Landscape Ecol
DOI 10.1007/s10980-016-0480-9
RESEARCH ARTICLE
Distribution of invasive plants in urban environment is
strongly spatially structured
Kateřina Štajerová
. Petr Šmilauer . Josef Brůna . Petr Pyšek
Received: 11 March 2015 / Accepted: 11 December 2016
Ó Springer Science+Business Media Dordrecht 2017
Abstract
Context Urban environments create a wide range of
habitats that harbour a great diversity of plant species,
many of which are of alien origin. For future urban
planning and management of the green areas within
the city, understanding of the spatial distribution of
invasive alien species is of great importance.
Objectives Our main aim was to assess how availability of different ecosystem types within a city area,
as well as several parameters describing urban
Electronic supplementary material The online version of
this article (doi:10.1007/s10980-016-0480-9) contains supplementary material, which is available to authorized users.
K. Štajerová (&) P. Pyšek
Department of Invasion Ecology, Institute of Botany,
The Czech Academy of Sciences, CZ-252 43 Průhonice,
Czech Republic
e-mail: [email protected]
P. Pyšek
e-mail: [email protected]
K. Štajerová P. Pyšek
Department of Ecology, Faculty of Science, Charles
University, Viničná 7, CZ-128 44 Praha, Czech Republic
structure interact in determining the cover and identity
of invasive alien species.
Methods We studied the distribution of chosen
invasive plant species in a mid-sized city in the Czech
Republic, central Europe, on a gradient of equal sized
cells from the city centre to its outskirts.
Results A great amount of variation was explained
by spatial predictors but not shared with any measured
variables. The species cover of invasive species
decreased with increasing proportion of urban greenery and distance from the city centre, but increased
with habitat richness; road margins, ruderal sites, and
railway sites were richest in invasive species. In
contrast, the total number of invasive species in cells
J. Brůna
Department of GIS and Remote Sensing, Institute of
Botany, The Czech Academy of Sciences,
CZ-252 43 Průhonice, Czech Republic
e-mail: [email protected]
J. Brůna
Institute for Environmental Studies, Faculty of Science,
Charles University, Benátská 2, CZ-128 01 Praha 2,
Czech Republic
P. Šmilauer
Faculty of Science, University of South Bohemia,
Branišovská 1760, CZ-370 05 České Budějovice,
Czech Republic
e-mail: [email protected]
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Landscape Ecol
significantly decreased with increasing distance from
the city centre, but increased with habitat richness.
Conclusions Our results suggest that different invasive species prefer habitats in the vicinity of the city
centre and at its periphery and the spatial structure and
habitat quality of the urban landscape needs to be
taken into account, in efforts to manage alien plant
species invasions in urban environments.
Keywords Alien Species cover Central Europe Invasive Neophyte Species richness Urban
environment
Introduction
Rapidly growing human activities associated with
disturbances of the landscape are reflected by increasing interest in urban floras, with special regard to
species of alien origin, which, on average, comprise
*28% of plant species in cities worldwide (Aronson
et al. 2014). Cities represent a specific environment for
plants, both in terms of ecological factors and
vegetation with novel species assemblages (Gilbert
1989; Hobbs et al. 2006). From the viewpoint of plant
invasions, human settlements serve as immigration
foci from which alien species spread into surrounding
landscapes (Chytrý et al. 2005, 2008b; CelestiGrapow et al. 2006; Lososová et al. 2012b); this
usually happens not randomly but along linear corridors such as rails, roads, rivers or canals (Asmus and
Rapson 2014, Ricotta et al. 2014). Alien species are
more closely associated with the urban environment
than native species (e.g. Williams et al. 2015). This is
due to opportunities for introduction and transportation of propagules (Sukopp and Werner 1983; Lockwood et al. 2005; Malavasi et al. 2014), habitat
heterogeneity (Pyšek 1995; Deutschewitz et al. 2003),
adaptation to high levels of disturbance (CelestiGrapow and Blasi 1998; Davis et al. 2000; Chytrý
et al. 2008a), and higher temperature demands that are
met due to the phenomenon of ‘urban heat islands’
(McKinney 2006; Lososová et al. 2012b). For these
reasons, the urban environment harbours a high
number of plant species distributed in a wide range
of habitats, and represents a unique ‘‘unnatural
phenomenon’’ (Sukopp and Werner 1983). Due to
greater habitat heterogeneity and enrichment by alien
species, cities are generally richer in species than
123
surrounding landscapes (Haeupler 1974; Kühn et al.
2004), and these differences have become increasingly
more pronounced over time (Chocholoušková and
Pyšek 2003; Pyšek et al. 2004a). In central Europe,
aliens in the floras of big cities make up *40% of the
total number of taxa (e.g., Pyšek 1998; Ricotta et al.
2009; Lososová et al. 2012a), and in the flora of the
Czech Republic, for which there is detailed information available, more than half of 1454 alien taxa
(representing about one third of the total flora) are
confined to human settlements, i.e. cities and villages
(Pyšek et al. 2012).
In the last decades habitat alteration and destruction, together with human-mediated introductions of
alien plants, have resulted in dramatic changes in the
structure of European urban floras. Typical of these
trends is a gradually increasing proportion of neophytes (alien species introduced to central Europe
after 1500 AD) in the total flora, while archaeophytes
(pre-AD 1500 aliens; see Pyšek et al. 2004b for
definitions) and native species proportions have
decreased (Kowarik 1995) or remained stable. Some
studies (e.g., Pyšek et al. 2003; Kühn and Klotz 2006)
explain such a pronounced turnover of species during
a relatively short time by the rapid growth of cities,
which creates novel habitats, i.e. industrial areas and
waste dumps, suitable for only a few species adapted
to new, and markedly different, conditions. Such
habitats are under a strong human influence and
mostly invaded by neophytes that are more urbanophilous compared to archaeophytes that prefer habitats
less affected by humans (Hill et al. 2002). Also, the
presence of neophytes has been shown to depend more
closely on propagule pressure than that of archaeophytes, which is generally high in human settlements
(Chytrý et al. 2008a). This implies that neophytes are a
greater threat to the native flora because they, unlike
archaeophytes, have not yet occupied all suitable habitats (Chytrý et al. 2008a). The city of Plzeň, western
Bohemia, Czech Republic, can be used to illustrate
these trends; here the proportion of neophytes in the
city flora increased from 73 to 177 species between
1880–1910 and the 1990s (Chocholoušková and Pyšek
2003). Similar trends are reported from other cities in
Europe (e.g., La Sorte et al. 2008; Lososová et al.
2012b; Ricotta et al. 2012). Consequently, understanding the behaviour of neophytes, as relatively
recent newcomers and likely invaders of the future, in
the urban environment is of crucial importance. This is
Landscape Ecol
especially relevant for this group of alien species
because many neophytes are able to spread to considerable distances from parental plants, which allows
them to rapidly colonize large geographical areas.
This subset of taxa is called invasive neophytes (see
Richardson et al. 2000; Pyšek et al. 2004b for
definitions).
In this study, we assessed the role of different
ecosystem types within a city area resulting from
landscape transformation due to urbanization and
heterogeneity, as well as several parameters describing urban structure in shaping the performance of
invasive neophytes. We ask how these factors interact
in influencing the cover and identity of invasive
neophytes, and determined their relative importance
along a gradient from the city centre, defined as the
densely urbanized inner city, to the outskirts, defined
as rural exurban environment. Although distance to
city center is a widely used metric, it is a simple
measure that does not consider the organic growth of a
city (see McDonell and Hahs 2008 for a review).
However, in this study area we have used this measure
as there was a clear gradient from old city center
through suburban housing to agricultural land (see
Fig. 1).The effect of distance from the city centre has
been often examined in previous studies (e.g., Klotz
1990; Kowarik 1995; Kühn et al. 2004; CelestiGrapow et al. 2006) based on which we hypothesized
that invasive species richness significantly increases
towards the more urbanized, less natural sites, which
are located closer to the city centre.
Our main aims were: (i) to investigate the relationships between the species richness and total cover of
invasive neophytes and the ecosystem types, (ii) to
compare the relative importance of invasive neophytes
in higly transformed and low/medium transformed
ecosystem types, (iii) to examine how much of the
variation in the composition of invasive neophytes is
accounted for by spatial structure predictors in the
highly transformed and low/medium transformed
ecosystem types.
Methods
Study area
The study was carried out in the city of Hradec
Králové, eastern Bohemia, with a population of
*100,000, which ranks it among the ten largest cities
in the Czech Republic. The city was founded in the
early thirteenth century. It is located at 235 m a. s. l., in
a warm and slightly dry climatic region with moderate
winters, mean annual temperature of 8.0 °C and mean
annual rainfall of 600 mm (Tolasz et al. 2007).
According to the phytogeographic division of the
Czech Republic (Skalický 1988), Hradec Králové
belongs to the Thermophyticum; this district is located
mostly in lowlands that were first colonized in the
Neolithic (Chytrý et al. 2008a), which implies an
intensive and long-lasting human impact.
Using the approach of McDonnell and Pickett
(1990) and Pyšek (1995), a sampling grid of 200 cells
(200 9 200 m each) running from the city centre to its
outskirts (2 9 4 km in size) was used. The study area
included arable land, old city centre, railway station
and adjacent industrial zone, as well as important biocorridors; they are, besides railways and roads, two
rivers (the Orlice river empties into the Labe river in
the study area), Chaloupská svodnice stream and
Labe’s water-channel (Fig. 1). With the exception of
inaccessible private gardens and army barracks, the
whole study area was sampled, including managed
spaces such as parks and lawns.
Data collection
The field work was carried out from July to September
2004 and we identified a list of 64 invasive neophytes.
The species selection was based on the catalogue of
alien plants of the Czech Republic and included all
invasive neophytes occuring in our territory (Pyšek
et al. 2002). Of the species labelled as invasive in the
catalogue, we excluded the water macrophyte Elodea
canadensis, and three species (Cytisus scoparius,
Peucedanum ostruthium, Mimulus guttatus) considered post-invasive in Pyšek et al. (2002) and currently
classified as naturalized rather than invasive (Sádlo
et al. 2007; Pyšek et al. 2012). Arrhenatherum elatius
and Myrrhis odorata were also excluded as their
neophyte status is doubtful and they are now regarded
as archeophytes in the Czech Republic (Chytrý et al.
2005; Pyšek et al. 2012). Even though some species
were labelled as naturalized in the updated catalogue
(Pyšek et al. 2012) that used a more conservative
approach compared to the previous edition (Pyšek
et al. 2002), we included them in this study as they are
common in the Czech urban alien flora: Epilobium
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Landscape Ecol
m
2000
0
Study area
Germany
Poland
Square cells
Old city centre
Railways and associated land
Czech Republic
Water bodies
Ortophoto © ČÚZK 2014
Austria
Slovakia
Fig. 1 Study area depicted on the ortophoto of Hradec Králové
adenocaulon, Galeobdolon argentatum, Mahonia
aquifolium, Matricaria discoidea, Oenothera biennis,
Physocarpus opulifolius, Rhus typhina, Rumex thyrsiflorus and Syringa vulgaris. Introduction, region of
origin and traits of the species included in our study as
well as their taxonomy and nomenclature were taken
from Pyšek et al. (2012); a synoptic taxon group was
used for Erigeron annuus agg. (see online Appendix 1
for the list of particular species with detailed information on the traits considered).
Different sources were used to obtain predictors.
Most of the chosen predictors allow us to distinguish
ecosystem types with prevailing level of transformation (adapted and simplified after Kowarik 2011). For
each cell in the study area, the length of roads and
length of water courses were obtained from Urban
Atlas 2006–2008. Other descriptors were not reliable
123
enough in this source so ortophotographs for the year
of study (Czech Office for Surveying, Mapping and
Cadastre 2004) were manually classified into other
ecosystem types: built-up areas and sealed surface,
agricultural land, railways and associated land (see
online Appendix 2 for the list of particular ecosystem
types with their detailed description), and public urban
greenery, i.e. a summary descriptor including all types
of vegetation in the public space (e.g. spontaneous
vegetation, parks and plant cultivations). Their proportions for each cell were computed in ArcGIS Pro
1.1 using tool Summarize Within (ESRI 2015).
Based on the local knowledge of the studied city,
we distinguished ten habitat categories (listed and
described with other ecosystem types in online
Appendix 2); their total number was taken as the
measure of ‘habitat richness’ that was used in
Landscape Ecol
statistical analyses. In the field we recorded (i) presence/absence of the ten habitat categories in each of
the 200 cells, (ii) the abundance of each invasive
neophyte, expressed as visually estimated total cover
(in m2) of all its populations growing outside cultivation, and also its affiliation to the habitat categories
present in a cell, and (iii) whether the species is
cultivated (yes or no). The distance from the city
centre was measured in cell ‘‘units’’ (200 9 200 m)—
each cell that included the city centre or its edge was
treated ‘‘0’’, a cell next to it ‘‘n’’, the next one ‘‘n ? 1’’
etc.
Finally, in the case we had two predictors describing similar features, the more precise predictor was
used in statistical analyses, e.g. the length of roads
instead of presence/absence of roads.
Statistical analyses
Multivariate constrained ordination was used to compare and jointly test the effects of ecosystem types and
other predictors on relative importance of invasive
species, using Canoco 5 package (ter Braak and
Šmilauer 2012). We included only species occurring
in at least three cells; hence the analyses are based on
30 species (highlighted in bold in online Appendix 1).
The relative importance value of individual invasive neophytes was expressed as a percentage of the
visually estimated proportion of urban greenery.
These values were log-transformed and the linear
model of RDA (redundancy analysis) was chosen
because a very short compositional gradient was
sampled, so a linear response of species along this
gradient was assumed (Šmilauer and Lepš 2014,
p. 27). We also standardized the relative importance
values of the species using case norm in the multivariate analyses, so that they reflect only the changes
in the relative proportions of individual invasive
neophytes along the gradient (Šmilauer and Lepš
2014, p. 30). In this way, the ordination results
complement the regression models predicting total
cover and richness of invasive species.
To investigate how the spread of invasive neophytes and different ecosystem types distinguished
within the study area are spatially structured and
whether this creates an indirect correlation between
them (spatial nuisance sensu Peres-Neto and Legendre
2010), we used the spatial eigenfunction approach to
represent the spatial variation at multiple scales as a
set of additional predictors (Legendre and Legendre
2012, pp. 859–905). In particular, we computed socalled distance-based Moran eigenvector maps (dbMEM) and used a selected subset of significant spatial
eigenvectors both as a third group in the variation
partitioning analyses (ter Braak and Šmilauer 2012)
and as covariates in the regression models.
The importance of low/medium transformed vs
highly transformed ecosystem types (see online
Appendix 2 for classification) was compared by first
performing forward stepwise selection within each
group and then comparing the effects of selected
predictor subsets using a three-way variation partitioning procedure (Šmilauer and Lepš 2014,
pp. 88–91), which included significant spatial eigenvectors (hereafter PCOs) as a third group of predictors
together with X and Y coordinates of cells and the
distance from the city centre. The independent effects
of selected ecosystem type descriptors or of their
groups were studied with simple constrained ordinations. We also evaluated the simple (independent) and
conditional (dependent) effects of individual variables
within each predictor group. The estimated Type I
errors for both simple and conditional effects were
adjusted by converting them into false discovery rate
(FDR; Benjamini and Hochberg 1995) estimates.
To focus on the unique effects of the distance from
the city centre, we performed another RDA with this
distance as the only explanatory variable. All constrained analyses were accompanied by Monte Carlo
permutation tests of the significance. With the exception of analyses using the spatial eigenvectors as
explanatory variables or covariates, we used constrained permutation tests where the spatial autocorrelation between adjacent cells is taken into account
(ter Braak and Šmilauer 2012, p. 74).
Generalized linear models (hereinafter GLM) were
used to evaluate the influence of selected ecosystem type
descriptors and habitat richness on two summary characteristics: log-transformed sum of invasive neophytic
cover and the diversity of invasive species, using R
software (R Development Core Team 2008). Significant
predictors were chosen by forward stepwise selection,
using a model with assumed Poisson distribution when
predicting the count of species and assumed gamma
distribution (and log link function) when predicting the
total cover. The stepwise selection was based on
Bayesian information criterion (BIC) values (Schwarz
1978), stopping the selection when the BIC of the best
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Landscape Ecol
candidate predictor was larger or equal to BIC value of
the present model or it was smaller by less than 0.5% of
the present model’s BIC. For predictors selected into the
model based on the parsimony criterion BIC, parametric
tests of significance were done post hoc using v2-statistic
or F-statistic based tests, respectively for taxon count or
total cover. To compare the (confounding) effect of
spatial structure, these two models were selected both
without and with important spatial eigenvectors (preselected again for each response variable using the BIC
criterion).
increase with each additional habitat type), see
Table 1a. The model predicting the estimated total
cover of invasive neophytes yielded slightly different
results with the inclusion of public urban greenery
(Table 1b). The total cover of invasive species
decreased with increasing proportion of the public
urban greenery and the distance from the city centre
(*11% decrease with DistCent increasing by one
cell), and increased with habitat richness (*44% with
each additional habitat type). When including important spatial predictors into the model first, none of
those effects was retained (Table 1a, b).
Results
Determinants of the relative importance
of invasive neophytes
Number of invasive neophytes and their total cover
Effects of highly transformed ecosystem types
Forty-two invasive neophytes were recorded in the
study area. The highest species richness was found in
road margins (32 species), ruderal sites (28 species),
and railway sites (23 species); 21 species occured on
water edges and in cultivated areas. The lowest
numbers of invasive neophytes were recorded in
meadows (5 species) and field margins (5 species).
The most common life history was annual (14
species), most species were deliberately introduced
(28 species), native to North America (20 species) and
from the Asteraceae family (11 species) (see online
Appendix 1 for details).
Based on the GLM results, the total number of
invasive species in cells significantly decreased with
increasing distance from the city centre (*4%
decrease with DistCent increasing by one cell, i.e.
200 m), but increased with habitat richness (*12%
Table 1 Overview of
selected predictors and their
effects on (a) the number of
invasive species per cell
(species richness), and on
(b) the total cover of
invasive neophytes per cell
in fitted GLMs. For
abbreviations see online
Appendix 2
123
According to computed RDA, the four selected
descriptors together explained *6% of variation.
When evaluating the independent contributions of
individual descriptors, the proportion of built-up areas
and sealed surface was the most important predictor,
explaining 3.5% of data variation, followed by the
length of roads (Table 2a, simple effects). When the
joint effect was examined, the second best predictor
was the presence of ruderal sites (see Table 2a,
conditional effects).
Effects of low/medium transformed ecosystem types
The predictors significantly affected (pseudo-F = 2.6,
p = 0.005) the relative importance of invasive species
and explained *5% of the variability in this measure.
(a)
Without spatial eigenvectors
With spatial eigenvectors
Predictor
v21
p
v21
p
(Intercept)
Estimate
SE
1.5150
0.1121
DistCent
-0.0365
0.0068
29.58
\0.0001
–
(not selected)
HabRich
0.1110
0.0260
17.96
\0.0001
–
(not selected)
(b)
Predictor
Estimate
SE
Without spatial eigenvectors
With spatial eigenvectors
F1,196
p
F1,189
p
(Intercept)
4.0725
0.5818
PubUrbGr
-0.2108
0.0509
17.46
\0.0001
–
(not selected)
HabRich
DistCent
0.4334
-0.1073
0.1095
0.0417
11.83
5.33
\0.0001
\0.05
–
–
(not selected)
(not selected)
Landscape Ecol
Table 2 Simple (independent) and conditional (dependent) effects of (a) highly transformed ecosystem types, and (b) low/medium
transformed ecosystem types on the relative importance of invasive neophytes in the study area, based on RDA model
Predictor
Simple effects
Explains %
Conditional effects
pseudo-F
padj
Explains %
pseudo-F
padj
a. Highly transformed ecosystem types
BuiAreAn
3.5
7.2
0.0107
3.5
7.2
0.0118
Length_R
3.2
6.5
0.01
1.1
2.4
0.039
Ruderal
2.1
4.2
0.01
1.8
3.7
0.018
RaiAnAs
1.4
2.8
0.0043
1.1
2.3
0.039
0.012
b. Low/medium transformed ecosystem types
AgrcLand
3.0
6.1
0.012
3.0
6.1
Lawn
2.0
4.1
0.0015
0.6
1.3
0.372
Length_W
1.6
3.2
0.015
1.8
3.7
0.018
Cultivat
1.5
3.1
0.015
1.1
2.4
0.039
Meadow
ParkGrdn
1.1
0.8
2.1
1.6
0.0924
0.349
0.8
0.5
1.7
1.1
0.06
0.627
For abbreviations see online Appendix 2. Conditional effects show the results of stepwise selection. The results of significance tests
are presented using pseudo-F statistic of the permutation test and the false discovery rate (FDR) estimate padj calculated from the
estimated Type I errors. Terms with FDR \ 0.05 are shown with a bold typeface
When each descriptor was tested independently (see
Table 2b, simple effects), five of the six considered
descriptors had a significant effect. Given an obvious
dependence in their occurrence, their joint effect was
examined and only three descriptors (agricultural land
proportion, length of water courses and plant cultivations) were retained (Table 2b, conditional effects).
However, the effect of plant cultivation is doubtful
because it contributes only a small amount of
variability in addition to the two already selected
predictors.
Effects of habitat richness and distance from the city
centre
Habitat richness and the seven most predictive descriptors of ecosystem types (see Table 2, conditional
effects) were retained in the constrained ordination
(Fig. 2). They significantly affect (pseudo-F = 3.6,
p = 0.005) the relative importance of invasive species
and explained 9.3% of the variability. Plotted isolines
demonstrate the increase in species richness towards
increasing habitat richness. Species in the upper right
corner, Bidens frondosa and Impatiens parviflora, are
predominantly found close to water courses. Species
located in the left part of the diagram (Conyza
canadensis, Erigeron annuus agg., Matricaria
Fig. 2 Redundancy analysis ordination diagram displaying the
relation between the habitat richness, the seven most predictive
ecosystem types (see Table 2, conditional effects) and the
relative importance of invasive neophytes (nine taxa with the
highest variance explained by the predictors are shown). The
axes shown explain 7.9% of the total variation. Plotted isolines
represent the change of species richness across ordination space
as fitted by a loess smoother model. For abbreviations see online
Appendix 1, 2
discoidea, Galinsoga quadriata and G. parviflora),
represent the common ruderal alien flora.
The significant effect of distance from the city
centre on the relative importance of invasive
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Landscape Ecol
neophytes is summarized in Fig. 3. This effect is
represented by the horizontal axis of the diagram,
explaining 1.9% of the total variation (pseudoF = 4.8, p = 0.006). Nine taxa with the highest
variance explained by the city centre distance are
shown.
In two partial constrained ordinations, both the
descriptors of highly transformed ecosystem types
(pseudo-F = 3.8, p = 0.005) and those of the low/
medium transformed ecosystem types (pseudoF = 2.1, p = 0.005) retained significant effects on
the composition of invasive neophyte composition
after accounting for the distance from the city centre.
In addition, we found that the effects of distance from
the city centre and proportion of the public urban
greenery are strongly interrelated. When taking the
distance into the model as a predictor and the greenery
as a covariate, the distance explains mere 1.2%
(pseudo-F = 3.3, p = 0.001), while the effect of the
public urban greenery is non-significant when testing
its effect in addition to the distance to city centre.
Fig. 3 Redundancy analysis ordination diagram displaying the
effect of distance from the city centre on the relative importance
of invasive neophytes (nine taxa with the highest variance
explained by the town centre distance, along the horizontal axis
of the diagram). The first, constrained axis explains 2.4%
(pseudo-F = 4.8, p = 0.006) and the second (unconstrained,
vertical) axis 11.4% of the total variation. Plotted isolines
represent the species richness change across ordination space as
fitted by a loess smoother model. For abbreviations see online
Appendix 1, 2
123
Comparing the effects of highly transformed and low/
medium transformed ecosystem types
Variation partitioning (Table 3) indicates that the
major parts of the variation explained by highly and
low/medium transformed ecosystem types are spatially structured, while their unique contributions are
relatively small (and non-significant for the former
group, pseudo-F = 1.2, n.s.), which indicates that a
very large part of the variation in the composition of
invasive neophytes is accounted for by spatially
structured predictors, not corresponding to those we
were able to measure, and that the (relatively important) effect of measured predictors is mostly spatially
structured.
Discussion
By employing descriptors of different types of
ecosystems within a city area as proxies for structured
urban landscape we can identify the sites within the
city with a high probability of invasive species’
occurence. Both measures of the invasive neophytes’
performance we used, species richness and total cover,
respond consistently to these factors; they decrease
with increasing distance from the city centre and are
supported by habitat richness—more habitats recorded
for a cell might be a ‘‘prerequisite’’ for the occurence
of more species in the cell. This implies that invasive
neophytes in the urban environment perform better in
areas that harbour a wide range of habitats—available
niches for newcomers. Although the assumption that
habitat diversity triggers a high plant species richness
in urban areas has been mentioned in the previous
studies (e.g. Sukopp and Werner 1983), a rigorous
evidence based on purposely collated primary data is
lacking. For the total cover of invasive neophytes, we
also found that it decreases with increasing proportion
of public urban greenery. The peripheries in cities in
the Czech Republic are usually less populated, with a
lower proportion of built-up areas, and still keep their
relatively rural character (Celesti-Grapow et al. 2006;
Chytrý et al. 2008a). The higher proportion of
greenery at the city margins increases the competition
among species, which makes the invasion by alien
species and their dominance in local communities
more difficult; only a few alien species are able to
penetrate into these resident plant communities,
Landscape Ecol
Table 3 Results of variation partitioning among three groups: highly transformed ecosystem types (HT), low/medium transformed
ecosystem types (LMT) and spatial predictors (SP)
Fraction
% of explained variation
% of total variation
Dfs
MS
HT (BuiAreAn, Length_R, RaiAnAs, Ruderal): unique effects
2.0
0.3
4
0.0049
LMT (AgrcLand, Cultivat, Length_W): unique effects
5.3
0.9
3
0.0068
SP (PCOs, X, Y, DistCent): unique effects
51.4
8.6
16
0.0094
Overlap of HT & LMT
0.2
\0.1
–
–
Overlap of LMT & SP
10.8
1.8
–
–
Overlap of HT and SP
21.8
3.6
–
–
Joint overlap of HT, LMT & SP
8.5
1.4
–
–
Total explained
100.0
16.7
23
0.0114
All variation
–
100.0
199
–
2
The values in the two percentages of variation columns are calculated using the adjusted R approach (ter Braak and Šmilauer 2012,
p. 161). MS represents a variance component estimate that accounts for different number of predictors in each group, so that the
relative strength of predictor groups can be better compared
establish there and create large stands. For neophytes,
the sites close to the city centre seem to be more
suitable as these species are well-adapted to the
limited water supply and high temperatures, which
provides them with an advantage over archaeophytes
and native species (Pyšek et al. 1995). Although their
populations usually do not reach high covers due to the
limited spatial extent of sites in which the vegetation
can occur, e.g. trampled or otherwise heavily disturbed
sites (Sádlo et al. 2007), their total cover is higher
compared to the periphery. However, the species
richness and total cover within the city (or the
considered descriptors themselves) must be strongly
spatially correlated as none of the considered descriptors remained in the model when the predictors
describing spatial structuring were included.
The gradient from the city centre to the outskirts not
only influences the invasive species richness and
cover, but also has an important effect on the
composition of neophyte assemblages, as illustrated
by changes in the relative importance of individual
species. This implies that species confined to habitats
close to the city centre are different from those typical
of the periphery. It is also important to emphasize that
both the descriptors of the highly transformed ecosystem types and the low/medium transformed ecosystem
types retained explanatory power of the invasive
neophytes’ composition even after accounting for the
distance from the centre, while the public urban
greenery itself did not. Obviously, we cannot distinguish the effect of large distance from the city centre
from the effect of high proportion of public urban
greenery, unless we include in our studies more towns
with different location of urban greenery with respect
to their city centres.
As regards the invasive species characteristics, we
find similar results as previous studies. Most of the
invasive neophytes belong to the plant family Asteraceae, which is in accordance with for example Pyšek
et al. (2002) and Weber et al. (2008). Regarding the
life-history, type of introduction into the country and
origin, most of the recorded species are annuals,
deliberately introduced and native to North America
and this correspond with the findings of other studies
not only from Europe (e.g. Lambdon et al. 2008) but
also from Asia (Zerbe et al. 2004; Weber et al. 2008).
The effect of different ecosystem types on plant
invasions has been documented for urban areas
(Gilbert 1989; Sukopp 2002; Celesti-Grapow et al.
2006; Vilà and Ibáñez 2011) as well as for entire
landscapes (Chytrý et al. 2008a; Pyšek et al. 2010;
Kowarik 2011). When explaining the changes in
relative importance of individual invasive species,
agricultural land, length of water courses and plant
cultivations were the most important predictors from
the group of low/medium transformed ecosystem
types, and built-up areas and sealed surface, length
of roads, ruderal sites and railways and associated
landscape from the group of highly transformed
ecosystem types. These findings correspond to the
strong effect of factors generally considered as driving
invasion in different ecosystem types, such as the
disturbance regime, high amount of available nutrients, and propagule pressure, including opportunities
123
Landscape Ecol
for spread by water or human activities (e.g., Davis
et al. 2000; Chytrý et al. 2008b; Blumenthal et al.
2009; Pyšek et al. 2010; Foxcroft et al. 2011; Vieira
et al. 2014).
Although, the results demonstrate that the effects of
low/medium transformed ecosystem types and highly
transformed ecosystem types are almost independent,
the large amount of variation explained by the spatial
predictors, but not shared with any measured variables
used, implies that some important characteristics
determining the identity and cover of present neophytes were missed from the model. Other explanation
could be that the significant predictors might be
events, structures or patterns no longer in existence,
which cannot be traced in any presently measurable
property (‘‘historical dynamics’’ sensu Legendre and
Legendre 2012, p. 878). However, similar results were
also acquired by Gulezian and Nyberg (2010), who
found almost no effects of urban land-use descriptors
on invasive species’ abundance in their study. This,
together with the fact that different factors are likely to
be important for different species, points to the
necessity to study the whole spectrum of characteristics should the invasions in urban areas be predicted
effectively. For example, Niggemann et al. (2009)
suggest that the human mobility in urban areas is a
much better predictor compared to habitats or habitatrelated factors. Also, the approach of Hahs and
McDonnell (2006) seems to be promising. They
attempted to assess commonly used urban descriptors
and provided an example of how to select objectively a
subset of predictors that could help to understand
ecological responses to urbanization.
In conclusion, different invasive species prefer
habitats either in the vicinity of the city centre or at its
periphery and the structure of the urban landscape
needs to be taken into account in efforts to manage
alien plant species invasions in urban environments.
Our study has also implications for future urban
planning and the management of green areas within
the city, such as parks and gardens. It is also obvious
from the results that the management of the habitats
itself is the central issue to control alien species. To
prevent greater numbers of invasive species from
establishment, low/medium-transformed habitat types
should be promoted in urban areas, and the habitats
that are most suitable for alien species should be
suppressed especially near the city center, where the
competition from native plant species is low. Highly
123
transformed habitats such as ruderal sites and road and
railway margins should be closely monitored to avoid
spread of invasive species into habitats of a more
natural character within the city.
Acknowledgements Our special thanks are due to Věra
Samková (East Bohemian Museum, Hradec Králové) for her
extensive help in the field and for providing us with local
floristic literature, Lukáš Sekerka for his patience and
permanent support, Martin Hejda, Jan Pergl and Stanislav
Mihulka for their critical insights on the first drafts of the
manuscript, and to Christina Alba who kindly improved English
and also commented on the manuscript. We also thank Amy
Hahs, Jill Rapson and two anonymous reviewers for valuable
comments that helped us to improve the manuscript. JB, KŠ, PP
and PŠ were supported by the Project No. 14-36079G (Centre of
Excellence PLADIAS from the Czech Science Foundation), PŠ
by the project of GAJU 04-142/2010/P, KŠ and PP by long-term
research development project RVO 67985939 (The Czech
Academy of Sciences), and Praemium Academiae award to PP.
References
Czech Office for Surveying, Mapping and Cadastre
(2004) Archive Colour Orthophoto of the Czech Republic
Aronson MFJ, La Sorte FA, Nilon CH, Katti M, Goddard MA,
Lepczyk CA, Warren PS, Williams NSG, Cilliers S,
Clarson B, Dobbs C, Dolan R, Hedblom M, Klotz S,
Kooijmas JL, Kühn I, MacGregor-Fors I, McDonnell M,
Mörtberg U, Pyšek P, Siebert S, Sushinsky J, Werner P,
Winter M (2014) A global analysis of the impacts of
urbanization on bird and plant diversity reveals key
anthropogenic drivers. Proc R Soc B 281(1780):20133330
Asmus U, Rapson GL (2014) Floristic homogeneity underlies
environmental diversification of northern New Zealand
urban areas. New Zeal J Bot 52:285–303
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple
testing. J R Statist Soc Ser B 57:289–300
Blumenthal D, Mitchell CE, Pyšek P, Jarošı́k V (2009) Synergy
between pathogen release and resource availability in plant
invasion. Proc Natl Acad Sci USA 106:7899–7904
Celesti-Grapow L, Blasi C (1998) A comparison of the urban
flora of different phytoclimatic regions in Italy. Glob Ecol
Biogeogr 7:367–378
Celesti-Grapow L, Pyšek P, Jarošı́k V, Blasi C (2006) Determinants of native and alien species richness in the flora of
Rome. Divers Distrib 12:490–501
Chocholoušková Z, Pyšek P (2003) Changes in composition and
structure of urban flora over 120 years: a case study of the
city of Plzeň. Flora 198:366–376
Chytrý M, Pyšek P, Tichý L, Knollová I, Danihelka J (2005)
Invasions by alien plants in the Czech Republic: a quantitative assessment across habitats. Preslia 77:339–354
Chytrý M, Jarošı́k V, Pyšek P, Hájek O, Knollová I, Tichý L,
Danihelka J (2008a) Separating habitat invasibility by alien
plants from the actual level of invasion. Ecology
89:1541–1553
Landscape Ecol
Chytrý M, Maskell LC, Pino J, Pyšek P, Vilà M, Font X, Smart
FM (2008b) Habitat invasions by alien plants: a quantitative comparison among Mediterranean, subcontinental and
oceanic regions of Europe. J Appl Ecol 45:448–458
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources
in plant communities: a general theory of invasibility.
J Ecol 88:528–534
Deutschewitz K, Lausch A, Kühn I, Klotz S (2003) Native and
alien species richness in relation to spatial heterogeneity on
a regional scale in Germany. Glob Ecol Biogeogr 12:299–
311
ESRI (2015) ArcGIS Pro 1.1, Redlands, CA, USA
Foxcroft LC, Jarošı́k V, Pyšek P, Richardson DM, Rouget M
(2011) Protected-area boundaries as filters of plant invasions. Conserv Biol 25:400–405
Gilbert OL (1989) The ecology of urban habitats. Chapman and
Hall, London
Gulezian PZ, Nyberg DW (2010) Distribution of invasive plants
in a spatially structured urban Landscape. Landscape
Urban Plan 95:161–168
Hahs AK, McDonnell MJ (2006) Selecting independent measures to quantify Melbourne&s urban-rural gradient. Landscape Urban Plan 78:435–448
Haeupler H (1974) Statistische Auswertung von Punktrasterkarten der Gefässpflanzenflora Süd-Niedersachsens.
Scripta Geobot 8:1–141
Hill MO, Roy DB, Thompson K (2002) Hemeroby, urbanity and
ruderality: bioindicators of disturbance and human impact.
J Appl Ecol 39(5):708–720
Hobbs RJ, Arico S, Aronson J, Baron JS, Bridgewater P, Cramer
VA, Epstein PR, Ewel JJ, Klink CA, Lugo AE, Norton D,
Ojima D, Richardson DM, Sanderson EW, Valladares F,
Vilà M, Zamora R, Zobel M (2006) Novel ecosystems:
theoretical and management aspects of the new ecological
world order. Glob Ecol Biogeogr 15:1–7
Klotz S (1990) Species/area and species/inhabitants relations in
European cities. In: Sukopp H, Hejný S (eds) Urban ecology, plants and plant communities in urban environments.
SPB Academic Publishing, The Hague, pp 99–104
Kowarik I (1995) On the role of alien species in urban flora and
vegetation. In: Pyšek P, Prach K, Rejmánek M, Wade M
(eds) Plant invasions: general aspects and special problems. SPB Academic Publishing, The Hague, pp 85–103
Kowarik I (2011) Novel urban ecosystems, biodiversity, and
conservation. Environ Pollut 159:1974–1983
Kühn I, Brandl R, Klotz S (2004) The flora of German cities is
naturally species rich. Evol Ecol Res 6:749–764
Kühn I, Klotz S (2006) Urbanization and homogenization—
comparing the floras of urban and rural areas in Germany.
Biol Conserv 127:292–300
La Sorte FA, McKinney ML, Pyšek P, Klotz S, Rapson GL,
Celesti-Grapow L, Thompson K (2008) Distance decay of
similarity among European urban floras: the impact of
anthropogenic activities on b diversity. Glob Ecol Biogeogr 17:363–371
Lambdon PW, Pyšek P, Basnou C, Hejda M, Arianotsou M, Essl
F, Jarošı́k V, Pergl J, Winter M, Anastasiu P, Andriopoulos
P, Bazos I, Brundu G, Celesti-Grapow L, Chassot P,
Delipetrou P, Josefsson M, Kark S, Klotz S, Kokkoris Y,
Kühn I, Marchante H, Perglová I, Pino J, Vilà M, Zikos A,
Roy D, Hulme PE (2008) Alien flora of Europe: species
diversity, temporal trends, geographical pattern and
research needs. Preslia 80:101–149
Legendre P, Legendre L (2012) Numerical ecology, 3rd, English
edn. Elsevier Press, Amsterdam
Lockwood JL, Cassey P, Blackburn T (2005) The role of
propagule pressure in explaining species invasions. Trends
Ecol Evol 20:223–228
Lososová Z, Chytrý M, Tichý L, Danihelka J, Fajmon K, Hájek
O, Kintrová K, Kühn I, Lanı́ková D, Otýpková Z, Řehořek
V (2012a) Native and alien flora in urban habitats: a
comparison among 32 cities across central Europe. Glob
Ecol Biogeogr 21:545–555
Lososová Z, Chytrý M, Tichý L, Danihelka J, Fajmon K, Hájek
O, Kintrová K, Lanı́ková D, Otýpková Z, Řehořek V
(2012b) Biotic homogenization of Central European urban
floras depends on residence time of alien species and
habitat types. Biol Conserv 145(1):179–184
Malavasi M, Carboni M, Cutini M, Carranza ML, Acosta ATR
(2014) Landscape fragmentation, land-use legacy and
propagule pressure promote plant invason on coastal
dunes: a patch-based approach. Landscape Ecol 29:1541–
1550
McDonnell MJ, Pickett STA (1990) Ecosystem structure and
function along gradients of urbanization: an unexploited
opportunity for ecology. Ecology 71:1231–1237
McDonell MJ, Hahs AK (2008) The use of gradient analysis
studies in advancing our understanding of the ecology of
urbanizing landscapes: current status and future directions.
Landscape Ecol 23:1143–1155
McKinney ML (2006) Urbanization as a major cause of biotic
homogenization. Biol Conserv 127:247–260
Niggemann M, Jetzkowitz J, Brunzel S, Wichmann MC, Bialozyt R (2009) Distribution patterns of plants explained by
human movement behavior. Ecol Model 220:1339–1346
Peres-Neto PR, Legendre P (2010) Estimating and controlling
for spatial structure in the study of ecological communities.
Glob Ecol Biogeogr 19:174–184
Pyšek P (1995) Approaches to studying spontaneous settlement
flora and vegetation in Central Europe: a review. In:
Sukopp H, Numata M, Huber A (eds) Urban ecology as the
basis of urban planning. SPB Academic Publishing,
Amsterdam, pp 23–39
Pyšek P (1998) Alien and native species in Central European
urban floras: a quantitative comparison. J Biogeogr
25:155–163
Pyšek P, Prach P, Šmilauer P (1995) Relating invasion success
to plant traits: an analysis of the Czech alien flora. In: Pyšek
P, Prach K, Rejmánek M, Wade M (eds) Plant invasions:
general aspects and special problems. SPB Academic
Publishing, The Hague, pp 39–60
Pyšek P, Sádlo J, Mandák B (2002) Catalogue of alien plants of
the Czech Republic. Preslia 74:97–186
Pyšek P, Sádlo J, Mandák B, Jarošı́k V (2003) Czech alien flora
and the historical pattern of its formation: what came first
to Central Europe? Oecologia 135:122–130
Pyšek P, Chocholoušková Z, Pyšek A, Jarošı́k V, Chytrý M,
Tichý L (2004a) Trends in species diversity and composition of urban vegetation over three decades. J Veg Sci
15:781–788
Pyšek P, Richardson DM, Rejmánek M, Webster G, Williamson
M, Kirschner J (2004b) Alien plants in checklists and
123
Landscape Ecol
floras: towards better communication between taxonomists
and ecologists. Taxon 53:131–143
Pyšek P, Bacher S, Chytrý M, Jarošı́k V, Wild J, Celesti-Grapow
L, Gassó N, Kenis M, Lambdon PW, Nentwig W, Pergl J,
Roques A, Sádlo J, Solarz W, Vilà M, Hulme PE (2010)
Contrasting patterns in the invasions of European terrestrial and freshwater habitats by alien plants, insects and
vertebrates. Glob Ecol Biogeogr 19:317–331
Pyšek P, Danihelka J, Sádlo J, Chrtek J Jr, Chytrý M, Jarošı́k V,
Kaplan Z, Krahulec F, Moravcová L, Pergl J, Štajerová K,
Tichý L (2012) Catalogue of alien plants of the Czech
Republic (2nd edition): checklist update, taxonomic
diversity and invasion patterns. Preslia 84:155–255
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical
Computing, Vienna
Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta
FD, West CJ (2000) Naturalization and invasion of alien
plants: concepts and definitions. Divers Distrib 6:93–107
Ricotta C, La Sorte FA, Pyšek P, Rapson GL, Celesti-Grapow L,
Thompson K (2009) Phyloecology of urban alien floras.
J Ecol 97:1243–1251
Ricotta C, La Sorte FA, Pyšek P, Rapson GL, Celesti-Grapow L,
Thompson K (2012) Phylogenetic beta diversity of native
and alien species in European urban floras. Glob Ecol
Biogeogr 21(7):751–759
Ricotta C, Celesti-Grapow L, Kühn I, Rapson G, Pyšek P, La
Sorte FA, Thompson K (2014) Geographical constraints
are stronger than invasion patterns for European urban
floras. Plos ONE 9(1):e85661
Sádlo J, Chytrý M, Pyšek P (2007) Regionals species pools of
vascular plants in habitats of the Czech Republic. Preslia
79:303–321
Schwarz G (1978) Estimating the dimension of a model. Ann
Stat 6(2):461–464
Skalický V (1988) Regionálně fytogeografické členěnı́ [Phytogeographic land classification]. In: Hejný S, Slavı́k B (eds)
123
Květena České socialistické republiky [Flora of the Czech
Socialist Republic]. Academia, Praha, pp 103–121
Sukopp H, Werner P (1983) Urban environments and vegetation. In: Holzner W, Werger MJA, Ikusima I (eds) Man’s
impact on vegetation. Dr. W Junk Publishers, The Hague,
pp 247–260
Sukopp H (2002) On the early history of urban ekology in
Europe. Preslia 74:373–393
Šmilauer P, Lepš J (2014) Multivariate analysis of ecological
data using Canoco 5, 2nd edn. Cambridge University Press,
Cambridge
ter Braak CJF, Šmilauer P (2012) Canoco reference manual and
user’s guide: software for ordination (version 5.0).
Microcomputer Power, Ithaca, NY
Tolasz R, Mı́ková T, Valeriánová A, Voženı́lek V (eds) (2007)
Atlas podnebı́ Česka [Climate atlas of Czechia]. ČHMÚ,
Univerzita Palackého v Olomouci, Praha & Olomouc
Urban Atlas (2006) Owner: Directorate-General Enterprise and
Industry (DG-ENTR), Directorate-General for Regional
policy, custodian: EEA. http://www.eea.europa.eu/dataand-maps/data/ds_resolveuid/9df69b925454fd267512ea6
5898dbbdc
Vieira R, Finn JT, Bradley BA (2014) How does the landscape
context of occurrence data influence models of invasion
risk? A comparison of independent datasets in Massachusetts, USA. Landscape Ecol 29:1601–1612
Vilà M, Ibáñez I (2011) Plant invasions in the landscape.
Landscape Ecol 26:461–472
Weber E, Sun S, Li B (2008) Invasive alien plants in China:
diversity and ecological insights. Biol Invasions 10:1411–
1429
Williams NSG, Hahs AK, Vesk PA (2015) Urbanisation, plant
traits and the composition of urban floras. Perspect Plant
Ecol Evol Syst 17:78–86
Zerbe S, Choi I, Kowarik I (2004) Characteristics and habitats of
non-native plant species in the city of Chonju, Southern
Korea. Ecol Res 19:91–98