The influence of biodiversity on invasibility of terrestrial plant communities
<Student Name>
Department of Biology
St. Francis Xavier University
Antigonish, Nova Scotia, Canada
25 March 1873
Introduction
The concept of invasibility refers to how susceptible an ecosystem is to invasion. The idea
that the diversity of an ecosystem could affect invasibility was first proposed by Charles Elton in
1958. The premise of his theory is that with greater diversity an ecosystem has greater
partitioning of resources, and this lack of free resources (low niche opportunity), impedes the
establishment of invaders.
Recently, Elton’s theory has been the topic of debate. Research, review and opinion
articles run the gamut from full support of Elton’s theory to diametrically opposed, with attempts
for unbiased experiments caught in the middle. This issue certainly is a contentious one in the
scientific community.
This paper will argue (1) diversity can affect invasibility, but (2) it depends largely on the
factors leading to that diversity. I will make the argument that the effect of diversity on
ecosystem invasibility is inconsistent, and often overwhelmed by other factors in natural settings.
Ultimately, regardless of whether diversity affects invasibility, it may be so minor a factor that it
is not worth consideration while trying to study dynamics of invasive species. I will review
modern theories regarding the diversity-invasibility hypothesis, and the theories that influence or
contradict Elton’s original thesis. I will then examine how modern research supports or refutes
these hypotheses.
Modern Theories
Experiments in environmentally controlled microcosms suggest that diversity does render
an ecosystem less invasible (Kennedy et al. 2002, van Ruijven et al. 2003). However,
observational studies show that the most diverse communities are often the most heavily invaded
(Lonsdale 1999).
Tilman (1999) agrees that diversity should decrease invasibility, but he stresses the
importance of the ability of the organisms to acquire resources. He calls the resource
requirements of a species, the resources an organism needs to survive, reproduce and spread, R*.
If a resident species has a greater R* than the invader, meaning the invader requires fewer
resources than the resident, than the invader will be successful. Thus TIilman (1999) argues that
the characteristics of the invading species are just as important as those of the native species.
Shea and Chesson (2002) argue the response of an invader to a predator, P*, is also important in
invasion. Effects of predators will be discussed later in the context of disturbance. Thompson
(1991) argues that studying species that invade is more fruitful for gaining an understanding of
invasion biology than studying native species or predators.
He argues that species that
successfully invade share common characteristics. Furthermore, he says that to be successful, the
invasive species must have some advantage over the native species.
Another model argues that characteristics of the community are even less important.
Davis et al. (2000) posit that fluctuating resources are the key factor controlling invasibility.
Furthermore, resource availability changes with time and disturbance and therefore is not a
characteristic of the community, but a stochastic feature of the environment. Davis et al. (2000)
say that competition should be inversely correlated with resource availability. Under this model,
diversity could be important inasmuch as it leads to resource partitioning or consumption.
Invasion would be largely stochastic, based on invaders happening upon free resources. This
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theory lends itself nicely to the idea of propagule pressure: the intensity at which invading
species arrive. Increasing propagule pressure increases the probability that invasion will occur.
Experimental Evidence
Experimental manipulations suggest that diversity does affect invasibility. However,
observational evidence suggests that the highest diversity areas are the most heavily invaded.
Typical field studies attempting to manipulate diversity use a seed pool of native plants to
sow plots with various numbers of species. Other studies have taken native plots and weeded
selected species from the area, usually over a period of at least one growing season to allow the
remaining species to dominate the plot. These plots are then subjected to propagules of invasive
species and after a certain amount of time the biomasses of native species and invaders are
compared within and between plots. These experiments generally demonstrate that there is an
effect of diversity on invasibility.
The results from these experiments usually have stipulations. For example: Kennedy et al.
(2002) showed a negative correlation between diversity and invasibility, but at a neighbourhood
scale (a scale directly relevant to an individual plant). It seems that in this study, crowding, which
increased in species-rich plots, was a significant factor in reducing invasion. Dukes (2001)
manipulated both species diversity and functional diversity. He found that manipulating species
diversity while keeping functional diversity constant had little effect on invader success. These
manipulations tend to deal with relatively few species. It would seem that functional diversity
naturally increases with species diversity.
Levine (2000) manipulated diversity by removing grass species from tussocks along a
river in California. Although he found that species diversity was negatively correlated with
invasion, he also found a gradient of both diversity and invasion increasing in the downstream
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direction of the river. This trend seems to point to the importance of propagule pressure on both
diversity and invasion.
The fact that diverse areas are often heavily invaded has posed a conundrum to
researchers. In a study of biomes in the USA, Stohlgren et al. (1999) found a positive correlation
between diversity and invasion of 1-m2 plots (five forest and meadow vegetation types) as well as
at the 1000-m2 scale. Elton’s hypothesis was supported in plots of four prairie vegetation types at
the 1-m2 scale. When diversity was positively correlated with invasion, most of the variation in
exotic species richness could be explained by soil nutrients (nitrogen and carbon), and foliar
cover, regardless of species.
Stohlgren et al. (1998) found that riparian zones in central US grasslands were heavily
invaded compared with less diverse uplands. This study may be support for the fluctuating
resource model proposed by Davis et al. (2000). Riparian zones are subject to nutrient loading
and seasonal disturbance, an important point to be discussed in the next section.
Lonsdale (1999) examined global patterns of diversity and found that invasion increased
with latitude and there is a positive correlation between native species diversity and invasion on a
community scale. Rejmanek (1996 as cited in Stadler et al. 2000) argues that Europe and North
America are source pools for invasive species, introduced through a vector of human movements.
This can explain the high number of invasions in North America but few in the tropics, where
species from Europe are generally not suited to compete.
How do supporters of Elton’s theory respond to these trends? A common argument
invoked to explain increased invasion in high diversity areas in light of experiments showing
diversity increases resistance is the notion of extrinsic factors that co-vary with diversity. When
these factors, such as resource heterogeneity (Kennedy et al. 2002) and disturbance, climate and
soil (Naeem et al. 2000) are removed from experimental situations, it is argued that diversity still
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shows a strong effect on invasion (Naeem et al. 2000, Shea and Chesson 2002). Shea and
Chesson (2002) suggest the co-varying factors cause the observed overall positive relationship,
but comparing similar ecosystems would show negative relationships (Figure 1).
Figure 1. The apparent positive correlation of native diversity and invasive species. A facsimile of
hypothetical data presented in Shea and Chesson (2002). Extrinsic factors are assumed to be the same in
each cluster, but co-vary with diversity to create an overall positive relationship.
Experiments that would have controlled extrinsic factors (Naeem et al. 2000) (and
previously mentioned experiments would have controlled for extrinsic factors) receive strong
criticism for not accounting for the effects of single species that are competitively dominant.
Wardle (2001) argues that by not including monoculture plots, researchers cannot separate the
effects of diversity from the effects of competitively dominant species. He argues that many
experiments, including Levine (2000) and Naeem et al. (2000) can be explained with the
sampling effect, whereby increasing diversity increases the likelihood of including one of these
competitively dominant species. Tilman (1997 as cited in Wardle 2001) has suggested that this
may be the mechanism in which a negative relationship between diversity and invasion may
express itself. However, if the invasibility of an ecosystem can be attributed to the presence or
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absence of one species, and diversity only affects the probability of that species occurring, then
this is not in accordance with Elton’s original theory – it has nothing to do with diversity’s
influence on low niche opportunities – and it is even a stretch to claim that in this case diversity
is affecting invasibility.
Wardle (2001) also criticized experiments that generate disturbance to manipulate species
diversity. For example: Levine (2000) weeded grass tussocks to create specific species diversity.
Crawley et al. (1999) killed species with treatments of methyl bromide. van Ruijven (2003)
maintained diversity in man-made plots by weeding. These methods generate disturbance, which
Chapin et al. (2002) identify as a means of disrupting ecosystem processes and providing
opportunities for establishment. Hobbs and Huenneke (1992) highlight the importance of
disturbance in community structure, and argue that the same disturbance can influence
invasibility. Davis et al. (2000) recognize disturbance as a major factor for freeing resources and
allowing for invasion. If species were equal competitors, then plots manipulated for low diversity
would have the most disturbance, and hence the most invasion. Similarly, if a strong competitor
is being removed, it would have equal (independent) probabilities of being removed from low
diversity plots and remaining in high diversity plots. Thus low diversity plots would have a lot of
disturbance, and high diversity plots would have little disturbance and probably a dominant
competitor.
Dukes (2001) performed a similar study in which species and functional diversity were
manipulated in man-made grassland microcosms. This study included bare soil and monoculture
controls. Dukes (2001) found monocultures of the forb Hemizona congesta, in the same
functional group as the invader, Centaurea, strongly suppressed the growth of Centaurea. He
found that diversity of four or more species (and thus including all for functional groups)
suppressed growth of Centaurea regardless of the presence of absence of Hemizona. Invasion
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success was also strongly correlated for part of the year with water availability and soil nitrate.
Dukes (2001) concluded that species had a greater chance of invading if their functional group
was not present in the community. Although this result could be confused with the sampling
effect, it seems that the important point is the presence of a functional group and not the specific
species, and hence a function of species diversity and not species composition.
Discussion
There seems to be one major hitch with Elton’s theory. Theorists and researchers alike
consider diversity a gradient from low to high, and otherwise equal across ecosystems. However,
I posit that the same factors creating diversity in some environments may for the same reasons
favour invasions. This parallel would lead to the much debated positive relationship between
native species diversity and invasions. Conversely, in other situations the nature of the diversity
may impede invasions. For a conclusion I will now look at the factors influencing diversity, and
relate them to invasibility in reference to research and studies already mentioned.
Krohne (2001) lists ten factors that can produce high biodiversity, which are: evolutionary
time, ecological time, climatic stability, climatic predictability, structural heterogeneity,
predation, competition, primary production, biotic interactions, and intermediate levels of
disturbance. These will be considered as they influence two broad categories: assembly time and
disturbance regime.
There are few species which can tolerate frequent disturbance. In such a situation, only
competitively dominant species can survive, hence the ecosystem is not very diverse. On the
other end of the scale, infrequent disturbance can lead to competitive exclusion by dominant
species. Connell (1978 as cited in Krohne 2001) proposed the intermediate disturbance
hypothesis, whereby intermediate levels and intensities of disturbance generate enough instability
in populations that competition is reduced between species and competitive exclusion does not
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occur (Figure 2). Predation and parasites can have the same effect on populations. In light of
Connell’s intermediate disturbance hypothesis, Davis et al.’s (2000) fluctuating resource model
of invasibility would essentially predict a positive correlation between diversity and invasion.
Disturbance or reduced competition prevents outright competitive exclusion, hence there are
unused resources. This in turn allows high levels of diversity to develop. For this same reason,
invasive species can happen upon opportunities to sequester free resources. If the invader has a
lower R* than the native species, invasion is almost a sure thing. If there are free resources, the
invader may be able to invade and avoid competitive exclusion. Under this model, invasion of
foreign species would occur through he same mechanisms as colonization by local species (Davis
and Thompson 2000). It should be noted that Davis et al.’s theory (2000) has also received
experimental support. Davis and Pelsor (2001) found that altering variables such as resources
(water) and disturbance affected competition in simple experimental plant communities; resource
availability was in turn positively correlated with invasive species.
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Figure 2. A graphical depiction of Connell’s Intermediate Disturbance Hypothesis (Krohne 2001). An
intermediate level of disturbance lowers competition and favours diversity. This graph also shows a
possible decrease in invasibility concurrent with free resources caused by disturbance.
Assembly time is another major factor that can affect biodiversity. Krohne (2001)
suggests that climatic stability and climatic predictability will lead to high biodiversity. The ice
ages are a recent source of disturbance for temperate areas. It is possible that in these areas,
ecosystems assembly acts on an ecological scale. The short time since the last major disturbance
may limit the niche specialization of these communities, which is why areas with intermediate
disturbance have high diversity, but areas with low disturbance frequencies show competitive
exclusion. On the other hand, areas such as the tropics have climatic stability and predictability,
and it has been a long time since the last major disturbance. Ergo, it is possible that evolution has
led to high levels of niche specialization and complementarity. In this case, true resource
partitioning may be occurring, and it may not be necessary to invoke the intermediate disturbance
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hypothesis to explain diversity. If this is true, Elton’s original hypothesis may still apply, but the
nature of the diversity is important in interpreting the situation.
The major feature of diversity which negatively affects invasion is resource partitioning.
As evidenced by the intermediate disturbance hypothesis, resource partitioning is not a
prerequisite for diversity. Even if diversity has arisen in stable environments, competition can
still be interrupted by factors such as predators and parasites. Thus there are inevitably some
resource opportunities which invaders can exploit through the same mechanisms as local
colonizers. Invasion is also influenced by characteristics of the invader (i.e. R* value) and
propagule pressure. The strongest arguments that diversity does influence invasibility come from
Dukes (2001) and Fargione et al. (2003) who manipulated functional diversity, and accounted for
the sampling effect. I feel I have shown that biodiversity can influence invasibility, if resource
portioning has occurred, but it is trumped by many other factors, namely free resources.
Further work attempting to decipher relationships between diversity and invasibility is
inextricably reliant on working knowledge of diversity itself. The effect of diversity is not
mutually exclusive from Davis et al.’s (2001) fluctuating resource model. Interspecific
competition must be examined to unite all three ideas (diversity, competition and resources), even
if diversity is a minor factor. It is quite possible that diversity effects may not be reliable enough
to be considered in a general model of invasion biology.
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