Journal of Ecology 2008, 96, 46–57
doi: 10.1111/j.1365-2745.2007.01324.x
Is invasiveness a legacy of evolution? Phylogenetic
patterns in the alien flora of Mediterranean islands
Blackwell Publishing Ltd
Philip W. Lambdon*
NERC Centre for Ecology and Hydrology, Hill of Brathens, Banchory, Aberdeenshire, AB31 4BW, UK
Summary
1. The Mediterranean region has been invaded by a wide range of introduced plant species which
differ greatly in their ecology, morphology and human utilization. In order to identify a suite of
traits which characterize invasiveness, recent studies have advocated the use of evolutionary
relationships to unravel highly confounded influences.
2. This study attempts to identify an evolutionary component to invasiveness and other complex
invasion-related traits in the Mediterranean alien flora using an autocorrelation technique, the
‘phylogenetic association test’. I compared a traditional hierarchical taxonomy with the recent
phylogeny of the Angiosperm Phylogeny Group.
3. Invasiveness did not have a significant phylogenetic component. Any weak clustering was
generally at the genus level.
4. Several associated ‘meta-traits’ (high introduction frequency, adaptation to several habitat types
and favourability for different modes of introduction), exhibited stronger phylogenetic components. Although each of these conveys some of the attributes of invasiveness, their clustering
patterns differed considerably, suggesting that they arise from independent evolutionary pressures.
Furthermore, within each meta-trait, different clusters may have been selected for different reasons.
5. Other reasons for the lack of a detectable evolutionary component to invasiveness are discussed.
Firstly, the results of our test simulations suggested that incorrect phylogeny could result in a moderate
degree of error. Secondly, over evolutionary time, complex or stochastic events such as ecosystem
change could radically alter the adaptive advantages of particular traits.
6. Synthesis. Since invasiveness has little phylogenetic component, I argue that it is less likely to be
predictable from as yet unidentified traits in any simple way. Although trait syndromes could
develop without leaving a phylogenetic pattern, its absence probably indicates that the dominant
selective forces are responses to short-term ecological shifts, and a greater mechanistic understanding
of these is needed.
Key-words: biological invasions, cladistic relationships, macro- vs. microevolution, relatedness
measures, screening protocols, taxonomy, trait analysis.
Introduction
Substantial research effort and funding goes into the
development of predictive methods for detecting potential
invasiveness traits in introduced plants (Simberloff 2005).
The Mediterranean basin is one such area where screening is
currently much in need, containing a complex of vulnerable
islands where invasive species are spreading rapidly (le Floc’h
1991; Hulme 2004). Concern is growing that the problem is
*Correspondence and present address: Global Programmes Department, Royal Society for the Protection of Birds, The Lodge, Sandy,
Bedfordshire SG19 2DL, UK. E-mail: [email protected].
being exacerbated by climate change, habitat degradation
and large volumes of trade and tourism (Blondel & Aronson
1999).
Given the high cost of eradication programmes for invasive
species which are already established (Manchester & Bullock
2000; Pimentel et al. 2005), screening protocols promise a
highly cost-effective management option, but they have yet to
achieve the levels of accuracy which would make them truly
effective (Smith et al. 1999; Williamson 1999; Joly 2000). The
reasons for this disappointing performance are not yet fully
understood, although there is a growing recognition that the
general approach needs critical appraisal (Ewel et al. 1999;
Hulme 2003). One argument for their continuation is that
© 2007 The Author. Journal compilation © 2007 British Ecological Society
Phylogeny of Mediterranean alien plants 47
better indicators may exist: we have merely not identified
them yet. Inevitably, there is little evidence we can draw on to
indicate whether this stance is correct or incorrect. However,
a circumstantial line of evidence remains open. Many of the
characteristics attributed to successful alien plant species,
such as growth forms, pollination and dispersal types or
allelopathy, are strongly associated with particular taxa, and
we may expect the same from as yet unidentified predictors. If
invasiveness is conferred by simple traits, then, as one likely
consequence, these may well have a clear ‘heritable’ component
on an evolutionary time-scale.
The potential existence of phylogenetic patterns in
invasiveness has been recognized since the time of Darwin
(1859), and recent trait analyses increasingly include phylogenetically independent contrasts, in order to control for
evolutionary associations in the traits examined (Perrins et al.
1992; Kelly & Woodward 1996; Thompson et al. 1999; Kühn
et al. 2004). Several studies have focused on phylogenetic
patterns in their own right, generally revealing small effects,
although these relationships are fraught with biases and the
reasons may be difficult to unravel. Some effects are related to
the composition of the invader pool (large families tend to
have many invaders, e.g. Heywood 1989; Crawley et al. 1996;
Pysek 1998) and others may be due to associations with external
biological factors rather than directly with the acquisition of
traits (Lambdon & Hulme 2006b). For example, the highest
incidences of invaders often occur in families dominated by
ruderal and agricultural weeds (Pysek 1998). These habitats
are particularly susceptible to colonization, and the patterns
may reflect the evolution of adaptations to one specific
environment rather than invasiveness in an unconditional sense.
Daehler (1998) consequently found very different patterns
amongst species occurring in ‘natural areas’.
One consistent shortcoming is that these analyses have
tended to look for high incidences of invasiveness amongst
orders or families only. Within a regional flora, many taxonomic
units at family rank have few members (Weber 1997), leading
to weak resolution in probability tests. The approach is not
only statistically restrictive, but also ignores a large amount of
information regarding the interrelation of families to each
other (Lambdon & Hulme 2006a). Unfortunately, it is
difficult to describe cladistic interrelationships using linear
variables which lend themselves easily to standard analytical
techniques. Also, current knowledge of plant phylogeny
remains very incomplete, and so any trends are likely to be
influenced heavily by the interpretation adopted. Despite this
latter concern, understanding of evolution and systematics is
increasing rapidly due to advances in molecular techniques,
and a correspondingly more sophisticated use of the improved
information is overdue.
In this paper, I test for a taxonomic component to the
invasiveness of plant species which have been introduced to
Mediterranean islands. To circumvent some of the problems,
I adopt an approach analogous to one which is sometimes
used to detect spatial auto-correlation (the Mantel test; see
Koenig & Knops 1998). Rather than asking ‘Do families/
orders differ in their levels of invasiveness?’, it asks ‘Are
closely related species more likely to share similar levels of
invasiveness than distantly related species?’. This can be
addressed by a simpler analysis of association between two
variables: the measure of relatedness and a measure of similarity in invasiveness, for each species pair. The potential of
this technique has started to be explored by other authors
(Purvis et al. 1994; Strauss et al. 2006). I consider how such a
measure of association is affected by the interpretation of
phylogeny by comparing a modern cladistic tree with a more
traditional taxonomic classification, and I examine the trees
for clades displaying high proportions of invasive species,
which would allow some insights into possible evolutionary
origins. Finally, I examine how the distribution of such clades
compares to that obtained for other, simpler, traits which may
partly facilitate invasiveness, to assess how important their
contribution might be.
Methods
SPECIES DATA BASE
The species pool was compiled from over 100 published floras covering
islands of the Mediterranean basin. It included all non-native vascular
plants mentioned, whether naturalized, casual or prominent in
cultivation. However, species which were considered to be native in
some parts of the region were omitted, since their inclusion would
have lead to complications. The measure of invasiveness was the
number of islands where the species was fully naturalized, sensu
Richardson et al. (2000b).
I also compiled data on other invasion-related parameters,
although since most floras did not provide the necessary information, these were only available as regional statistics. A ‘frequency of
introduction’ index was created from questionnaires completed by
local experts on eight key islands. The contributors were asked to
rank all species on a seven point scale, reflecting the frequency with
which propagules were introduced to the island. Mean scores for
each species were standardized to range between 0 and 1 and lntransformed to achieve normality, and the resultant measure was
treated as a continuous variable. The two remaining descriptive traits
were categorical, recorded as binary presence or absence in one or
more of several subcategories, based on information extracted from
various literature sources (see Table 1). Firstly, species were classified according to their mode of introduction to the Mediterranean,
with seven subcategories identified. Secondly, habitat descriptions
were scored into nine subcategories. In order to limit the influence of
rare or casual occurrences in this assessment, habitats where the
species was noted less than three times were rejected, unless they were
mentioned in the more comprehensive Flora Europaea (Tutin et al.
1964–1980).
PHYLOGENETIC RELATIONSHIPS
Two classification systems were compared:
1 Mabberley (Fig. 1). This was created from Mabberley (1997), who
presented a purely hierarchical classification of vascular plants based
largely on morphological characteristics. The taxonomic levels
included in this treatment were Class, Subclass, Order, Family,
Genus and Species. A cladogram was derived by assuming that all
branches are equal in length (1 unit) and all subtaxa radiate equally
from their parent taxon.
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57
48
P. W. Lambdon
Table 1. Tests of phylogenetic patterns in binary traits. Data represent the proportion of pair-wise species combinations less than or equal to
the given phylogenetic distance where both species show the trait/the proportion of combinations less than or equal to the phylogenetic distance
where only one species shows the trait. Asterisks indicate that this ratio is significantly greater than unity (P < 0.05), based on a one-tailed χ2
test of the frequencies
Phylogenetic distance for χ2 test:
2
Mode of introduction
Crop species (field-scale)
Forestry species
Horticultural (small-scale uses, often a few plants in garden or village)
Amenity (grown in public for practical purposes, e.g. landscaping)
Ornamental (grown for ornament in gardens or indoors)
Contaminant (Introduced accidentally with seeds or soil)
Accidental (other accidental introductions)
Habitat preference
Ruderal (waste or disturbed ground)
Agricultural (cultivated land)
Urban (towns, buildings, parks and gardens)
Walls
Grassland (rangeland or improved pasture)
Woodland (all woodland types)
Freshwater (rivers, permanent streams, lakes and margins, marshes)
Coastal (dunes, beaches, coastal rocks or cliffs)
Xeric (dry shrublands (garrigue, phrygana), semisteppe)
2 APG (Fig. 2). This was based on recent cladograms published
by the Angiosperm Phylogeny Group (Stevens 2001 onwards). Their
synthesis uses a combination of morphological and genetic data and
is an attempt to integrate the latest thinking on angiosperm evolution.
However, it remains incomplete since there are still major gaps in
current knowledge (Cantino et al. 1997), and, at best, extends only to
subfamily level. To provide a complete phylogeny, the gaps have been
filled-in as for the Mabberley approach, using radial diversification
and standardized branch lengths. The Angiosperm Phylogeny Group
treatment focuses on describing accurate pathways and does not
claim to represent evolutionary distances accurately. However, in
lieu of a better alternative, relative distances have been retained as
presented on the web site. All families, genera and species are treated
as if equidistant from the origin at five, six and seven units, respectively. Since there were very few non-angiosperms in the species
list, and only one family per class, these were fitted into the system
following the same rules of interpolation as above.
DETECTING A PHYLOGENETIC COMPONENT TO
INVASIVENESS
The following analysis will subsequently be termed the phylogenetic
association (PA) test. All possible two-species comparisons were
identified. For each pair, two divergence measures were calculated,
one for evolutionary distance and one for the difference in a given
measure of invasiveness. Evolutionary divergence was estimated
from the phylogenetic distance between them; that is, the distance
necessary to move along the cladogram from species A back to a
common node and forward again to species B. Calculation of the
invasion divergence measure, and the subsequent statistical test,
differed depending on whether the invasion-related variable was
continuous or binary.
1 For binary variables, the species pairs were divided into two groups:
those combinations where both species possessed the invasion trait
were allocated to Group 1 and those where only one species possessed
the trait were allocated to Group 2. If neither species possessed the
4
6
8
2.80*
13.22*
2.34*
5.31*
1.44
4.01*
2.80*
1.71*
5.29*
1.41*
1.85*
1.26
2.26*
1.92*
1.38*
2.85*
1.15*
1.07*
1.08
1.25*
1.01
1.23*
1.50*
1.04
1.24*
1.00
0.98
0.98
2.21*
4.33*
2.47*
2.88*
1.23
1.79
2.21
1.06
11.00*
1.55*
1.48*
1.43*
1.95*
0.88
1.39
1.14
1.58*
1.40*
1.09
1.21*
1.00
1.74*
1.37*
1.89*
1.08
1.06
0.94
1.00
1.02
0.99
1.39*
0.99
1.39*
0.96
0.99
1.06
trait, the pair was excluded from the analysis. The two groups
were then compared for differences in their average phylogenetic distances. Since the frequency distribution of the values was unknown,
a categorical test was used. Species-pairs were sorted by phylogenetic
distance and cumulative frequency curves were generated, which
were more stable than the instantaneous distributions. Four χ2
tests were evaluated, at distances two, four, six and eight. Although
classical taxonomies are rather artificial and the hierarchies cannot
be considered equivalent (Stevens 1997), as a rule of thumb, the distances could be considered to represent divergence at the species,
genus, subfamily and family levels. In each case, the number of pairs
greater than and less than the critical distance in Group 1 were
compared against expected values based on proportions in Group 2.
A one-tailed test was employed because I expected species sharing a
trait to be more closely related to each other than species not sharing
a trait – it seems unlikely that they would be less closely related. In
order to correct for confounding statistical effects, the critical Pvalue was adjusted to achieve an unbiased experiment-wise Type 1
error rate of 5%. This was obtained from 200 Monte-Carlo simulations with the same trait frequency as the observed data. The trait
was allocated at random (i.e. there was no intrinsic difference
between Groups 1 and 2), and the critical P reduced until only 10 of
the 200 tests were significant at one or more of the four distances.
2 For continuous variables, a regression analysis was employed.
Divergence in the measure of invasiveness was calculated as the
positive difference between the members of the pair, and this was
ln-transformed to achieve an approximate normal distribution.
Again, there was a high level of variability in the individual values,
so phylogenetic distance (independent variable) was compared against
the cumulative mean invasiveness measure (dependent variable).
Using a general linear model solved by maximum-likelihood iteration
(the GENMOD procedure, SAS/STAT 9.1; SAS Institute Inc. 2002),
I tested whether the phylogenetic distance coefficient was significantly greater than zero, i.e. that species are more similar in their
invasiveness properties the more closely they are related (as above,
I did not expect the gradient to be negative because this would imply
that closely related species diverge in invasiveness).
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57
Phylogeny of Mediterranean alien plants 49
Fig. 1. Phylogeny constructed from Mabberley (1997). The axis reflects taxonomic
rank (an artificial designation in arbitrary
units). Relationships are shown to the level of
family, although only orders are named
(abbreviations: Cas = Casuarinales, Jug =
Juglandales, Eup = Euphorbiales, The =
Theales, Fab = Fabales, Pro = Proteales,
Lin = Linales, Pol = Polygalales, Com =
Commelinales, Eri = Eriocaulales, Jun =
Juncales).
VALIDATING THE DETECTION TECHNIQUE FOR
CONTINUOUS VARIABLES
In order to validate the regression technique, 13 scenarios were
tested using five simulated runs each. The simulations were based on
Monte-Carlo randomizations of the invasiveness data. The first scenario was a null model with no phylogenetic pattern: for each run
the invasiveness scores were sorted randomly across species. In the
other scenarios, a degree of phylogenetic clustering was forced on
the data set, described by two variables: the number of clusters and
the degree of within-cluster trait dominance. The number of
clusters (sub-clades rich in species with the given trait) was 3, 6 or
10, and their initial nucleating points were allocated to randomly
chosen species with a specified minimum separation to ensure that
the clusters did not overlap. In each run, all non-zero invasiveness
scores were allocated sequentially to consecutive clusters until fully
deployed. During the allocation, the most closely related unattached
species was added to the cluster. I assumed that once a trait has
evolved, it may be either functionally lost again or masked by other
phenotypic characters in the daughter species. Within-cluster
trait dominance (henceforth, trait dominance) was the probability
that a species in the cluster would display the invasiveness trait, and
was set at 0.25, 0.5, 0.75 or 1. If a single ‘die-throw’ (a randomly
generated number between 0 and 1) exceeded the trait dominance,
the species was considered to be an inert cluster member and
another species was added.
Each simulation was subjected to the PA test for continuous data,
as described in the previous section, and the discriminatory ability of
the method was evaluated. The model parameters (intercepts and
coefficients of the distance term) were then regressed against the
number of clusters and trait dominance to examine whether the PA
test could be used to determine how the clusters were structured.
EVOLUTIONARY PATTERNS IN INVASIVENESS TRAITS
For traits where a significant phylogenetic relationship was detected,
I attempted to identify the main clusters. Every sub-clade in the phylogeny comprising six or more species was examined. The trait values
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57
50
P. W. Lambdon
Fig. 2. Phylogeny constructed from the APG
(2005). Relationships are shown to the level
of family with a few prominent subfamily
divisions also included, although only
orders are named (abbreviations: Cer =
Ceratophyllales, Lau = Laurales, Pip =
Piperales, Pro = Proteales, Bux = Buxales,
Gun = Gunnerales).
of all members were listed, and the means of the sub-clades compared. The GENMOD procedure in SAS/STAT 9.1 (SAS Institute
Inc. 2002) was used to facilitate the comparison: binary traits were
assumed to be binomially distributed and a logit transformation was
adopted, whereas for continuous variables a Poisson distribution
and a log transformation were assumed. Since high trait scores were
relatively rare, the mean was close to zero in most sub-clades, but
several conspicuously higher values were easily identified for each
trait. When plotted on the cladograms (see Fig. 7), the ‘high-scoring’
nodes were usually traceable to a small number of phylogenetic
lineages. The origin of the cluster was designated at the node where
the mean value was highest.
Whilst the PA test addresses the central theme of this paper (is
invasiveness a legacy of evolution?) in non-specific terms, it remains
of interest to consider which traits may have contributed most
strongly to the evolution of invasiveness. The cluster patterns determined above permit an exploration of this question, with the various
species characteristics (habitat type, frequency or mode of introduction) used as explanatory factors. For each, cluster occurrences were
digitized into an evolutionary pattern variable (EPV) by recording
the cluster status (within a cluster = 1, cluster absent = 0) of all nodes
in the phylogeny. The explanatory EPVs were correlated against that
of invasiveness using the product-moment correlation coefficient (r).
It is possible that no single trait has been important in determining
invasiveness, but that it only arises when a number of traits interact.
To examine this possibility, a principal components analysis was
performed (via the PRINCOMP procedure in SAS/STAT 9.1) to
resolve the main elements of joint variation across all explanatory
EPVs. The various principle axis scores were again correlated with
the EPV of invasiveness as above.
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57
Phylogeny of Mediterranean alien plants 51
Fig. 3. Relationship between phylogenetic distance (APG system)
and the cumulative mean difference in invasiveness (i.e. the PA test)
for simulated scenarios. Each data series is averaged across five
simulated sets (error bars are omitted for clarity, although the runs
gave very similar results within series), and was generated around 10
clusters. In the ‘random’ treatment, invasiveness scores were not
clustered, but in the remainder clustering was determined by the trait
dominance parameter (high trait dominance = strong clustering).
The dashed guide-line indicates the expected null trend.
Fig. 5. Analysis of how the PA test is affected by the phylogeny used.
The graph depicts the relationship between trait dominance and the
regression coefficient of the PA test, comparable to Fig. 4. The filled
data points were obtained from simulated data sets where the
clustering patterns were generated using the same phylogeny (APG
system) as assumed in the analysis. The hollow data points were
obtained when distances were based falsely on the Mabberley system.
The relative difference between the two series shows the perceived
reduction in trait dominance when the analysis is based on an
incorrect phylogeny (approximately 15%).
Fig. 4. Analysis of how the PA test (APG system) is affected by
clustering pattern. Linear regression models were fitted to this
relationship for each of the simulated data sets (see Fig. 3). The
diagram shows how the regression coefficients vary according to
different levels of trait dominance and the numbers of clusters.
Confidence bars represent standard errors of the model estimates.
positive (the result was still rejected because the test was
one-tailed). The final test was significantly negative which
suggests a high Type 2 error rate (i.e. more trends are detected
than actually exist, sensu Sokal & Rohlf 1980). An experimentwise adjustment should therefore ideally be applied, although
I did not calculate such a correction as none of the real data
analyses merited critical evaluation.
In Fig. 3, the cumulative mean difference in trait value
increases with phylogenetic distance as it tends towards the
overall mean. Although these relationships are natural sigmoid
curves, a good linear fit was obtained across the range examined.
The strength of the clustering is clearly manifested in the
changing intercept and slope of the relationship. I conducted
a further analysis to ascertain whether the clustering patterns
could be predicted from such regression data (Fig. 4). The
number of clusters could not be explained by model parameters, but the degree of trait dominance showed a clear linear
trend (r2 = 0.91, P < 0.0001). Strong clusters resulted in lower
model intercepts and higher slope gradients. Responses of
the two indicators were highly correlated (r 2 = 0.96), so subsequently, only the GLM on slope was used to estimate trait
dominance in the real data.
Because these artificial clusters were generated using the
APG system, this can be said to be the true phylogeny. When
the analysis was repeated using the false Mabberley system,
the slopes of the PA tests were reduced. By extrapolation
between any two comparable true and false slopes, it is
estimated that using the Mabberley phylogeny to construct
distances confuses the clustering and reduces the perceived
trait dominance by approximately 15% (Fig. 5).
Results
SIMULATED DATA SETS
The PA test proved to be effective at detecting the presence
and strength of phylogenetic clustering (Fig. 3). Where
phylogenetic patterns exist, closely related species are more
similar in levels of invasiveness than distantly related species,
and one may therefore expect a significant relationship
between taxonomic distance and the difference in invasiveness. This was indeed found. If clustering was forced on the
simulated data sets, a strongly significant negative relationship was always obtained (P < 0.0001). In the random
simulations, where no clustering was specified, the relationship
was not significant in three of the five runs. The remaining two
runs produced extremely small effects, one of which was
PHYLOGENETIC PATTERNS IN INVASIVENESS
Invasiveness showed no clear phylogenetic component
(Fig. 6a). The slope of the PA test was not significantly
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57
52
P. W. Lambdon
Fig. 6. PA test for two invasion-related parameters: (a) the number of islands where naturalized (‘invasiveness’), and (b) frequency of
introduction.
different from zero using the APG phylogeny (r2 = 0.0013).
Under the Mabberley system, a trend was detected (r 2 = 0.54),
but the gradient of the slope was shallow (0.0092), corresponding to a trait dominance of only 0.13. Despite this null
result, I continued to examine the phylogenies for clades of
high trait frequency (Fig. 7). Not surprisingly, few were suggested and those were weak and mainly at a low taxonomic
level. Under the Mabberley system, most clusters constituted
individual genera, although the clustering was slightly more
coherent under the APG system and some families were
identified with significantly higher than average trait frequencies
(Asclepiadaceae, Solanaceae, Chenopodiaceae, Agavaceae
and Asteraceae).
PHYLOGENETIC PATTERNS IN INVASION-RELATED
TRAITS
In contrast to the lack of relationship for invasiveness, several
associated traits displayed clear phylogenetic patterns. The
only continuous variable tested was frequency of introduction.
Closely related species shared greater similarity in this trait
than more distantly related species (Fig. 6b), and the slope of
the trend line suggested a moderate level of clustering (trait
dominance was estimated to be 0.29). Of the binary variables
considered, there appeared to be an evolutionary component
to both the pathways via which species enter the region, and
the habitats they occupy (Table 1). Most of these effects were
small (Fig. 8), but in some, significant differences were detectable due to the high sensitivity of the methodology.
Species introduced for forestry purposes clustered strongly,
being mainly fast-growing trees in the Coniferales and a few
dicotyledonous genera (e.g. Eucalyptus). Seed contaminants
and those favouring agricultural habitats (two groups with
considerable overlap) also displayed a reasonably well-defined
phylogenetic component. However, there was no detectable
pattern in those species selected as ornamentals (Fig. 8a).
Adaptation to habitat types varied between clades, and in
contrast to invasiveness, the trends were stronger at higher
taxonomic levels (subfamily and family). Only freshwater
species did not display a detectable trend. This somewhat
surprising result is partly due to the paucity of aquatic invaders
on Mediterranean islands at present. Many species which
have become aggressive colonists elsewhere are yet to be
recorded, and those that have been are indeed rather randomly
distributed in taxonomic terms.
All of the traits examined differed quite strongly in their
clustering patterns (Fig. 9). With the exception of species
likely to be introduced accidentally, which were moderately
correlated with species of agricultural land (r = 0.39) and seed
contaminants (r = 0.40), EPVs of the explanatory variables
were only weakly correlated (r < 0.17). The principle components analysis used to identify relationships between the
EPVs revealed little joint variation between them, with only
the first four axes explaining more than 10% of overall model
deviance (16%, 14%, 11% and 10%, respectively). Invasiveness
was not related strongly to any of the principle components
(univariate GLMs based on binomial error distribution,
P > 0.05), although a significant relationship was obtained with
two of the original explanatory variables: denoting frequently
introduced species and forestry species. For high introduction
frequency, 51% of clusters with the trait shared high invasiveness, compared with 17% of those without the trait (P =
0.002). The forestry trait was only detected in four clusters,
three of which displayed high invasiveness (P = 0.029). Cluster
patterns are only very approximate, but these results suggest
that the very weak phylogenetic patterns in invasiveness did
not coincide with the evolution of adaptations to a particular
habitat, and they were only weakly related to traits which
influence introduction dynamics. However, frequency of
introduction appears to be a more important influence using
this phylogeny-related technique than has been shown using
simple correlations of trait presence between species (cf.
Lloret et al. 2004).
Discussion
The PA test was shown to be very efficient at detecting even
low levels of phylogenetic clustering, and was able to identify
patterns in most variables examined. However, the overall
trait of invasiveness produced very weak trends only. The few
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57
Phylogeny of Mediterranean alien plants 53
Fig. 7. Phylogenetic sub-clades identified
as displaying high invasiveness (the criterion
for display is that the node mean was
significantly different from zero at P < 0.05,
although this is somewhat arbitrary and
probabilities were not adjusted experimentwise). Key sub-clades are highlighted at the
parent node, and the shading of the marker
indicates the mean value of all daughter
species, based on the logit-transformed mean
number of islands (‘high’ means indicate
more reliable clusters). Sub-clades at the level
of genus are named. In order to interpret the
patterns, it is important to note that values
for some of the higher-level clades are
influenced by a single daughter branch.
Therefore, only the node of highest intensity
should be considered as the origin of the
cluster.
Fig. 8. Binary PA test (APG system) for two example invasion-related parameters: (a) suitability as an ornamental species, and (b) presence as an
accidental introduction. Species pairs where both species exhibit the trait are plotted separately from those where only one species exhibits the
trait (taken to be the ‘null’ distribution). In (a) the series were not significantly different but in (b) they differed at distances 2 and 4 (see Table 1).
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57
54 P. W. Lambdon
Fig. 9. Schematic representation of phylogenetic clusters identified in 16 traits. Because
the designation of clusters was very approximate and the level of certainty varied in
each case, this is reflected in the shading: high
(probability that the cluster mean differed
from zero, P < 0.10), medium (P < 0.15) and
low (P < 0.25).
clades tentatively identified were, in most respects, rather
heterogeneous: including some which are predominantly
weedy (Amaranthus, Euphorbia, Oxalis and Solanum), a genus
of succulents (Opuntia), clades of very widely introduced trees
(Eucalyptus and Pinaceae), and one of bulbaceous Monocotyledonae (parts of the order Liliidae). Since the methodology is
effective at controlling for the influence of family size, large
taxa which are often associated with invasiveness are not
prominent (e.g. the only potential cluster in the Asteraceae
was centred around the genus Senecio). Grasses, which are
often found to have a high potential for invasiveness (Weber
1997; Lonsdale 1999), were identified as a only minor cluster,
but this may be partly because the summer-arid climate is less
suited for pasture and domestic lawns than elsewhere in the
world.
Patterns were stronger in the less complex traits contributing
to invasiveness (suitability to a particular habitat or purpose
of introduction), implying some inheritance (on an evolutionary
time-scale) of adaptive characteristics which may indirectly
facilitate invasion. However, even these variables corresponded
to complex meta-traits, and clearly do not indicate individual
mutuations or even single syndromes (cf. Daehler 1998; Pysek
1998). For example, an examination of clades displaying a
high introduction frequency suggests that the properties
deemed desirable for import vary considerably. The cluster
centred around the genus Citrus undoubtedly arose as a result
of the evolution of the fleshy, nutritious fruits, whereas those
comprising the genera Eucalyptus, Acacia and the family
Pinaceae are associated with a fast-growing, woody growth
form suitable for timber. Other clusters are related to aesthetic
appeal (e.g. in the Arecaceae).
It is relatively easy to envisage the processes involved with
the evolution of habitat preference. Not surprisingly, there
was a moderately strong phylogenetic pattern amongst the
habitat variables examined, although secondary radiations
within clades have undoubtedly lead to a reduction in trait
dominance. Thus, families which have evolved suitable adaptations to a given life style may have subsequently speciated
allopatrically, and possibly sympatrically (Widmer 2002),
into other environments. The main point of note is that the
traits have arisen repeatedly, mainly at lower taxonomic levels,
which suggests that it is moderately easy to find viable solutions
to the environmental problems posed.
Suitability for a given mode of introduction is a more
abstract concept. Over evolutionary time, relatively few species
have undergone selection for such traits except some which
are accidentally transported, and have acquired adaptations
to enable dispersal and survival in ruderal environments
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57
Phylogeny of Mediterranean alien plants 55
(Baker 1965). Most others have evolved as a result of indirect
selection pressures, which, by chance, now happen to facilitate
success in the anthropogenic world. As in the example given
above for citrus and forestry species, the modes often involve
selection of a characteristic by humans, although these
characteristics are generally simple and specific. Modes of
introduction therefore tended to display similar, high levels
of clustering to the habitat preferences. Only the ornamental
attribute, which could be related to a range of factors from
desirable physical features to ease of cultivation, failed to
demonstrate such a pattern.
Introduction and establishment in a suitable habitat are
two of the key processes in successful invasion. Given that
both were very clearly influenced by phylogeny, it is perhaps
surprising to find that there were no comparable patterns in
invasiveness. One reason for this is the obvious difference in
evolutionary patterns exhibited for the different traits examined: it seems that distinct adaptations are required for each
of them, and that these have often arisen in entirely different
clades. This has consequences for the issue raised in the
introduction: if invasiveness is only ‘inherited’ very weakly at
the evolutionary level, it seems unlikely that there are traits
which could be used to predict it. The future therefore looks
bleak for screening protocols. But is such a conclusion inevitable, and if not, how could predictive traits arise without
leaving a phylogenetic trace? I discuss five further possible
explanations for the negative PA test.
(1) Inaccurate phylogenies
Since the goal of elucidating complete and true phylogenies
is still some way off, the potential for misleading results to
arise from erroneous assumptions has generated considerable
debate. Purvis et al. (1994) found a traditional taxonomic
classification to give less accurate results than a true phylogeny, but both approaches were moderately useful and Kelly &
Woodward (1996) identified several reasons why discrepancies
may be less extreme in analyses on real data than in such
simulations. Comparable conclusions may be drawn from the
present study. There were appreciable differences between true
and false phylogenies in a simulated scenario, and generally
the taxonomy-based Mabberley tree gave lower apparent
levels of clustering with real data than the phylogeny-based
APG system. The APG tree is probably the closer to the truth,
although large elements remain as conjecture. This suggests
that real phylogenetic patterns may be stronger than those
suggested by either system. However, inaccuracies can inflate
perceptions of clustering as well as deflate them (Stevens
1997). Furthermore, in practice most of the key evolutionary
nodes appear to have arisen no higher than the level of genus,
where the APG and Mabberley treatments are similar, and
consequently both identified similar invasiveness clusters.
(2) Stochastic introduction events
Whilst certain clades could evolve traits which favour
invasion at the habitat level, the expression of invasiveness
can only be facilitated once the species has been introduced to
the appropriate area. This may be particularly unpredictable
on Mediterranean islands, since migration between them is
largely dependent on human transport. Current distributions
suggest that the majority of invasive plant species have not
yet colonized their maximum potential ranges, some after
centuries of presence (Lambdon & Hulme 2006b). This would
undoubtedly lead to a high degree of noise in observed trends.
However, the PA test is sensitive enough to detect associations
despite considerable interference in the clustering pattern,
and should give a significant result when as few as 10% of
species exhibit a trait. Furthermore, our results suggest that
evolutionary trends are not restricted to the naturalization
process but also to introduction, and indeed, the weak clustering pattern obtained was more strongly related to introduction
frequency than any other variable, a trend repeated amongst
invasive bird species (Lockwood 1999). Another confounding
aspect of the transport issue is that more species are introduced from regions with strong trade links. Taxa which have
radiated in these biogeographical hotspots (e.g. the Middle East
or the Spanish colonies) may therefore be over-represented in
the Mediterranean alien flora (Pysek 1998).
(3) Changing selection pressures
The abundance of plant species is related to their success (i.e.
competitive ability, survival and dispersal) in the habitats
where they occur naturally. When environments change, the
favourability of traits may be expected to change with them,
which may result in a rapid randomization of selection processes and a disruption of any relationship between phylogeny
and adaptive suitability (Wiens 2004). Such drastic changes
in environments have taken place in the last few millennia
as humans have exerted strong influences on the world (Sala
et al. 2000; Mooney & Cleland 2001), so much so that invasive
potential now depends less on efficient natural dispersal but
on the ability to coexist with commerce. Most existing
habitats have been heavily modified and new ones created which
now dominate large areas. As a result, any invasive attributes
which evolved in prehistory are unlikely to confer the same
advantage today.
Despite this effect, it is still surprising that no phylogenetic
trends were detected when they persist in habitat adaptation,
whether these are residual traces of evolution in ancient natural environments or signs of recent selection for agricultural
and urban pressures. The latter are very well illustrated in
clades which have already radiated into a diversity of agricultural weeds, including a large part of the order Caryophyllales,
the Brassicaceae and the Papaveraceae/Fumariaceae. Clusters
were also detected in favourability for introduction by humans,
even though the selection pressures have only been operating
for a few millennia and advantages may have arisen partly
through chance secondary selection rather than direct coevolution. Based on this evidence, some persistent effect on
invasiveness might correspondingly be expected. One possible
manifestation of this is that several highly invasive taxa
correspond to those which Magallón & Sanderson (2001)
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57
56
P. W. Lambdon
identified as possessing particularly high rates of evolutionary
diversification – a property which would increase the probability that a few lineages are suited to changing environments.
(4) ‘Evolution’ of ecological interactions
Natural communities are usually extremely complex. Many
plant species can coexist in a given area, and it is usually
presumed that most occupy slightly different niches. They
interact both positively and negatively with each other, and
with a wide range of symbionts (Richardson et al. 2000a),
herbivores and pathogens (Keane & Crawley 2002). Each of
these species must be successful over some part of the niche
space in order to persist, and their success is therefore entirely
relative. What we term ‘invasiveness’ is usually associated
with certain visible manifestations, such as the ability to
colonize rapidly, to out-compete a given native or to occupy
an unusually broad niche space. These characteristics are not
only dependent on the inherited genes of the species, but also
on those of the organisms around it, and are likely to be highly
specific to the environmental conditions (Lonsdale 1999).
Under such situations, one would not expect a phylogenetic
pattern to emerge, nor any simple traits to predict the outcome
without considering the ecological ‘evolution’ of the affected
ecosystems. Traits influenced by phylogeny and which facilitate
‘relative’ ecological comparisons, such as the presence of
native congeners in the invaded range, could still influence
invasiveness. However this particular example appears to
have limited predictive value in the Mediterranean (Lambdon
& Hulme 2006a).
(5) Transient disequilibria of ecological interactions
When a species arrives in a new habitat, it takes time (perhaps
centuries) for stable ecological interactions to be established
within the invaded community. The incomers may possess
certain initial advantages which make them efficient competitors, although these may not persist. For example, they may
have the advantage of bringing no adapted pests and pathogens, although these are gradually recruited from immigrants
or by adaptation of local populations (Frenzel & Brandl
2003; Carpenter & Cappuccino 2005). Some may interbreed
with close local relatives and the progeny can develop shortterm hybrid vigour (Ellstrand & Schierenbeck 2000). Furthermore, aggressive dominants may be able to overwhelm the
ecosystem in the short term, but collapse due to the loss of
essential facilitative interactions which disappear as the
community becomes degraded.
Since, in the long term, species evolve to succeed under a
balanced set of environmental conditions, their performance
in such unbalanced circumstances may not be directly predictable. It would be difficult to model traits which should
prove to be beneficial when ecological pressures are changed,
or even to assess what the changes in ecological pressures are in
extant invasion case studies. Therefore, previous evolutionary
history is unlikely to be very relevant. If disequilibrium is a
major feature of current global invasion phenomena, one
would not expect strong phylogenetic patterns to emerge.
Although some simple traits could be favoured where circumstances are similar, trends are perhaps likely to become
confused in the face of highly stochastic, complex interactions.
Also, some apparent traits may be consequences rather than
mediators of invasiveness. Large leaf size or specific leaf area,
which has been reported as a correlate of invasion success
in a number of studies (e.g. Williamson & Fitter 1996; Lake &
Leishman 2004; Lloret et al. 2005), could simply be ‘less
selected against’ in the absence of herbivores than it would be
in a stable ecosystem.
Future developments and conclusions
The complex property of invasiveness displays little phylogenetic clustering within the Mediterranean alien flora.
Despite this, the evolutionary approach offers a sensitive and
reasonably well-controlled method for trait analysis, which
facilitates clearer mechanistic interpretation of the trends
uncovered.
Due to our limited understanding of phylogenetic relationships, the true level of precision in such analyses remains
unknown. One disadvantage of the APG and Mabberley
systems is that neither has branch lengths adjusted to account
for evolutionary time, which would provide a truer reflection
of divergence between species. Although substantial progress
has been achieved towards this goal (e.g. Wikström et al.
2001), there remain too many gaps in coverage for use with the
current data set. Furthermore, the most common calibration
approaches rely on fossil records and therefore measure time
directly, which may not be the best indicator of divergence if
clades have experienced different rates of evolution. However,
the effect is not likely to bias the pattern too much provided
that true branch lengths are randomly distributed with
respect to depth in the tree, and Ackerly (2000) suggests that
the assumption of equal branch length usually approximates
this condition reasonably well. Ultimately, relatedness patterns
are unlikely to be greatly affected although the strength of the
relationships may change slightly.
The fact that there is little persistent phylogenetic pattern
has wider implications for our ability to predict invasiveness:
if there is no clear evolutionary legacy, does this preclude the
idea that invasiveness is imparted by a syndrome of traits?
The arguments seem to be equivocal: traits with no clear
phylogenetic lineage could still be important in the face of the
rapidly changing environments which are being colonized.
However, the time-scale of the changes is critical. Explanations (2) to (5) operate over increasingly short periods and
small spatial scales: centuries in the case of (2) and (3) down to
a few decades in the case of (5). If the latter (microevolutionary
effects are important), then trait evaluation becomes prohibitively difficult.
Acknowledgements
Thanks to Guiseppe Brundu, Frederic Médail, Anna Travaset, Andreas Trombis,
Montse Vilà, Luca Viegi and their associated research teams for supplying
data, and to Louise Ross and Marie Pandolfo for contributing substantially to
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57
Phylogeny of Mediterranean alien plants 57
the data collation, and to Phil Hulme for additional discussion. This study was
conducted as part of the EU Framework 6 project ALARM (GOCE-CT-2003506675), and the data base assembled during the Framework 5 project EPIDEMIE (EVK2-CT-2000-00074).
References
Ackerly, D.D. (2000) Taxon sampling, correlated evolution, and independent
contrasts. Evolution, 54, 1480–1492.
Baker, H.G. (1965) Characteristics and modes of origin of weeds. The Genetics
of Colonizing Species (eds H. G. Baker & G. L. Stebbins), pp. 141–172.
Blondel, J. & Aronson, J. (1999) Biology and Wildlife of the Mediterranean
Region. Oxford University Press, Oxford, UK.
Cantino, P.D., Olmstead, R.G. & Wagstaff, S.J. (1997) A comparison of phylogenetic nomenclature with the current system: a botanical case study.
Systematic Biology, 46, 313–331.
Carpenter, D. & Cappuccino, N. (2005) Herbivory, time since introduction and
the invasiveness of exotic plants. Journal of Ecology, 93, 315–321.
Crawley, M.J., Harvey, P.H. & Purvis, A. (1996) Comparative ecology of the
native and alien floras of the British Isles. Philosophical Transactions of the
Royal Society of London Series B-Biology Sciences, 351, 1251–1259.
Daehler, C.C. (1998) The taxonomic distribution of invasive angiosperm
plants: ecological insights and comparison to agricultural weeds. Biological
Conservation, 84, 167–180.
Darwin, C. (1859) On the Origin of Species. John Murray, London, UK.
Ellstrand, N.C. & Schierenbeck, K.A. (2000) Hybridization as a stimulus for
the evolution of invasiveness in plants? Proceedings of the National Academy
of Sciences of the United States of America, 97, 7043–7050.
Ewel, J.J., O’Dowd, D.J., Bergelson, J., Daehler, C.C., D’Antonio, C.M.,
Gomez, L.D., Gordon, D.R., Hobbs, R.J., Holt, A., Hopper, K.R., Hughes,
C.E., LaHart, M., Leakey, R.R.B., Lee, W.G., Loope, L.L., Lorence, D.H.,
Louda, S.M., Lugo, A.E., McEvoy, P.B., Richardson, D.M. & Vitousek,
P.M. (1999) Deliberate introductions of species: research needs – Benefits
can be reaped, but risks are high. Bioscience, 49, 619–630.
le Floc’h, E. (1991) Invasive plants of the Mediterranean Basin. Biogeography
of Mediterranean Invasions (eds R. H. Groves & F. di Castri), pp. 67–80.
Cambridge University Press, Cambridge, UK.
Frenzel, M. & Brandl, R. (2003) Diversity and abundance patterns of
phytophagous insect communities on alien and native host plants in the
Brassicaceae. Ecography, 26, 723–730.
Heywood, V.H. (1989) Patterns, extents, and modes of invasions by terrestrial
plants. Biological Invasions: A Global Perspective (eds J.A. Drake, H.A.
Mooney & F. di Castri), pp. 31–60. John Wiley & Sons, New York.
Hulme, P.E. (2003) Biological invasions: winning the science battles but losing
the conservation war? Oryx, 37, 178–193.
Hulme, P.E.E. & P. (2004) Invasions, islands and impacts: a Mediterranean
perspective. Island Ecology (ed. J.M. Fernandez Palacios), pp. 337–361.
Asociación Española de Ecología Terrestre, La Laguna, Spain.
Joly, P. (2000) Biological invasions – State of the art and perspectives. Revue
d’Ecologie–la Terre et la Vie, Supplement 7, 21–35.
Keane, R.M. & Crawley, M.J. (2002) Exotic plant invasions and the enemy
release hypothesis. Trends in Ecology and Evolution, 17, 164–169.
Kelly, C.K. & Woodward, F.I. (1996) Ecological correlates of plant range size:
taxonomies and phylogenies in the study of plant commonness and rarity in
Great Britain. Philosophical Transactions of the Royal Society of London
Series B-Biology Sciences, 351, 1261–1269.
Koenig, W.D. & Knops, J.M.H. (1998) Testing for spatial autocorrelation in
ecological studies. Ecography, 21, 423–429.
Kühn, I., Brandenburg, M. & Klotz, S. (2004) Why do alien species that reproduce in natural habitats occur more frequently? Diversity and Distributions,
10, 417– 425.
Lake, J.C. & Leishman, M.R. (2004) Invasion success of exotic plants in natural
ecosystems: the role of disturbance, plant attributes and freedom from herbives. Biological Conservation, 117, 215–226.
Lambdon, P.W. & Hulme, P.E. (2006a) How strongly do interactions with
closely-related native species influence plant invasions? Darwin’s naturalization hypothesis assessed on Mediterranean islands. Journal of Biogeography,
33, 1116–1125.
Lambdon, P.W. & Hulme, P.E. (2006b) Predicting the invasion success of Mediterranean alien plants from their introduction characteristics. Ecography,
29, 853 – 865.
Lloret, F., Lambdon, P.W., Hulme, P.E.I.C., Brundu, G. & Médail, F. (2004)
Local and regional abundance of exotic plant species on Mediterranean
islands. Species Traits or Island Attributes? 10th International Conference on
Mediterranean Climate Ecosystems (MEDECOS) (eds M. Arianoutsou &
V. P. Papanastasis), pp. 129. Millipress, Rotterdam, Netherlands, Rhodes,
Greece.
Lloret, F., Médail, F., Brundu, G., Camarda, I., Moragues, E., Rita, J.,
Lambdon, P.W. & Hulme, P.E. (2005) Species attributes and invasion success
by alien plants on Mediterranean islands. Journal of Ecology, 93, 512 –520.
Lockwood, J.L. (1999) Using taxonomy to predict success among introduced
avifauna: relative importance of transport and establishment. Conservation
Biology, 13, 560–567.
Lonsdale, W.M. (1999) Global patterns of plant invasions and the concept of
invasibility. Ecology, 80, 1522–1536.
Mabberley, D.J. (1997) The Plant Book. Cambridge University Press,
Cambridge, U.K.
Magallón, S. & Sanderson, M.J. (2001) Absolute diversification rates in
Angiosperm clades. Evolution, 55, 1762–1780.
Manchester, S.J. & Bullock, J.M. (2000) The impacts of non-native species on
UK biodiversity and the effectiveness of control. Journal of Applied Ecology,
37, 845–864.
Mooney, H.A. & Cleland, E.E. (2001) The evolutionary impact of invasive
species. Proceedings of the National Academy of Sciences of the United States
of America, 98, 5446–5451.
Perrins, J., Williamson, M. & Fitter, A. (1992) Do annual weeds have predictable
characters? Acta Oecologica, 13, 517–533.
Pimentel, D., Zuniga, R. & Morrison, D. (2005) Update on the environmental
and economic costs associated with alien-invasive species in the United
States. Ecological Economics, 52, 273–288.
Purvis, A., Gittleman, J.L. & Luh, H.-K. (1994) Truth or consequences: effects
of phylogenetic accuracy on two comparative methods. Journal of Theoretical
Biology, 167, 293–300.
Pysek, P. (1998) Is there a taxonomic pattern to plant invasions? Oikos, 82, 282 –
294.
Richardson, D.M., Allsopp, N., D’Antonio, C.M., Milton, S.J. & Rejmanek,
M. (2000a) Plant invasions – the role of mutualisms. Biology Reviews of the
Cambridge Philosophical Society, 75, 65–93.
Richardson, D.M., Pysek, P., Rejmánek, M., Barbour, M.G., Panetta, F.D. &
West, C.J. (2000b) Naturalization and invasion of alien plants. Concepts and
definitions. Diversity and Distributions, 6, 93–107.
Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R.,
Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans,
R., Lodge, D.M., Mooney, H.A., Oesterheld, M., LeRoy Poff, N., Sykes,
M.T., Walker, B.H., Walker, M. & Wall, D.H. (2000) Global Biodiversity
Scenarios for the Year 2100. Science, 287, 1770–1774.
SAS Institute Inc. (2002) SAS/STAT ® User’s Guide, Version 9.1. SAS Institute
Inc, Cary, NC, USA.
Simberloff, D. (2005) The politics of assessing risk for biological invasions: the
USA as a case study. Trends in Ecology and Evolution, 20, 216–222.
Smith, C.S., Lonsdale, W.M. & Fortune, J. (1999) When to ignore advice:
invasion predictions and decision theory. Biological Invasions, 1, 89 – 96.
Sokal, R.R. & Rohlf, F.J. (1980) Biometry. W.H. Freemon & Co., New York, USA.
Stevens, P.F. (1997) How to interpret botanical classifications – suggestions
from history. Bioscience, 47, 243–250.
Stevens, P.F. (2001 onwards) Angiosperm Phylogeny Website, Version 7. May
2006. www.mobot.org/MOBOT/research/APweb
Strauss, S.Y., Webb, C.O. & Salamin, N. (2006) Exotic taxa less related to native
species are more invasive. Proceedings of the National Academy of Sciences of
the United States of America, 103, 5841–5845.
Thompson, K., Gaston, K.J. & Band, S.R. (1999) Range size, dispersal and
niche breadth in the herbaceous flora of central England. Journal of Ecology,
87, 150–155.
Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H.,
Walters, S.M. & Webb, D.A., eds. (1964–1980) Flora Europaea, Vol., pp. 1–5.
Cambridge University Press, Cambridge, U.K.
Weber, E.F. (1997) The alien flora of Europe: a taxonomic and biogeographic
review. Journal of Vegetation Science, 8, 565–572.
Widmer, A. (2002) A tight link between specialization and speciation. Trends in
Ecology and Evolution, 17, 161.
Wiens, J.J. (2004) Speciation and ecology revisited: Phylogenetic niche conservatism and the origin of species. Evolution, 58, 193–197.
Wikström, N., Savolainen, V. & Chase, M.W. (2001) Evolution of the
angiosperms: calibrating the family tree. Proceedings of the Royal Society of
London Series B-Biology Sciences, 268, 2211–2220.
Williamson, M. (1999) Invasions. Ecography, 22, 5–12.
Williamson, M.H. & Fitter, A. (1996) The characters of successful invaders.
Biological Conservation, 78, 163–170.
Received 19 April 2007; accepted 8 October 2007
Handling Editor: Ray Callaway
© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Ecology, 96, 46–57