Biological invasions are having a major impact on
the Earth's ecosystems [1], giving urgency to a better
understanding of the factors that affect them. Some
recent reviews have considered invasions from a
variety of viewpoints, including the characteristics
of invaders [2], the characteristics of invaded
communities [3], resources [4,5] and natural enemies
[6].As these issues are not independent, it is essential
to find a means of considering them jointly. Towards
this goal, a theoretical framework for invasion ecology
based on community ecology theory is proposed here.
We show how this framework applies to the analysis
of the factors promoting invasion, and use it to
examine correlations between invasion resistance
and species diversity.
Invasion involves two essential stages: transport
of organisms to a new location [7,8]; and
establishment and population increase in the invaded
locality [9].A third stage, applicable to the most
worrisome invasions, is regional spread from initial
successful populations [10]. We focus on the second
stage, where community ecology theory has most to
offer. There is much evidence that the chance of
establishment increases markedly with the rate of
arrival of an alien species at a potential invasion site
[2]. However, for establishment and growth, a species
must be able to increase in abundance at the invaded
locality. This depends on the opportunities that the
particular invaded community provides for the
invader in question.
Niches and niche opportunities
Three main factors contribute to an invader's growth
rate: resources [4,5,11,12], natural enemies [7,13,14]
and the physical environment [15,16],all of which
vary in time and space. How a species responds to
these factors, including their spatial and temporal
variation, determines its ability to invade. Once an
invader has achieved an appreciable density, it will
have effects on the invaded locality ­ for example,
by consuming resources and maintaining natural
enemies. Such responses and effects are the two
defining aspects of an organism's niche, according to
a recent definition (Box 1). The response aspect of
the niche is fundamental to an alien species'ability
to invade, and the effect aspect is fundamental
to the impact that the invader has in the invaded
community (Box 2). Both effects and responses of
resident species in a community determine whether
that community provides opportunities for invasion that
is, whether it provides niche opportunities
(Box 1). In simple circumstances, niche opportunities
can reduce to either resource opportunities or natural
enemy escape opportunities.
TRENDS in Ecology & Evolution Vol.17 No.4 April 2002
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170 Opinion
Community ecology
theory as a
framework for
biological invasions
Katriona Shea and Peter Chesson
Community ecology theory can be used to understand biological invasions by
applying recent niche concepts to alien species and the communities that they
invade. These ideas lead to the concept of `niche opportunity', which defines
conditions that promote invasions in terms of resources, natural enemies, the
physical environment, interactions between these factors, and the manner in
which they vary in time and space. Niche opportunities vary naturally between
communities but might be greatly increased by disruption of communities,
especially if the original community members are less well adapted to the
new conditions. Recent niche theory clarifies the prediction that low niche
opportunities (invasion resistance) result from high species diversity.
Conflicting empirical patterns of invasion resistance are potentially explained
by covarying external factors. These various ideas derived from community
ecology provide a predictive framework for invasion ecology.
Katriona Shea*
Dept of Biology,
208 Mueller Laboratory,
The Pennsylvania State
University, University
Park, PA 16802, USA.
*e-mail: k-shea@psu.edu
Peter Chesson
Section of Evolution and
Ecology, University of
California, Davis,
CA 95616, USA.
45 Fowler, S.V. et al. (1996) Comparing the
population dynamics of broom, Cytisus
scoparius, as a native plant in the United
Kingdom and France, and as an invasive alien
weed in Australia and New Zealand. In
Proceedings of the Ninth International
Symposium of Biological Control of Weeds
(Moran, V.C. and Hoffmann, J.H., eds),
pp. 19­26, University of Cape Town
46 DeLoach, C.J. (1995) Progress and problems in
introductory biological control of native weeds in
the United States. In Proceedings of the Eighth
International Symposium on Biological Control of
Weeds (Delfosse, E.S. and Scott, R.R., eds),
pp. 111­112, CSIRO Publishing
47 Hawkins, B.A. et al. (1999) Is the biological
control of insects a natural phenomenon? Oikos
86, 493­506
48 Hosking, J.R. (1995) The impact of seed- and podfeeding
insects on Cytisus scoparius, In
Proceedings of the Eighth International
Symposium on Biological Control of Weeds
(Delfosse, E.S. and Scott, R.R., eds), pp. 45­51,
CSIRO Publishing
49 Straw, N.A. and Sheppard,A.W. (1995) The role of
plant dispersion pattern in the success and failure
of biological control. In Proceedings of the Eighth
International Symposium on Biological Control of
Weeds (Delfosse, E.S. and Scott, R.R., eds),
pp. 161­168, CSIRO Publishing
50 Southwood, T.R.E. et al. (1982) The richness,
abundance and biomass of the arthropod
communities on trees. J. Anim. Ecol. 51, 635­649
51 MacFarlane, R.P. and van den Ende, H.J. (1995)
Vine-feeding insects of old man's beard (Clematis
vitalba), in New Zealand. In Proceedings of the
Eighth International Symposium on Biological
Control of Weeds (Delfosse, E.S. and Scott, R.R.,
eds), pp. 57­58, CSIRO Publishing
52 Burki, C. and Nentwig, W. (1997) Comparison of
herbivore insect communities of Heracleum
sphondylium and H. mantegazziaum in
Switzerland (Spermatophyta:Apiaceae).
Entomol. Gen. 22, 147­155
53 Syrett, P. and Smith, L.A. (1998) The insect fauna
of four weedy Hieracium (Asteraceae) species in
New Zealand. New Zealand J. Zool. 25, 73­83
54 Hight, S.D. (1990)Available feeding niches in
populations of Lythrum salicaria L. (purple
loosestrife) in the northeastern United States. In
Proceedings of the Seventh International
Symposium on Biological Control of Weeds
(Delfosse, E.S., ed.), pp. 269­278, Istituto
Sperimentale per la Patologia Vegetale
TRENDS in Ecology & Evolution Vol.17 No.4 April 2002
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171Opinion
Resource opportunities
Resource opportunities arise when the resources that
a species needs are high in availability. This is not
simply because resources are supplied at a high rate,
but also because the effects of resident species have
not reduced resource densities [17­20] or interfered
with access to resources too greatly [21].
In cases where a potential invader and a resident
species are limited by a single resource, Tilman's
R* rule (where R is resource availability; Box 2)
predicts that invasion will occur if the resident's R*
is greater than the invader's R*. For example,
invasion would result if the invader had a higher
resource acquisition rate than that of the resident
species at the same resource densities (e.g. by having
a superior foraging technique; Box 2 [11]). Invasion
would also occur if the invader had a lower
maintenance requirement than that of the resident
(Box 2). Simple resource limitation might be
approximated in the case of space or food competition
of a species invading the habitat of a very similar
species [11,22]. Invader success, however, is also
predicted for the case of limitation by multiple
resources [23], as long as the invader always has
a higher response (per-capita growth) than the
resident. Most importantly, these conclusions are
Ecological niches are defined by the relationships between
organisms and the physical and biological environment,
taking into account both time and space. A particular
combination of physical factors (e.g. temperature and
moisture) and biological factors (e.g. food resources and
natural enemies) at a particular point in time and space
defines a point in niche space. A modern definition of a
species' ecological niche is the response that the species
has to each point in niche space and the effect that the
species has at each point [a]. Responses are defined in
terms of demographic variables, such as survival and
individual growth; but of most importance is the overall
outcome of these responses, the per-capita rate of increase.
Effects include consumption of resources, interference with
access to resources by other organisms, support of natural
enemies and occupancy of space.
Organisms respond to resource availability [b], which
is the density of unused resource in the environment ­ soil
water content, for example. Resource supply [b] is the net
rate at which resources enter the system, discounting use
by the organisms present (for example, rainfall minus
evaporation and runoff but not transpiration). Resource
availability is the net resource result of the effects of all the
organisms in a system and the supply of the resource.
A resource opportunity is defined as a high availability
of resources on which a potential invader depends.
Resource opportunity includes the effects of mutualists,
such as pollinators, because they provide services [c,d]
that could also be considered resources. Similarly, a
natural enemy escape opportunity is defined as a low level
or low efficiency of natural enemies to which invaders
might be susceptible.
A niche opportunity is the potential provided by a given
community for alien organisms to have a positive rate of
increase from low density. This might occur because of a
resource opportunity, an escape opportunity or because of
some favorable combination of resources, natural enemies
and physical environmental conditions, including their
fluctuations in time and space (Fig. I). Low levels of niche
opportunities lead to invasion resistance of a community that
is, few alien species are able to successfully invade
the community.
Maturity is the opportunity a system has had to
accumulate species, and for adaptation to the system to
have taken place. It depends on the time that the system
has had the current climate, including its short-term
fluctuations and recurring disturbance events. Maturity
depends also on the size of the species pool that has
historically served as a source of species to the system [e].
References
a Chesson, P. (2000) Mechanisms of maintenance of species
diversity. Annu. Rev. Ecol. Syst. 31, 343­366
b Tilman, D. (1982) Resource Competition and Community
Structure, Princeton University Press
c Richardson, D.M. et al. (2000) Plant invasion ­ the role of
mutualisms. Biol. Rev. 75, 63­93
d Mack, R. et al. (2000) Biotic invasions: causes, epidemiology,
global consequences, and control. Ecol. Appl. 10, 689­710
e Huston, M. (1994) Biological Diversity, Cambridge
University Press
TRENDS in Ecology & Evolution
Enemy escape
opportunities
CompetitorsResources
Specialist Generalist
Environment
Resource
opportunities
Invader
Fig. I. Main components of niche opportunity. Blue arrows are
positive effects on the invader; red arrows are negative effects.
Arrows from the outer boxes to the inner box represent direct
effects of the community on the invader. Arrows between
community components represent indirect effects on the invader,
and they are colored according to their indirect effect on the
invader, which is opposite to their direct effect on the community
component. The environment directly affects all components and
modifies their interactions with other components. Not shown are
the effects of specialist natural enemies of community members.
These specialists will limit community members and so have
positive indirect effects on the invader. Sometimes generalists
might not attack the invader, in which case their effects would be like
those of specialists on community members. (Weevil photograph
courtesy of CSIRO, Australia.)
Box 1. Concepts and definitions
robust to environmental fluctuations [24] and are not
restricted to strict equilibrium scenarios, even though
the R* rule was first derived in that context (Box 2).
Such uniform superiority of an invader would make
it an invader of large effect, because it would depress
or displace all resident species relying on the same
resources, with the details of the invasion depending
on the effect component of the invader's niche (Box 2).
More generally, an invader would not be
uniformly superior to any resident species, but
instead might have a superior response to a
particular resource, certain abundances of resources,
or resources found in certain places or times [25].Any
situations in which residents do not keep resources
at uniformly low levels are a potential resource
opportunity [4,5] (Box 3).
In some situations, the effect aspect of a species'
niche can also have a role in its invasion. Where a
species has spatially localized effects, as in the case
of plants, it will potentially have a strong effect on a
small spatial scale, benefiting itself more than other
species. For example, allelopathic effects of an
invader might reduce densities of other species,
increasing resource availability to the invader [26].
Also, some species generate disturbance or alter
disturbance regimes, freeing resources and thereby
facilitating their own and other invasions [4,27­29].
Natural enemy escape opportunities
Escape opportunities arise when natural enemies,
such as diseases, predators and parasites, are in low
abundance or are less effective against new species
[13,14]. Community ecology theory claims strong
symmetries between the effects of natural enemies
and the effects of resources on community dynamics
[30­32]. Thus, parallel to the R* rule for resources,
there is a P* rule for natural enemies (where P
indicates predator, pathogen or parasite density).
Responses to natural enemies include elevated
mortality rates and reduced feeding rates, leading to
lower per-capita growth rates. Effects of residents on
natural enemy densities are parallel to the effects of
resident species on resource availability.Although
species can vary greatly in resource dependence,
natural enemies vary greatly in their specificity [33].
An invader might not be affected by specialist
natural enemies preexisting in the invaded
community and might gain a considerable advantage
because it leaves its own specialist natural enemies
behind or loses them early in the invasion process
while at too low a density to maintain them [13,14].
This potential forms the basis of biological control
of invaders [7,8] (but see Keane and Crawley in this
issue [6]). Generalist natural enemies of the invaded
community, however, will have effects that vary with
their ability to attack the invader [6].A naive invader
might not be well defended against these enemies,
in which case they reduce the escape opportunity
of that invader [34]. However, generalists of the
invaded community might not be equipped to attack
the invader, in which case they increase the invader's
escape opportunity [6].
Interactions between the physical environment,
resources and natural enemies
In some studies, there has been a strong emphasis
on the physical environment as a constraint on
invasions [15,16]. However, many species have broad
environmental tolerances, and the interaction of
environmental factors with resources and natural
enemies has a potentially important role. For
example, with plant species, higher temperatures
could mean higher evaporative water loss, lower
water-use efficiency and, therefore, higher demand
for water as a resource [35]. Similarly, a harsh
physical environment could lead to a higher
maintenance requirement as a result of higher
mortality, higher biomass attrition rates (in plants)
or higher metabolic costs (Box 2).A harsher physical
environment might therefore require higher resource
availability to achieve the same capacity for increase.
However, as both residents and invaders respond to
environmental harshness, it is the difference in the
response of the residents and invader that determines
TRENDS in Ecology & Evolution Vol.17 No.4 April 2002
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172 Opinion
The per-capita growth rate of a population limited by a single resource is the net
effect of the gain from consumption of the resource, and the losses due to
metabolism, tissue death (e.g. leaf fall and herbivory) and death of individuals. Thus:
(I)
where N is population density, R is resource availability, af (R) defines the gain (the
response of the species to the resource), and m (the maintenance requirement) is
the total of all losses. The gain consists of the two parts: the constant a defining the
overall magnitude of the response to the resource and the function f (R) defining
how response to the resource changes with resource abundance. The dynamics of
the resource are given by:
(II)
where S(R) is the supply rate of the resource, and g(R) the per-capita effect of the
species on the resource. Multiplying g(R) by N gives the total effect of the species
and determines the impact of the invader in the invaded community.
Normally, there would be a unique value R* of R at which equilibrium would
occur ­ that is, af (R*) = m. For an alien species to invade, it must have a smaller
value of R* than does a resident at equilibrium with the resource, because this is
the value of resource availability that the alien experiences when it arrives in the
system. Only if the resident's R* value exceeds that of the invader can the invader
have a positive growth rate. This is Tilman's R* rule [a]. An alien might have a
smaller R* value by having a smaller maintenance requirement. Alternatively, it
might have a higher response than a resident [i.e. a larger value of af (R)]. This
might be achieved by taking up the resource at a faster rate or by being more
efficient at converting that uptake into gain. Different responses for different
species might be modeled by having a vary with the species. In this case, R* would
be an increasing function of m/a, and an invader would be successful if it had a
smaller value of m/a than that of a resident.
Although this R* theory was originally developed as an equilibrium theory [a], in
the form where species can differ in a or m, the theory is robust to fluctuations in R
and m, with the result being that an alien having a mean of m/a smaller than that of a
resident can invade [b]. See Box 3 for situations in which R* theory does not hold.
References
a Tilman, D. (1982) Resource Competition and Community Structure, Princeton
University Press
b Chesson, P. and Huntly, N. (1997) The roles of harsh and fluctuating conditions in the
dynamics of ecological communities. Am. Nat. 150, 519­553
( ) ( )NRgRS
dt
dR
-=
( ) mRaf
dt
dN
N
-=
1
Box 2. Resource competition ideas
whether invasion is promoted or inhibited by
harshness [24].An invader will be at an advantage
if its maintenance requirement does not increase
as much as that of a resident with environmental
harshness, or if it has a stronger response to
increased resources than the residents (Box 2).
Environmental fluctuations in time and space
also have major effects. The key issues again are
differential effects of the fluctuations on invaders and
residents, with the added parameter that different
species might be favored at different times and in
different places [4,5,25] (Box 3).
Environment­resource interactions naturally
have parallels in environment­natural enemy
interactions, but one should also consider natural
enemy­resource interactions. Indeed, important
invader advantage might accrue as a result of these
interactions, because residents and invaders could
be differentially susceptible to specialist natural
enemies of the residents. In particular, high densities
of specialist natural enemies should lead to lower
densities of resident species, increasing resource
availability [24,30,36].Although generalist natural
enemies might have similar effects on resources as
the specialists, the increased resource availability
for an invader could be countered by a decrease in
escape opportunity [24,30]. The net outcome of
all these different interactions determines the
magnitude and nature of the niche opportunities
provided by the community.
How niche opportunities arise
Natural enemy escape opportunities
Most communities provide escape opportunities
because they do not have the specialist natural
enemies of invaders from geographically distant
locations [7].Although invasions are sometimes
compared with range expansions [5,37], escape
opportunities imply an important distinction,
because specialist natural enemies must be lost at
much lower rates during range expansions than they
are during invasions of relatively small numbers
from great distances.
Invaders that offset losses to natural enemies
in their native range by having high fecundity or
individual growth (grazed plants and clonal animals)
[38] could gain a strong advantage in a system
without their specialist natural enemies. Potentially
diminishing this advantage are generalist naturalist
enemies to which the invader might be particularly
vulnerable in the invaded location because it has
no evolutionary history with them and might not
be adequately protected against them [34]. The
spectacular success of biological control for some
invaders, however, implies that loss of natural
enemies is sometimes an important escape
opportunity [7,39].
Escape opportunities can allow a species to win
in resource competition in a similar way to a low
maintenance requirement (Box 2), potentially
allowing an invader to reach high densities and have
a large effect on resources.Apparent competition
can have a similar outcome.An invader with few
specialist natural enemies could rise to a high density,
maintaining generalist natural enemies that severely
impact the native community.
Resource opportunities
Disturbance is commonly assumed to release
resources and provide opportunities for invaders [5],
an idea that has been generalized to consider any
form of temporal variation in resource availability
[4,5].As emphasized by spatio-temporal resource
competition theory (Box 3) an invader still must
have some advantage over residents. However, that
advantage might occur at particular times or in
TRENDS in Ecology & Evolution Vol.17 No.4 April 2002
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173Opinion
Community ecology theory predicts that spatial and temporal environmental
variation has an important role in species coexistence [a]. For invaders, this can
mean spatial and temporal niche opportunities, provided that invaders and
residents differ in their responses to varying factors. Most species have periods of
relative activity and relative inactivity during a year [b]. Niche opportunities arise
during times when resident species are relatively inactive and are not placing high
demands on resources. Using the notation given in Box 2, the per-capita growth
rate of a species might be represented as:
[I]
with a now a function of time to represent temporally varying growth activity: it is the
response of the organism to time. The theory of the storage effect [b] shows that a
species can invade even if it has an average value of a(t) less than that of resident
species, provided that the invader's a(t) is sufficiently large compared with residents'
a(t)s some of the time; for example, the activities of the invader and residents might
fluctuate out of phase. Fluctuations in a(t) can be deterministic (e.g. seasonal) or
stochastic (e.g. in response to yearly weather variation) [b,c]; the key feature is that the
invader must show a different temporal pattern of response than that of the residents.
An invader might also gain an advantage by responding differently to changes
in resource levels than do residents ­ that is, by having a function f(R) that differs
nonlinearly from that of residents [a,d]. For example, the invader might have a
stronger response than residents at both high and low resource availabilities, but
not at intermediate resource availabilities. Resource fluctuations between high and
low values would then be a resource opportunity for the invader, a mechanism
referred to as `relative nonlinearity of competition' [a].
Spatial variation can also provide niche opportunities, and this can occur through
spatial versions of the storage effect and relative nonlinearity of competition [e].
Much emphasized in the literature, however, are competition­colonization
tradeoffs [f,g], which can work on a variety of scales. At the level of a local
community, the mechanism can be driven by disturbance. In sessile communities,
death of an individual is a substitute for disturbance. Most importantly, this
mechanism means that an inferior competitor for resources could invade if it had
superior colonization or local resource exploitation ability [g].
References
a Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annu. Rev. Ecol.
Syst. 31, 343­366
b Chesson, P. et al. (2001) Environmental niches and ecosystem functioning. In Functional
Consequences of Biodiversity(Kinzig,A.et al., eds), pp. 213­245, Princeton University Press
c Lehman, C.L. and Tilman, D. (2000) Biodiversity, stability, and productivity in
competitive communities. Am. Nat. 156, 513­552
d Armstrong, R.A. and McGehee, R. (1980) Competitive exclusion. Am. Nat. 115, 151­170
e Chesson, P. (2000) General theory of competitive coexistence in spatially-varying
environments. Theor. Popul. Biol. 58, 211­237
f Tilman, D. (1994) Competition and biodiversity in spatially structured habitats. Ecology
75, 2­16
g Bolker, B. and Pacala, S. (1999) Spatial moment equations for plant competition:
understanding spatial strategies and the advantages of short dispersal. Am. Nat.
153, 575­602
( ) ( ) mRfta
dt
dN
N
-=
1
Box 3. Resource opportunities in fluctuating environments
particular places, or it might be in a life-history trait,
such as colonizing ability (Box 3). Sher and Hyatt [4]
emphasize that an advantage to invaders commonly
arises through disruption of the historical pattern of
resource supply and consumption.
There are many ways in which human activities
disrupt historical patterns of resource fluctuations,
including alteration of patterns of fire [40], harvesting
of biomass, nutrient enrichment [12], alteration of
patterns of spatial heterogeneity, and climate change
[1,41,42]. Resident species might not be adapted to
the changed environmental conditions, lessening
their ability to reduce resource availability uniformly
in time and space, and thus providing resource
opportunities for invaders. Some invaders, such as
species that inhabit human disturbed environments
in their native range, might have critical adaptations
to human disturbed environments that resident
species lack [43,44], giving them the advantages they
need for successful invasion.
Community maturity
Do natural communities vary in the niche
opportunities that they provide, independently of the
disruptions discussed above? Particular systems and
geographical regions have relatively high rates of
invasions.Among these are freshwater systems,
oceanic islands, regions with a Mediterranean
climate, and NorthAmerica in comparison with
Eurasia [29]. Greater disruption by humans and
greater rates of commerce between geographically
similar regions might contribute to some of these
elevated rates, but particular features of the
communities themselves could also contribute [45].
Species in different systems might vary in
competitive ability [11,26] or their degree of
specialization [29] ­ that is, the breadth of conditions
under which individual members have positive
responses to their environment. In the presence of
tradeoffs that benefit specialization [46], several
specialized species would reduce resources more
effectively than one generalist species covering the
same range of circumstances.
The maturity concept (Box 1) might explain such
community differences: communities that have
had less time to assemble, and less time for their
constituent species to adapt to the local conditions,
are likely to have fewer species with broader niches.
Their species might also have lower competitive
abilities than those in communities that have had
a longer time under their present environmental
regime. These communities tend to be less invasion
resistant (Box 1). Similar effects on invasion
resistance might result from the size of the species
pool from which a community has assembled.
Maturity undoubtedly also affects invasion resistance
through escape opportunities, but clear predictions in
this area are not so apparent.
Variation in niche opportunities with resident diversity
Maturity is one theoretical approach to explaining
invasion resistance. Ideally, invasion resistance could
be predicted from directly observable community
properties. In a classic work, Elton [47] proposed
that communities with high species diversity should
be invasion resistant. Indeed, models and some
experimental studies suggest that high species
diversity does lead to invasion resistance ­ that is,
there is a negative relationship between invasion
success and species diversity [48­51]. However, largescale
observational patterns mostly show that more
diverse systems tend to have higher numbers of exotic
species [3,51,52]. There have been various attempts
to understand these conflicting patterns.
Scale and the role of covarying factors
Species diversity varies widely with physical
extrinsic factors, such as latitude, climate (given
latitude), soils and the supply rates of physical
resources to a system. This observation can help
explain the discrepancy between different studies. If
extrinsic factors favorable to high species diversity
also lower invasion resistance, the positive
relationship between species diversity and invasion
success seen on broad spatial scales is explained [50].
A negative pattern of invasion success as a function
of diversity, for fixed extrinsic conditions, is
consistent with this proposal, as illustrated in Fig. 1:
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174 Opinion
TRENDS in Ecology & Evolution
Number of native species
Numberofexoticspecies
Fig. 1. Reconciliation of relationships between invasion success and
species richness on different spatial scales. In this illustration, extrinsic
conditions are assumed to be the same within each cluster of points
but to differ between clusters. Within any cluster, higher numbers of
native species lead to poorer niche opportunities for invaders,
generating the negative relationship between the numbers of alien
species and native species often observed in models, experiments
and at small spatial scales. However, extrinsic factors can vary
considerably on broad spatial scales. If extrinsic factors that favor high
numbers of native species also directly increase niche opportunity for
invaders, changes in these extrinsic factors will lead to clusters of
points whose mean numbers of alien and native species are positively
related, as depicted. Thus, there is an overall positive relationship
between alien and native species when the data are combined on a
broad spatial scale.
the broad-scale positive relationship is the outcome
of combining data from a series of negative
relationships, where each negative relationship
comes from different extrinsic conditions.
This reconciliation of conflicting patterns is
consistent with the outcome of models [51] in which
extrinsic factors are not generally varied. Species
diversities differ because of different sizes of the
species pool colonizing the local system, or different
amounts of time for species to accumulate in the local
system, or simply due to chance: randomness in the
process of community assembly leaves some systems
with fewer species than others. In all these ways
of varying species diversity, there is a consistent
tendency in models for invasion success to decrease
with species diversity. Generally, equivalent results
have been obtained by experimental studies that
carefully control extrinsic factors, or randomize them,
and define species diversity as the number of species
supplied to the system [53]. By contrast, studies that
define species diversity as the number of species
successfully established might confound uncontrolled
variation in extrinsic factors, including propagule
pressure.According to Fig. 1, a positive relationship
between invasion success and diversity could result.
The role of positive interactions
An alternative explanation of positive relationships
between species diversity and invasion success, which
has some support from experiments in agricultural
systems, is that high species diversity creates niche
opportunities ­ for example, by mutualisms, both
direct and indirect, that facilitate the entry of other
species [54]. The modeling and experimental studies
that found negative relationships might not have
provided the conditions for sufficiently beneficial
mutualisms to occur, possibly explaining why
invasion success did not increase with diversity.
The role of niche differentiation
Theoretical explanations of why higher species
diversity might confer invasion resistance, when
extrinsic factors are controlled, depend on how the
niches of the various residents and invaders relate to
one another.According to the empty niche hypothesis
[55], lower species diversity might simply mean the
existence of circumstances where resources are not
being exploited efficiently because species with
suitable niches are lacking. Niche opportunities
therefore exist for species able to benefit from
resources in those particular circumstances [7]. In
this case, it should not be just the diversity of resident
species that matters but how their niches differ
functionally [56],including their spatial and temporal
patterns of effects on resources [48].
At the opposite extreme is the sampling
hypothesis, where species are not differentiated
functionally but vary in their ability to reduce
resources [57], or (presumably) to maintain natural
enemies.According to this hypothesis, higher
diversity does not broaden the circumstances under
which resources are exploited efficiently but instead
increases the probability that a high-ranking
competitor is present. Invasion success depends
not on filling a vacant niche but on being a better
exploiter of resources or a better avoider of natural
enemies than resident species. However, a
competitor's rank might vary in space and time,
allowing a high diversity of species to be maintained
in the system [25] (Box 3). Thus, invader success
depends on finding a time or place where it is
superior to resident species, and the distinction
between the empty niche hypothesis and the
sampling hypothesis is lost [57,58].
Conclusion
Over much of its history, invasion ecology has
developed on a relatively separate path from other
areas of ecology, potentially to the detriment of the
discipline [59]. The framework presented here,
however, shows how core issues of invasion ecology
can be discussed as topics in community ecology.
Recent advances in community ecology theory have
made this possible by providing detailed predictions
about topics of particular importance in invasion
ecology, such as resource and natural enemy
interactions [30,32], and disturbance and more
general kinds of variation in space and time
[24,25,60]. The link between community and
invasion ecology is a natural one, because the
essential criterion for a species to persist in a
community is its ability to increase from low density,
TRENDS in Ecology & Evolution Vol.17 No.4 April 2002
http://tree.trends.com
175Opinion
The niche opportunity framework raises many questions and provides many
avenues for new research. The following are some of the most immediate.
ˇˇ Interactions between resource and escape opportunity: much of the recent
invasion literature emphasizes resources. However, an invader released from
natural enemies would have a low maintenance requirement and therefore a low
R* value. It would thus be a strong competitor. Hence, the cause of the invasion
might appear to be a resource opportunity when, in fact, it is an escape opportunity.
Studies of the interaction between natural enemies and competition in the native
range of the invader, and in the invaded community, would resolve this issue.
ˇˇ Community maturity: the theoretical concept of community maturity has been
explored implicitly through models of community assembly [a]. However, there
is a need for systematic studies of invasion resistance distinguishing the effects
of time, species pool, the number of established species and established
functional diversity. Important challenges are to understand the accumulations
of natural enemies over time, their degree of specialization and their interactions
with resources.
ˇˇ Covarying extrinsic factors in field studies: covarying extrinsic factors easily
confound the relationship between invasion resistance and diversity. There is a
need for field techniques to control for extrinsic factors. Methods of data analysis
accounting for covarying extrinsic factors also need to be developed.
ˇˇ Improved understanding of coexistence mechanisms in nature: a better
understanding of how species coexist in natural systems would give a better
appreciation of the kinds of niche opportunity that a system might provide. For
example, studies of changes in dominance patterns over time and in space could
test whether species coexist by having different responses to spatially and
temporally varying environmental factors. This information would also reveal
the kinds of changes to the system that might favor invasion.
Reference
a Morton, R.D. and Law, R. (1997) Regional species pools and the assembly of local
ecological communities. J. Theor. Biol. 187, 321­331
Box 4. Future directions
Acknowledgements
K.S. is a collaborator via
a fellowship under the
OECD Co-operative
Research Programme:
Biological Resource
Management for
Sustainable Agricultural
Systems and also
acknowledges the
Australian CRC for Weed
Management Systems,
NMFS (grant to
M. Mangel, UC Santa Cruz)
and NIH/NSF Ecology of
Infectious Diseases grant
(1R01ES11067-01) for
support. P.C. was
supported by NSF grant
DEB 9981926. We also
thank Ottar Bjrnstad,
Ryan Keane, Mark
Lonsdale, Marc Mangel,
Peter Moyle, Bill Murdoch,
Marcel Rejmánek,
Jay Stachowicz,
Don Strong, Mark Torchin,
Michael Turelli and Mark
Williamson for comments.
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176 Opinion
which is also the condition for an alien to be able
to invade a community. This means that invasion
ecology has the potential to contribute greatly to
community ecology. Invasions provide case studies on
particular communities subject to perturbation by
invaders; they also provide the challenge of
explaining invader success and invader impact.
Indeed, there is every reason to expect a healthy
synergy between invasion ecology and community
ecology (Box 4).