistence of heterotrophic bacteria and algae in the plankton of lakes. Both require phosphorus, but
13
only bacteria require organic compounds
for their growth. Bacteria have much lower
requirements for phosphorus than algae
(Currie and Kalff, 1984a, b), but are limited by organic matter (Rhee, 1972; Mayfield and Innis, 1978; Meffert and Overbeck, 1979; Cole, 1982; Currie and Kalff,
1984a, b). Diagrams such as Figure 3A and
B, and the associated differential equations
could be used to model these cases.
If more than two species were to compete for two essential resources (Fig. 3B),
their requirements could define habitats in
which various pairs of species could coexist. If there were spatial heterogeneity in
the supply rates of the limiting resources
within a region, it would be possible for
many more than two species to coexist on
two limiting resources. For instance, the
circle shown in Figure 3B could represent
the range of point to point spatial variation
in the supply rates of limiting resources in
a habitat (Tilman, 1982). Such spatial variation in the resource supply points would
allow all four species to coexist in this habitat. Indeed, there is no simple limit to the
number of plant species that can potentially coexist on two essential resources in
a spatially heterogeneous habitat (Tilman,
1982).
In contrast, for animals competing for
switching resources, the number of species
that can coexist in a spatially heterogeneous habitat can be no greater than the
number of switching resources (Tilman,
1982). Consider, first, two species competing for switching resources (Fig. 3C). The
equilibrium point is locally stable, allowing
these two animal species to coexist much
as do the two plants of Figure 3A. However, no matter how isoclines may be drawn
for cases with many species competing for
two switching resources (Fig. 3D), there is
only one stable two-species equilibrium
point. This equilibrium point is shown with
a dot in Figure 3D. The points at which
the other isoclines cross are not stable equilibrium points because they are further
from the origin than the stable point.
Species A and B will be able to continue
growing until they reduce resource levels
down to their two-species equilibrium
14
DAVID TILMAN
point, at which point there are insufficient
resources for the survival of species C and
D. Thus, in either a spatially homogeneous
or spatially heterogeneous habitat, only two
species can coexist on two switching
resources (Fig. 3D). Similar arguments can
be made for antagonistic resources. However, for all other types of resources, spatial heterogeneity can allow many more
species to coexist than there are limiting
resources. Thus, for plants, spatial heterogeneity in the supply rates of limiting
resources may be a very important factor
in determining the diversity of a community. For animals, which are motile consumers, spatial heterogeneity can cause
them to switch from one resource to
another. Switching, though, means that no
more animals can coexist than there are
limiting resources, no matter how spatially
heterogeneous the habitat may be. If many
animal species respond to their resources
by switching, spatial heterogeneity may be
less important in allowing many animals to
coexist than it may be for plants (Tilman,
1982).
Two
TROPHIC LEVELS: TEMPORAL
VARIABILITY
Many processes do not go to equilibrium.
Even for the simple case of a physically
homogeneous habitat with one limiting
resource and two trophic levels, the longterm pattern in dynamically-changing
communities can differ markedly from that
in otherwise comparable communities that
go to equilibrium. Armstrong and McGehee(1976a, b, 1980)and Levins(1979)have
demonstrated that several species can stably persist on a single limiting resource if
resource levels fluctuate. A qualitative
insight into the processes involved may be
gained from Figure 4. (For more details,
see Tilman, 1982, pp. 237-243.) If resource
levels fluctuate, the growth rate of a species
can depend both on the average availability of the resource and the variance in
resource availability through time. Some
species, such as species B in Figure 4A and
B, can exploit variance in resource supply
by having the gain in their reproductive
rate when resource levels go above the
mean be greater than the loss when levels
fall below the mean. For species B, temporal variance in resource supply functions, in a sense, as another resource. For
species A, which has a linear dependence
of its growth rate on resource levels, fluctuations in resource levels around the mean
do not influence its mean reproductive rate.
This is because its decrease in growth when
resource levels fall is exactly balanced by
its increase when resource levels rise. Thus,
species A responds only to average availability. For other species (not illustrated),
fluctuating resources could act as a limiting
factor (Tilman, 1982). As shown by Armstrong and McGehee (1980), these two
species can coexist on one fluctuating
resource because species A is relatively
more limited by the average availability and
species B is relatively more limited by the
variance in resource availability (Fig. 4B).
Armstrong and McGehee (1980) suggest
that, in theory, an unlimited number of
species could coexist on a few limiting but
fluctuating resources as long as the species
have the appropriate differences in their
growth responses to average resource
availabilities versus variance.
There are many habitats in which there
are continual fluctuations in the availabilities of the limiting resources. If these represent small fluctuations around the mean,
it is likely that the dominant species will be
those that are the best competitors for the
limiting resources in the absence of fluctuations. If the fluctuations are large relative to the mean, it is possible for the
species that exploit variance (or are least
limited by variance) to be the dominants.
However, whatever their magnitude, such
fluctuations could explain the long-term
persistence of many more species than there
were limiting resources. It may be that the
high diversity of many planktonic algal
communities and terrestrial plant communities can be explained by such dynamic
processes, with many species persisting in
a habitat by exploiting resource fluctuations.
An experimental study of the effects of
periodic nutrient pulses on the diversity of
algal communities grown in chemostats
revealed that 5 to 7 species persisted in the
periodically perturbed chemostats (Som-
COMMUNITY STRUCTURE: CONSUMER-RESOURCE APPROACH
A. Growth Curves
15
B. Resource Isoclines
Species B
09
rr
*
o
O
R, Resource Average
FIG. 4. A. The solid curves are resource-dependent growth (reproduction) curves for species A and B. The
broken curve shows the mortality rate, m experienced by each species. Note that species A has a lower R*
for this resource than does species B. B. Species A and B of part A above will respond differently to resource
fluctuations. Because of its linear response to resource levels, the growth rate of species A will be determined
by the average resource availability, and will be unaffected by fluctuations. In contrast, at a low average
availability of the resource, the growth rate of species B will increase with fluctuations because of the initial
exponential increase in its growth rate with resource level at low resource levels. Thus, species B requires
less resource, on average, to survive in a fluctuating habitat than to survive in a constant habitat. This could
allow the species to stably persist in a fluctuating habitat, as illustrated. The solid lines in this figure are
resource-dependent growth isoclines, and the dotted lines show the potential region of coexistence.
mer, 1984), but that only 1 to 3 species
coexisted in the equilibrium chemostats
(Sommer, 1983, 1984). The results of the
equilibrium chemostat experiments are
consistent with the predictions of the equilibrium theory of consumer-resource
interaction illustrated in Figure 3B (Sommer, 1983), as are the results of numerous
other studies of algal nutrient competition
in equilibrium chemostats (Tilman et al.,
1982). One of the most notable examples
of such dynamic coexistence may be deserts, in which one of the main limiting
resources, water, has extremely high
unpredictability. Different plant species
may be able to specialize on rainfall events
of different magnitudes or frequencies, and
thus there is the theoretical potential for
many species to coexist on this one
resource. There are other limiting resources in deserts, especially soil nitrogen
(Power, 1980), that may help explain
coexistence. In the deserts of the southwest
United States, long-lived plants such as
creosote and mesquite may be mainly
exploiting seasonal average rainfall patterns whereas the numerous species of
annual plants may be exploiting temporal
variance in rainfall. In theory, at least, it
is possible for each species to be a superior
competitor at a particular point along the
continuum from exploiting only the average rainfall to exploiting only the variance.
THREE TROPHIC LEVELS
Let us go back to the simplest two-trophic
level model and modify it by adding a third
trophic level. What kind of structure could
an equilibrial, spatially homogeneous community have if it had three trophic levels and a single limiting resource? Consider a food web with a resource level, a
consumer, and a top consumer (predator)
level. An extension of the ideas developed
by Levin et al. (1977) shows that there is
no limit to the number of species that can
potentially coexist in such a community if
the consumer which is the superior competitor for the limiting resource in the
absence of predation is the most suscepti-
16
DAVID TILMAN
ble to predation, the consumer which is the
next best resource competitor is the next
most susceptible to predation, and so on
(Tilman, 1982). This comes from two inequalities. If the number of resource types
is R, the number of primary consumer
species is C, and the number of top consumer (predator) species is T, theory predicts that the number of top consumer
species must be less than or equal to the
number of consumer species (their prey).
The number of consumer species must be
less than or equal to the sum of the number
of their resources and the number of top
consumer species (their predator) (Tilman,
1982). Thus,
C< R+ T
and
T < C.
One resource could support one consumer, which could support one top consumer. However, with one resource and
one top consumer, two consumers could
coexist. With two consumers, there could
be two top consumers. Two top consumers
and a resource, though, could allow three
consumers to coexist. This process could
go on indefinitely, as long as the top consumers and consumers had the appropriate
traits (Tilman, 1982).
The experimental studies of Paine (1966)
on an intertidal invertebrate community
showed that species richness was highly
dependent on the presence of a top predator, the starfish Pisaster, which preyed
preferentially on the species that were the
best competitors for open space, a major
limiting resource. The rocky intertidal
community studied by Paine thus had three
trophic levels: a limiting resource, space;
sessile, filter-feeding invertebrates; and a
predator on the sessile invertebrates. When
Paine removed starfish from an area, the
species richness of the second trophic level
fell from about 15 to about 8. Lubchenco
(1978) also studied a three-trophic level,
intertidal system. For the macrophytic algae
of tide pools, light and nutrients were
probably major limiting resources. The
algae were fed upon by an herbivorous
snail, Littorina littorea. Lubchenco found
that the species richness of the algal community was highest at intermediate snail
densities. The snail was found to feed preferentially on the algae which were the best
competitors in the absence of herbivory.
Both of these studies show that the structure of the middle trophic level can be
greatly influenced by the action of species
on a third trophic level. Qualitatively, these
studies seem to be similar to predictions
made by a simple model of a three-trophic
level system. When the effect of the third
trophic level was minimal, as when Pisaster
or Littorina was in low abundance, species
diversity was low, as would be expected for
a simple two-trophic level system consisting of one or a few limiting resources and
some consumer species. Comparably, when
Littorina was in very high density, the interactions between the macrophytic algae and
their limiting resources may have been relatively unimportant, and the system might
have approximated a two-trophic level system, with the original resource level no
longer important. At intermediate densities of Littorina, all three trophic levels
would have been important.
Several recent discussions of food webs
suggest that there is constancy in the structure of food webs, independent of the type
of habitat or the equilibrium or non-equilibrium nature of the habitat (Cohen 1978;
Briand and Cohen, 1984). This constancy,
first expressed as there being a constant
ratio of prey to predators in food webs, is
now thought to result from there being a
constant proportion of the species on the
first, second and third trophic levels. For
a three trophic level system, the inequalities above state that the number of consumer species must be less than or equal
to the sum of the number of resources and
predators. The data in Briand and Cohen
(1984), though only expressed on a percent
basis, are amazingly consistent with this
prediction. Their survey of 62 food webs
showed that the proportion of species in
any given trophic level was independent of
the total number of species in the food
webs. They found that 19% of the species
were on the first level, 52% were on the
second level, and 29% were on the third
level. The sum of 19% and 29% is 48%,
17
COMMUNITY STRUCTURE: CONSUMER-RESOURCE APPROACH
very close to the observed 52% for the middle trophic level. If species were randomly
distributed among the three trophic levels,
33% of the species would be expected to
be on each level. If this were so, the ratio
of the sum of the number of species on the
first and third levels to the number of
species on the second level would be 2.0.
The ratio predicted by the inequalities
above is 1.0. The actual ratio, 0.90, is much
closer to that predicted by theory than to
that expected by chance alone. This is consistent with the hypothesis that a significant
portion of the species diversity of communities may be explained by the interplay
of competition andpredation. However, as
is the case for all such correlational data
sets, there are numerous alternative explanations for these observations.
DIRECT VERSUS INDIRECT EFFECTS
Within the framework of the consumerresource approach, when only two trophic
levels are considered, the interactions
included are simple ones caused directly by
resource consumption. Thus, two consumers, both of which were limited by the
same resources, would functionally behave
as competitors for the limiting resources.
However, as soon as a third trophic level
is added, it is possible for the total effect
of one species on another to be qualitatively different than might be assumed from
their trophic positions. For instance, the
two species in the top consumer level of
Figure 5A always function as competitors
because they are both limited by the same
resources. In contrast, the top consumers
in Figure 5B may function as if they are
competitors or mutualists depending on the
strength of the various links (Levine, 1976;
Lawlor, 1979; Vandermeer, 1980).
This major shift in the functional relations between these top consumer species
is caused by the several pathways whereby
species may affect each other in systems
with at least three trophic levels. Top consumer 1 will affect top consumer 2 (Fig.
5B) directly through consumption of consumers 1 and 2, and indirectly through the
effects of changes in the densities of consumers 1 and 2 on their resource levels. If,
for Figure 5B, top consumer 1 preferen-
A.
i
i
Resource
Resource 2
Consumer I
Consumer 2
Resource
Resource 2
Consumer I
Consumer 2
Top Consumer I
| Top Consumer 21
B.
C.
Resource I
| Resource 2
FIG. 5. Parts A, B and C show increasingly complex
approximations to a food web. All of the links are
either consumer-resource interactions or are resource
supply. For part C, the top consumers may effect each
other "indirectly" in two different ways: through their
effects on the availabilities of resources 1 and 2 or
through effects mediated via the competition of the
consumer species for the resources. It may be that
the process of resource re-supply is as important or
more important than differential consumption in
structuring this community. The appropriate subsection of the food web would directly include the direct
and indirect interactions important in a given community.
18
DAVID TILMAN
tially feeds on consumer 1 and top consumer 2 preferentially feeds on consumer
2, increases in the density of top consumer
1 would lead to decreases in the density of
consumer 1, indirectly providing more
resources for consumer 2, and thus increasing the growth rate of top consumer
2. The comparable process causes increases
in the density of top consumer 2 to increase
the growth rate of top consumer 1. Thus,
the two top consumer species, which are
directly competing for the consumer
species, can function as if they are mutualists (Levine, 1976; Lawlor, 1979; Vandermeer, 1980). Experimental studies by
Lynch (1978) support the ability of such
indirect effects to modify the direct effect
of one species on another. Lynch (1978)
found that two species of herbivorous zooplankton functioned as indirect mutualists
during the time of the season when their
resources, algae, were severely nutrient
limited, but functioned as competitors
when the algae were not as strongly competing for nutrients.
This major, qualitative change, caused
by indirect effects, illustrates how a broader
view of the food web may be needed to
understand community structure. I want
to stress, though, that the "indirect effects"
of one species on another are indirect only
in the sense that they are mediated through
another factor. They are directly included
in a food web, such as Figure 5C. By their
act of consumption, top consumers decrease the density of their prey, and thus
directly influence them. Top consumers
also may directly influence the rate of supply of limiting resources. If the consumers
are plants and the resources are nutrients,
top consumers may supply nutrients
through excretion of wastes which contain
N, P, K, etc. If light is a limiting resource,
a top consumer which ate one plant would
increase the availability of light for other
plants (Tilman, 1983). For Lubchenco's
(1978) study, increased densities of the
herbivorous snail Littorina littorea probably
led to increased availability of light on rock
surfaces. It also probably increased the
point-to-point variance in light availability
on rock surfaces. If light were a limiting
resource in that study, it would be possible
to interpret the effect of Littorina littorea
as being caused by its influence on the rate
of supply and spatial heterogeneity of a
limiting resource, light. In this case,
resource competition theory would predict
a humped diversity curve (Tilman, 1982),
as Lubchenco observed. Similarly, for
invertebrates of the rocky intertidal (Paine,
1966), there is a humped relationship
between species diversity and disturbance,
whether the disturbance is caused by Pisaster predation or wave or log action. All such
disturbances influence the rate of supply
of the limiting resource, space, and thus
are predicted to lead to a humped diversity
curve (Tilman, 1982). Thus, top consumers can have three types of effects on
their prey: a direct effect from their consumption of the prey, indirect effects
mediated through other species that influence their prey, and indirect effects from
the resupply of the resources required by
the prey. The alternative interpretations
of the work by Lubchenco (1978) and Paine
(1966) presented in this paper indicate that
further experimentation will be needed to
determine the relative importance of direct
and indirect pathways in particular systems. Both paths are easily included in a
consumer-resource model with three trohic
levels.
OVERVIEW
The most simplified, idealized food web
has two trophic levels, a spatially homogeneous habitat, and temporal homogeneity. This idealized case can be considered
to be the simplest functional element of
the food web. In such a food web, theory
predicts that the number of consumer
species must be less than or equal to the
number of limiting resources. When any
of the simplifying assumptions of this idealized case are relaxed, theory predicts that
there is no simple limit to the number of
consumer species which could potentially
coexist. Thus, if it is assumed that the habitat has spatial heterogeneity in a physical
limiting factor, or variability in the supply
rate of a limiting resource, or that interspecific interactions do not go to equilibrium, or that there are three trophic levels,
it is possible for a potentially unlimited
COMMUNITY STRUCTURE: CONSUMER-RESOURCE APPROACH
number of species to coexist when competing for a few limiting resources.
However, even given such complexity, it
is possible for more than one species to
coexist on several resources only if the
species have the appropriate traits relative
to each other. For many species to coexist
on one limiting resource in a habitat with
spatial variability in a physical limiting factor, each species must be a superior competitor for that resource for some particular level or range of the physical factor,
and must be an inferior competitor outside
that range. For species to coexist because
of spatial heterogeneity in the supply rates
of two limiting resources, the species must
be inversely ranked in their requirements
for one resource versus the other, and each
species must consume the resources in the
ratio in which it is limited by them. The
tradeoffs required for species to coexist
because of nonequilibrium interactions are
less clear, but available results suggest that
species have to be differentiated in their
ability to compete for the average availability versus the variance in the resource.
For species to coexist because of interactions among three or more trophic levels,
species on intermediate trophic levels must
be inversely ranked in terms of their competitive abilities for resources versus their
susceptibility to predation. In addition, if
any of these mechanisms is operative in a
given community, the pattern of variation
in the traits of individuals within a given
species should also be consistent with the
trends predicted above. For example, if
there is genotypic variation in a plant
species, and if this plant species is coexisting with other plants because it is specialized on a particular proportion of two limiting essential resources, each genotype
should also be specialized on a particular
proportion of the resources such that it can
coexist with the other individuals in its own
and other species.
Each mechanism which could explain a
high diversity community places different
constraints on the traits of the coexisting
species. One way to determine what level
of complexity might be necessary to explain
the structure of a given community would
be to determine the traits of the coexisting
19
species. If the species were observed to have
traits consistent with the constraints
imposed by one of the food web structures
but inconsistent with the others, the other
structures could be rejected as being of
lesser importance. If it seemed that the
traits were partially consistent with several
of the constraints, it could be that several
were operative. In that case, it would be
necessary to determine the predicted relationships between the multiple constraints
which could allow the species to coexist,
and determine if the species had the appropriate suite of characteristics.
In this paper I have presented a greatly
simplified view of some of the factors which
may influence the structure of natural
communities. There are many complicating factors which I have not mentioned.
Among these are the complexities of multiple stable equilibria that may result from
age or size structure in populations (Hassell
and Commins, 1976), coexistence that may
result from differential immigration and
extinction rates in patchy habitats (Levin
and Paine, 1974; Slatkin, 1974; Armstrong, 1976), and patterns caused by
genetic variability within and among
species.
There is little empirical evidence currently available that would support the view
that one or another of the models outlined
in this paper is of general importance or is
always unimportant in natural communities. To some extent, the complexity of
theory required in ecology will reflect the
complexity of the questions being asked. I
would like to suggest, though, that all of
the above models are extensions of the consumer-resource approach to ecology. This
approach, by emphasizing the feeding relations among organisms, incorporates one
of the most basic processes in the biology
of populations. Each species is a consumer
and each, eventually, is consumed. It may
be that much of the structure of natural
communities can be explained by considering greatly simplified subsections of the
food web. In many complex processes, a
few steps often become rate-limiting, and
control of the majority of the observed
dynamics. Perhaps by explicitly studying
the mechanisms of consumer-resource
20
DAVID TILMAN
interactions and using these to build and
test models of food webs, we will be able
to find a minimal subset of the food web
that explains most of the patterns we
observe.
ACKNOWLEDGMENTS
This material is based on work supported by the National Science Foundation
under Grant No. BSR-8114302-A02. I
thank two anonymous reviewers and Mary
Price for their comments on this paper,
and Sue McEachran for help preparing this
manuscript. I also thank the John Simon
Guggenheim Memorial Foundation for
supporting me during part of the time I
prepared this manuscript.
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