Global Change Biology (2005) 11, 490–501, doi: 10.1111/j.1365-2486.2005.00919.

Global change alters the stability of food webs

M A R K E M M E R S O N *, M A R T I J N B E Z E M E R w 1 , M A R K D . H U N T E R z and T . H E F I N J O N E S §
*Department of Zoology, University College Cork, Lee Maltings, Prospect Row, Cork, Ireland, wNetherlands Institute of Ecology
(NIOO-KNAW), PO Box 40, 6666 ZG Heteren, The Netherlands, zInstitute of Ecology, University of Georgia, Ecology Building,
Athens, GA 30602-2202, USA, §Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff, CF10 3TL, UK

Abstract
Recent research has generally shown that a small change in the number of species in a
food web can have consequences both for community structure and ecosystem processes.
However ‘change’ is not limited to just the number of species in a community, but might
include an alteration to such properties as precipitation, nutrient cycling and
temperature. How such changes might affect species interactions is important, not just
through the presence or absence of interactions, but also because the patterning of
interaction strengths among species is intimately associated with community stability.
Interaction strengths encompass such properties as feeding rates and assimilation
efficiencies, and encapsulate functionally important information with regard to
ecosystem processes. Interaction strengths represent the pathways and transfer of
energy through an ecosystem. We review the best empirical data available detailing the
frequency distribution of interaction strengths in communities. We present the
underlying (but consistent) pattern of species interactions and discuss the implications
of this patterning. We then examine how such a basic pattern might be affected given
various scenarios of ‘change’ and discuss the consequences for community stability and
ecosystem functioning.
Keywords: community, ecosystems, food webs, herbivore, persistence, plant, predators, prey, resilience,
stability

Received 9 September 2004; and accepted 15 October 2004

levels and global warming might effect change in species

Introduction
Pioneering early ecologists (for example Odum, 1953;
MacArthur, 1955; Elton, 1958) held that the dynamics of
complex ecological systems should be more stable than
simpler systems. They based this view on the premise
that those ecological systems, which were more species
rich, have more interspecies pathways along which
energy can flow. These pathways can be depicted
graphically as food web diagrams and energy flow
may be characterized by the trophic interactions that
take place among species within the food web. The
biological strength of these trophic interactions details
the conversion of abundance or biomass from one
trophic level to another. In this paper, we will explore
how increased productivity brought about by rising CO2
Correspondence: Mark Emmerson, tel. 1 353 (0)21 490 4190.
fax: 1 353 (0)21 427 0562, e-mail: m.emmerson@ucc.ie
1
Present address: Nature Conservation and Plant Ecology Group,
Wageningen University and Research Centre, Bornsesteeg 69, 6708
PD Wageningen, The Netherlands.
interactions at local scales. This is important because a
disruption to the strength or arrangement of interspecific
interactions in food webs can have consequences for the
stability of those same systems. For instance, in the early
1970s, Rosenzweig (1971) warned against the artificial
enrichment of ecosystems (to increase productivity) in
terms of increased nutrient and energy supply. He
showed that for two trophic-level systems, either
scenario would destroy steady states in simple models.
Throughout this paper, we describe a scenario of global
change (increased productivity) brought about by
coincident global increases in temperature and CO2
concentration. We explore this scenario of change using
a simple three-species food web consisting of a basal
resource (plant), primary consumer (herbivore) and
secondary consumer (omnivorous predator).
Although the study of species interactions has tradi-
tionally been concerned with their effects on community
stability (sensu May, 1973), recent research has focused
more on how ecosystem processes such as productivity,
nutrient flux and nutrient retention are affected by the

490 r 2005 Blackwell Publishing Ltd

 G L O B A L C H A N G E A LT E R S T H E S TA B I L I T Y O F F O O D W E B S
loss of species (Chapin et al., 2000; McCann, 2000; Loreau
et al., 2001; Madritch & Hunter, 2002). The transfer of
energy (or carbon) through an ecosystem represents one
such ecosystem process and interaction strengths provide
a direct link between the diversity and ecosystem
functioning of a community and its ecological stability
(Duffy, 2002). Interaction strengths have been quantified
in a number of ways and this general term has been used
variously to describe both (i) the biological flux of
material or energy from one trophic level to another and
(ii) per-capita effects of a species on the growth rate of
another. In this paper, we will focus on the latter use of
the term interaction strength.
Concerns over increased global rates of species
extinction are driven by the urgent need to understand
and predict the consequences of species loss for the
stable and reliable provision of ecosystem services
(Duarte, 2000; Engelhardt & Ritchie, 2001; Loreau
et al., 2001; Lerdau & Slobodkin, 2002). To understand
how communities might respond locally to global
change (changes in productivity driven by increased
temperature and CO2 concentrations), requires that we
identify the basic arrangement of species interaction
strengths in communities and investigate how one
measure of global change might affect that pattern at
the local ecological scale. To achieve this, we now
review and detail measures of interaction strength, and
present what we consider to be some of the best data
currently available detailing the patterns of interaction
strengths in ecological systems; this is necessary for our
exploration of change. We then define some simple and
biologically reasonable scenarios of ecological change
and explore how the patterning of interaction strengths
might be affected by such changes using a Lotka–
Volterra modelling framework. Our aim in using Lotka–
Volterra dynamics is to make qualitative forecasts
regarding the consequences of change, not to make
quantitative predictions. Our goal is to make a heuristic
exploration of these scenarios using this simple model-
ling approach. Finally, we will discuss the consequences
of ‘change’ for community and ecosystem stability.
What is the pattern of interaction strengths in
communities?
The effects of species’ interactions on community stability
were first explored by May (1973) using linear stability
analyses. May used Lotka–Volterra models of the form:
0 1
dXi Xn
¼ Xi @ri þ aij Xj A; ð1Þ
dt j¼1
where Xi and ri define the population density and
intrinsic rate of increase of species i, to explore the
r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 490–501
491
dynamical behaviour of model communities close to
equilibrium. The interaction between a predator and its
prey is defined by the coefficient aij and represents the
negative per-capita effect of a predator species j on a prey
species i. The negative effects of species i on itself are
denoted aii, while the positive effects of the prey species
i on the predator j are given by aji. A system of such n
linear equations describing the dynamics of a set of
species can be represented in matrix algebra terms so that
the interaction coefficients (aij terms) are the elements of
an n
n matrix (here called A). Using matrix algebra, (1)
above can be rewritten as:
dX
¼ X  ðr þ AXÞ;
dt
where X and r are vectors containing the densities (Xi,n)
and intrinsic rates (ri,n) of those species present in the
community or food web. In fact, May (1973) explored
the stability of these model systems at equilibrium; he
explored the dynamics of a matrix known as the
Jacobian (C) whose elements (cij terms) were the
product of the interaction coefficients contained in A
and an n
n matrix containing the vector of nontrivial
equilibrium population densities (Xi where Xi does not
equal zero) on the diagonal and zeros elsewhere (so
that cij ¼ aij Xi ). Essentially, the Jacobian matrix de-
scribes the dynamics of a community close to an
equilibrium point and details population-level interac-
tions. May (1973) explored randomly constructed
model communities by assigning interaction strengths
(cij) from a uniform distribution to the elements of the
Jacobian (C). He found that in systems with randomly
assigned trophic interactions, an increased species
richness tended to decrease the stability of model
communities. Pimm & Lawton (1977, 1978) investigat-
ing simple model food webs subsequently showed that
the patterning of species interactions (that is the
presence or absence of omnivorous links and therefore
food web structure alone) could have dramatic effects
on the stability of such systems. Yodzis (1981) working
with a compiled set of 40 real, as opposed to model,
food webs found that the arrangement of species
interaction strengths was essential for food web
stability. When the detailed pattern of interaction
strengths in stable food webs was disrupted the
resulting webs were, on average, less stable.
These classic studies using linear stability analyses, all
made use of the Jacobian matrix for the determination of
food web stability (May, 1973; Pimm & Lawton, 1977,
1978; Yodzis, 1981). From these theoretical studies, there
are two quantities that emerge as characterizing the
interactions among species, aij the interaction coefficient
and aij Xi the element of the Jacobian matrix at equili-
brium (it should be noted that the Jacobian exists
492 M . E M M E R S O N et al.
whether a system is at equilibrium or not). The value aij
is a per-capita effect and a constant coefficient of the
model, while aijXi will be dependent on the density of
species i (Xi). The elements of the Jacobian matrix at
equilibrium are the partial derivatives of the growth
equations with respect to each species (dfi/dXj, where
fi 5 dXi/dt and dfi =dXj ¼ cij ¼ aij Xi ), and describe the
dynamic forces acting around the equilibrium point.
The quantity dfi =dXj ¼ aij Xi represents the effect of
species j on the growth rate (fi) of species i at
equilibrium. Any process (whether intrinsic or extrin-
sic) that changes the size of species’ populations will
therefore have quantifiable effects on the elements of
the Jacobian matrix (aijXi terms). This provides a useful
way of exploring how ‘change’ might affect the strength
of trophic interactions. Interaction strength is a generic
term that refers to the interactions that exist among sets
of species and can be measured or quantified in any
number of ways. To avoid confusion we hereafter
explicitly refer to the elements of the matrix A as
interaction coefficients (per-capita effects) and the
elements of the Jacobian matrix (C) as interaction
strengths (population-level effects).
The empirical study of species’ interaction strengths
is not trivial, requiring that a predator or consumer be
removed from a community and the numerical re-
sponse of its prey and predators be quantified.
Empiricists studying the strength of trophic interactions
are logistically constrained in the number of species’
interactions that they can investigate. This constraint is
evident in a number of recent studies that have
quantified the strength of species interactions (Paine,
1992; Fagan & Hurd, 1994; Raffaelli & Hall, 1996;
Wootton, 1997). These studies represent some of the
best empirical data available quantifying interaction
strengths, but because of the small sample sizes, the
authors have resorted to bootstrapping techniques to
obtain a reliable estimate of the variability associated
with interaction strength (Paine, 1992; Wootton, 1997).
A recent review (Berlow et al., 1999) deals comprehen-
sively with the behaviour of different empirical mea-
sures of interaction strength. In this study, we concern
ourselves with a measure of interaction strength known
as the dynamic index or log ratio, which is equivalent to
the interaction coefficient in discrete time versions of the
Lotka–Volterra equation (aij) and describes the per-capita
effects of a predator on its prey (see Berlow et al., 1999
for details). Data from a number of well-known studies
(Paine, 1992; Fagan & Hurd, 1994; Raffaelli & Hall, 1996;
Wootton, 1997) indicate that these indices (which
represent some of the best data currently available) are
skewed strongly towards weak interactions.
De Ruiter et al. (1995) estimated Jacobian elements
using biomass densities rather than density per se, for a
r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 490–501
range of soil food webs that differed in complexity. De
Ruiter et al.’s (1995) formulation of interaction strength
was calculated for both the negative effects of predators
on prey ðaij Xi Þ and the positive effects of prey on
predators ðaij Xi Þ, and was equivalent to the elements of
the Jacobian matrix at equilibrium. The frequency
distributions of these Jacobian elements also show strong
skews towards weak interactions for both positive and
negative predator–prey interaction strengths. The stu-
dies on both interaction coefficients and interaction
strengths present a consistent pattern of predominantly
weak effects in communities, although it should be
noted that some studies report differing patterns
determined by species body size (Sala & Graham, 2002).
Using a nonlinear modelling approach, McCann et al.
(1998) showed that this empirical pattern of weak
interactions could stabilize community dynamics when
typically destabilizing links (for example omnivorous
links) were weak. Neutel et al. (2002) obtained a similar
result using linear stability analyses and showed that
the stability of a food web was intimately associated
with the strength of Jacobian elements in omnivorous
food web loops.
In summary, a considerable body of evidence
indicates that the patterning of interaction strengths is
vital for food web and community stability. Empirical
data show a strong skew towards weak interaction
coefficients and weak Jacobian elements. Theoretical
studies suggest that, within food webs, it is the specific
patterning of weak interactions that promotes food web
stability. How might the patterning of species interac-
tions be affected by predicted changes to the global
biosphere? Would a change to the patterning of species
interaction strengths caused by such predicted changes
be sufficient to cause instabilities in community
dynamics? We next consider a scenario of global change
and examine how this scenario might affect the strength
and patterning of species interactions.
How could global change affect interaction strength?
Productivity is influenced by the interacting effects of
numerous global changes including elevated atmo-
spheric CO2, rising temperatures, altered precipitation
patterns, nitrogen deposition and species loss. Our aim
is to examine (by whatever mechanism) changes in
primary productivity and consequent effects on trophic
interaction strengths. Clearly, taking into account all of
these interacting factors and their effects on productiv-
ity is not possible in the space of this paper. To make
our task somewhat more manageable, we only consider
scenarios of increased global productivity associated
with increasing concentrations of atmospheric CO2.
 G L O B A L C H A N G E A LT E R S T H E S TA B I L I T Y O F F O O D W E B S
Predictions suggest that atmospheric CO2 levels will
rise from around 350–700 ppm by the end of this
century (IPCC, 2001). Associated with this increase in
CO2 levels are: (1) direct effects of atmospheric carbon
on plant photosynthesis and primary production; (2)
increases in average global temperature (global average
surface temperature has already increased by 0.6 1C in
the 20th century, IPCC, 2001), and (3) changing patterns
of precipitation (Aber & Melillo, 2001). Coupled atmo-
sphere–ocean general circulation models provide us
with the best predictions on how patterns of tempera-
ture and precipitation will change as CO2 levels rise
(IPCC, 2001). Most terrestrial regions will experience an
increase in mean annual temperature between 3 and
10 1C whereas rates of precipitation may either decrease
or increase by up to 2 mm day1, depending on region.
To begin integrating these climatic predictions into an
understanding of species interactions, we begin our
analysis with anticipated effects upon primary produc-
tion. Then we will suggest how changes in primary
production might influence the strength of trophic
interactions. Critical to this last step is distinguishing
between changes in the rate of primary production and
changes in the quality of the plant tissue that is
produced. Whether plants react in a qualitative or
quantitative way, or even both, is likely to have very
different effects on species interactions.
Direct effects of CO2 on primary production. It is generally
accepted that photosynthetic rates are limited primarily
by carbon (Drake et al., 1997; Norby et al., 1999; Aber &
Melillo, 2001). Hence, most models predict that net
primary production will increase as atmospheric
concentrations of CO2 increase. Various models
predict changes that range from 0.7% to 1 32.4%
(VEMAP, 1995). Overall, the average predicted increase
in net primary production is around 20%. In many
plant communities, primary production will increase
below ground as well as above ground (Tate & Ross,
1997) and elevated CO2 may increase fine root
production of some forest trees by as much as 96%
(King et al., 2001). For most plant species, increased
rates of primary production are associated with
increases in relative growth rate (Saxe et al., 1998). For
example, in their study of 10 Acacia species, Atkin et al.
(1999) reported that the relative growth rates of Acacia
trees increased by an average of 10% over a 12-week
period under elevated CO2 conditions.
CO2-mediated changes in temperature and precipitation.
While the prediction of increased productivity in
response to rising concentrations of CO2 appears to be a
relatively robust generalization, the effects of concomitant
changes in temperature and precipitation are harder to
r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 490–501
493
predict (Aber & Melillo, 2001). Temperature effects are
particularly difficult to predict because while photo-
synthesis has a bell-shaped response to temperature,
respiration increases exponentially (Larcher, 1995).
Carbon gain relative to loss may therefore decline at
high temperatures, resulting in a decline in production.
The responses of various ecosystems to the
interactive effects of changes in CO2, temperature and
precipitation will depend, in part, on their relative
sensitivities to those environmental factors. Simply put,
an ecosystem whose productivity is limited by
precipitation is more likely to respond to a change in
precipitation than one that is limited by temperature
(Schloss et al., 1999). Broad generalizations that operate
across many different ecosystems therefore, become less
robust as the number of climatic variables considered is
increased. Our ability to make predictions is also limited
because models that include multiple interactive effects
of global change are still relatively rare (Aber & Melillo,
2001). One noteworthy study is that by Yu et al. (2002).
This study incorporates predicted changes in CO2
concentration, precipitation and temperature from
seven general circulation models into predictions of
ecosystem change in a forest transect in east China.
While all seven general circulation models predicted
increases in net primary productivity under elevated
CO2, effects of precipitation were relatively weak
whereas productivity was negatively correlated with
temperature. Broadleaf forests were predicted to
increase while conifer forests, shrubs and grasses were
predicted to decrease. Overall, however, primary
production was still seen to increase under all
scenarios of elevated CO2 (Yu et al., 2002).
Despite Yu et al. (2002) and predictions made from the
bell-shaped relationship between photosynthesis and
temperature (Aber & Melillo, 2001), increases in
temperature under rising CO2 levels may still have an
overall positive impact on net primary production,
particularly if growing seasons are extended. A meta-
analysis of available studies suggests that ecosystem
warming should increase plant productivity by an
average of 19%, with a 95% confidence interval of 15–
23% (Rustad et al., 2001). If true, then the effects of global
warming on productivity may operate in exactly the
same direction as the direct effects of CO2 on
productivity.
Quality vs. quantity. In a food chain context, the
predicted increases in primary production may
appear to favour herbivore populations; however,
many empirical studies suggest that plant quality for
consumers will decline as CO2 levels rise (Bezemer &
Jones, 1998). This will have implications for the strength
of per-capita trophic interactions between a consumer
494 M . E M M E R S O N et al.
and its plant resource. Specifically, the accumulation of
carbon under elevated CO2 dilutes concentrations of
nitrogen in plant tissues by 15–25% (Lincoln et al., 1993;
Lindroth et al., 1995) thereby increasing C : N ratios
(Ceulemans & Mousseau, 1994; Wilsey, 1996; Hughes &
Bazzaz, 1997). Given that nitrogen is considered a
limiting factor for many herbivore species (Mattson,
1980), dilution of nitrogen under elevated CO2 may
place further constraints on the growth rates of
herbivores. In addition, the concentrations of carbon-
rich secondary metabolites sometimes increase under
elevated CO2 (Lindroth et al., 1995; Agrell et al., 2000).
While there appears to be considerable variation in the
responses of plant chemical defences to rising CO2
levels (Hunter, 2001), some classes of tannin, such as
condensed tannins, seem to respond most frequently.
To summarize, in nearly every case examined to date,
foliar nitrogen concentrations decline under elevated
CO2 and, when present, foliar concentrations of
condensed tannins increase (Fajer et al., 1989, 1991;
Johnson & Lincoln, 1991; Lincoln et al., 1993; Lindroth
et al., 1995; Jones & Hartley, 1999).
Herbivores confronted with low-quality plant tissue
would be expected to compensate by eating more. This
prediction usually holds true, particularly for chewing
insects (Lincoln et al., 1984, 1986, 1993; Fajer et al., 1989;
Lindroth et al., 1993, 1995; Salt et al., 1995; Docherty
et al., 1996; Kinney et al., 1997; Williams et al., 1997;
Whittaker, 2000). Likewise, the area damaged by leaf-
mining insects may also increase, for example, the area
of leaf mines on Quercus myrtifolia increase by over 25%
under elevated CO2, apparently because nitrogen
concentrations fall by over 11% (Salt et al., 1995;
Stiling et al., 2003). Nonchewing insects have been less
well studied and in general patterns are yet to emerge.
Bezemer et al. (1998), for example, showed that peach
potato aphid (Myzus persicae) abundance was enhanced
by elevated CO2 and temperature, but in a companion
study, Bezemer et al. (1999) found that plant and aphid
species significantly influenced the response.
As well as separating quality and quantity effects, it
is also crucial that we distinguish between overall
levels of defoliation and per-capita consumption by
insects. Increases in plant productivity and nitrogen-
mediated declines in insect density can result in lower
levels of defoliation on plants despite increases in per-
capita consumption rates by herbivores (Hughes &
Bazzaz, 1997, Stiling et al., 2003). A 2-year study of
herbivore communities under open-topped CO2
chambers in scrub oak forest has shown that all
herbivore species decline in density under elevated
CO2 (Stiling et al., 2003).
While there is little information on how primary
consumers (herbivores) respond, in the longer term, to
r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 490–501
changes in temperature and atmospheric CO2
concentrations, there is even less information on the
effects of climate change on secondary consumers
(parasitoids and predators). In the few studies
currently available on the direct effects of elevated
CO2 on parasitoids, CO2 did not influence Cotesia
melanoscela, a parasitoid of the gipsy moth (Lymantria
dispar), although pre-enclosure mortality of the
parasitoid was slightly increased when CO2 was
elevated (Roth & Lindroth, 1995). Bezemer et al. (1998)
also showed that parasitism rates of M. persicae
remained unchanged in elevated CO2. Using
mathematical models Hassell et al. (1991) have shown
that host–parasitoid relationships are altered by
environmental change; temperature elevation, for
example, may differentially affect developmental rates
of hosts and parasitoids. Such differences can
potentially result in the breakdown of synchronization
between the two populations, which, in turn, may have
major effects on population dynamics.
Models and methods
Simulating the effects of change
We use a Lotka–Volterra framework, within which to
explore the effects of ‘change’ (defined here as an
increase in productivity) on interaction strength. To
investigate how increased productivity might affect
species population sizes (Xi), per-capita interaction
coefficients (aij) and, in turn, the elements of the
Jacobian matrix (aijXi), we determined the period
doubling bifurcations for a simple three species food
chain featuring omnivory in discrete time. The bifurca-
tions occur when the stability of a system changes as a
model parameter passes through a critical value.
Essentially, the bifurcations describe how the dynamics
of a species population change as a function of the
species intrinsic rate of increase. The bifurcation
diagram describes how a species population will
change from a stable equilibrium, to limit cycles of
varying amplitude and periodicity, to chaotic dynamics
as the intrinsic rate of the basal species increases. In the
simple food chain investigated here, Species 1 is basal,
Species 2 is an herbivore and Species 3 is an omnivore
feeding on Species 1 and 2 (see simple food web
detailed in Fig. 1). Species population dynamics were
determined using a discrete time version of the Lotka–
Volterra equation;
X1;tþ1 ¼ X1;t þ X1;t ðb1  a11 X1;t  a12 X2;t  a13 X3;t Þ;
X2;tþ1 ¼ X2;t þ X2;t ðd2 þ a21 X1;t  a22 X2;t  a23 X3;t Þ;
X3;tþ1 ¼ X3;t þ X3;t ðd3 þ a31 X1;t þ a32 X2;t  a33 X3;t Þ;
ð2Þ
 G L O B A L C H A N G E A LT E R S T H E S TA B I L I T Y O F F O O D W E B S
Fig 1 Period doubling bifurcations for a three species omnivor-
ous food web featuring (a) primary producer, (b) primary
consumer and (c) omnivorous secondary consumer (for the food
web diagram also shown filled circles indicate the position of the
species in the food web). The omnivorous secondary consumer
feeds on both the primary producer and the primary consumer.
Three scenarios are represented: (i) Interspecific and consumer
species intraspecific interactions are considered constant. (ii)
Herbivorous interactions (aij) are considered a function of basal
species intrinsic rates (r1), because as plant growth increases,
plant quality declines and plant consumers must ingest more to
compensate. (iii) Both herbivorous interactions and consumer
assimilation efficiencies are considered to be functions of the
primary producers intrinsic rate. This simulates increased plant
quality at low levels of productivity and decreased quality at
high levels of plant productivity (see accompanying text for
further details).
where birth and death processes have slightly different
meanings for different trophic levels. b1 defines the
positive per-capita birth rate of Species 1; basal species
population growth is logistic so that b1 5 r1/K1, r1 being
the intrinsic rate of increase of Species 1 and K1 the
carrying capacity which is set equal to 1. For nonbasal
species, d2 and d3 define the negative per-capita death
r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 490–501
495
rates of Species 2 and 3, set equal to 0.01 and 0.001,
respectively (in the absence of food these species
populations could not increase as for the basal auto-
trophs. Consequently, they have a negative intrinsic
population growth rate, which is offset by the food that
they eat). The biological justification for this decline
with increasing trophic height being that death rate is
strongly correlated with a species body size. Body size
tends to increase with trophic height and so death rate
would decline. Finally, t is time. Intraspecific terms also
have different meanings for the different species
present in the system. For the basal species a11 5 r1/K1,
while for nonbasal species intraspecific competition is
set equal to 0.1 (a22 and a33). Therefore, as r1 increases,
the strength of basal species intraspecific competition
increases relative to nonbasal species intraspecific
competition.
In this simple food chain, the secondary consumer
(omnivorous predator) is capable of feeding on both the
primary consumer (herbivore) and the basal resource
(plant). A gradient of productivity was established by
incrementing the intrinsic rate of increase (0.01 incre-
ments), of the basal species r1 in the food chain. r1 was
incremented over the interval [0, 4]. To produce the
bifurcations, at each value of r1, the three discrete time
equations’ of system (2) above, were iterated for 40 000
time steps. Initial conditions for each run were set at
X1 5 1, X2 5 0.5, X3 5 0.01, reflecting a biologically
plausible pyramidal population structure (population
density tends to decrease with increasing trophic height
and is negatively correlated with increasing body size).
The population density over the last 500 time steps of
this series is represented in one dimension as a function
of the basal species intrinsic rate. Over this time interval,
the system of equations converged either to an equili-
brium value or onto stable attractors in the system.
We explored three different scenarios to investigate
how the persistence of this simple three species food
chain might be affected given an increase in basal
species productivity. These differing scenarios repre-
sent situations where:
(i) Interspecific and nonbasal species intraspecific
interactions (a22 and a33) are considered constant over
the range of basal species intrinsic rates. The per-capita
effects of prey on predators (aji) are related to the per-
capita effects of predators on prey (aij) by a predator’s
conversion efficiency so that aji 5 e  aij, where e is 0.1.
For the simulations presented here, the interaction
coefficient matrix A was parameterized in the following
way:
2 3
r
K 0:5 0:05
A ¼ 4 0:05 0:1 0:3 5:
0:0005 0:03 0:1
496 M . E M M E R S O N et al.

(ii) As the intrinsic rate of a plant increases, plant interactions of the primary and secondary consumers
quality may decline. To compensate for this a herbivore (Jonsson & Ebenman, 1998).
must compensate and ingest more plant material to
fulfil its nutritional requirements. Therefore, as the
Results
basal species’ intrinsic rate increases so too will the
herbivores per-capita effects (aPH), where P and H refer
Population size
to plant and herbivore, respectively. To simulate this
scenario, we assumed herbivorous interactions (a12 and We constructed the period doubling bifurcations for
a13) in the simple food chain to be functions of the basal each of the scenarios ((i)—(iii)) (Fig. 1). When interac-
species’ intrinsic rate so that: tion coefficients are independent of basal species
aPH ¼ Fðr1 Þ; ð3Þ intrinsic rate (Fig. 1, a–c, i) the abundance of both
primary and secondary consumer is low, being largely
where unresponsive to the behaviour of basal species popula-
r1 tion dynamics. However, the simple food web is not
Fðr1 Þ ¼ l þ u : ð4Þ
b þ r1 feasible when the intrinsic rate of the basal species is
43 (there are no positive population densities). When
Here, l and u are constants, approximately defining the
herbivorous interaction coefficients are considered to be
lower and upper bounds to the interaction coefficient
a function of basal species intrinsic rate (Fig. 1, a–c, ii),
and were set at 0.2 and 0.8 for the primary consumer
basal species population dynamics remain largely
and 0.002 and 0.008 for the secondary consumer,
unaffected. Nonbasal species populations, on the other
respectively, b is a constant, set equal to unity. For
hand, increase monotonically until the first basal
interaction coefficients, this choice of l and u give a
species period doubling occurs. Subsequent increases
range from 0.2 to 1 for the primary consumer, and
in basal species intrinsic rate result in a slight decline in
0.002 to 0.01 for the secondary consumer. Using this
nonbasal species population size and an increased
function, the interaction coefficient asymptotes as the
variability of each species population. When both,
intrinsic rate of the basal species increases. The
predator assimilation efficiency and interaction coeffi-
biological justification for choosing this function is that
cient are considered functions of basal species intrinsic
herbivores are only capable of handling food at some
rate (Fig. 1, a–c, iii), the population size of nonbasal
maximal rate. This is essentially a Holling Type II
species both declines substantially and becomes more
functional response, but in this study, rather than
variable as basal species intrinsic rate increases. The
ingestion being a function of prey density, it is a
decline in average population size and coincident
function of prey growth rate.
increase in variability mean, that each population of
(iii) At low levels of productivity, plant quality
these species may well be more prone to stochastic
should be high, when prey intrinsic growth rates are
environmental perturbations as productivity increases.
low, the per-capita effects of herbivores on prey are
This is especially so when the scenarios that lead to a
consequently small. However, the benefits to predators
suggested increase in productivity also predict in-
should be large, because plant quality is high. It is
creased occurrence of extreme climatic events. Despite
difficult to represent this if it is assumed that the
this, both scenarios ((ii) and (iii)) result in consumer
ecological efficiency of the predator remains constant.
population sizes that are still on average much larger
To simulate an increase in plant quality at low levels of
than for Scenario (i) where interaction coefficients and
plant productivity we assume that the ecological
assimilation efficiencies are independent of basal
efficiency of a predator is also a function of plant
species productivity.
intrinsic growth rate so that:
e ¼ Fðr1 Þ; ð5Þ
Patterns of stability
where
The mechanisms detailed above such as increased
r1
Fðr1 Þ ¼ u  l : ð6Þ consumption with increased productivity, underlie
b þ r1
herbivorous interactions and have implications for the
As plant productivity increases, so the ability of a stability of the simple three species food chain
predator to convert plant biomass into predator examined. Stability in the present context refers to the
biomass decreases asymptotically reflecting the fact persistence of species in the food chain. For all three
that plant quality declines. Here, we set l and u both at scenarios, persistence is determined largely by basal
0.3 this provides a biologically plausible range of 0.3– species population dynamics at high levels of produc-
0.06 for the ecological efficiency used in the herbivorous tivity. When interaction coefficients are insensitive to

r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 490–501

 G L O B A L C H A N G E A LT E R S T H E S TA B I L I T Y O F F O O D W E B S 497

basal species productivity the chain does not persist

when the basal species intrinsic rate exceeds 3 (r143).
When only interaction coefficients are considered to be
a function of basal species intrinsic rate, no species are
lost from the food chain up to an intrinsic rate of 3.16
(and the food chain persists). When both interaction
coefficient and assimilation efficiency are considered as
functions of r1, the chain does not persist above
r1 5 3.11. At no point in the simulations do either
species 2 or 3 become extinct, affecting the persistence
of the entire food chain. This potentially could occur
with either the primary consumer becoming extinct,
leaving the omnivorous secondary consumer or the
omnivorous secondary consumer itself could become
extinct, leaving only the basal species and the primary
consumer. Despite the three differing scenarios, we find
that there is little qualitative difference in terms of
species persistence. However, the differing scenarios do
affect consumer population sizes differently. What,
then, are the implications for the patterning of Jacobian
elements (aijXi)?

Patterning of interaction strengths

To examine the distribution of predatory interaction
coefficients or Jacobian elements for a simple three-
species food chain is inappropriate, as the three
predatory food chain interactions detailed here do not
constitute a comprehensive distribution. Instead, we
consider what happens to the Jacobian elements in the
food chain as basal species productivity increases. Put
simply, the patterning of Jacobian elements (here a12 see
Fig. 2a) mirrors the patterning of each species popula-
tion size. As basal species productivities increase, and
each species population undergoes bifurcations, so the
Jacobian elements become more variable. For Scenario
(ii), Jacobian elements become increasingly negative
(stronger) with increases in productivity. As interaction
coefficients increase as a function of basal species
intrinsic rate and assimilation efficiency remains con-
stant, each consumer population size increases. For
Scenario (iii), the Jacobian elements become weaker but
still increase in variability. This decline in the strength
of Jacobian elements is a consequence of the predatory
interaction coefficients increasing as basal species
productivities increase while the predator’s assimila-
tion efficiency declines, resulting in a smaller predator
population size overall. Given the scenarios we explore
here, the patterning of the Jacobian elements seems to
have little consequence for the persistence of the food
chain, which remains feasible over the gradient of basal
species productivities. At high productivities, the
simple food chain and its constituent species popula-
tions do not exist at a simple equilibrium (Fig. 1a–c),
Fig. 2 The consequences of Scenarios (i)–(iii) (see text) for (a)
Patterning of Jacobian elements (c12) as a function of primary
producers intrinsic rate (r1) using Lotka–Volterra dynamics in
discrete time (Eqn (2)), and (b) Stability of three species food
web measured as return time (1/Re(l1)) to equilibrium. For the
determination of return time the model parameterizations
suggested by Scenarios (i)–(iii) are used to parameterize
Lotka–Volterra dynamics in continuous time (see Eqn (1)).
but rather exist in proximity to some form of cyclic or
chaotic attractor.
Continuous time
Until now, we have only considered the discrete time
version of the Lotka–Volterra equation ((2) above) and
we have seen that the system converges to an
equilibrium point or stable attractor in phase space. If
we use the same parameter values for the interaction
coefficients and birth and death processes using the
continuous form of the Lotka–Volterra equation (Eqn
(1)), then a local stability analysis of the omnivorous
food chain can be carried out. A stability analysis
determines the ability of a community to return to
equilibrium following a small perturbation that moves
a community away from the equilibrium point. Such a
stability analysis reveals that in close proximity to an
attractor the food chain is always stable (see Fig. 2b),
although if a perturbation moves a community a
large distance from the attractor (which defines the

r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 490–501

498 M . E M M E R S O N et al.
equilibrium point) the system may not return to that
same attractor. Stability is determined by evaluating the
real parts of all eigenvalues l of the Jacobian matrix (C),
if these are all negative then the food web is stable. The
reciprocal of the dominant eigenvalue (1/Re(l1)) is a
measure of resilience or the return time to equilibrium
following a small perturbation from the equilibrium
point). A long return time indicates a system with a low
resilience and vice versa. The behaviour of the Lotka–
Volterra system in continuous time is quite different;
we do not see the system settling onto limit cycles or
chaotic orbits. When interaction coefficients are invar-
iant with respect to basal species growth rate (r1), and
primary consumer population size is small, the Jaco-
bian elements are weak and return times are long,
irrespective of productivity (Scenario (i)). When the
interaction coefficients increase with intrinsic rate, but
assimilation efficiency remains constant, return times
decline asymptotically as Jacobian elements become
stronger (Scenario (ii)). For Scenario (iii), when both
interaction coefficients and assimilation efficiency are a
function of r1, the Jacobian elements detailing the
herbivorous interactions become weaker as productiv-
ity increases and return times increase. The implication
is that when Jacobian elements are weak, the system
takes longer to recover from small perturbations close
to equilibrium. Weak interactions might, therefore,
delay the recovery of food webs.
Discussion
Using Lotka–Volterra models, we have incorporated
some additional basic assumptions regarding the likely
response of consumer–resource interactions to different
scenarios of change. We find that these assumptions
have implications for the stability of real communities.
Increased herbivore consumption associated with a
decline in plant quality results in an overall decline in
herbivore population size when a predator’s conversion
efficiency is also considered a function of basal species
intrinsic rate (ri). A decline in herbivore densities is also
seen in empirical studies investigating the effects of CO2
enrichment on plant growth (Hughes & Bazzaz, 1997,
Stiling et al., 2003). Evidence for increased per-capita
consumption is mixed; McNaughton et al. (1989) for
example have shown that there is a positive relationship
between primary production and the amount of that
productivity that is consumed by herbivores in grass-
lands (while McNaughton’s study involved a compar-
ison of sites that varied in productivity, there was no
explicit test in McNaughton’s work of changes in
quality). In theoretical studies, there have been contrast-
ing viewpoints. Resource-controlled models assume no
relationships between the strength of consumer control
r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 490–501
and primary productivity, while consumer controlled
models predict that the interaction strength of the
highest trophic level should increase with productivity
(Chase et al., 2000). We have envisaged a scenario
whereby, primary consumer consumption increases as
plant productivity increases because quality declines.
It could also be argued that secondary consumer
consumption of primary consumers will increase. In
insect systems, primary consumers would be required to
eat more, with the consequence that growth is slowed,
this could lead to a higher exposure of primary
consumers to their natural enemies (slow growth–high
mortality hypothesis). We have not considered such
effects in the present study.
Similarly, we have not explicitly considered the
dynamical consequences of ecological stoichiometry.
The premise of the present paper is that resource
quality will decline because of increased plant produc-
tivity (simplistically assuming a scenario of elevated
CO2 and increased temperature) and that consequently
consumers will have to eat more to sustain their
nutritional requirements. In the present study, we do
not explicitly explore the dynamics of nutrient flows
across trophic levels and an exploration of such models
might reveal quite different dynamics (see Sterner&
Elser (2002) for a comprehensive review). Surprisingly,
this is an area where there is an equal paucity of
fundamentally important empirical data.
To predict the consequences of global change will
require that we are able to extrapolate the findings of
simplistic modelling studies such as those detailed here
to large-scale ‘real’ systems. Yet, usable and relevant
descriptions of real systems describing the size and
content of different nutrient pools, biomass and trophic
structure simply do not exist. Clearly, there is an urgent
need to collect such relevant data. Unfortunately, such
studies would be very descriptive and consequently
difficult to fund. Predicting the consequences of global
change will require a combination of theoretical and
empirical approaches. Well-resolved descriptions of
‘real’ systems are desperately needed if we are to make
predictions regarding the consequences of global
change as envisaged here.
Recently, Emmerson & Raffaelli (2004) have studied
the effects of body-size patterns in food webs and have
used body-size ratios of predators and prey to predict
the strength of trophic interactions in food webs using
Lotka–Volterra models as used here. They found that
predator prey body-size ratios raised to the power of 3/
4 could be used to parameterize complex food webs for
which body-size data were known. They hypothesized
that the 3/4 scaling of the predator–prey body-size ratio
was a reflection of basal metabolic rate scaling with
body size. Basal metabolic rate is also strongly
 G L O B A L C H A N G E A LT E R S T H E S TA B I L I T Y O F F O O D W E B S
temperature dependent and clearly scenarios of global
warming also have implications for the strength of
trophic interactions via a quite different mechanism
than those we envisage here. The temperature depen-
dence of basal metabolic rate clearly has implications
for food web dynamics and ecosystem functioning.
Linking the study of ecosystem dynamics through the
study of interacting populations, metabolic theory and
ecological stoichiometry would be a fruitful area of
research.
In the present study, we chose a simple food web and
a range of parameter values that produced feasible
communities (where all species populations have
positive densities) and have explored how changes to
these parameter values affect community feasibility. At
first, this might seem trivial but feasibility is of
paramount importance. The exploration of complex
food web dynamics is problematic mainly because
finding parameter values that result in feasible com-
munities is very difficult. We explored three scenarios
that might affect a community’s coordinates in para-
meter space and investigated whether predicted sce-
narios of change might lead a community along some
trajectory into an unfeasible region, where one or more
species populations would decline or become extinct. In
general for the scenarios we have explored, increased
productivity does not result in decreased community
persistence. However, we have investigated just one
possible food web structure. There are many possible
(simple) food web scenarios that remain to be explored,
for example those that include apparent competition or
intraguild predation.
Our discussion of change has been limited to the
effects of increased productivity on the strength of a
class of consumer resource interactions (plant–herbi-
vore). We have not considered other forms of change
for example; changes in the size distribution of
harvested populations, and how this might affect the
strength or existence of size-based feeding relation-
ships. We have not considered the effects of increased
O3 on ultraviolet light radiation levels and how this
might affect species in food webs detrimentally. There
is a range of climatic factors that we have not
considered and importantly, these remain to be ex-
plored. We have not considered how species might
adapt or respond evolutionarily to possible changes in
the global biosphere and such scenarios remain an area
ripe for research. Here, we show that simplistic models
can provide important mechanistic insights into the
causes of empirically observed patterns in real com-
munities and the types of patterns we might expect to
see as the global biosphere changes.
Even within the limited scope of this study, we can
suggest a number of consequences of ‘change’ for
r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 490–501
499
communities. When ‘change’ is envisaged as an
increase in productivity: (1) herbivorous interaction
coefficients (per-capita effects) will become stronger as
consumers fulfil their dietary requirements, faced with
a fast-growing poor-quality food resource. While per-
capita interactions could increase, the strength of
population-level effects (described by the Jacobian
matrix) might decline if population sizes coincidentally
decrease. Neutel et al. (2002) using complex soil food
webs have shown that the pattern of weak interactions
in omnivorous loops is vital for food web stability. A
disruption to the patterning of such interactions in
more complex food webs than the simplistic web we
explore here could have dramatic consequences for
food web and ecosystem stability. (2) Average popula-
tion size of consumers will likely decline as a
consequence of poor-quality food resources; (3) Jaco-
bian elements will become weaker as a consequence of
reduced population size; and (4) species populations
will become more variable and may take longer to
recover from environmental or anthropogenic pertur-
bations. This last point (4), is important as extreme
stochastic environmental effects are predicted to in-
crease with predicted scenarios of global warming. The
combined effect of small population size, increased
population variability and increased occurrence of
stochastic environmental effects will likely result in an
increased chance of extinction for the resulting popula-
tions. In conclusion, empirical validation of our
simulations is necessary but on the basis of this study
communities may become inherently less stable, that is
less resilient, smaller, more variable and hence more
prone to extinction as they respond to predicted global
environmental change.
Acknowledgements
Special thanks to Bob Paine, Tim Wootton, Bill Fagan, Dave
Raffaelli and Peter deRuiter for the provision of raw data. John
Pitchford for valuable comments. We thank all those that
participated in discussion during the ‘Food webs in a changing
world’ meeting, Texel, the Netherlands. We also thank three
anonymous reviewers for constructive and useful comments.
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